seminario i: realidad y conceptos de especies

Transcripción

EVOLUCIÓN
DEPARTAMENTO DE ECOLOGÍA, GENÉTICA Y EVOLUCIÓN
FACULTAD DE CIENCIAS EXACTAS Y NATURALES
UNIVERSIDAD DE BUENOS AIRES
2° CUATRIMESTRE 2014
GUÍA Nº 2
ESPECIACIÓN BIOGEOGRAFÍA HISTÓRICA
CRONOGRAMA EVOLUCIÓN
2º cuatrimestre 2014
Fecha
teórica
Turnos MAÑANA, TARDE Y NOCHE
Tema Teórica
Fecha TP
Tema TP
Mi 13/8
Introducción
Vi 15/8
Historia del pensamiento evolutivo
Mi 20/8
Variabilidad genética
Vi 22/8
Genética de Poblaciones I
Ma 26/8
Historia del pensamiento evolutivo I
Mi 27/8
Genética de Poblaciones II
Ju 28/8
Historia del pensamiento evolutivo II
Vi 29/8
Genética de Poblaciones III
Ma 2/9
Genética de Poblaciones (TP cables)
Mi 3/9
Teoría Neutralista
Ju 4/9
Genética de Poblaciones (Problemas)
Vi 5/9
Plasticidad feno
Ma 9/9
Genética de Poblaciones (Populus)
Mi 10/9
Teoría y Realidad de Especie
Ju 11/9
Teoría Neutralista I
Vi 12/9
Especiación I
Ma 16/9
Teoría Neutralista II
Mi 17/9
Especiación II
Ju 18/9
Especiación I
Vi 19/9
Especiación III
Ma 23/9
Especiación II
Mi 24/9
Especiación IV
Ju 25/9
Especiación III
Vi 26/9
Filogenia I
Ma 30/9
REPASO
Mi 1/10
Filogenia II
Ju 2/10
LIBRE
Vi 3/10
REPASO
Ma 7/10
LIBRE
Miércoles 8 / 10 Primer Parcial Teórico-Práctico
Vi 10/10
Filogenia III
Ju 9/10
LIBRE
Mi 15/10
EvoDevo
Ma 14/10
Filogenia I
Vi 17/10
Macro
Ju 16/10
Filogenia II
Mi 22/10
LIBRE
Ma 21/10
Filogenia III
Vi 24/10
LIBRE
Ju 23/10
Biogeografía
Mi 29/10
Adaptación
Ma 28/10
EvoDevo I
Vi 31/11
Evolución del Sexo
Ju 30/10
EvoDevo II
Mi 5/11
Evolución Humana I
Ma 4/11
Macroevolución I
Vi 7/11
Evolución Humana II
JuV6/11
Macroevolución II
Mi 12/11
Evolución Humana III
Ma 11/11
Evolución Humana I
Vi 14/11
LIBRE
Ju 13/11
Evolución Humana II
Mi 19/11
REPASO
Ma 18/11
Evolución Humana III
Vi 21/11
LIBRE
Ju 20/11
REPASO
Mi 26/11
PARCIAL
Ma 25/11
LIBRE
Vi 28/11
LIBRE
Ju 27/11
Miércoles 26/11: Segundo Parcial Teórico-Práctico
Miércoles 10/12 y viernes 12/12: RECUPERATORIOS
14
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MÓDULO VI: ESPECIACIÓN 31
32
SEMINARIO I: REALIDAD Y CONCEPTOS DE ESPECIES Marcela Rodriguero & Abel Carcagno En este seminario se discutirá la existencia de las especies como entidades reales y válidas como objeto de estudio. Además, se reflexionará sobre los distintos conceptos de especie y los criterios, principalmente metodológicos, ligados a su adopción. Nota: Se recomienda especialmente la lectura crítica del trabajo “The meaning of species and speciation: a genetic perspective”, de Alan Templeton (versión traducida al español), disponible en http://www.ege.fcen.uba.ar/materias/evolucion/material.htm Parte I: Realidad de las especies • Hey J. 2001. The mind of the species problem. Trends in Ecology and Evolution 16 (7): 326‐
329. • Hey J., Waples R.S., Arnold M.L., Butlin R.K. & Harrison R.G. 2003. Understanding and confronting species uncertainty in biology and conservation. Trends in Ecology and Evolution 18 (11): 597‐603. (Fragmento). 1‐ Para comenzar a discutir: ¿cree Ud. en la realidad de las especies? 2‐ ¿En qué consiste el “problema de las especies”? 3‐ De acuerdo a lo discutido en el item anterior, en las clases teóricas y a lo que le dicta el sentido común… ¿cuáles son los posibles significados que pueden otorgarse a la palabra “especie”? 4‐ De acuerdo a lo discutido en los item 2 y 3 anterior, ¿qué clases de ambigüedad pueden desprenderse de las definiciones de especie enunciadas y cómo se podría confrontar este problema? 5‐ ¿Cuál es el resultado del proceso evolutivo según Hey (2001) y de qué manera podría abordarse su estudio? ¿Qué problemas podrían surgir al encarar un trabajo de esta magnitud? 6‐ ¿Cree que existe alguna correspondencia entre las especies y los grupos evolutivos? Fundamente su respuesta. Parte II: Conceptos de especie • Gross L. (2007) Who needs sex (or males) anyway? PLoS Biology 5(4): e99. • de Meeûs T., Michalakis Y. & Renaud F. (1998) Santa Rosalia revisited : or why are there so many kinds of parasites in “the garden of earthly delights”? Parasitol. Today 14(1): 10‐
13. 33
• “Species in Time”, fragmento del miniensayo “The Species concept”, de Richard Cowen (Departamento de Geología de la Universidad de California Davis). • Schlick‐Steiner B.C., Seifert B., Stauffer C., Christian E., Crozier R.H., Steiner F.m. 2007. Without morphology, cryptic species stay in taxonomic crypsis folowing discovery. Trends Ecol. Evol. 22(8): 391‐392. 7‐ ¿Cuál es la principal característica de la clase Bdelloidea y cómo repercute en la aplicación del CBS a este taxón? 8‐ De acuerdo al Concepto Biológico de Especie… ¿cuántos grupos esperaría encontrar dentro de la clase? ¿Cómo podría explicar entonces la ocurrencia de discontinuidades dentro de Bdelloidea? 9‐ ¿Qué otro concepto podría explicar a las categorías existentes dentro de esta clase? Discuta los potenciales problemas de cada alternativa propuesta. 10‐ Enuncie al menos dos características que dificulten la aplicación del Concepto Biológico de Especie a los organismos parásitos. 11‐ De acuerdo a los problemas analizados y a los conceptos que Ud. conoce… ¿cuáles aplicaría a las discontinuidades identificadas dentro de los grupos de organismos que exhiben un modo de vida parasitario? (Como antes, considere las posibles desventajas). 12‐ Teniendo en cuenta la diversificación de los organismos estrictamente asexuales y de los parásitos, por ejemplo… ¿Considera al sexo como a una condición sine qua non para el origen de los grupos evolutivos? 13‐ ¿Cuál es el problema que encaran los paleontólogos al incluir el factor tiempo en el estudio de la diversidad biológica y cómo redunda esto en la aplicación del Concepto Biológico de Especie a organismos extintos? 14‐ ¿Cómo solucionaría Ud. estos inconvenientes? (No olvide discutir ventajas y desventajas de sus propuestas). 15‐ ¿Cómo repercute la existencia de las especies crípticas en el concepto de especies morfológico? ¿Puede nombrar otro inconveniente para la aplicación de este concepto? Preguntas unificadoras 16‐ De acuerdo a lo discutido, está en condiciones de contestar la siguiente pregunta: ¿Cuáles son las dificultades que impiden la adopción de un único concepto de especie? 17‐ ¿Cree que algún día se arribará a una “solución radical al problema de las especies” (Ghiselin 1974)? 18‐ Explique la siguiente afirmación: “… [como el Concepto Biológico de Especie] se enfoca en el resultado y no en el proceso, ha resultado perjudicial para los estudios de los mecanismos de especiación…”. 19‐ ¿Qué fuerza/s mantiene/n la cohesión dentro de cada “especie”, y a la vez permite/n que estas se conserven como entidades discretas? ¿Qué concepto de especie hace alusión a esta cuestión? 34
326
Opinion
TRENDS in Ecology & Evolution Vol.16 No.7 July 2001
The mind of the
species problem
Jody Hey
The species problem is the long-standing failure of biologists to agree on how we
should identify species and how we should define the word ‘species’. The
innumerable attacks on the problem have turned the often-repeated question
‘what are species?’ into a philosophical conundrum. Today, the preferred form of
attack is the well-crafted argument, and debaters seem to have stopped inquiring
about what new information is needed to solve the problem. However, our
knowledge is not complete and we have overlooked something. The species
problem can be overcome if we understand our own role, as conflicted
investigators, in causing the problem.
Have enough words been said and written on the
subject of what species are? How many evolutionary
biologists sometimes wish that not one more word, in
speech or text, be spent on explaining species? How
many biologists feel that they have a pretty good
understanding of what species are? Among those who
do, how many could convince a large, diverse group of
scientists that they are correct?
At this last and most essential task, many great
scientists have tried and failed. Darwin, Mayr, Simpson
and others have taught us about species, but none has
been broadly convincing on the basic questions of what
the word ‘species’ means or how we should identify
species. For its entire brief history, the field of
evolutionary biology has simply lacked a consensus on
these two related questions. Indeed, there was broader
consensus before Darwin. Given the once widespread
acceptance of an essentialist view of species, perhaps
Linnaeus was our most capable and persuasive species
pundit1, although he was wrong, of course. Darwin
killed species essentialism, but in so doing, he fostered
rather than settled questions about what species really
are. Since then, the species problem has beseeched us
like the mythical sirens. Again and again, we pose and
seek an answer to the question ‘what are species?’.
Other allegories seem apropos as well2: consider that the
species problem is like a sword, thrust by Darwin into
the stone, and left for us to yank upon with
determination and futility. The often dreamed of
magic is a compelling definition of ‘species’ that fits our
understanding of the causes of biological diversity and
that leads us to identify species accurately and agreeably.
Jody Hey
Dept of Genetics, Rutgers
University, Nelson
Biological Labs, 604
Allison Rd, Piscataway,
NJ 08854-8082, USA.
e-mail:
[email protected]
The focus on definitions
A recent listing found two dozen different definitions
of ‘species’ (i.e. species concepts, Box 1), most of which
were invented within the past few decades3; and, since
then, new ones have continued to appear4. I was also
seduced by the ‘what are species?’ question, and once
devoted much time to puzzling over definitions. The
result was an apparently unpublishable ‘species’
manifesto. Although it attracts some readers on the
Internet, it has so far failed to inspire the groundswell
of consensus that I once felt it deserved.
A striking commonality of these numerous
definitions is that, with few exceptions, they are clearly
not to be interpreted as the different meanings of a set
of homonyms, but rather as competitors for the single
best meaning. There seems to be something about the
perceived extensions and the intensions (the ideas in the
minds) that are shared between these many definitions.
This commonality can also be appreciated whenever two
or more evolutionary biologists use the word ‘species’
in scientific conversations. This happens frequently,
usually with a seamless exchange of ideas. Despite
many different notions of ‘species’, and uncertainty and
disagreement over them, the word almost always gets
passed back and forth with tacit understanding. This
apparent consensus thrives until that awkward moment
when someone asks another what he or she means by
‘species’, at which point the consensus and the shared
thread of understanding can evaporate. It is as if on
one hand we know just what ‘species’ means, and on
the other hand, we have no idea what it means.
I cannot think of any other word that garners as
much lexicographical attention as ‘species’. Certainly
evolutionary biology is full of difficult ideas, and words
such as ‘adaptation’ and ‘fitness’ often deserve and
receive a lot of attention5. But those discussions are
broadly conceptual and do not focus on definitions per se,
the way that ‘species’ debates do. Of course, many
words resemble ‘species’ in having fuzzy extensions
(i.e. wide-ranging, sometimes vague referents) and
some are the subject of debates over definitions. For
example, the definition of ‘drought’ can matter greatly
for public policy6,7, and the meaning of ‘disease’
generates both philosophical and practical debates8.
But neither of these examples, nor any others that I can
think of, resemble ‘species’in being the subject of so
much attention that is both broadly theoretical and so
narrowly focused on achieving the best single definition.
Consider the parallels between the motives and
the species concepts of two of our most practiced
‘species’ definers. Ernst Mayr has been tweaking the
Biological Species Concept for decades1,9,10. Joel
Cracraft has been doing exactly the same thing with a
version of the Phylogenetic Species Concept11–13. Both
scientists are exceptional evolutionary biologists and
ornithologists. Both argue that species are real and
distinct entities in nature and that we need a succinct
species concept that sums up the way in which they
exist, and they both argue that we need a species
concept that helps investigators to identify such
things10,12–14. In short, they both want to understand
real species and to be able to identify them, and both
perceive a crucial role for a pithy definition. Despite
these similarities, they are led to dissimilar
definitions, and neither finds much utility in the
other’s concept. Of course, their concepts have some
compatibility with each other and with evolutionary
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02145-0
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Opinion
327
Box 1. Species conceptsa
•
•
•
•
•
•
•
•
•
•
•
•
Agamospecies Concept
Biological Species Concept*
Cladistic Species Concept
Cohesion Species Concept*
Composite Species Concept
Ecological Species Concept*
Evolutionary Significant Unit*
Evolutionary Species Concept*
Genealogical Concordance Concept
Genetic Species Concept*
Genotypic Cluster Concept
Hennigian Species Concept*
•
•
•
•
•
•
•
•
•
Internodal Species Concept
Morphological Species Concept
Non-dimensional Species Concept
Phenetic Species Concept
Phylogenetic Species Concept
(Diagnosable Version)*
(Monophyly Version)
(Diagnosable and Monophyly Version)
Polythetic Species Concept
Recognition Species Concept*
theory15, but, for those needing the single best
definition, that is beside the point.
It is best to be plain about these and other similar
efforts to find a definition that dispels the species
problem. Descriptive definitions are not great containers
of knowledge and they are not great tools for arbitrating
the natural world. Individually, descriptive definitions
are but small bundles of information or theory, and if
they seem to be of any great aid in arbitration, it is
because they are backed up by a far larger fund of
knowledge. In short, if you have got the knowledge
then the definitions are the easy part and fall readily
into place. If your knowledge is incorrect or incomplete,
no amount of wordplay will set it right. Those who have
tried to puzzle out the species problem by focusing on
definitions are missing something, and that something
is bigger and more important than any definition.
But how could our knowledge, upon which the species
debates have been built, be missing something? Do not
evolutionary biologists know of genetics, fossils,
geography and the vast organismal diversity that exists
on our planet? Does not every evolutionary biologist
know, from theory and mountains of evidence, that
evolution gives rise to organismal groups, within which
individuals are similar and closely related, and between
which divergence can and does accrue? But, despite
these intellectual riches, we must recognize that our
knowledge of species has not been sufficient to resolve
the species problem. Our obdurate debates16 and our
misplaced ambitions for ‘species’ definitions are a slap
in the face – they forcefully remind us that there are
some things that we just do not know about or
understand sufficiently to describe them adequately17.
The awkward juxtaposition of apparent ignorance and
seemingly complete knowledge can also be seen in one
of our most common modes of explanation. Consider the
now traditional method in which the nature of species and
the meaning of ‘species’ are addressed first by summing
up the inadequate state of affairs, followed by an exertion
of pure reason. There are dozens, if not hundreds, of
elegant articles that employ this approach. These articles
are permeated with the presumption that new argument,
and not new information, will settle the question. Species
pundits do not ask ‘what new information do we need?’.
http://tree.trends.com
36
• Reproductive Competition Concept*
• Successional Species Concept
• Taxonomic Species Concept
Reference
a Mayden, R.L. (1997) A hierarchy of species concepts:
the denouement in the saga of the species problem.
In Species: the Units of Biodiversity (Claridge, M.F.
et al., eds), pp. 381–424, Chapman & Hall
*Concepts that make reference to biological
processes (e.g. reproduction and competition) that
occur among organisms within species (and less so
between species) and that contribute to a shared
process of evolution within species.
By taking this approach, we are not acting like
scientists. We are acting like some philosophers,
particularly Aristotle, who addressed and supposedly
solved questions of the natural world by giving words
to intuited essences; that is, by making up definitions18.
An untapped source of information
Fortunately, we can learn rather a lot from our
unscientific behavior. Not only do we see in it a sure sign
that we lack information about the species problem, but
we also find a place in which to look for that information.
That place is within ourselves, in the ways that our
minds handle questions about species. To be clear, I am
saying that one source of new information and insight,
to which we should turn if we are to solve the species
problem, is our own behavior. Note that several authors
have concluded that we demand too much of species
concepts and that some of our demands are inherently
contradictory2,19–22. It is but a short step (and a great leap)
to cast such arguments in terms of the question: what is
it about our minds and our motives that mislead us?
Once we are introspective in this way, we
immediately obtain one clear answer to the question
‘what are species?’. In our minds and in our language,
species are categories. That is to say, the names for
species and the usage of those names take an entirely
conventional syntactical role that is taken by all
categories. Just as ‘planet’ is the name of a category,
and appears as a predicate in sentences (e.g. ‘The
Earth is a planet.’), so ‘polar bear’ is also a category
and a frequent predicate in sentences. Whatever else
they are, categories are things in the mind and in our
language, and they are used for organizing our
thoughts and language about organismal diversity.
Taxa
Of course, ‘species are categories’is just a starting point,
but it is one that helps us to tap into a large tradition of
inquiry on the connections between categories in the
mind and things in the real world17,23–26. Categories are
motivated by recurrent observations about the world27.
Humans are great observers of patterns of repetition,
and we devise our categories as a response. These socalled ‘natural kinds’ are in our heads, but they are also
328
Opinion
out there in the world, in some way. For example, frozen
wispy crystals of water sometimes fall to earth in great
numbers and we identify them as snowflakes. The
‘snowflake’category exists in our minds, but in some
sense it is also a feature of the world outside ourselves, a
world that is disposed to repeatedly generate individual
falling wispy crystals of water. Each of the species that
we identify is a category, but it is also a natural kind that
exists as a pattern of recurrence in the world. We call
these natural kinds ‘taxa’ and, whatever else they are,
there is no escaping the fact that we identify them first
on the basis of recurrent patterns that we find in nature.
What does it take to make such a species taxon? One
answer is that it does not take much: given a simple
observation of a few organisms that seem similar to one
another, and different from others, and a biologist is off
and thinking about devising a new taxon. Another
answer is that it varies tremendously with the
observer. Not surprisingly, biologists cannot agree on
how distinct a seemingly new pattern must be to
motivate a new named category. These lumper/splitter
debates go round and round, much as they have for
hundreds of years. Consider the situation with birds,
which for people are probably the most observable
animals on the planet. Conventional classifications
place the number of bird species worldwide at around
9000. But some feel that a proper evaluation would
yield a count closer to 20 000 (Refs 28,29).
So now we have one answer to ‘what are species?’.
They are categories and, more particularly, they are
named natural kinds of organisms: taxa. We also
know what causes them, and that they are the result
of two processes: (1) the evolutionary processes that
have caused biological diversity; and (2) the human
mental apparatus that recognizes and gives names to
patterns of recurrence.
Evolutionary groups
For many biologists, however, species taxa are entirely
inadequate for many of the purposes for which we use
‘species’. These biologists are interested in the causes
of species, not our mental contributions to taxa, but
rather the evolutionary processes that create patterns
of biodiversity. Of the many concepts listed by Mayden3,
many either strongly imply or explicitly state that a
species is a group of related organisms, one that is
enjoined by evolutionary processes that go on within
it, and that is separate from other groups because of
the absence of shared evolutionary processes with
those other groups (Box 1). It is these theoretical ideas
of evolving groups that descend fairly directly from
Darwin’s teachings, and they mark a drastic
departure from purely categorical or taxonomic ideas
of species. But be sure to note the vagueness of these
commonplace ideas of evolutionary groups. As much
as they are backed by strong theory, any attempt to
translate this theory into strict criteria for the
unequivocal identification of evolutionary groups
requires much work (and if the history of the species
problem is any indication, is bound to fail).
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Fundamental conflicts
Now let us compare and contrast the idea of a species
taxon with the idea of a species as an evolutionary
group. To begin with, these two meanings of ‘species’
refer to things that are fundamentally and ontologically
dissimilar. To the extent that instances of either of them
exist, they do so in very different ways. An evolutionary
group is an entity, somewhat discrete in space and time,
and capable of changing and being acted upon30–34. It
does not matter that its parts (individual organisms) can
move around with respect to one another, and it does
not matter that it is not entirely distinct and separate
from other such entities. Evolutionary groups share
these properties with all sorts of other entities, and the
arguments about their ontology (the way they exist) are
fairly simple, at least compared with those for categories
and taxa32. Whether natural kinds exist is an oftendebated question, but even if they do, it is an altogether
different sort of existence than for individual entities35–37.
Another major difference between the two viewpoints
is the role that distinction plays in their existence. We
recognize and devise species taxa pretty much as a direct
result of having perceived a seemingly distinct pattern of
recurrence. We devise taxa because they usefully serve
our drive to categorize things, and so their very existence
(such as it is) goes hand-in-hand with their perceived
degree of distinction. By contrast, evolutionary groups
exist regardless of our recognition of them, and they
might or might not be distinct. Note that as much as
the word ‘group’ can be taken to convey distinction, in
fact the world is full of things that exist and are not at
all distinct. Some that we are familiar with are clouds,
populations, and ecosystems. Since the early 20th
century, evolutionary biologists have been well trained
in the many ways that evolving groups of organisms
might not be distinct. Genes can be and are exchanged
at varying rates between such groups, and there are
myriad ways that levels of gene exchange can be
structured to create groups within groups38.
Finally, consider our very different motivations
towards the different usages of ‘species’. Names of taxa
are among children’s very first words (not the technical
jargon, of course, but words like ‘dog’and ‘bird’) and
adult biologists employ taxa in exactly the same manner:
that is, as named categories. Consider too that all
human societies have taxa that are part of taxonomic
systems that share some remarkable similarities with
each other and with those systems used by professional
biologists25,39. Surely humans have been devising and
using taxa ever since their ancestors evolved the capacity
for language. If there is one thing at which our brains are
adept, it is recognizing and devising different kinds of
organisms. But the idea of species as evolutionary groups
is in stark contrast to this categorical tradition that is
imbedded within our minds. The tradition of thinking of
species as evolutionary groups is only 140-years old, and
it is knowledge that comes to a person late in life, at least
compared with the knowledge of categories of organisms.
In short, we have two widely differing ways of
appreciating biological diversity17,21,33. We have the
Opinion
ages-old instinct to categorize, and we have the modern
tradition of scientific inquiry. Our instincts give us taxa,
but our inquires have only recently led us to understand
evolutionary groups. The taxa are relatively easy to
find and invent, whereas the evolutionary groups are
difficult to study, for they are often truly indistinct
with fuzzy boundaries between groups, and the forces
that conjoin them can be subtle. Research on a species,
as an evolutionary group, requires study of the very
processes of direct and indirect interaction among
organisms, including reproduction and competition,
that can cause those organisms to be a species.
The causes of the species problem
In addition to carrying conflicting ideas of species, we
evolutionary biologists also try to do something else –
we try to find a way to have the taxa be the same as the
evolutionary groups. The two things are ontologically
different, but they can correspond when all those
organisms that we would place in a category also
collectively and completely constitute an evolutionary
group. The human species is probably our most accessible
example of a species taxon that also corresponds well to
an evolutionary group. In general, our taxa can serve as
hypotheses of the organisms that constitute evolutionary
groups. Evolutionary biologists are very familiar with
this mode of thought. However, we will fail in our studies
if we forget the reasons why the two sorts of things
might have little correspondence with one another.
(1) The patterns that we observe are a function of
our own capacity for perception and judgment.
Furthermore, there is no reason why our senses should
be as subtle as all of nature. When we devise taxa, we
are not objective, and we must keep in mind that
References
1 Mayr, E. (1982) The Growth of Biological Thought,
Harvard University Press
2 Stebbins, G.L. (1969) Comments on the search for a
‘perfect system’. Taxon 18, 357–359
3 Mayden, R.L. (1997) A hierarchy of species concepts:
the denouement in the saga of the species problem.
4 de Queiroz, K. (1999) The general lineage concept
of species and the defining properties of the species
category. In Species (Wilson, R.A., ed.), pp. 49–89,
MIT Press
5 Keller, E.F. and Lloyd, E.A. (1992) Keywords in
Evolutionary Biology, Harvard University Press
6 Wilhite, D. and Glantz, M.R. (1987) Understanding
the drought phenomenon: the role of definitions.
In Planning for Drought (Wilhite, D. et al., eds),
pp. 11–27, Westview Press
7 Dracup, J.A. et al. (1980) On the definition of
droughts. Water Resour. Res. 16, 297–302
8 Caplan, A.L. et al., eds (1981) Concepts of Health
and Disease, Addison–Wesley
9 Mayr, E. (1942) Systematics and the Origin of
Species, Columbia University Press
10 Mayr, E. (1996) What is a species and what is not?
Philos. Sci. 63, 262–277
11 Cracraft, J. (1983) Species concepts and speciation
analysis. Curr. Ornithol. 1, 159–187
12 Cracraft, J. (1989) Speciation and its ontology: the
empirical consequences of alternative species
concepts for understanding patterns and
processes of differentiation. In Speciation and its
Consequences (Otte, D. and Endler, J.A., eds),
different human observers will find different taxa. It is
also useful to imagine a thought experiment of the taxa
that would be devised by an alien observer, by one who
uses different senses and who operates on a different
scale of observation.
(2) Real evolutionary groups need not be distinct, and
can overlap or be nested within one another, whereas
categories are created as a direct function of perceived
distinction. Attempts to delimit evolutionary groups by
the boundaries of the categories will cause some groups
to be missed and others to be wrongly circumscribed.
(3) Most importantly, we must keep in mind that the
evolutionary processes that caused the patterns that we
recognize, and which we use to form taxa, are processes
that acted long ago. As time passes, the wave front of
evolutionary processes leaves behind strong patterns of
similarity and differences among organisms. It is those
patterns that we use for the taxa, but the place where
evolutionary groups exist is at that wave front – they are
caused by the evolutionary processes that are going on
right now. The patterns of similarity that we recognize
are the remnants of former evolutionary groups that
might have long since shifted and splintered.
The species problem is caused by two conflicting
motivations; the drive to devise and deploy categories,
and the more modern wish to recognize and understand
evolutionary groups17. As understandable as it might be
that we try to equate these two, and as reasonable and
correct as it might be to use taxa as starting hypotheses
of evolutionary groups, the problem will endure as long
as we continue to fail to recognize our taxa as inherently
subjective, and as long as we keep searching for a
magic bullet, a concept that somehow makes a taxon
and an evolutionary group both one and the same.
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20 Endler, J.A. (1989) Conceptual and other problems
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(Otte, D. and Endler, J.A., eds), pp. 625–648,
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21 Hull, D.L. (1997) The ideal species concept – and
why we cannot get it. In Species: the Units of
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22 Heywood, V.H. (1998) The species concept as a
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23 Smith, E.E. and Medin, D.L. (1981) Categories and
Concepts, Harvard University Press
24 Lakoff, G. (1987) Women, Fire, and Dangerous
Things: What Categories Reveal About the Mind,
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Review
TRENDS in Ecology and Evolution
Vol.18 No.11 November 2003
597
Understanding and confronting
species uncertainty in biology and
conservation
Jody Hey1, Robin S. Waples2, Michael L. Arnold3, Roger K. Butlin4 and Richard
G. Harrison5
1
Department of Genetics, Rutgers University, Piscataway, NJ 08854, USA
National Marine Fisheries Service, Northwest Fisheries Science Center, Seattle, WA 98112, USA
3
Department of Genetics, University of Georgia, Athens, GA 30602, USA
4
Centre for Biodiversity and Conservation, School of Biology, The University of Leeds, Leeds, UK LS2 9JT
5
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA
2
species, but the problem endures with a steadily increasing literature on how to define ‘species’. A recent listing of
species concepts found 24 in the modern literature [1] and
new books appear steadily [2 – 4].
In recent years, a recurring claim with regard to the
species problem is that most species concepts have strong
implicit similarities, and that most are consistent with the
idea that species are evolving lineages or evolving
populations [1,3,5,6]. We agree with this consensus.
However, we remain concerned that it does little to
address the fundamental cause of the species problem,
which is the inherent ambiguity of species in nature. Here,
we focus directly on the nature of this ambiguity and
review a modern synthesis under which species-related
research and conservation efforts can proceed without
suffering from, and without fear of, the ambiguity of
species.
Recent essays on the species problem have emphasized
the commonality that many species concepts have with
basic evolutionary theory. Although true, such consensus fails to address the nature of the ambiguity that is
associated with species-related research. We argue that
biologists who endure the species problem can benefit
from a synthesis in which individual taxonomic species
are used as hypotheses of evolutionary entities. We discuss two sources of species uncertainty: one that is a
semantic confusion, and a second that is caused by the
inherent uncertainty of evolutionary entities. The former can be dispelled with careful communication,
whereas the latter is a conventional scientific uncertainty that can only be mitigated by research. This
scientific uncertainty cannot be ‘solved’ or stamped
out, but neither need it be ignored or feared.
For researchers, few ideals are as sought after as those of
the independent observer; preferably, a scientist should
discover and transmit his or her story, and not be a part of
it. But what if that cannot be arranged? In some fields,
most notably quantum physics and human behavioral
research, observation per se can have a direct effect on
outcomes, so that studies must be designed to incorporate
those effects. Of course, research in these fields does not
come to a halt. Neither does research halt in other fields
where the impact of the observer cannot be avoided or
ignored safely, but rather is addressed directly as part of
the research program. Here, we argue that biological
research on species will benefit from an explicit recognition of the inherent limitations that biologists experience as investigators of species.
Many evolutionary biologists, systematists and ecologists struggle with the related questions of how to identify
species and how to define the word ‘species’. These
persistent questions constitute what is known as the
‘species problem’. The problem is not new. Indeed, Darwin
drew upon the persistence of wide taxonomic disagreements to support his arguments for the evolution of
Background and synthesis
Prominent in species debates are questions regarding the
role played by human investigators in the creation of
species taxa, particularly with regard to taxonomic rank
designations. Darwin argued that decisions to apply the
taxonomic rank of species were sometimes arbitrary, and
that species are not different essentially from varieties [7].
Spurway drew upon the ways that animals learn to
identify different kinds of organism to argue that species
designations are caused by basic human instincts, and
that we could not expect to find a universally applicable
definition of ‘species’ [8]. Haldane supported this view [9],
and it has been articulated more recently from different
directions by Levin [10] and Nelson [11]. Yet, these
skeptics notwithstanding, the view has emerged since
Darwin that species have special properties that set them
apart from taxa of other ranks, and that species are
objective and real to some extent because of these
properties. Dobzhansky’s Genetics and the Origin of
Species portrayed species as real genetical and evolving
entities that could be studied with modern genetic
approaches [12]. Huxley’s The New Systematics [13] is
Corresponding author: Jody Hey ([email protected]).
39
http://tree.trends.com 0169-5347/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2003.08.014
598
Review
the historical touchstone for modern systematic research
programs that see species not just as categories with
representatives in museums, but also as dynamic evolving
entities that exist independently of human observers and
of human-assigned categories [14,15].
These two ideas – that species are categories that are
created essentially by the biologists who study them, and
that species are objective, observable entities in nature –
have long been in conflict. On the one hand, we have
species taxa that have been identified traditionally on the
basis of distinctive characteristics. On the other hand, we
have an idea of a species as a kind of entity in nature, an
evolutionary unit made up of related organisms that are
evolving together. Over the years, various authors have
recognized this fundamental distinction [3,16 –22]. Yet, is
it possible that these two perspectives on species can be
joined? That has been the intended purpose of some
popular species concepts, and much of the modern debate
over species concepts has been a struggle over how best to
describe species in a way that preserves both the accepted
taxonomic traditions and the modern understanding of
evolutionary processes. Both the Biological Species Concept of Mayr [23,24] and the Phylogenetic Species Concept
of Cracraft [25,26] are intended to help biologists identify
species taxa that are real evolutionary role players in
nature. Neither view admits a distinction between species
taxa and species as evolutionary entities.
But, hidden partly in the debates over the nature of
species lies a direct and complementary connection
between species as taxa and species as entities. The
connection represents a conceptual linkage that circumvents many aspects of the species problem and that leads
directly to ways that research can proceed without species
conflicts. To see this connection, consider that newly
devised species taxa serve as hypotheses that might be
supported by new data and that, notwithstanding the rule
of precedence, might require later revision. Growing
collections, improving methods of morphological analysis,
and the increasing use of ecological, behavioral and genetic
data have moved biologists necessarily away from the view
of taxa as fundamentally static to a view in which species
taxa can be revised on the basis of increasing information
from diverse sources [13– 15,27,28]. This view, that our
ideas regarding a particular species should be subject to
examination in light of data from natural populations, has
also emerged in the population genetic literature [29,30].
In particular, Templeton argues that population genetic
data should be used to test whether populations do indeed
exist as cohesive species [31].
These twin strands of thought on the hypothesis-testing
aspect of species designations, from the perspectives of
both systematics and population genetics, lead to the idea
that a species taxon can serve as a hypothesis of a species
as an evolutionary and ecological unit in nature [3,32– 35].
This synthesis draws directly upon the practice in
systematics in which taxa are subject to revision, but, in
addition, there is the idea that a species taxon presents a
general hypothesis that all existing organisms that would
be assigned to that taxon actually constitute a biological
entity in nature.
In principle, species taxa that are used as hypotheses
might be simply confirmed or rejected, although more
typical outcomes are likely to be fuller descriptions of the
evolutionary processes that occur among the organisms
that would be identified as members of a taxon. Some
species taxa can be expected to be highly explanatory as
evolutionary hypotheses, in which case they are likely to
be affirmed by the discovery of additional characters that
are shared uniquely among the organisms assigned to the
taxon. At some point following research on these evolutionary processes, a taxon might come to be paired with a
full description of the population or populations that it
represents, including the degrees of isolation and distinction that occur among populations. Also, the degree or
quality of correspondence between a taxon and its evolving
counterparts might be used to devise more taxa as
necessary.
The ambiguity of species entities
From a purely ontological perspective, entities are real
things that have a location in space and time, and that can
be acted upon or can change [36]. Entities have a different
kind of existence than do categories, such as taxa, which
have defining properties. To be clear, by way of a deliberate
example, consider the species taxon Ursus maritimus
(polar bear). The defining properties of this taxon were
described first by Constantine Phipps [37]. Today, many
animals that we assign to this taxon live in zoos, but most
constitute a circumpolar arctic population, comprising
multiple connected regional populations; that is, an
evolving entity [38]. Even if this entity were to disappear,
and the natural population of polar bears were to become
extinct, the species taxon would still exist as a set of
defining characteristics and would still have representatives in museums or zoos.
Species are but one kind of multi-organismal entity, and
organisms can also be components of social groups within
species as well as parts of commensal interspecies
assemblages. Biologists also recognize ecological entities
that consist of many different kinds of organisms, and
individual organisms are parts of ecosystems, both on very
local and broad scales. To complete the point, we need not
be monistic with regard to species entities and so might
wish to consider different kinds of species entities as a
function of how they arise and persist. Templeton [39]
articulated two general processes that will cause a group of
organisms to evolve together: gene exchange and ecological equivalence (or demographic exchangeability). Both
processes, alone or together, can cause genetic drift and
adaptations to be shared by a group of organisms, and
cause that group to evolve cohesively and separately from
other such groups.
Our perceptions of an evolving group of organisms will
be least ambiguous for those taxa whose only representatives exist in a single, small distinct population (e.g. a
species restricted to a single lake or mountain peak). But
even small populations that appear cohesive and well
bounded in some respects might not be in others. The
population of finches of the species taxon Geospiza fortis
that lives on Isla Daphne Major in the Galapagos is not
separated completely from populations on other islands,
neither is it completely separate from populations that are
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Review
assigned to other taxa [40,41]. Episodic hybridization
results in gene flow, and introgressing traits from other
species are sometimes favored by natural selection. In this
case, detailed genetic and ecological data reveal both the
presence of a cohesive evolving population, as well as ways
in which that population is not entirely separate from
other populations, some of which are assigned to the same
taxon and others to different taxa.
We might expect that large populations, especially if
they are subdivided geographically, will often comprise
multiple evolutionary entities. A taxon might include
organisms that are found in isolated populations, each of
which is evolving separately. Such populations might be
connected tenuously by occasional gene flow, and thus
might share some common selective sweeps (i.e. fixations
of advantageous mutations) and adaptations [42], but they
might still occur mostly as separate populations. In these
contexts, the nature of the evolutionary entity could be
inherently ambiguous, and even intensive field research
will not reveal a clear demarcation. In short, all the
organisms of a species taxon will often not constitute an
evolutionarily cohesive entity, particularly for species taxa
with representatives that are widespread or have disjunct
distributions [43].
599
Type II uncertainty
The second kind of uncertainty arises from basic limitations of empirical scientific research. This uncertainty is
caused by the inherently ambiguous correspondence
between a species taxon and the entity or entities for
which it is used as a hypothesis. Even with clarity over the
distinction between a taxon and an evolutionary entity, it
might be very difficult to assess empirically the actual
correspondence for a particular taxon. This practical,
empirical uncertainty is conventional in the sense that
scientists are rarely fully assured of a correspondence
between their hypothesis and reality. At base, this
uncertainty arises because of the subjective component
of devising categories. Species taxa are devised by
investigators and are partly a function of biologists’
tools, circumstances and inclinations. For species that
can be observed easily and have distinguishing morphological characters, this subjective element will seem
remote and biologists can agree on the organisms to be
included in a species taxon. However, for many organisms
that live in soil or water, or within or upon other larger
organisms, the subjective element might be large. Two
investigators working with a common sample of organisms
might well disagree on the weight to be given to particular
patterns of variation in such cases, and thus on the
designations and descriptions of new species taxa. When
we turn to the field, and use species taxa as hypotheses, we
see also that the uncertainty is difficult to mitigate. In
short, species entities are very difficult to study, for they
are evolutionarily and demographically dynamic. They
will often not be very distinct and the degree to which they
are distinct can change over time [5] if, for example,
separated populations exchange genes occasionally (as is
the case with the Galapagos finches).
Understanding species uncertainty
Using species taxa as a framework to study evolving
species in nature reveals two different kinds of uncertainty
that might persist in species-related research and
discussions.
Type I uncertainty
One persistent component of the species problem is that
‘species’ is a confusing homonym, with different meanings
that are disparate ontologically and yet related semantically. Three ontologically distinct meanings predominate
in the literature of the species problem: (1) ‘species’ is the
name of a taxonomic rank; (2) ‘species’ is the word that we
apply to a particular taxon of that rank (e.g. the species
taxon Homo sapiens); and, finally, (3) ‘species’ is a word
that we apply to an evolving group of organisms. The
potential for confusion between the first two meanings, the
taxonomic rank and particular taxa, has been recognized
for some time [18,44,45]. Less widely realized is that
confusion also arises between the second and third
meanings, between the ideas of a species as a taxon
(i.e. a category of organism or a group of organisms with a
shared set of traits) and a species as an evolving group of
closely related organisms. Although biologists and philosophers have recognized that evolution creates entities
that comprise multiple related individuals [23,36,46,47] it
has been understood only at times that such things are not
literally the same things as taxa (i.e. kinds of organisms)
[3,16,17,34]. That one word, ‘species’, is sometimes
used to refer to a taxonomic rank, at other times a
particular taxon, and at other times an entity in
nature, causes confusion and requires that authors and
speakers take care to articulate their meaning when
they use the term.
Confronting species uncertainty
Across the breadth of species-related research, biologists
vary in their use of species taxa. In systematics, taxa are
the essential starting point for classification and phylogenetic research. In population biology, some taxa are also
used in the course of ecological or genetic research on the
structure of evolving populations, although only a few can
be examined in this way. In the continuum of research
programs, which lies between focused taxonomic research
on the one hand, and research that is focused on particular
populations in nature on the other, there lies a great deal of
research by ecologists, evolutionary biologists and conservation biologists that rely upon taxa as indicators of
evolutionary entities. For example, many multi-species
studies, including ecosystem studies and biodiversity
assessments, rely strongly upon species taxon counts.
Such counts suffer several limitations depending on the
context, but one that is typically overlooked is the usually
unknown correspondence between taxa and evolutionary
entities [22,48,49].
What do we gain by considering species taxa explicitly
as hypotheses of species entities in nature, and by dividing
our species-related uncertainty into semantic (type I) and
empirical (type II) components? For research on natural
populations, for evolutionary and ecological questions or
for efforts to conserve biological diversity, we gain a
41
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general research protocol that is not hindered by some of
the traditional species-problem debates. Of course, the
method is not thereby made easy or simple. No synthesis
can do that because species in nature are difficult subjects.
However, we can appreciate that the difficulty of studying
species is a conventional scientific difficulty; it is caused by
the need to devise and test hypotheses, just as in other
fields with difficult subjects.
The framework of treating species taxa as hypotheses of
species entities leads us to distinguish those aspects of
species uncertainty that are inherent to research and
discovery of biological diversity, and to set aside some
aspects of species-related debate that are avoidable. Two
basic questions are inescapable. First, by what criteria
shall species taxa be identified? For systematists, this
question lies at the heart of species-concept debates
[2,15,50,51]. However, when a taxon is to be a tool for the
study of evolutionary entities, then the question becomes
the following: what criterion will aid best in the discovery
of the locations, boundaries and properties of evolutionary
entities? Importantly, the answer might not be the same
for all kinds of organisms.
The second question is when does one decide that there
is one, or more than one, evolving entity? Two kinds of
answer come fairly readily. One is simply not to decide
whether or where to draw lines of demarcation, but rather
to present the full picture that research has revealed, and
to do so in its full complexity rather than to reduce that
complexity artificially. A second kind of resolution, which
might be demanded because of practical concerns, is to
make a decision regarding demarcations, while also
recognizing the decision as an oversimplification
demanded by the practical concerns.
The principal aspect of the species problem that is
avoided by our proposed synthesis is the traditional debate
over a ‘best’ species concept. Consider that if taxa are to
serve as hypotheses, then there are several common
species concepts and associated taxonomic criteria that
could provide a good starting point for the study of
populations. In particular, the use of reproductive traits
and the use of diagnostic characters are both well
motivated by evolutionary theory, and each is expected
to provide a rough guide to the presence of evolutionary
units in nature [6]. This is not to say that one is as good as
another in a particular context, simply that each is
justifiable in principle, and that it remains to investigators to make that justification for their particular
subjects of research.
A key inspiration of the species-concept debate is the
often-described need for species-related clarity. These
appeals say in part that we need a common concept of
species to handle the uncertainties that arise in speciesrelated research. Although true in strictly systematic
contexts, the same arguments have also been applied in
reference to the study of evolving populations in nature
[26,52,53]. However, no species concept or protocol can
remove the inherent difficulty and ambiguity of research
on evolving populations. The demarcation of two different
sources of species uncertainty leads to a fairly straightforward parsing of conventional demands for species-related
clarity into those that are tractable and those that are not.
The common assertions, that we must be able to both count
species and to distinguish species, are directly answerable:
(1) species taxa can be counted, and they are distinguished
in the course of their devising; whereas, (2) evolutionary
entities will often be truly indistinct, and will sometimes
not be countable strictly or distinguishable unambiguously no matter how thoroughly they are studied [34].
Identifying units for conservation
The contrast between species taxa and evolutionary
entities is stark when considering conservation. Species
taxa can often be preserved in the sense of having living
representatives by culturing organisms in zoos and
botanical gardens; that is, by maintaining living counterparts to the taxon representatives that are kept in
museums. But if species taxa are to have representatives
living in nature, then they must be part of evolving
populations. In recent decades, this simple realization of
the fundamental insufficiency of taxa as the focus of
conservation efforts has shifted those efforts towards
research on how best to conserve evolving populations [54].
For population-based conservation efforts to be effective, goals must be articulated clearly both in terms of
what kinds of populations are to be conserved and in terms
that recognize the inherent difficulties and ambiguities. To
appreciate how such apparently offsetting demands (for
conservation criteria that recognize inherent ambiguities)
can be implemented, and to appreciate the issues raised by
their application, we consider the entity-based idea of an
evolutionary significant unit (ESU) [55– 58]. An ESU is a
population, or group of closely connected populations, that
belong to a species taxon. Furthermore, an ESU shows
evidence of being genetically separate from other
populations, and contributes substantially to the
ecological or genetic diversity found within the species
taxon as a whole.
In recent years, the ESU concept has been applied
broadly to salmon populations on the west coast of the
USA, as well as to a variety of other species [58,59]. The
intent in defining salmon ESUs has been to identify
entities that are on largely independent evolutionary
trajectories. Although it is problematic to predict which
ESUs will be important to the future evolution of the
taxon, conservation of as many ESUs as possible should
minimize anthropogenic constraints on natural evolutionary processes and maximize the probability that the taxon
and some of its populations will persist into the future.
However, this formulation provides no specific, quantitative standards and offers no guarantees that type II
uncertainties will be resolved. Thus, several variations
of the ESU concept have been proposed, and the concept
has been criticized as being too broad [60], too narrow
[61,62] or non-operational [52,63]. Two different kinds of
approach have been suggested to address the apparent
vagueness of the ESU concept. One suggestion is that, for
the purposes of efficiency, ESU status should be decided
using a uniform standard of genetic cohesiveness and
uniqueness. For example, Moritz [60] suggested a specific
genetic cutoff (based on mitochondrial DNA monophyly
and nuclear gene differences) for conferring ESU status.
The obvious concern that application of that standard will
42
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appear arbitrary in many applications, or capricious in the
face of other kinds of evidence of cohesiveness and
uniqueness is perhaps answered by the considerable
need for a readily applicable, if imperfect, yardstick.
Given that mitochondrial DNA diversity will often be a
poor indicator of demographic boundaries [64– 66], this
particular proposal might not be ideal. However, this does
not mean that some standardized method might not
provide a reasonable balance between biological realism
and the needs for efficiency.
A different kind of suggestion is that the current ESU
criteria should be replaced by a single, better criterion that
would, inherently by its nature, dispel uncertainty. The
principal claim of this sort is that ESUs should be groups
of individuals that share a unique character, or suite of
characters, that distinguish them from individuals of
other ESUs [52,63]. In other words, an ESU should be
identified by the criteria used in one version of the
Phylogenetic Species Concept [67,68], not for reasons of
efficiency (which could also be claimed), but because such
criteria are inherently unambiguous indicators of real
evolutionary entities. These proposals, which equate the
presence of a disjunct pattern of characters with the
presence of an evolving population, have two limitations.
First, they assume accuracy on the part of taxonomic
criteria and overlook the reasons why species taxa will
often be a poor guide for elucidating evolutionary entities.
Second, by directly equating ESUs with species taxa they
have nothing to offer to the question of how best to
conserve diversity below the species level.
In the case of Pacific salmon, the recognized species
taxa that are based on diagnostic characters are considerably more inclusive than ESUs that have been identified,
each of which is limited to the populations in a restricted
geographic area [58]. For this species, taxa based on
diagnostic characters appear to be too coarse a guide for
identifying evolutionary entities, which is not surprising
given the highly structured populations of anadromous
fish. In other contexts, it might happen that a strong focus
on diagnostic characters could lead to taxa that are less
inclusive than true evolutionary entities, either because of
the vagaries of sampling or because of the near infinity of
possible characters to examine [69].
601
taxa as a strategy to serve conservation goals, or to shift
the rank of a taxon solely as a way to preserve biodiversity
[71]. In other words, legitimate conservation concerns,
combined with a reliance on taxa as conservation units,
can have the unfortunate consequence of shifting taxonomic decisions away from biological criteria and towards
political or economic concerns.
Second, the uncertainty of species entities is not
different in kind to that associated with other scientific
subjects. Importantly, many scientific pursuits have high
levels of uncertainty and also play a highly visible role in
the formation of public policy. Consider droughts, for
example, which, as phenomena, are not circumscribed
easily, their intense environmental and financial impact
notwithstanding. Meteorologists, hydrologists and policy
planners have worked to develop practical guidelines for
drought identification, even as they debate how best to do
so [72]. Consider as well the difficulties associated with
medical diagnosis and the identification of health-risk
factors. Physicians must make judgment calls regularly in
the care of their patients, and they must also provide
public health guidelines that are as unambiguous as
possible, often in the face of substantial inherent
ambiguity.
The question of how best to identify populations for
conservation has much in common with questions of how
to identify droughts, and to prevent or treat disease, and
with other areas where imperfect scientific knowledge is
used to shape public policy. The choices of what to conserve
must often be made with regard to populations that are not
separate completely from others, or when information
regarding the relationships and degrees of distinction
among populations is very incomplete. Such decisions,
although difficult because of the uncertainties that are not
mitigated easily, are not different in kind from those
decisions made in other contexts where scientists have
imperfect knowledge or where nature does not present
clear boundaries.
Prospects
Biologists cannot hope to avoid or eradicate species
uncertainty. Whether such hope arises from a wish to
‘solve’ the species problem, or from a wish to simplify the
tasks of biodiversity conservation, or from fear that policymaking and legal institutions cannot accommodate uncertainty about species, we should recognize that there is not
a single species concept, nor a research protocol, that can
remove the inherent difficulty and uncertainty that
accompanies research on evolving populations. These are
conventional scientific uncertainties, and we cannot
shelter ourselves from them.
The first reward of treating species taxa as hypotheses
and by recognizing the inherent uncertainties of speciesrelated research is a research protocol that is conventionally hypothetico-deductive. But beyond this aspect, which
already characterizes the work of many investigators, the
largest gains will be in the area of explanation. Researchers of biological diversity are sometimes entangled by
species-problem-related questions that come from colleagues and biologists in other specialties, as well as from
laypersons, students and professionals in fields who rely
Policy implications of species uncertainty
If conservation efforts do focus on evolving populations and
treat species taxa as research guides, then the ambiguity
of evolving populations and their uncertain connection to
taxa will often be manifest. If biologists making conservation recommendations are revealed as being uncertain in
their species assessments, will this hinder the legal and
policy-making components of species conservation? Perhaps if biologists admitted uncertainty over species, then
they could not play as constructive a role in conservation
efforts [70]. For two reasons, we think that such a concern
is misplaced.
First, the traditional practice of treating species taxa as
the primary focus of conservation efforts has a cost, quite
apart from that associated with the possible misidentification of evolving populations. A strong reliance on taxa as
conservation units creates a pressure to devise new species
43
602
Review
upon the conservation recommendations of biologists. By
explaining how research begins with taxa and proceeds to
the study of populations, many species puzzles can be
explained in the familiar language of the uncertain
relationship between our hypotheses and the realities of
nature.
26
27
28
29
Acknowledgements
We are grateful to three reviewers for very helpful comments and to John
Avise for input on the article. Jim Mallet provided valuable input
throughout much of the preparation of the paper, although he disagrees
with some important aspects. M.L.A. acknowledges support from the
National Science Foundation, grant DEB-0074159.
30
31
32
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Endeavour
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The history of reductionism versus holistic approaches to scientific research by H. Andersen
Reading and writing the Book of Nature: Jan Swammerdam (1637–1680) by M. Cobb
Coming to terms with ambiguity in science: wave–particle duality by B.K. Stepansky
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45
Who Needs Sex (or Males) Anyway?
Liza Gross | doi:10.1371/journal.pbio.0050099
If you own a birdbath, chances are
you’re hosting one of evolutionary
biology’s most puzzling enigmas:
bdelloid rotifers. These microscopic
invertebrates—widely distributed
in mosses, creeks, ponds, and other
freshwater repositories—abandoned
sex perhaps 100 million years ago, yet
have apparently diverged into nearly
400 species. Bdelloids (the “b” is silent)
reproduce through parthenogenesis,
which generates offspring with
essentially the same genome as
their mother from unfertilized eggs.
Biologists have yet to find males,
hermaphrodites, or any trace of
meiosis—the process that creates
sex cells—challenging the long-held
assumption that evolutionary success
requires genetic exchange.
The genetic variation created by
meiosis and fertilization, theory holds,
bolsters a species’s capacity to weather
shifting environmental conditions
or resist rapidly evolving parasites.
(During meiosis, the genome splits
in two, and chromosome pairs swap
bits of their DNA; during fertilization,
the sex cells fuse to restore the
complete genome.) Many multicellular
eukaryotes pass through a sexual and
asexual phase in their life cycle. But
eschewing sex altogether, à la bdelloids,
is not theoretically consistent with a
long-lived evolutionary life span or
extensive species diversification.
In a new study, Diego Fontaneto,
Timothy Barraclough, and colleagues
developed new statistical techniques
for combined molecular and
morphological analyses of rotifers
to test the notion that species
diversification requires sex. The
researchers show that, despite an
ancient aversion for interbreeding,
bdelloids display evolutionary patterns
similar to those seen in sexually
reproducing taxa. How they have
avoided the pitfalls of a lifestyle widely
regarded as evolutionary suicide
remains an open question.
Bdelloids have remained such an
enduring enigma in part because
biologists are still debating whether
species exist as true evolutionary
entities. And if they do, what forces
determine how they diverge?
Traditional taxonomy relies on
morphological differences to classify
PLoS Biology | www.plosbiology.org
doi:10.1371/journal.pbio.0050099.g001
Scanning electron micrographs showing morphological variation of bdelloid rotifers and
their jaws. Have these asexual animals really diversified into evolutionary species? (Image:
Diego Fontaneto)
species, but it can’t distinguish
whether such differences reflect
physical variations among a
group of clones or adaptations
among independently evolving
populations. In the traditional
view of species diversification,
interbreeding promotes cohesion
within a population—maintaining the
species—and barriers to interbreeding
(called reproduction isolation)
promote species divergence. With no
interbreeding to maintain cohesion,
the thinking goes, asexual taxa might
not diversify into distinct species.
Fontaneto et al. defined species
as independently evolving, distinct
populations (or units of diversity)
subject to distinct evolutionary
mechanisms. They predicted that if
factors other than interbreeding—such
as niche specialization—controlled
0001
46
species cohesion and divergence, then
asexual taxa should diverge along the
same lines as sexually reproducing
organisms. And if this were the case,
they would expect to find genetic
and morphological cohesion within
independently evolving populations
and divergence between them.
To detect independently evolving
populations, the researchers analyzed
marker genes isolated from clones
of bdelloids collected from diverse
habitats around the world. They
constructed evolutionary trees using
both mitochondrial and nuclear
DNA sequences (the molecular
“barcode” cox1 and 28S ribosomal DNA
sequences, respectively) to identify
species within the samples. For the
morphological analysis, they measured
the size and shape of the rotifers’ jaws
(called trophi).
April 2007 | Volume 5 | Issue 4 | e99
The morphological results largely
fell in line with traditional taxonomic
classifications for most bdelloid
species. And species identified as
related on the DNA trees typically
had similar morphology. The
correspondence between the molecular
and morphological results suggests
that the majority of traditionally
identified bdelloid species are what’s
known as monophyletic—individuals
in the same species assort together
on the evolutionary tree and share a
common ancestor. Only two of these
traditional, monophyletic species
showed significant variation in trophi
size or shape among the populations;
both also showed significant divergence
in the DNA trees.
Using statistical models to determine
the likely origin of the observed
DNA tree branching patterns, the
researchers show that these distinct
monophyletic genetic clusters
represent independently evolving
entities (rather than variations within
a single asexual population). But what
caused them to evolve independently?
Are they geographically isolated
populations that evolved under neutral
selection, or did they evolve into
ecologically discrete species as a result
of divergent selection pressures on
trophi morphology?
If bdelloids have experienced
divergent selection, the researchers
explain, they would expect to see
high variation in trophi traits between
species, and low intraspecies variation
(compared to neutral changes). And
that’s what they found—bdelloids have
experienced divergent selection on
trophi size (and to a lesser degree, on
trophi shape) at the species level.
0002
47
Altogether, these results show that
the asexual bdelloids have indeed
experienced divergent selection on
feeding morphology, most likely as
they adapted to different food sources
found in different niches. By showing
that asexual organisms have diverged
into “independently evolving and
distinct entities,” the researchers argue,
this study “refutes the idea that sex
is necessary for diversification into
evolutionary species.” They hope others
use their approach to study mechanisms
underlying species divergence in sexual
taxa to clarify the hazy nature of species
and biological diversity.
Fontaneto D, Herniou EA, Boschetti
C, Caprioli M, Melone G, et al. (2007)
Independently evolving species in asexual
bdelloid rotifers. doi:10.1371/journal.
pbio.0050087
Reviews
Santa Rosalia Revisited:
or Why Are There So Many Kinds of Parasites in
‘The Garden of Earthly Delights’?*
T. de Meeûs, Y. Michalakis and F. Renaud
As is the case for free-living species, a very large number of
parasitic species are not described adequately by the biological
species concept. Furthermore, Thierry de Meeûs, Yannis
Michalakis and François Renaud argue that because hosts
represent a highly heterogeneous and changing environment
as well as a breeding site, favouring the association of hostadaptation and host-choice genes, sympatric speciation may
occur frequently in parasitic organisms. Therefore, parasites
appear to be ideal biological models for the study of ecological
specialization and speciation. Beyond the relevance of such
considerations in fundamental science, the study of the origin
and evolution of parasite diversity has important implications
for more applied fields such as epidemiology and diagnosis.
Limitations of the BSC for parasites
Parasitic organisms constitute a large proportion of
the cases problematical to the BSC. Many parasite taxa
exhibit extremely restricted cross fertilization. Such
restrictions may be due to extreme rates of clonal
reproduction, selfing or biparental inbreeding such as
sib-mating. Parthenogenesis is very well documented
in numerous families of nematodes parasitic on plants
and animals12. The large controversy concerning the
clonality of many microparasites illustrates clearly the
opposition between parasites and the BSC13–15. The
most spectacular examples of selfing lie within the
cestode group. Taenia solium, which is nearly always
found alone in the human intestine, can only selfreproduce16. In the Cyclorchida genus, because of anatomical constraints of the genitalia, self-fertilization is
the only possibility16. Sib-mating is also often encountered among parasites. For instance, in many hymenopteran parasitoid wasps, such as Nasonia vitripennis,
mating occurs only between brothers and sisters17.
Finally, many species undergo phases of asexual
reproduction and sib-mating. For example, in many
helminths the intermediate host is infected only by one
individual, which undergoes asexual multiplication.
The products of this asexual multiplication in the intermediate host are likely to mate together in the definitive host. Such a mating system, genetically synonymous with selfing, occurs in cestodes8 and trematodes18.
Applying the BSC to any of the previous examples
would lead us to consider each individual as a single
species and each egg hatching as a speciation event.
‘Too much’ sex, however, is also encountered in
parasites. The most well-known example concerns
the genus Schistosoma, where hybridizations have
been described between different species19,20. This is
also known to occur between Echinostoma species21.
Furthermore, bacteria can exchange DNA even between distant ‘species’22,23. Hybridization itself may
also lead to speciation through polyploidization in
parasites as, for example, in Paragoni-mus flukes24,
thus fully contradicting the BSC. This process is
probably largely overlooked in parasites and the few
examples available concern human parasites.
The biological species concept (BSC) which emphasizes
the role of reproductive isolation1 remains widely used
despite the fact that it cannot account satisfactorily for a
large number of biological examples2. Furthermore, because it focuses on the outcome and not the process, it
has been detrimental to studies on mechanisms of speciation3 and, in particular, it has served as a background
to the main arguments against the existence of sympatric speciation. Santa Rosalia was first mentioned by
Hutchinson4 to provide a functional explanation for the
origin and apportionment of animal species. Several
authors subsequently referred to him in order to discuss
the existence of non-allopatric modes of speciation5,6.
As mentioned previously by Lymbery7,8, for some
parasites the BSC has many limitations. Indeed, it focuses on reproductive isolation as the unique criterion to
delimit the species boundaries. Thus, the BSC confuses
one consequence and its cause: reproductive isolation
and the processes leading to it3. Given these limitations,
several alternatives to the BSC have been proposed2,3,8.
Many examples illustrate the inadequacy of the
BSC. Indeed, large parts of the living world lie outside the BSC’s logical domain, because they display
either ‘too little’ or ‘too much’ sex3. Obviously, the BSC
is applicable only to sexually reproducing organisms9.
Moreover, self-mating and sib-mating organisms and
any other closed system of mating cannot be accounted for satisfactorily by the BSC. In addition,
many species are able to hybridize with others without losing their ecological and genetic identities
through time3,10. Paradoxically, in some cases it is the
hybridization itself that leads to new species. Indeed,
many polyploid lineages are known to result from a
hybridization event between two different species11.
Sympatric speciation in parasites
All these examples illustrate the fact that the BSC
cannot be applied to a large number of parasite
species. These considerations are, arguably, only
semantic, requiring a solution only for the exceptions. However, BSC, by definition, brings problems
of another order: it may lead to the mechanisms
Thierry de Meeûs and François Renaud are at the Laboratoire
de Parasitologie Comparée, UMR 5555 CNRS, Université Montpellier
II, Place E. Bataillon, 34095 Montpellier Cedex 05, France. Yannis
Michalakis is at the Laboratoire d’Ecologie URA 258, Université
Paris 6 CC 237, 7 quai Saint Bernard, Bât. A, 75252 Paris Cedex 05,
France. Tel: +33 4 67 14 37 09, Fax: +33 4 67 14 46 46,
e-mail: [email protected]
10
* ‘The Garden of Earthly Delights’ refers to the triptych by Hieronymus
Bosch (c. 1500; Museo del Prado, Madrid) and, particularly, to its right panel
which exhibits an impressive collection of tormenting creatures that a biologist could recognize as the likely outcomes of recombination, hybridization
and mutation combined with diversification.
48
Copyright © 1998, Elsevier Science Ltd All rights reserved 0169–4758/98/$19.00 PII: S0169-4758(97)01163-0
Parasitology Today, vol. 14, no. 1, 1998
Reviews
responsible for reproductive isolation being overlooked3. Indeed, even if many sexually reproducing
species can be recognized through the BSC, one can
consider that the reproductive isolation they display
against other species originated from other processes,
independent of those that led to such an isolation.
Thus, any evidence of reproductive isolation between
two closely related species provides no information on
the processes responsible for such an outcome. The
real problem here is less to testify the existence of
reproductive isolation than to understand the underlying mechanisms. When speciation is allopatric, reproductive isolation is coincidental: while the different gene
pools are allopatric, selection will not act in favour of
isolating mechanisms. Characters diverge between gene
pools either by chance, or to adapt to different environments or genomic composition. Reproductive isolation
on secondary contact may arise only coincidentally to
this divergence. Selection for such isolating mechanisms
comes into action only after secondary contact, ie. when
different genetic entities are sympatric.
Under the BSC, the factors responsible for reproductive isolation in general play no direct role in
species divergence3; therefore, all theoretical attempts
using the BSC as a basis have failed to describe sympatric speciation as a probable event5,25. Indeed, the
evolution of reproductive isolation per se is unlikely
because it will behave as a deleterious character when
rare, ie. in any case at the initial stage of the process.
Alternatively, sympatric speciation may occur without the need to invoke reproductive isolation, through
adaptive polymorphism and habitat preference26. As
a recent study shows27, the result of these mechanisms
may be reinforced by any non-habitat-associated
assortative mating. This process has been supported
by some experimental work28 but the most convincing
evidence is provided by the natural example of the
phytophagous insect Rhagoletis pomonella29 – a parasite.
Because parasites provide particular situations,
Box 1 illustrates the difference between true allopatric
and true sympatric situations found in host–parasite
systems. Allopatric speciation alone can hardly account for the diversity of unambiguous species of
related parasites often encountered in a single host
(Fig. 1). Considering the parasitological literature this
situation is far from marginal. Among the platyhelminths, the monogeneans and cestoda provide
the most striking examples. In the Tchad Basin (West
Africa) the characid fish Alestes nurse is known to
harbour on its gills eight monogenean species of the
Anulotrema genus, each of which displays specific
genitalia (Fig. 1). These parasites, as well as their host,
live only in this area so that their divergence and
speciation probably occurred in sympatry. In the
Mediterranean, the gills of the fish Liza saliens
(Mugilidae) are parasitized by four species of Ligophorus. In both cases, different parasite species are
distributed non-randomly on different parts of the
gills (Fig. 1). Niche differentiation and specialization
most likely led to speciation of these parasites on the
same host species in a single geographical area. Among
the Cestoda, four species of Acanthobothrium are described in the spiral valve of the stingray Dasyatus
longus from the Gulf of Nicoya (Costa Rica)30.
Other examples can be found among terrestrial
arthropods (lice). The bird Ibis falcinellus is parasitized
Box 1. Concepts of Allopatry and Sympatry in
Parasitic Organisms
Different entities will be allopatric only if isolated geographically. Individuals belonging to allopatric groups
cannot interact. This is the case when different parasite
species live on different host species in areas where hosts
are separated by physical barriers (a; solid lines), or in
areas where vicariant host species replace one another
without any obvious physical barriers (b). On the contrary, when encountered in the same geographical areas,
such entities will be considered sympatric, even if exploiting different resources. Indeed, in such co-existing
groups, individuals may still interact during their life
cycle. For example, all helminths parasitizing the vertebrates living in a pond are sympatric, because of all the
existing ecological interconnections between the hosts
and their parasites (c). More spectacular sympatric cases
arise when parasites specialize on different organs of the
same host species (d). G, geographical areas; H, host
species (triangles), partitioned into different organs (internal triangles); closed circles represent parasites.
by at least seven species of mallophagous insects,
each of which is specialized on a single feather type31.
Less spectacular in diversity, but necessarily recent, is
the case of the three species of human lice32.
Furthermore, the most relevant evidence of ongoing sympatric divergences comes from the parasitological literature. In the Caribbean, the acquisition of
a murine host by the human parasite Schistosoma
mansoni leads to an adaptive divergence depending on
the periodic behaviour of the host towards water33.
The sea louse Lepeophtheirus europaensis also displays
a sympatric divergence between the two flatfishes it
parasitizes in the Mediterranean (brill and flounder) –
a supposedly recent phenomenon34. However, the
better-documented studies come from insect parasites
of plants35–38. Among these, Rhagoletis pomonella represents a well-studied model29,39.
When one considers the realm of microparasites,
reproductive isolation appears irrelevant as a mechanism for discriminating species. The tremendous
diversity observed in groups such as the yeast Candida
49
11
Reviews
factor is supported by comparative
analyses of herbivorous insects. Phytophagy is encountered in only nine
of the 13 orders of insects44, but
these orders account for approximately half of all insect species.
Furthermore, phytophagous taxonomic groups are significantly more
speciose than homologous groups
of the same evolutionary age with
a non-parasitic feeding habit44. A
possible explanation for this diversifying role of parasitism may
lie in the fact that sympatric speciation is much more likely in
parasitic species. Indeed, as stated
previously, hosts provide ample
opportunities for niche diversification among parasite populations,
a necessary condition for sympatric speciation. Thus, sympatric
speciation may play a much more
central role in parasite evolution
and evolutionary biology as a whole,
with parasites representing ideal
biological models for the study
of ecological specialization and
speciation mechanisms.
In the face of this acute potential
Fig. 1. Two relevant examples of multiple monogenean congeners found in one host
for diversification, hosts have
species and for which allopatric speciation alone cannot explain the observed diverfailed to eliminate all their parasity16. Morphology of male and female genitalia of eight species of Annulotrema
sites. For instance, even though
observed on Alestes nurse in Tchad (a). Morphology of genitalia and hamuli haptors of
the four species of Ligophorus parasitizing the Teleost Liza saliens in the Meditermankind has managed to elimiranean (b). (Reproduced, with permission, from Ref. 16.)
nate (almost) all of its competitors
and predators, current knowledge
indicates that it has been unable to
albicans16 suggests other modes of speciation instead
eliminate any of its parasites (smallpox being the
of the classical allopatric model.
exception that proves the rule). This is illustrated by
modern prophylactic campaigns against malaria that
Does the parasitic way of life favour phylogenic
are followed by the emergence of more and more
diversification?
Plasmodium strains resistant to nivaquine. As previParasitism represents the conquest of life by life.
ously underlined45, this genetic variability is crucial
The living environment evolves continuously. Thus,
in both therapy and susceptibility to immune attack.
in order to persist in their living environments paraThere is a need to obtain the most precise knowledge
sites must continuously adapt to their hosts. Hosts
of parasite diversity before developing therapeutics
represent a major part of the ecological needs of their
or vaccines. In the same way, the identification of the
parasites (habitat, resource, etc.)40. Hosts may repreexisting diversity of parasitic organisms must be
sent many different kinds of resources and habitats
taken into account in epidemiological surveys. This
(communities, species, populations, cohorts, sexes,
may allow us to discriminate more effectively, within
individuals, organs, cells and molecules). Furtherparasite communities, those that are pathogenic and
more, hosts develop defences against such intruders,
those that are not. This can be illustrated by the genby behavioural, physiological and demographic means.
etic divergences found between strains of C. albicans,
Such defences impose an additional source of selecwhich are comparable to that existing between the
tive and diversifying pressures on parasites. Such condifferent mammalian species of the same genus16.
tinuous mutual aggressions resulting from the neverMoreover, genetic distances between C. albicans samending modifications of the living environment have
pled in one human host46 exceeded that seen between
largely shaped the life history traits and the evolugreat apes and humans47, which diverged 5–7 million
tionary pathways in host–parasite systems (Red
years ago48. In addition, when compared with the
Queen concept)41.
protozoan species Trypanosoma cruzi, for example, the
The potential number of diversifying factors is
overall genetic variability of the species C. albicans is at
much larger for parasitic organisms than for freeleast four times lower (M. Tibayrenc, pers. commun.).
living organisms. All living species are involved in
parasitism, either as parasites or as hosts42 and, as
Concluding remarks: many or no species concepts?
suggested by Timm and Clauson43, parasites constiProviding a general and satisfactory species definitute the main part of the known species diversity.
tion appears to be a very difficult task, especially
That the parasitic way of life might be a diversifying
given the very large number of potential applications
12
50
Reviews
or ‘clonal’ populations? Parasitol. Today 7, 232–235
15 Pujol, C. et al. (1993) The yeast Candida albicans has a clonal
mode of reproduction in a population of infected human
immunodeficiency virus-positive patients. Proc. Natl. Acad. Sci.
U. S. A. 90, 9456–9459
16 Euzet, L. and Combes, C. (1980) in Les Problèmes de l’Espèce dans
le Règne Animal (Vol. 3), Mem. Soc. Zool. 40, 238–285
17 Werren, J.H. (1980) Sex ratio adaptations to local mate competition in a parasitic wasp. Science 208, 1157–1159
18 Combes, C. (1988) in L’Adaptation, Pour La Science, pp 166–173, Belin
19 Brémond, P. et al. (1993) Argument en faveur d’une modification du génome (introgression) du parasite humain
Schistosoma haematobium par les gènes de S. bovis, au Niger.
C. R. Acad. Sci. Life Sci. 316, 667–670
20 Tchuem Tchuente, L.A. et al. (1993) Choice of mate, a reproductive isolating mechanism between Schistosoma intercalatum
and S. mansoni in mixed infections. Int. J. Parasitol. 23, 179–185
21 Voltz, A. et al. (1988) Isoenzyme analysis of Echinostoma liei:
Comparison and hybridization with other African species.
Exp. Parasitol. 66, 13–17
22 Maynard-Smith, J. et al. (1991) Localised sex in bacteria. Nature
349, 29–31
23 Heinemann, J.A. (1991) Genetics of gene transfer between
species. Trends Genet. 7, 181–185
24 Agatsuma, T. et al. (1992) Electrophoretic evidence of a hybrid
origin for tetraploid Paragonimus westermani discovered in
north-eastern China. Parasitol. Res. 78, 537–538
25 Fialkowski, K.R. (1988) Lottery of sympatric speciation. A computer model. J. Theor. Biol. 130, 379–390
26 De Meeûs, T. et al. (1993) Polymorphism in heterogeneous
environments, habitat selection and sympatric speciation: soft
and hard selection models. Evol. Ecol. 7, 175–198
27 Johnson, P.A. et al. (1996) Conditions for sympatric speciation
– a diploid model incorporating habitat fidelity and nonhabitat assortative mating. Evol. Ecol. 10, 187–205
28 Rice, W.R. and Salt, G.W. (1988) Speciation via disruptive
selection: experimental evidence. Evolution 131, 911–917
29 Bush, G. L. (1992) Host race formation and sympatric speciation
in Rhagoletis fruit flies (Diptera: Tephrtidae). Psyche 99, 335–357
30 Marques, F. et al. (1995) Five new species of Acanthobothrium
van Beneden, 1849 (Eucestoda: Tetraphyllidea: Onchobothriidae) in stingrays from the gulf of Nicoya, Costa Rica. J. Parasitol.
81, 942–951
31 Dogiel, V.A. (1964) General Parasitology, Oliver and Boyd
32 Ludwig, H.W. (1982) Host specificity in anoplura and coevolution of anoplura and mammalia. Mem. Mus. Natn. Hist. Nat.
Paris 123, 145–152
33 Théron, A. and Combes, C. (1995) Asynchrony of infection timing, habitat preference, and sympatric speciation of schistosome parasites. Evolution 49, 372–375
34 De Meeûs, T. et al. (1995) Maintenance of two genetic entities
by habitat selection. Evol. Ecol. 9, 131–138
35 Wood, T.K. and Guttman, S.I. (1983) Euchenopa binotata complex: sympatric speciation? Science 220, 310–312
36 Craig, T.P. et al. (1993) Behavioural evidence for host-race formation in Eurosta solidaginis. Evolution 47, 1696–1710
37 Ronquist, F. (1994) Evolution of parasitism among closely related
species: phylogenetic relationships and the origin of inquilinism
in gall wasps (Hymenoptera, Cypinidae). Evolution 48, 241–266
38 Emelianov, I. et al. (1995) Genetic differentiation in Zeiraphera
diniana (Lepidoptera: Tortricidae, the larch budmoth): polymorphism, host races or sibling species? Heredity 75, 416–424
39 Berlocher, S.H. and McPherson, B.A. (1996) Population structure
of Rhagoletis pomonella, the apple maggot fly. Heredity 77, 83–99
40 Renaud, F. et al. (1996) Biodiversity and evolution in host–
parasite associations. Biodiv. Conserv. 5, 963–974
41 Van Valen, L. (1973) A new evolutionary law. Evol. Theor. 1, 1–30
42 Barbault, R. (1988) Population biology and evolutionary ecology in France: current state prospects. J. Evol. Biol. 1, 211–231
43 Timm, R.M. and Clauson, B.L. (1987) in Coevolution, pp 212–214,
McGraw–Hill
44 Mitter, C. et al. (1988) The phylogenetic study of adaptive
zones – has phytophagy promoted insect diversification? Am.
Nat. 132, 107–128
45 Cox, F.E.G. (1991) Variation and vaccination. Nature 349, 193
46 Reynes, J. et al. (1996) Simultaneous carriage of Candida albicans strains from HIV-infected patients with oral candidiasis:
multilocus enzyme electrophoresis analysis. FEMS Microbiol.
Lett. 137, 269–273
47 Bruce, E.J. and Ayala, F.J. (1979) Phylogenetic relationships
between man and the apes: electrophoretic evidence. Evolution
33, 1040–1056
48 Ridley, M. (1996) Evolution (2nd edn), Blackwell Science
with different functional requirements (taxonomy,
conservation biology, functional ecology, evolutionary biology and medicine). In fact, we do not believe
that it is possible to reach a species definition that will
satisfy everybody. In this paper, our aim is not to provide a new species definition because we feel the
extant ones (typological, BSC, etc.) will continue to
work in their different domains of application. Our
goal is to draw attention to the fact that the most currently used concept (the BSC) might not be very helpful in parasitology, because of the reasons outlined
above, and that it may prevent researchers from considering several evolutionary processes. The strong
potential for diversification displayed by parasites,
possibly due to the larger opportunities for sympatric
speciation in such groups, should allow parasitologists to play a major role in different fields of biology.
In evolutionary biology, parasites appear as ideal
models for the study of specialization and speciation
and much can be learned from them. In phylogenetic
studies the genetic consequences of such potential for
diversification should allow different hypotheses, such
as the molecular clock, to be tested, in particular in
groups where such a diversification is evident (eg.
monogeneans and bird lice). Too few such studies are
available at the present time. Parasite communities
should provide very useful models for studying the
interaction between species, competition and exclusion and biological diversity maintenance, because
the ecological niche of a parasite will often be easier
to define (as it is concentrated in the host). In medicine, the mechanisms involved in parasite diversification (in the wide sense) should allow a better understanding of eradication failures. Also, it should be
considered more often that what appears to be a single pathogenic entity might actually comprise several
very different genetic entities. As mentioned previously, the tremendous levels of genetic diversity found
within C. albicans and T. cruzi reveal that these taxa
are complex and surely made up of different biological entities (species). Because they co-exist, these different biological entities might have different ecological niches (ie. needs) and thus different sensitivities to
one or another treatment.
References
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2 Mallet, J. (1995) A species definition for the modern synthesis.
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11 Futuyma, D.J. (1986) Evolutionary Biology (2nd edn), Sinauer
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51
13
52
53
Update
aspects of avian sex chromosome evolution that are
inevitable from those that are due strictly to chance.
Additionally, even though the palaeognathous sex
chromosomes are as old as those of the Neognathae, something has slowed the process of sex chromosome evolution
in the group. This presents a living series of slow-motion
time-shots in the progression of avian sex chromosomes,
from the largely undifferentiated ostrich and emu Z and W,
to the distinguishably different intermediate tinamou Z
and W, to the terminal neognathous sex chromosomes that
only recombine in a small and highly constrained pseudoautosomal region (Figure 1). These characteristics offer a
powerful clade for the study of sex chromosome evolution,
which future sequence, linkage and cytogenetic analysis
can exploit.
Acknowledgements
We thank the Wenner-Gren Foundation and the Swedish Research
Council for support, as well as two anonymous reviewers for helpful
suggestions.
References
1 Bachtrog, D. (2006) A dynamic view of sex chromosome evolution. Curr.
Opin. Genet. Dev. 16, 578–585
2 Ezaz, T. et al. (2006) Relationships between vertebrate ZW and XY sex
chromosome systems. Curr. Biol. 16, R736–R743
3 Ellegren, H. (2000) Evolution of the avian sex chromosomes and their
role in sex determination. Trends Ecol. Evol. 15, 188–192
4 Fridolfsson, A.K. et al. (1998) Evolution of the avian sex chromosomes
from an ancestral pair of autosomes. Proc. Natl. Acad. Sci. U. S. A. 95,
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clocks. Mol. Biol. Evol. 18, 206–213
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10 Tsuda, Y. et al. (2007) Comparison of the Z and W sex chromosomal
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0169-5347/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tree.2007.05.003
Letters
Without morphology, cryptic species stay in
taxonomic crypsis following discovery
Birgit C. Schlick-Steiner1,2,3, Bernhard Seifert4, Christian Stauffer2, Erhard Christian1,
Ross H. Crozier3 and Florian M. Steiner1,2,3
1
Institute of Zoology, Department of Integrative Biology and Biodiversity Research, Boku, University of Natural Resources and
Applied Life Sciences Vienna, Gregor Mendel Str. 33, A-1180 Vienna, Austria
2
Institute of Forest Entomology, Forest Pathology and Forest Protection, Department of Forest and Soil Sciences, Boku, University
of Natural Resources and Applied Life Sciences Vienna, Hasenauerstr. 38, A-1190 Vienna, Austria
3
School of Marine and Tropical Biology, James Cook University, DB23, Townsville, Queensland 4811, Australia
4
State Museum of Natural History Görlitz, Post Box 300154, D-02806 Görlitz, Germany
Recently, Bickford et al. [1] highlighted the importance of
exploring cryptic diversity. Their biology-focused contribution is a reminder of the original questions regarding the
current debate between molecular and traditional taxonomy [2], and a call for synergies between these approaches.
Only an integration of all disciplines can promote biological
research at the tempo set by the biodiversity crisis [3,4].
But one point is left unemphasized: the undiminished
relevance of morphology-based alpha taxonomy (MOBAT),
which is still the most important discipline for assigning
Corresponding author: Schlick-Steiner, B.C. ([email protected]).
Available online 15 June 2007.
www.sciencedirect.com
taxonomically valid names on the basis of name-bearing
specimens (types). Types often date back to Linnaeus’ time
and are frequently unsuitable for molecular studies,
despite progress in this field [5], even setting aside that
museum curators usually refuse molecular sampling of
fragile type specimens. MOBAT can link cryptic species
to Linnean nomenclature and to established biological
knowledge. Once discovered, many cryptic species can be
identified by means of external physical characters [6],
especially with methods of morphometric statistics [7].
Badly under-resourced [8], MOBAT cannot keep pace
with the discovery of cryptic species, as illustrated by a
54
Update
392
TRENDS in Ecology and Evolution Vol.22 No.8
topical example. An integrative approach revealed at least
seven sympatric species hidden in two nominal species of
western Palearctic Tetramorium ants [9]. Because most of
these species are both common and widespread, it is risky to
guess which were used for types by previous taxonomists;
approximately 50 taxon names in synonymy, and their types
(the oldest from 1850), demand scrutiny [10]. More than 500
publications over 150 years contain information on life
history, ethology, social biology, semiochemistry, ecology
and invasion biology of these ant species. But of which
ant species? Biological knowledge that would help elucidate
patterns and consequences of cryptic diversification [1] lies
idle. Only analysing historical voucher material could tap
these resources. However, the current working capacity of
ant MOBAT is slight. Just two of >200 European myrmecologists work in numerical MOBAT as full-time professionals. We guess that the situation is similar with
other groups of organisms. While the discovery of cryptic
species increases exponentially [1], the number of experienced MOBATists stagnates.
Even when uncovered by modern methods, many cryptic
species remain taxonomically cryptic. Investment in all
disciplines contributing to integrative taxonomy, including
MOBAT, is essential if the promise of ‘profound implica-
tions for evolutionary theory, biogeography and conservation planning’ [1] is to be realised.
References
1 Bickford, D. et al. (2007) Cryptic species as a window on diversity and
conservation. Trends Ecol. Evol. 22, 148–155
2 Smith, V.S. (2005) DNA barcoding: perspectives from a ‘Partnerships for
Enhancing Expertise in Taxonomy’ (PEET) debate. Syst. Biol. 54, 841–
844
3 Will, K.W. et al. (2005) The perils of DNA barcoding and the need for
integrative taxonomy. Syst. Biol. 54, 844–851
4 Whitfield, J. (2007) We are family. Nature 446, 247–249
5 Hajibabaei, M. et al. (2006) A minimalist barcode can identify a
specimen whose DNA is degraded. Mol. Ecol. Notes 6, 959–964
6 Saez, A.G. and Lozano, E. (2005) Body doubles. Nature 433, 111
7 Seifert, B. (2002) How to distinguish most similar insect species –
improving the stereomicroscopic and mathematical evaluation of
external characters by example of ants. J. Appl. Entomol. 126, 1–9
8 Wheeler, Q.D. et al. (2004) Taxonomy: impediment or expedient? Science
303, 285
9 Schlick-Steiner, B.C. et al. (2006) A multidisciplinary approach
reveals cryptic diversity in western Palaearctic Tetramorium ants
(Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 40, 259–273
10 Bolton, B. et al. (2007) Bolton’s catalogue of ants of the world: 1758–
2005. Harvard University Press
0169-5347/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tree.2007.05.004
Book Review
Laws on growth and heat
In the Beat of a Heart: Life, Energy and the Unity of Nature by John Whitfield. Joseph Henry Press, 2006. US$ 27.95 hbk (270 pages)
ISBN 0309096812
Jaap van der Meer
Department of Marine Ecology and Evolution, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg
(Texel), the Netherlands
Organisms as diverse as yeast and moose
show striking similarities in their growth
trajectories, initially growing quickly, but
then gradually slowing their growth as
they get larger, eventually stopping altogether. They also follow Kleiber’s rule; that
is, their metabolic rate is proportional to
their mass raised to the 3/ 4 power. Many
scholars have tried to find laws valid for
all life forms that could explain these two
regularities, but none have yet convinced the scientific
community as a whole. By the end of the previous century,
the subject was receiving little if any attention; however,
work by the physicist Geoffrey West and ecologists Jim
Brown and Brian Enquist has since revitalized the topic
[1,2]. John Whitfield, an evolutionary biologist turned
science writer, has followed their work and, following a
popular paper [3], his debut science book In the Beat of a
Heart explores the quest for general laws on metabolism
and growth.
Corresponding author: van der Meer, J. ([email protected]).
Available online 9 May 2007.
www.sciencedirect.com
55
Beginning with an historical account, d’Arcy Thompson
is introduced as the godfather of mathematical thinking in
biology. In a letter to a former student Thompson writes
that, to understand growth patterns in foraminifera, ‘I
have taken to Mathematics . . .’. This quote is the leitmotiv
of Whitfield’s book, culminating in a modern version in
which Brown and Enquist did not literary ‘take Mathematics’, but joined forces with West. However, before these
contemporaries are discussed, their predecessors in the
quest are presented. Max Rubner, Max Kleiber and Ludwig von Bertalanffy feature, among many others.
Such mix of an historical sketch and a description of the
lives and work of present-day scientists who have only
recently launched ideas that are still debated, is, for
various reasons, a risky exercise. I found it amusing to
read that 18 years after signing a contract on a second
edition of On Growth and Form, Thompson received a
letter from his publisher with the remark ‘I must warn
you that you have already slightly exceeded the correction
allowance . . .’. I find it less diverting to hear that my
contemporaries always buy lots of beer when they go on
a field trip or that they are ‘foaming at the mouth of
excitement’ when they discuss their own ideas. But this
Lecturas traducidas. Laboratorio de Evolución, Facultad de Ciencias ______________________________________ 1
El significado de especie y de especiación:
una perspectiva genética.
Alan R. Templeton.
INTRODUCCIÓN
¿Qué es una especie? Esta cuestión fundamental debe ser respondida antes de que el
proceso de formación de las especies pueda ser investigado. Como cualquier vistazo general
a la literatura evolutiva rápidamente revelará, existen muchas definiciones de especie. Estas
diferentes definiciones reflejan los diversos tipos de preguntas evolutivas y/o de organismos
con los cuales sus autores estaban principalmente interesados. En consecuencia, un concepto
de especie sólo puede ser evaluado en términos de una meta o propósito particular. Mi meta
es entender la especiación como un proceso genético evolutivo. Una asunción fundamental
tras esta meta es que para la especiación, independientemente de una definición precisa de
especie, lo mejor es una aproximación mecanística examinando las fuerzas evolutivas que
operan sobre los individuos dentro de poblaciones o subpoblaciones y siguiendo sus efectos
hacia arriba hasta que en último término causen que todos los miembros de esa población o
subpoblación adquieran atributos fenotípicos que le confieran al grupo el status de especie.
Este énfasis en los mecanismos evolutivos genéticos que operan dentro de las
poblaciones de individuos ubica completamente a la especiación dentro del dominio de la
genética de poblaciones. De acuerdo con esto, lo que se requiere es un concepto de especie
que pueda ser relacionado directamente con el marco mecanístico de la genética de
poblaciones. Para alcanzar esta meta, repasaré en primer lugar tres conceptos de especie que
poseen fuertes partidarios en la literatura actual: el concepto evolutivo de especie, el
concepto biológico de especie, y el concepto de especie de reconocimiento. Todos estos
conceptos de especie consideran a las especies como entidades biológicas reales e intentan
definir a las especies en términos de alguna propiedad biológica fundamental. En este
aspecto, todas estas definiciones son conceptos biológicos de especie, aunque una de ellas es
referida usualmente como ‘el concepto biológico de especie’. Dado que ‘el concepto
biológico de especie’ define a las especies en términos de mecanismos de aislamiento, es
mejor conocida como el concepto de aislamiento (Patterson, 1985). La terminología de
Patterson será utilizada en el resto de este capítulo.
Luego de revisar los puntos fuertes y los débiles de estos tres conceptos, propondré
un cuarto concepto biológico de especie, el concepto de cohesión, el cual intenta utilizar los
puntos fuertes de los otros tres mientras evita sus puntos débiles con respecto a la meta de
definir las especies de una forma que sea compatible con el marco mecanístico de la
genética de poblaciones. De esta manera, puede lograrse una definición de especie que
ilumine, en vez de oscurecer o desencaminar, a los mecanismos de especiación y a sus
consecuencias genéticas.
TRES CONCEPTOS BIOLÓGICOS DE ESPECIE
El concepto evolutivo de especie.
Bajo esta definición, una especie consiste en una población o grupo de poblaciones
que comparten un destino evolutivo común a través del tiempo. Esta definición tiene la
ventaja de ser aplicable tanto a grupos vivientes como a grupos extintos y a organismos
sexuados y asexuados. Además, pone énfasis en el hecho de que una unidad de especie
puede mantenerse unida no sólo a través del flujo génico sino también a través de
restricciones del desarrollo, genéticas y ecológicas. Finalmente, este concepto es útil debido
Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
56
a que se asemeja a la definición operacional de especie utilizada por la mayoría de los
taxónomos y paleontólogos en ejercicio. Las decisiones de dar status de especie se toman
usualmente en base a patrones de cohesión fenotípica dentro de un grupo de organismos
versus la discontinuidad fenotípica entre los grupos. Sin embargo, cuando se estudia una
variedad de fenotipos, a menudo se descubre que los patrones de cohesión/discontinuidad
varían en función del fenotipo que se mida. Una falla del concepto evolutivo de especie es
que provee poca o ninguna guía acerca de cuáles son los rasgos más importantes en la
definición de las especies.
Existen otras dos dificultades principales con este concepto. En primer lugar, está el
problema de juzgar qué constituye un destino evolutivo ‘común’. Obviamente, los
polimorfismos pueden existir incluso dentro de las poblaciones locales, y muchas especies
son politípicas. Debido a esto, destino evolutivo ‘común’ no significa ‘idéntico’, por lo cual
debe hacerse algún juicio acerca de cuánta diversidad se permite dentro de un destino
evolutivo ‘común’. Finalmente, y lo más importante en relación a la meta de este capítulo, el
concepto evolutivo de especie no es una definición mecanística. Trata sólo con la
manifestación de la cohesión en vez de con los mecanismos evolutivos responsables de tal
cohesión. Por lo tanto, no provee un marco adecuado para la integración de factores de la
genética de poblaciones dentro del concepto de especie.
El concepto de especie de aislamiento.
El concepto de especie dominante en gran parte de la literatura evolutiva es conocido
popularmente como el concepto biológico de especie. Mayr (1963) definió el concepto de
especie de aislamiento como ‘grupos de poblaciones naturales actual o potencialmente
capaces de entrecruzamiento que se encuentran aisladas reproductivamente de otros grupos
similares.’ De forma similar, Dobzhansky (1970) afirmó que ‘Las especies son sistemas de
poblaciones: el intercambio genético entre estos sistemas se encuentra limitado o impedido
por un mecanismo de aislamiento reproductivo o quizás por una combinación de varios de
estos mecanismos.’ Como White (1978) ha subrayado, el concepto de aislamiento de especie
‘es al mismo tiempo una comunidad reproductiva, un pool de genes, y un sistema genético.’
Son estos dos últimos atributos los que hacen a este concepto de especie particularmente útil
para la integración de consideraciones de la genética de poblaciones en el problema del
origen de las especies. La genética de poblaciones se ocupa de las fuerzas evolutivas que
operan en los pools de genes y de los tipos de sistemas genéticos que surgen luego de que
operen estas fuerzas. El concepto de aislamiento de especie es por tanto potencialmente útil
en el análisis de la especiación desde la perspectiva de la genética poblacional, pero
desafortunadamente posee algunas serias dificultades que deben ser rectificadas antes de que
este potencial pueda ser comprendido.
Estas dificultades surgen del hecho de que este concepto de especie se define en
términos de mecanismos de aislamiento. La Tabla 1 presenta una breve clasificación de los
tipos de barreras de aislamiento, y tablas similares pueden encontrarse en cualquier libro
sobre especiación de Mayr o Dobzhansky. Bajo el concepto de especie de aislamiento, estas
barreras de aislamiento definen las fronteras de la comunidad reproductiva y del pool de
genes y preservan la integridad del sistema genético de la especie.
TABLA 1. Clasificación de los mecanismos de aislamiento.
1. Mecanismos precopulatorios que impiden los cruzamientos interpoblacionales
a. Aislamiento ecológico o de hábitat: las poblaciones se aparean en distintos hábitats en
la misma región
general, o utilizan distintos agentes polinizadores, etc.
b. Aislamiento temporal: las poblaciones se aparean en distintos momentos del año.
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c. Aislamiento etológico: parejas potenciales de distintas poblaciones se encuentran pero
no se aparean.
2. Aislamiento postcopulatorio pero precigótico
a. Aislamiento mecánico: ocurren apareamientos interpoblacionales pero no tiene lugar
la transferencia de
esperma.
b. Mortalidad gamética o incompatibilidad: ocurre transferencia de esperma pero el
óvulo no es
fertilizado.
3. Aislamiento postcigótico
a. Inviabilidad de la F1: los cigotos híbridos poseen viabilidad reducida.
b. Esterilidad de la F1: los adultos híbridos poseen fertilidad reducida.
c. Decaimiento de los híbridos: los híbridos de la F2 o de los retrocruzamientos poseen
viabilidad
o fertilidad reducida.
d. Interacciones coevolutivas o citoplasmáticas: los individuos de una población infectada
por un endoparásito o con un elemento citoplasmático particular son fértiles entre ellos pero
la viabilidad y/o la fertilidad decaen cuando los apareamientos ocurren entre individuos
infectados y no infectados.
Paterson (1985) ha señalado que una dificultad fundamental con el concepto de
especie de aislamiento es que conduce a error cuando se piensa en el proceso de especiación.
Por ejemplo, bajo el clásico modelo alopátrido de especiación, la especiación ocurre cuando
las poblaciones se encuentran totalmente separadas una de la otra por barreras geográficas.
Los mecanismos de aislamiento intrínsecos dados en la Tabla 1 son obviamente irrelevantes
como barreras de aislamiento durante la especiación debido a que en alopatría no pueden
funcionar como mecanismos de aislamiento. Por tanto, las fuerzas evolutivas responsables
de este proceso de especiación alopátrida no tienen nada que ver con el ‘aislamiento’. Esto
también se aplica a otros mecanismos de especiación (Templeton, 1981). Esto no significa
que el aislamiento no sea un producto del proceso de especiación en algunos casos, pero el
producto (i.e., el aislamiento) no debe ser confundido con el proceso (i.e., la especiación). El
concepto de aislamiento a sido perjudicial en los estudios de especiación precisamente
porque ha fomentado esta confusión (Paterson, 1985).
El concepto de especie de reconocimiento.
Paterson (1985) ha argumentado fuertemente que esta confusión puede ser evitada
viendo a los así llamados mecanismos de aislamiento desde otra perspectiva. Por ejemplo,
considérense los mecanismos de aislamiento precopulatorios listados en la Tabla 1. En la
literatura evolutiva es común hallar afirmaciones de que complejos rituales de cortejo,
señales para el apareamiento, etc. funcionan como barreras de aislamiento precopulatorias
que existen para impedir la hibridación con otras especies. Los trabajos de Dobzhansky
(1970) indican cuán dominante era esta idea en el pensamiento de uno de los principales
arquitectos y proponentes del concepto biológico de especie. No obstante, como Tinbergen
(1953) señaló, tales mecanismos precopulatorios tienen varias funciones además del
aislamiento: la supresión o escape del comportamiento agresivo en el animal cortejado, la
sincronización de las actividades del apareamiento, la persuasión de la pareja potencial para
continuar con el cortejo, la coordinación en el tiempo y en el espacio del patrón de
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apareamiento, la orientación de parejas potenciales para la cópula, y, finalmente, la propia
fecundación. La importancia de estas otras funciones del comportamiento precopulatorio es
ilustrada por el trabajo de Crews (1983) acerca del cortejo pseudomasculino y el
comportamiento copulatorio del lagarto partenogenético sin machos, Cnemidophorus
uniparens. En estos lagartos, la inseminación y el aislamiento precopulatorio son totalmente
irrelevantes ya que la reproducción es estrictamente partenogenética. Aún así, las hembras
muestran elaborados comportamientos de cortejo que se asemejan al cortejo de los machos
de especies cercanamente emparentadas. Estos comportamientos sirven como iniciador
neuroendócrino que coordina los eventos reproductivos. Obviamente, las conductas de
apareamiento facilitan la reproducción en estos lagartos, pero el aislamiento es irrelevante.
La pregunta crítica se convierte entonces en ¿cuál de éstas varias funciones (o cuál
combinación) es importante en el proceso de especiación? Paterson (1985) ha argumentado
que el aislamiento es una función irrelevante en el proceso de especiación. En consecuencia,
para examinar la razón de porqué surge una barrera ‘de aislamiento’ precopulatoria, es
necesario focalizar la atención en las otras funciones de estos mecanismos precopulatorios y
examinar las fuerzas evolutivas que operan sobre estas funciones (Paterson, 1985). Desde
este punto de vista, todas las otras funciones de estos comportamientos precopulatorios
pueden entenderse como facilitando la reproducción, no obstaculizándola como sucedía con
la función del aislamiento. La función del aislamiento puede surgir de hecho como un efecto
secundario de la evolución de las otras funciones, pero en general no es una parte activa del
proceso de especiación.
En consecuencia, los mecanismos de aislamiento constituyen una forma de pensar
acerca del proceso de especiación que conduce a error. Aunque todos los mecanismos
listados en la Tabla 1 se definen en términos de impedir la reproducción entre las
poblaciones, pueden también ser pensados de un modo intraespecífico como facilitando la
reproducción dentro de las poblaciones. En general, es esta inversión positiva de las
funciones dadas en la Tabla 1 la que juega el rol principal en la especiación. Paterson (1985)
se centró en la función positiva de estos mecanismos en la facilitación de la reproducción
entre los miembros de una cierta población. De acuerdo con esto, Paterson acepta la
premisa, compartida con el concepto de aislamiento, de que una especie es un campo para la
recombinación génica. A diferencia del concepto de aislamiento, el cual define los límites de
este campo en un sentido negativo a través de mecanismos de aislamiento, Paterson define
los límites de este campo en un sentido positivo a través de mecanismos de fertilización, es
decir, adaptaciones que contribuyen en los procesos de meiosis y fecundación. Las especies
se definen como la población más inclusiva de organismos biparentales individuales que
comparten un sistema de fertilización común.
En cierto sentido, los conceptos de especie de aislamiento y de reconocimiento son
las dos caras de una misma moneda. Dar vuelta la moneda es provechoso porque el concepto
de reconocimiento da una visión más clara de los procesos versus el patrón evolutivos,
mientras que el concepto de aislamiento conduce activamente a un error. Por tanto, dada la
meta de definir la especie de tal manera que facilite el estudio de la especiación como
proceso evolutivo, el concepto de reconocimiento es claramente superior al de aislamiento.
Paterson (1985) ha cargado al concepto de reconocimiento con varias restricciones
que no provienen necesariamente de su definición primaria. La más seria de éstas es el uso
exclusivo de los mecanismos de fertilización para definir una especie. Obviamente, un
campo de recombinación génica requiere más que la fertilización; requiere un ciclo de vida
completo en el cual los productos de la fertilización sean viables y fértiles. Además, los así
llamados mecanismos ‘de fertilización’ de Paterson poseen otras funciones evolutivas que él
ignora, como está bien ilustrado por el comportamiento de cortejo previamente discutido de
los lagartos partenogenéticos. Por tanto, así como Paterson criticó a los mecanismos de
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aislamiento porque éstos podían evolucionar por razones distintas al aislamiento, sus
mecanismos ‘de fertilización’ de igual forma pueden evolucionar por razones distintas a la
fertilización.
Puede hacerse otra crítica menor al concepto de Paterson (Templeton, 1987), pero
deseo concentrarme en dos dificultades serias y fundamentales que comparten ambos
conceptos, el de aislamiento y el de reconocimiento. Como muchos otros problemas en el
mundo biológico, estos problemas son causados por el sexo -o demasiado, o demasiado
poco.
RESTRICCIONES SEXUALES DE LOS CONCEPTOS DE AISLAMIENTO Y DE
RECONOCIMIENTO.
Demasiado poco sexo.
Tanto el concepto de especie de aislamiento como el de reconocimiento sólo se
aplican a organismos que se reproducen sexualmente (Vrba, 1985). De acuerdo con esto,
grandes porciones del mundo orgánico quedan fuera del dominio lógico de estas
definiciones de especie. Esta es una seria dificultad para las personas que trabajan con
organismos partenogenéticos o asexuales.
Un aspecto particularmente problemático de la exclusión de las especies asexuadas
es que la mayoría de las ‘especies’ partenogenéticas despliegan los mismos patrones de
cohesión fenotípica dentro de ellas y de discontinuidad entre ellas que las especies sexuadas.
Por ejemplo, Holman (1987) examinó cómo podían reconocerse las especies sexuadas y las
especies asexuadas de rotíferos. Contrariamente a las predicciones hechas por el concepto de
aislamiento, descubrió que las especies en los taxa asexuados eran de hecho
consistentemente más reconocibles que aquellas de los taxa sexuados. Por consiguiente,
concluyó que para los rotíferos asexuales ‘las especies son reales y pueden ser mantenidas
por factores no reproductivos.’ Como ilustra este ejemplo, el mundo asexual se encuentra en
su mayor parte tan bien subdividido (o quizás mejor) en taxa biológicos fácilmente definidos
como lo está el mundo sexual. Esta realidad biológica no debería ser ignorada.
Ignorar a los taxa asexuales es una falla importante de los conceptos de aislamiento y
de reconocimiento, pero esta falla es en realidad más extensa que lo que mucha gente cree.
Por ejemplo, la genética evolutiva de las poblaciones con autofecundación es simplemente
un caso especial de poblaciones partenogenéticas automícticas (ej., ver Templeton, 1974a).
Por tanto, las especies con autofecundación también se encuentran fuera del dominio lógico
de los conceptos de aislamiento y de reconocimiento. Pero el problema no termina con las
especies con autofecundación. Por ejemplo, muchas especies de avispas poseen
apareamientos obligados entre hermanos (Karlin y Lessard, 1986). Tal sistema de
apareamiento, así como cualquier otro sistema cerrado de apareamiento, desplegará una
dinámica evolutiva que puede ser considerada como un caso especial de automixis, tal como
la autofecundación. Por tanto, todos los taxa sexuados con un sistema cerrado de
apareamiento se encuentran por fuera del dominio lógico de los conceptos de aislamiento y
de reconocimiento.
El problema no termina aquí, sin embargo. Los modelos para el análisis de la
selección multilocus en poblaciones automícticas y con autofecundación fueron aplicados
con mucho éxito a una población de cebada que poseía un 99.43% de autofecundación
(Templeton, 1974b). La razón de este éxito es bien clara: con tanta autofecundación , la
dinámica evolutiva de la población se aproximó mucho a la de una población 100%
autofecundante. Cuando la exogamia se encuentra en un nivel tan bajo, su rol principal es el
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de introducir variabilidad genética dentro de la población. Una vez introducida, el destino
evolutivo de esa variación se asemeja más al de una población autofecundante que al de una
población exogámica. Además, el impacto genético de la exogamia ocasional es reducido
aún más por el aislamiento por distancia, lo que provoca que la mayor parte de la exogamia
ocurra entre individuos casi genéticamente idénticos. En consecuencia, desde la perspectiva
de la genética de poblaciones, esta población de cebada no puede ser considerada de ninguna
manera como un ‘campo para la recombinación génica’, y entonces yace fuera del dominio
lógico tanto del concepto de aislamiento como del de reconocimiento.
El problema del aislamiento por distancia previamente mencionado crea una
restricción más en el dominio lógico de los conceptos de aislamiento y de reconocimiento.
Una población exogámica caracterizada por un flujo génico muy limitado y tamaños
efectivos poblacionales pequeños tendrá casi las mismas consecuencias genéticas y la misma
dinámica evolutiva que una población predominantemente autofecundante. Ehrlich y Raven
(1969) estuvieron entre los primeros en señalar en términos fuertes que muchas especies
animales y vegetales no pueden ser consideradas como campo para la recombinación génica
en ningún sentido significativo con respecto a los mecanismos evolutivos básicos, y por lo
tanto también se encuentran por fuera del dominio lógico de los conceptos de aislamiento y
de reconocimiento.
El ejemplo de la cebada conduce a una pregunta interesante. Si una población con un
99,47% de autofecundación se encuentra fuera del dominio lógico de los conceptos de
aislamiento y de reconocimiento, ¿qué ocurre con una población con un 99% o con un 95%
de autofecundación? El trabajo de Ehrlich y Raven (1969) conduce a un conjunto de
preguntas similares: ¿en qué punto son el aislamiento por distancia y la subdivisión
poblacional suficientemente débiles como para incluir a un taxa dentro del dominio lógico
de los conceptos de aislamiento y de reconocimiento? A pesar de que no se trata de una
pregunta fácil de responder, el problema de los taxa genéticamente cerrados es a menudo
descartado en una o dos frases, siendo los taxa sexual o genéticamente cerrados tratados
como tipos de categorías distintivas (por ej., Mayr 1970; Vrba 1985). Sin embargo, desde el
punto de vista de los mecanismos evolutivos (y, por tanto, desde el punto de vista de la
especiación como proceso evolutivo), existe un continuo desde la dinámica evolutiva
panmíctica hasta la dinámica evolutiva genéticamente cerrada. En consecuencia, el dominio
lógico de los conceptos de aislamiento y de reconocimiento no está en absoluto claro ni bien
definido. La única certeza es que este dominio es mucho más restrictivo y limitado que lo
que en general se percibe.
Demasiado sexo.
Como se ha discutido, los sistemas reproductivos genéticamente cerrados causan
serias dificultades a los conceptos de aislamiento y de reconocimiento, pero también lo
hacen los sistemas genéticamente abiertos. Por ejemplo, Grant (1957), uno de los más
fuertes partidarios entre los botánicos del concepto de aislamiento, concluyó que menos del
50% de las especies exogámicas de 11 géneros de plantas californianas estaban bien
delimitadas por el aislamiento de otras especies. Una y otra vez en las plantas, los
taxónomos han definido especies que existen en grandes unidades conocidas como especies
singámicas (“syngameons”) que se caracterizan por una hibridación natural y un intercambio
genético limitado. Grant (1981) define a las especies singámicas como ‘la unidad más
inclusiva de entrecruzamiento en un grupo de especies con hibridación.’ La existencia
frecuente de especies singámicas en las plantas crea serias dificultades tanto para el
concepto de aislamiento como para el de reconocimiento debido a que el campo de la
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recombinación genética es obviamente mayor que la especie taxonómica y que los grupos
que se comportan como entidades evolutivamente independientes. Una solución es
simplemente negar el status de especie de los miembros del grupo de especies singámicas.
Por ejemplo, Grant (1981) se refiere a los miembros del grupo de las especies singámicas
como ‘semiespecies’. Bajo el concepto de reconocimiento, el propio grupo de especies
singámicas sería la especie, dado que la definición de especie singámica de Grant es
virtualmente idéntica a la definición de especie de Paterson (1985). Sin embargo, los
botánicos no han tomado estas decisiones taxonómicas arbitrariamente. Las especies dentro
de un grupo singámico son a menudo unidades reales en términos de morfología, ecología,
genética y evolución. Por ejemplo, el registro fósil indica que dos especies de álamos
americanos (los ‘balsam poplars’ y los ‘cottonwoods’, ambos del género Populus) han
divergido hace al menos 12 millones de años y han generado híbridos a lo largo de este
período (Eckenwalder, 1984). Aún cuando los híbridos se encuentran muy extendidos, son
fértiles y antiguos, estas especies de árboles poseen y mantienen una cohesión genética,
fenotípica y ecológica entre ellas y una distinción que las separa y se han mantenido como
linajes evolutivos distintivos por al menos 12 millones de años (Eckenwalder, 1984). Por
tanto, estos álamos son unidades biológicas reales que no deberían ser ignoradas.
Es común en los zoólogos reconocer que el concepto de aislamiento posee
dificultades cuando es aplicado a las plantas superiores, exogámicas, pero luego argumentar
que el concepto de aislamiento funciona razonablemente bien para animales multicelulares
que se reproducen sexualmente. Sin embargo, esta visión ya no puede ser sostenida con la
creciente resolución que proveen las técnicas del ADN recombinante. Por ejemplo, en
mamíferos, se están llevando a cabo estudios en mi laboratorio en babuinos, ganado salvaje,
cánidos, roedores subterráneos y ratas, ejemplos, respectivamente, de primates, ungulados,
carnívoros y roedores -los cuatro grupos principales de mamíferos. En cada caso, existe
evidencia de que ocurre hibridación interespecífica en forma natural (Baker et al., 1989;
Davis et al., 1988; datos no publicados). A pesar de la hibridación, muchas de las unidades
taxonómicas dentro de estos grupos representan unidades biológicas reales en el sentido
morfológico, ecológico, genético y evolutivo. Por ejemplo, los lobos y los coyotes pueden
formar híbridos, y de hecho lo hacen. No obstante, son bastante distinguibles
morfológicamente unos de otros, poseen comportamientos extremadamente diferentes en
términos de estructura social y caza, y representan linajes evolutivos distintivos con
diferencias genéticas diagnósticas (Figura 1). Además, el registro fósil indica que han
evolucionado como linajes distintivos y continuos por al menos 0,5 millones de años (Hall,
1978) y quizás por tanto tiempo como 2 millones de años (Nowak, 1978). Aunque estos taxa
no satisfacen el criterio del concepto de especie por aislamiento, Hall (1978) argumenta que
son grupos biológicamente reales y que el status de especie es claramente apropiado.
Las especies singámicas animales no se encuentran de ninguna manera limitadas a
los mamíferos. Drosophila heteroneura y D. silvestris son dos especies hawaianas de
Drosophila con las cuales hemos trabajado. Aunque son filogenéticamente muy cercanas y
en gran medida simpátridas en la isla de Hawaii (Carson, 1978), son extremadamente
distinguibles morfológicamente, siendo la diferencia más dramática que silvestris posee una
cabeza redonda y heteroneura una cabeza con forma de martillo (Val, 1977). Pueden ser
hibridadas en el laboratorio, y los híbridos y los F2 y retrocruzamientos subsiguientes son
completamente fértiles y viables (Val, 1977; Templeton, 1977; Ahearn y Templeton, 1989).
Debido a que la morfología de los híbridos es conocida gracias a estos estudios de
laboratorio, Kaneshiro y Val (1977) fueron capaces de descubrir que la hibridación
interespecífica ocurre en la naturaleza. Nuestros estudios moleculares (DeSalle y Templeton,
1987) confirmaron que los híbridos realmente se forman en la naturaleza, y, lo que es más,
que estos híbridos pueden retrocruzarse, y de hecho lo hacen, hasta tal punto que un
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haplotipo mitocondrial de heteroneura puede hallarse asociado a una morfología
aparentemente normal de silvestris. A pesar de esta hibridación natural, las especies pueden
mantener, y lo hacen, sus muy distinguibles morfologías de base genética (Templeton, 1977;
Val, 1977) y poseer distintas filogenias de su ADN nuclear (Hunt y Carson, 1983; Hunt et
al., 1984) a pesar de la limitada introgresión observada con el ADN mitocondrial (DeSalle et
al., 1986). Por tanto, tanto la morfología como las moléculas definen a estos taxa como
linajes reales y evolutivamente distinguibles.
Como ilustran estos y otros estudios, los taxa animales despliegan frecuentemente la
hibridación natural que produce híbridos fértiles y viables. Estos taxa se han reconocido
usualmente como especies debido a sus morfologías y ecologías distintivas y debido a que
los estudios moleculares modernos han revelado que se comportan como linajes evolutivos
independientes, al menos con respecto a sus genomas nucleares. En otras palabras, muchas
especies animales son miembros de grupos singámicos, tal como lo son las plantas. Por
tanto, las especies singámicas son un problema extendido para los conceptos de aislamiento
y de reconocimiento.
EL CONCEPTO COHESIVO DE ESPECIE.
Ahora es posible una nueva definición biológica de especie, la que llamo el concepto
cohesivo de especie. La especie en el concepto cohesivo es la población más inclusiva de
individuos que poseen el potencial para la cohesión fenotípica a través de mecanismos
intrínsecos de cohesión (Tabla 2). Trataré ahora sobre el significado de este concepto de
especie, mostrando cómo toma partes prestadas de los conceptos evolutivo, de aislamiento y
de reconocimiento, mientras que evita sus serios defectos.
Al igual que el concepto evolutivo de especie, el concepto cohesivo de especie define
a la especie en términos de cohesión genética y fenotípica. Como consecuencia, el concepto
de cohesión comparte con el concepto evolutivo su fortaleza de poder ser aplicable a los taxa
que se reproducen asexualmente (o por intermedio de otros sistemas cerrados o casi cerrados
de apareamiento), y a los taxa que pertenecen a grupos singámicos. Al contrario que el
concepto evolutivo de especie, el concepto de cohesión define a las especies en términos de
los mecanismos que producen la cohesión más que de la manifestación de la cohesión en el
tiempo evolutivo. Este es un enfoque mecanístico similar al que toma el concepto de
aislamiento, si bien en este caso el foco se encuentra sobre mecanismos de cohesión en vez
de mecanismos de aislamiento. Al definir una especie en términos de mecanismos de
cohesión, el concepto cohesivo puede ser fácilmente relacionado con un marco mecanístico
de genética de poblaciones y puede guiar en la comprensión de la especiación como proceso
evolutivo. En particular, la especiación es ahora considerada como la evolución de los
mecanismos de cohesión (como opuestos a los mecanismos de aislamiento). Esto significa
también que el concepto de cohesión se centra principalmente en los taxa vivientes más que
en los taxa fósiles.
TABLA 2. Clasificación de los mecanismos de cohesión.
I. Intercambiabilidad genética: los factores que definen los límites de dispersión de las
nuevas variantes
génicas a través del flujo génico.
A. Mecanismos que promueven la identidad genética a través del flujo génico
1. Sistema de fertilización: los organismos son capaces de intercambiar gametos que
conduzcan a una
fecundación exitosa.
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2. Sistema de desarrollo: los productos de la fertilización son capaces de producir
adultos viables y
fértiles.
B. Mecanismos de aislamiento: la identidad genética se pereserva por la falta de flujo
génico con otros
grupos.
II. Intercambiabilidad demográfica: los factores que definen el nicho fundamental y los
límites de dispesión
de las nuevas variantes génicas a través de la deriva genética y la selección natural.
A. Reemplazabilidad: la deriva genética (la descendencia de un ancestro común)
promueve la identidad
genética.
B. Desplazabilidad:
1. Fijación selectiva: la selección natural promueve la identidad genética favoreciendo
la fijación de
una variante genética.
2. Transiciones adaptativas: la selección natural favorece a las adaptaciones que
alteran directamente a
la intercambiabilidad demográfica. La transición está restringida por:
a. Restricciones mutacionales en el origen de la variación fenotípica heredable.
b. Restricciones en el destino de la variación heredable
i. Restricciones ecológicas.
ii. Restricciones del desarrollo.
iii. Restricciones históricas.
iv. Restricciones de la genética poblacional.
Como fue señalado por Paterson (1985), es útil definir los mecanismos subyacentes
al status de especie de tal forma que las definiciones reflejen la función evolutiva más
probable de los mecanismos durante el proceso de especiación. De acuerdo con esto, los
mecanismos de cohesión serán definidos para que reflejen su función evolutiva más
probable. La tarea básica es identificar esos mecanismos de cohesión que contribuyen a
mantener a un grupo como un linaje evolutivo. La esencia misma de un linaje evolutivo
desde una perspectiva de la genética poblacional es que nuevas variantes genéticas pueden
surgir en él, extenderse, y reemplazar a las variantes viejas. Estos eventos suceden por
intermedio de las fuerzas microevolutivas estándar como el flujo génico, la deriva genética,
y/o la selección natural. El hecho de que las variantes génicas presentes en un linaje
evolutivo puedan ser rastreadas hasta un ancestro común significa también que los
individuos que componen este linaje deben mostrar un alto grado de relacionamiento
genético. Los mecanismos de cohesión que definen el status de especie son, por tanto,
aquellos que promueven el relacionamiento genético y que determinan las fronteras
poblacionales de la acción de las fuerzas microevolutivas.
Los conceptos de aislamiento y de reconocimiento se centran exclusivamente en el
relacionamiento genético promovido a través del intercambio de genes vía reproducción
sexual. Estas definiciones han elevado a una única fuerza microevolutiva -el flujo génicocomo criterio concluyente y exclusivo del status de especie. No hay ninguna duda de que el
flujo génico es una de las principales fuerzas microevolutivas, y por tanto los factores que
definen los límites de dispersión de las nuevas variantes génicas a través del flujo génico son
criterios válidos para el status de especie. De acuerdo con esto, la intercambiabilidad
genética se incluye en la Tabla 2 como una importante clase de mecanismos de cohesión. La
intercambiabilidad genética se refiere simplemente a la capacidad de intercambiar genes por
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intermedio de la reproducción sexual. Esto implica un sistema de fertilización compartido en
el sentido de Paterson (1985). El intercambio efectivo de genes también exige que los
productos de la fertilización sean potencialmente viables tanto como fértiles (Templeton,
1987). Como se muestra en la Tabla 2, el rol del flujo génico en la determinación del status
de especie puede ser definido tanto en un sentido positivo (I.A en Tabla 2) como en uno
negativo (I.B en Tabla 2). Como se afirmó anteriormente, el sentido positivo provee
generalmente de una visión más certera de los procesos evolutivos involucrados en la
especiación.
El flujo génico no es la única fuerza microevolutiva que define las fronteras de un
linaje evolutivo. En realidad, la deriva genética y la selección natural juegan un rol mucho
más potente y universal debido a que estas dos clases de fuerzas microevolutivas son
aplicables a todos los organismos, no sólo a las especies sexuadas exogámicas. Una pregunta
importante es, por lo tanto, ¿qué factores definen los límites de dispersión de las nuevas
variantes génicas a través de la deriva genética y la selección natural? Dado que estas
fuerzas pueden operar en poblaciones asexuales, es obvio que los factores que limitan el
campo de acción de la deriva y la selección no son necesariamente los mismos que los que
limitan las acciones del flujo génico. Como vimos, el flujo génico requiere
intercambiabilidad genética, es decir, la capacidad de intercambiar genes durante la
reproducción sexual. Para que operen la deriva genética y la selección natural, se requiere
otro tipo de intercambiabilidad: la intercambiabilidad demográfica (Tabla 2).
Desde una perspectiva ecológica, los miembros de una población demográficamente
intercambiable comparten el mismo nicho fundamental (Hutchinson, 1965), aunque no
necesitan ser idénticos en sus capacidades de explotar ese nicho. El nicho fundamental se
define por las tolerancias intrínsecas (i.e., genéticas) de los individuos a varios factores
ambientales que determinan el rango de ambientes en los cuales los individuos son
potencialmente capaces de sobrevivir y reproducirse. El nicho realizado (Hutchinson, 1965)
se refiere al subconjunto del nicho fundamental que es efectivamente ocupado por una
especie. El nicho realizado es usualmente un subconjunto característico del nicho
fundamental debido a la falta de oportunidades de ocupar ciertas porciones del nicho
fundamental (por ejemplo, en alguna localidad los rangos ambientales pueden encontrarse
dentro de los límites de tolerancia, pero hay barreras geográficas que impiden la
colonización de dicha localidad) o debido a interacciones con otras especies que impiden la
explotación de todo el rango de tolerancia ecológica. Por tanto, el nicho realizado está
influenciado por muchos factores extrínsecos, pero la intercambiabilidad demográfica
depende solamente de las tolerancias ecológicas intrínsecas.
Mientras los individuos compartan el mismo nicho fundamental, serán
intercambiables entre ellos con respecto a los factores que controlan y regulan el crecimiento
de la población y otros atributos demográficos. Es la intercambiabilidad demográfica la que
es utilizada para definir a las poblaciones en la mayoría de los modelos de ecología de
poblaciones y de comunidades. En realidad, la mayor parte de los modelos de éstas
disciplinas ecológicas ni siquiera especifican el modo de reproducción, por lo que la
intercambiabilidad genética no es utilizada para definir una población.
Desde una perspectiva genética, las probabilidades de que una mutación neutral o
selectivamente favorable termine fijándose en una población demográficamente
intercambiable son distintas de cero sin importar el individuo particular sobre el cual ha
ocurrido la mutación. En otras palabras, cada individuo en una población demográficamente
intercambiable es un potencial ancestro común de toda la población en algún punto del
futuro. La relaciones ancestro-descendiente pueden ser tan sencillamente definidas en
poblaciones asexuales como en poblaciones sexuales. Por tanto, la intercambiabilidad
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demográfica no requiere de intercambiabilidad genética y es un atributo biológico distintivo
a nivel poblacional.
Así como la intercambiabilidad genética puede variar en fuerza, lo mismo puede
hacer la intercambiabilidad demográfica. Desde una perspectiva ecológica, la
intercambiabilidad demográfica completa sucede cuando todos los individuos de una
población poseen exactamente los mismos rangos y capacidades de tolerancia a todas las
variables ecológicas relevantes. La intercambiabilidad demográfica se debilita a medida que
los individuos comienzan a diferir en sus rangos o capacidades de tolerancia. Desde una
perspectiva genética, una población es completamente intercambiable demográficamente si
la probabilidad de una mutación neutral o selectivamente favorable que se dirige a la fijación
es exactamente la misma independientemente del individuo en el cual ocurra. Una población
débilmente intercambiable demográficamente consistiría de miembros que poseen
probabilidades de fijación muy diferentes (pero aún distintas de cero).
La intercambiabilidad demográfica nos permite incorporar fácilmente a otras fuerzas
microevolutivas aparte del flujo génico que son importantes en la definición de un linaje
evolutivo. Una de tales fuerzas microevolutivas es la deriva genética, que promueve la
cohesión genética a través de las relaciones ancestro-descendientes (i.e., el concepto de
idéntico por descendencia de la genética de poblaciones). Para el caso especial de los alelos
neutros (alelos que no tienen ninguna importancia selectiva), la tasa a la cual la deriva
genética promueve la identidad por descendencia depende solamente de la tasa de
mutaciones neutras y es por tanto igualmente importante en las poblaciones grandes que en
las pequeñas. Es interesante que esta predicción acerca de la tasa de evolución neutral y las
otras predicciones básicas de la teoría neutral estándar no dependan de asumir que existe
reproducción sexual -estas predicciones son igualmente aplicables a organismos asexuados.
Aunque la teoría neutral no requiere de intercambiabilidad genética, la intercambiabilidad
demográfica es una asunción crítica y necesaria (por ejemplo, Rothman y Templeton, 1980).
Haciendo solamente la asunción de que existe intercambiabilidad demográfica, es inevitable
que en algún punto en el futuro todos los alelos habrán descendido de un alelo que existe en
el presente. No hace ninguna diferencia para la operación de la deriva genética si son los
alelos o son los individuos que portan los alelos los que son intercambiables. Por tanto, la
intercambiabilidad demográfica debe ser considerada como uno de los principales
mecanismos de cohesión debido a que define los límites poblacionales para la acción de la
deriva genética. Este aspecto de la intercambiabilidad demográfica es llamado
‘reemplazabilidad’ en la Tabla 2.
La selección natural es otra fuerza poderosa que puede contribuir en la definición de
un linaje evolutivo. El concepto de selección natural no requiere de intercambiabilidad
genética debido a que los modelos de selección se formulan tan fácilmente para poblaciones
genéticamente cerradas como para las genéticamente abiertas (por ejemplo, Templeton,
1974a, 1974b). Como Darwin señaló, la selección natural requiere dos condiciones
demográficas: (1) que los organismos puedan producir más descendientes de los que son
necesarios para su estricto reemplazo, y (2) que un crecimiento poblacional ilimitado no
puede ser mantenido indefinidamente. Cuando estas condiciones demográficas son
acopladas a la variación heredable en rasgos que influyen en la supervivencia y la
reproducción, la consecuencia lógica es que los descendientes de algunos individuos
desplazarán a los de otros dentro de la población. Este aspecto de la intercambiabilidad
demográfica se denomina ‘desplazabilidad’ en la Tabla 2.
La selección natural promueve la cohesión tanto favoreciendo el relacionamiento
genético como afectando los límites de la propia intercambiabilidad demográfica. Siempre
que la selección natural cause que una nueva mutación favorable se dirija a la fijación, el
relacionamiento genético en ese locus es obviamente una consecuencia directa. Además,
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mientras esta mutación se dirige a la fijación, ese subconjunto de la variación genética de la
especie que permanece ligado a la nueva mutación también se dirige a la fijación. Esto se
conoce como el efecto ‘hitchhiking’ (o genes ligados), y es importante notar que a medida
que la intercambiabilidad genética declina en importancia, los efectos del ‘hitchhiking’
aumentan su importancia, por la simple razón de que la recombinación genética es menos
efectiva para romper los estados iniciales del ligamiento que fueron creados en el momento
de la mutación. Por tanto, la fijación selectiva de un alelo por intermedio de otro es un
mecanismo de cohesión extremadamente poderoso en las poblaciones con sistemas de
reproducción genéticamente cerrados (Levin, 1981). Como ejemplo, la Figura 2 muestra los
resultados de la selección en una cepa partenogenética de D. mercatorum (Annest y
Templeton, 1978). Como puede verse en esta figura, la población convergió rápidamente a
un único genotipo para todos los loci marcadores que se examinaron. La dinámica de esta
convergencia indicó que estaban operando fuerzas selectivas muy fuertes (Annest y
Templeton, 1978). Otras réplicas de esta misma población, todas sujetas a recombinación
génica durante la primera generación partenogenética, convergieron selectivamente hacia
otros estados fenotípicos de los loci marcadores, indicando así que los loci marcadores no
estaban siendo directamente seleccionados. Por consiguiente, la selección en quizás unos
pocos loci promovió la identidad genética de todos los loci en estas poblaciones
partenogenéticas.
El grado de intercambiabilidad demográfica está íntimamente entrelazado con los
requerimientos de nicho ecológico del organismo y los hábitats que se encuentran
disponibles para satisfacer dichos requerimientos. Son estos mismos requerimientos
ecológicos y hábitats disponibles los que proveen muchas de las fuerzas selectivas que
conducen el proceso de adaptación. Por tanto, el proceso de adaptación por selección natural
puede alterar directamente los rasgos que determinan el grado de intercambiabilidad
demográfica. Las transiciones adaptativas, por lo tanto, juegan un rol directo en la definición
de los grupos de organismos demográficamente intercambiables
La importancia de las transiciones adaptativas en la definición de la
intercambiabilidad demográfica abre un grupo enteramente nuevo de mecanismos de
cohesión que restringen los cursos posibles de las transiciones adaptativas, como muestra la
Tabla 2 (II.B.2). Los primeros son las restricciones mutacionales que limitan los tipos de
variantes fenotípicas probables de ser producidas. Tales restricciones dificultan la alteración
de algunos aspectos del sistema genético y de desarrollo que existe, pero facilitan el cambio
evolutivo a lo largo de otras líneas. Por ejemplo, el género Drosophila consiste en algunas
moscas que poseen pintas, nubes o patrones pigmentados en las alas, tal como la ‘picturewing’ hawaiiana, y en otras que poseen alas claras, como D. melanogaster. No obstante,
como señala Basden (1984), nunca una drosophila de alas pintadas ha producido una
mutante de alas claras, ni una mutante de alas claras ha producido jamás una mutante de alas
pintadas. Este resultado negativo posee significación biológica para D. melanogaster, ya que
probablemente ningún otro eucariota superior ha sido más extensamente analizado en busca
de mutaciones visibles. Por consiguiente, Basden concluyó que a nivel de especie existe una
traba para ciertos tipos de mutaciones. Esta es simplemente otra forma de afirmar que
existen las restricciones que hacen que ciertas mutaciones sean imposibles o altamente
improbables.
Dado que se ha producido variación fenotípica por el proceso mutacional, existen
restricciones que influyen en el destino evolutivo de dicha variación (Tabla 2, II.B.2.b). En
primer lugar, hay restricciones ecológicas que seleccionan en contra a ciertos fenotipos y
que restringen el rango de variabilidad ambiental experimentada por la especie. Además,
para que una transición adaptativa persista, debe haber un nicho disponible para los
organismos con la nueva adaptación. Las restricciones ecológicas son sin lugar a dudas uno
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de los mecanismos de cohesión más importantes que mantienen a las especies dentro de
grupos singámicos, como es demostrado por lo que sucede dentro de estos grupos cuando
las restricciones se alteran. Por ejemplo, bajo la mayoría de las condiciones ambientales, los
robles rojos y negros viven juntos en los mismos bosques y desarrollan polinización
cruzada. No obstante, pqermanecen como dos poblaciones distintas y cohesivas, debido a
que las bellotas híbridas de la F1 no germinan bien bajo las condiciones oscuras y frescas de
un bosque maduro. Cuando un bosque es parcialmente aclarado y raleado (principalmente
por la acción humana), las bellotas de los robles rojos y las de los robles negros germinan
mal, mientras que las bellotas híbridas lo hacen muy bien. Como resultado, muchos bosques
actuales consisten en una intergradación continua entre robles negros y rojos. Por tanto, la
cohesión normal de las poblaciones de robles rojos y negros se pierde cuando las
restricciones ecológicas son alteradas.
Las resticciones ecológicas son también importantes en los taxa asexuales debido a
que éstas restricciones a menudo determinan los límites poblacionales de la fijación
selectiva, lo cual es, como se mencionó previamente, un importante mecanismo de cohesión
en los taxa con sistemas cerrados de reproducción. Además, el trabajo de Roughgarden
(1972) predice que las poblaciones asexuales pueden desarrollar amplitudes de nichos más
nítidamente delimitadas de lo que podrían las poblaciones sexuales equivalentes. Esta
propiedad puede contribuir a explicar el hecho de que las especies asexuales sean más
fácilmente reconocibles que las especies sexuales (Holman, 1987).
Las restricciones del desarrollo constituyen la segunda clase de mecanismos de
cohesión relacionados al destino de la variación heredable en las transiciones adaptativas.
Cuando existe una fuerte selección sobre detrminado rasgo, la pleiotropía (una forma de
restricción del desarrollo) se asegura de que otros rasgos también evolucionen. Por tanto, la
pleiotropía puede facilitar los cambios evolutivos que de otra forma no ocurrirían. Aunque
muchos investigadores han puesto énfasis en la naturaleza no adaptativa, incluso mal
adaptativa, de estos cambios pleiotrópicamente inducidos, Wagner (1988) ha mostrado que
la pleiotropía es esencial para la evolución de rasgos adaptativos complejos. Examinó un
modelo en el cual la eficacia darwiniana depende de los estados simultáneos de varios rasgos
y luego contrastó modelos de evolución adaptativa en los cuales todos los rasgos eran
genéticamente independientes (no había pleiotropía ni restricciones del desarrollo) con un
modelo al cual se le imponían restricciones del desarrollo. Halló que, cuando no hay
restricciones del desarrollo, la tasa de evolución adaptativa decrece dramáticamente a
medida que aumenta el número de caracteres involucrados en la integración funcional. Por
tanto, las restricciones del desarrollo y la pleiotropía parecen ser necesarias para la evolución
de fenotipos funcionalmente integrados.
Aún más evolución adaptativa puede ser facilitada incluso cuando la adaptación
primaria induce efectos pleiotrópicos que son no adaptativos. Este fenómeno puede ser
ilustrado por las adaptaciones a la malaria en humanos (Templeton, 1982). Las adaptaciones
primarias a la malaria (tales como la condición falciforme) a menudo inducen efectos
pleiotrópicos altamente deletéreos (como la anemia), los cuales, a su vez, generan procesos
adaptativos secundarios en modificadores para disminuir o eliminar los efectos deletéreos
(tales como la persistencia de la hemoglobina fetal para suprimir la anemia). De esta forma
una sóla transición adaptativa puede disparar una cascada de transiciones secundarias, las
cuales se acumulan y pueden tener un gran impacto en la intercambiabilidad demográfica.
Otro mecanismo de cohesión que restringe el destino evolutivo de la variabilidad
fenotípica es la restricción histórica. La evolución es un proceso histórico y, en
consecuencia, el potencial evolutivo de un linaje está modelado por sus transiciones
adaptativas pasadas. Por ejemplo; un prerequisito para la evolución de la coloración
aposemática en insectos con larvas gregarias es la evolución de la mala palatabilidad. Sin la
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existencia previa del sabor desagradable, no hay fuerza selectiva a favor de la coloración de
advertencia dentro de la progenie (Templeton, 1979). Por tanto, la adaptación del mal sabor
es una restricción histórica para la evolución de la coloración aposemática y las larvas
gregarias. Esta predicción fue puesta a prueba recientemente por Sillen-Tullberg (1988),
quien mostró a través de un análisis filogenético que en todos los casos en los que la
resolución era posible, el mal sabor evolucionó previamente a la evolución de larvas
gregarias y aposemáticas. Como muestra este ejemplo, una adaptación puede hacer que una
segunda sea más probable, reforzando así la cohesión del linaje que comparte estas
transiciones adaptativas.
Las restricciones de la genética de poblaciones también limitan el destino evolutivo
de la nueva variabilidad fenotípica. Estas restricciones emergen de la interacción de la
estructura poblacional (sistema de apareamiento, tamaño poblacional, subdivisión
poblacional) con la arquitectura genética subyacente a los rasgos seleccionados (la relación
genotipo-fenotipo, número de loci, relaciones de ligamiento, etc.). Por ejemplo, en 1924
Haldane mostró que los genes dominantes selectivamente favorecidos son mucho más
probables de ser fijados que los genes recesivos selectivamente favorecidos en las
poblaciones con apareamientos al azar. Sin embargo, esta restricción desaparece si el
sistema de apareamiento cambia desde apareamientos al azar hacia la endogamia
(Templeton, 1982). De este modo, una alteración del sistema de apareamiento puede alterar
la cohesión genética y fenotípica de una población haciendo que clases enteras de
variabilidad genética nueva respondan a la selección natural.
VENTAJAS DEL CONCEPTO COHESIVO DE ESPECIE
El concepto cohesivo de especie define a la especie como linaje evolutivo a través de
los mecanismos que limitan las fronteras poblacionales de la acción de las fuerzas
microevolutivas básicas como el flujo génico, la selección natural y la deriva genética. La
esencia genética de un linaje evolutivo es que una nueva mutación puede dirigirse a la
fijación dentro del mismo; y la deriva genética así como el flujo génico son fuerzas
poderosas que pueden causar tales fijaciones. Por tanto, no existe ninguna buena razón por la
cual el flujo génico deba ser el único mecanismo microevolutivo utilizado para definir un
linaje evolutivo; no obstante esto es precisamente lo que hacen los conceptos de aislamiento
y de reconocimiento.
Bajo el concepto de cohesión, muchos mecanismos de cohesión con base genética
(Tabla 2) pueden jugar un rol en la definición de una especie. No todas las especies serán
mantenidas por los mismos mecanismos de cohesión o por las mismas combinaciones de
mecanismos de cohesión, tal como los partidarios del concepto de aislamiento reconocen
que no todos los mecanismos de aislamiento son igualmente importantes en todos los casos.
Ajustando la combinación de mecanismos de cohesión, es posible tener en cuenta bajo un
único concepto de especie a los taxa asexuales, a los taxa que caen dentro del dominio de los
conceptos de aislamiento y de reconocimiento, y a los miembros de grupos singámicos.
La Figura 3 ofrece una representación gráfica simpificada de la importancia relativa
en la definición de especie de la intercambiabilidad genética versus la demográfica sobre el
contínuo reproductivo completo. Para taxa asexuales, la intercambiabilidad genética no es
relevante, y el status de especie se determina exclusivamente por la intercambiabilidad
demográfica. A medida que el sistema reproductivo se vuelve más abierto, la
intercambiabilidad genética no sólo se convierte en un factor, sino que la intercambiabilidad
demográfica disminuye en importancia debido a que el reemplazo selectivo se vuelve cada
vez menos efectivo en promover el relacionamiento genético. En un rango intermedio,
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domina la intercambiabilidad genética porque los factores que determinan los límites del
flujo génico también limitan la acción de la deriva y la selección en las poblaciones
mendelianas exogámicas. En este dominio, los conceptos de aislamiento y de
reconocimiento son válidos, y por tanto, ambos constituyen casos especiales del concepto
cohesivo más general de especie. Finalmente, si nos movemos hacia el extremo del contínuo
de los grupos singámicos, decrece la importancia de la intercambiabilidad genética en
relación a las restricciones ecológicas que definen la intercambiabilidad demográfica.
Esta continuidad en la aplicación del concepto de cohesión es consistente con la
realidad biológica de que existe un continuo en el grado de apertura genética de los sistemas
de reproducción que se encuentran en el mundo orgánico. Esta es una ventaja tremenda
sobre los conceptos de aislamiento y de reconocimiento que son aplicables sólo al rango
medio de este continuo reproductivo y que tratan con el resto del rango o bien negando la
existencia de especies fuera de este rango (por ejemplo, Vrba, 1985) o utilizando conceptos
de especies cualitativamente distintos (por ejemplo, Mayr, 1970) para imponerle al continuo
reproductivo un carácter discreto artificial.
Otro punto fuerte del concepto de cohesión es que clarifica lo que se quiere decir con
una ‘buena especie’ y la naturaleza de las dificultades que pueden ocurrir con los conceptos
de aislamiento y de reconocimiento. Las ‘buenas especies’ son consideradas generalmente
como taxa geográficamente cohesivos que pueden coexistir por largos períodos de tiempo
sin ninguna ruptura en su integridad genética. El hecho de que no haya ruptura en la
integridad genética a pesar de la simpatría implica la falta de intercambiabilidad genética
entre los taxa. Sin embargo, la condición de coexistencia prolongada también implica que
poseen nichos ecológicos diferentes (Mayr, 1970). Luego, las ‘buenas especies’ son aquellas
que se encuentran bien definidas tanto por la intercambiabilidad genética como por la
demográfica. (En forma similar, los miembros de un taxón superior ‘bueno’ carecen tanto de
intercambiabilidad genética como demográfica.) Dada esta definición de ‘buena especie’,
hay dos maneras principales de desviarse de este ideal. Una sucede cuando las fronteras
poblacionales definidas por la intercambiabilidad genética son más estrechas que las
definidas por la intercambiabilidad demográfica. Este es precisamente el problema de los
taxa asexuales previamente discutido. La otra forma de desviación sucede cuando las
fronteras definidas por la intercambiabilidad genética son mayores que las definidas por la
intercambiabilidad demográfica -en otras palabras, el problema propuesto por las especies
singámicas. Por tanto, estos dos problemas aparentemente tan dispares bajo los conceptos de
aislamiento y de reconocimiento poseen de hecho un causa subyacente común: las fronteras
definidas por la intercambiabilidad demográfica son diferentes de las definidas por la
intercambiabilidad genética.
La especiación es generalmente un proceso, no un evento (Templeton, 1981).
Mientras el proceso esté ocurriendo, la tendencia es a tener ‘malas’ especies. Aunque los
taxa asociados con este proceso incompleto de especiación son la perdición para el
taxónomo, proveen la mejor visión dentro de la especiación. Al proveer una definición
precisa de ‘mala especie’ (el conflicto entre la intercambiabilidad genética y la
demográfica), el concepto de cohesión es una herramienta útil para obtener una visión
profunda dentro del proceso de especiación. Las ‘malas especies’ ya no deben ser
consideradas como un diverso grupo de casos especiales; más bien, el concepto de cohesión
provee los medios para ver los patrones observados en estos taxa problemáticos. Por
ejemplo, Levene (1953) postuló un modelo hace mucho tiempo en el cual diferentes
genotipos desarrollaban diferentes eficacias darwinianas en nichos demográficamente
independientes. Sin embargo, en este modelo, hay intercambiabilidad genética completa y
aún hay suficiente intercambiabilidad demográfica entre todos los genotipos dentro de los
varios nichos realizados (a través del desplazamiento selectivo dentro del nicho) que se trata
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claramente de un modelo de polimorfismo intraespecífico. La situación modelada por
Levene (1953) porta ciertas semejanzas con los ejemplos de los grupos singámicos
discutidos anteriormente en que surge un conflicto entre la intercambiabilidad genética y la
demográfica (a través de la adaptación a diferentes nichos ecológicos realizados que alteran
las tolerancias intrínsecas que definen al nicho fundamental). Por tanto, puede haber un
continuo de fuerza relativa entre estos conflictivos criterios de fronteras entre las especies.
Es interesante el hecho de que ha habido un reconocimiento implícito de esta tensión en la
literatura de la especiación. La mayor parte de los modelos de especiación simpátrida
comienzan con un modelo del tipo de Levene, siendo el modelo de Wilson (en este
volumen) un ejemplo de ello (ver también Maynard Smith, 1966). Aunque estos modelos en
detalle difieren en gran medida, el concepto de cohesión clarifica el significado evolutivo de
esta clase entera de modelos de especiación: es la evolución de la no-intercambiabilidad
demográfica lo que dispara en estos casos el proceso de especiación, y la especiación
procede a través de los cambios en la importancia relativa de la intercambiabilidad genética
y demográfica dentro y entre las poblaciones mientras se adaptan a diferentes nichos
realizados. De este modo, de un grupo aparentemente diverso de modelos de especiación
todos poseen un tema en común, y el concepto de cohesión permite discernir claramente este
tema.
Nótese también que la selección natural es la fuerza que dirige la especiación en
todos estos modelos de especiación simpátrida, siendo secundarios los efectos del flujo
génico. Debido a que el concepto de cohesión incorpora explícitamente a un amplio grupo
de fuerzas microevolutivas como importantes en la especiación, podemos tratar directamente
a la selección natural como si fuera en estos modelos el disparador primario de la
especiación en vez de tener que explicar constantemente el significado evolutivo de la
selección natural en términos de sus efectos secundarios sobre el flujo génico. El concepto
de cohesión por lo tanto facilita el estudio de la especiación como un proceso evolutivo
volviendo explícito el rol jugado por una amplia muestra de fuerzas evolutivas que incluyen
al flujo génico, pero que no están limitadas al mismo.
Como ilustran los modelos de especiación del tipo de Levene, una de las fuerzas
evolutivas importantes en la especiación es la selección natural. La selección natural es
importante para la definición de especie bajo el concepto de cohesión en parte debido al
impacto de las transiciones adaptativas en la intercambiabilidad demográfica. Es interesante
que Mayr (1970) argumenta que la mayoría de las especies poseen nichos ecológicos
distintivos (es decir, que no son demográficamente intercambiables) y que esta diferencia
ecológica es la ‘piedra angular de la evolución’ porque sirve como base de la diversificación
del mundo orgánico, de la radiación adaptativa, y del progreso evolutivo. Si bien Mayr
concluye por lo tanto que ‘el significado evolutivo de especie’ yace en su distinción
ecológica, aún argumenta que las transiciones adaptativas y la selección natural no juegan en
general un rol directo en la especiación y contribuyen a definir una especie sólo a través del
‘producto secundario incidental’ que constituyen los mecanismos de aislamiento. Mayr
permite que las presiones selectivas refuercen los mecanismos de aislamiento y acentúen la
exclusión ecológica si se ha establecido la simpatría, pero pone énfasis en que esto ocurre
sólo luego de que el proceso de especiación ha sido básicamente completado. Por tanto, bajo
el concepto de aislamiento, los factores responsables del ‘significado evolutivo de especie’
no juegan un rol directo en la definición de especie. Bajo el concepto de cohesión, el
significado evolutivo de una especie puede surgir directamente de los atributos que la
definen.
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ESPECIACIÓN
Ahora que la especie ha sido definida, ¿qué es la especiación? La especiación es el
proceso por el cual nuevos sistemas genéticos de mecanismos de cohesión evolucionan
dentro de una población. Este proceso puede considerarse análogo al proceso de asimilación
genética de los fenotipos individuales. La asimilación genética es un proceso discutido por
Waddington (1957) a la luz de su trabajo con la mosca de la fruta, Drosophila melanogaster.
Por ejemplo, descubrió que sometiendo algunas cepas de esta mosca a choques térmicos,
muchas de las moscas expresarían un fenotipo en el cual se observa la falta de cierta vena de
las alas. Inicialmente, este fenotipo ‘crossveinless’ parecía ser puramente ambiental.
Seleccionando artificialmente a las moscas que expresaban el fenotipo, Waddington
descubrió que estaba seleccionando también a la predisposición genética para expresar este
fenotipo. Por lo tanto, luego de varias generaciones este fenotipo ‘ambiental’ adquirió una
base genética hasta tal punto que eventualmente comenzó a expresarse aún en ausencia del
choque térmico. En forma similar, una alteración puramente ambiental en la manifestación
de la cohesión puede conducir a condiciones evolutivas que favorecen la asimilación del
nuevo patrón de cohesión dentro del pool génico. Por ejemplo, considérese el caso de la
especiacción alopátrida en el cual un taxa ancestral que se encontraba distribuido en forma
continua en una región es luego dividido, por la erección de alguna barrera geográfica, en
dos subpoblaciones totalmente aisladas. La erección de la barrera geográfica altera
potencialmente la manifestación de varios mecanismos de cohesión. Para taxa sexuados, se
altera el relacionamiento genético a través del flujo génico, y para taxa tanto sexuados como
asexuados, el potencial para el relacionamiento genético a través de la deriva génica y la
selección natural se altera tan pronto como las poblaciones se vuelven demográficamente
independientes debido a la separación geográfica. Además, si la barrera geográfica se asocia
con la alteración ambiental o con la alteración de los sistemas de apareamiento, las
alteraciones en las restricciones de las transiciones adaptativas pueden ser directamente
inducidas y un nuevo nicho realizado puede ser ocupado. Sin embargo, nada de esto
constituye la especiación hasta que estas alteraciones en la manifestación de la
intercambiabilidad genética y demográfica son genéticamente asimiladas dentro del pool
génico como nuevos mecanismos de cohesión. Por consiguiente, la especiación es la
asimilación genética de patrones alterados de intercambiabilidad genética y demográfica
dentro de los mecanismos intrínsecos de cohesión.
Esta es una definición simple de la especiación, pero debido a la amplitud del
concepto cohesivo de especie, esta definición puede utilizarse para estudiar una gran
variedad de procesos evolutivos que contribuyen a la formación de una nueva especie dentro
de un mismo marco mecanístico. Esta es una perspectiva excitante, y espero que resulte en
una aplicación más profunda de la genética evolutiva al problema del origen de las especies.
RESUMEN
El ‘concepto biológico de especie’ define a las especies como comunidades
reproductivas que están separadas de otras comunidades similares por barreras intrínsecas de
aislamiento. Sin embargo, existen otros conceptos ‘biológicos’ de especie, por lo cual el
concepto biológico clásico de especie se describe mejor como el concepto de especie ‘por
aislamiento’. El propósito de este capítulo era proveer una definición biológica de especie
que provenga directamente de los mecanismos evolutivos responsables de la especiación y
sus consecuencias genéticas.
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Los puntos fuertes y débiles de los conceptos evolutivo, de aislamiento y de
reconocimiento fueron revisados y los tres fueros juzgados como inadecuados para este
propósito. Como alternativa, propuse el concepto cohesivo que define a la especie como el
grupo más inclusivo de organismos que poseen el potencial para la intercambiabilidad
genética y demográfica. Este concepto toma ideas prestadas de los tres conceptos biológicos
de especie. A diferencia de los conceptos de aislamiento y de reconocimiento, es aplicable a
todo el continuo de sistemas reproductivos observados en el mundo orgánico. A diferencia
del concepto evolutivo, identifica mecanismos específicos que dirigen el proceso evolutivo
de la especiación. El concepto cohesivo facilita el estudio de la especiación a la vez que es
compatible con las consecuencias genéticas de dicho proceso.
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SEMINARIO II: MECANISMOS DE AISLAMIENTO Y MODELOS DE ESPECIACIÓN Marcela Rodriguero & Abel Carcagno En este seminario se analizarán dos modelos de especiación vinculados a distintos Mecanismos de Aislamiento Reproductivo (MARs) por medio de la discusión de dos casos particulares: el modelo de especiación infecciosa y el modelo de especiación simpátrica. Preguntas Introductorias 1‐ ¿Qué son los Mecanismos de Aislamiento Reproductivo (MARs) y qué concepto de especie los contempla? Clasifíquelos y de ejemplos. 2‐ ¿Cuál es la clasificación de los procesos especiogénicos de acuerdo con la escala geográfica en la que se producen? Modelo I: Especiación infecciosa • Wade M.J. (2001) Infectious speciation. Nature 409: 675‐677. • Bordenstein S.R., O’Hara F.P. & Werren J.H. (2001) Wolbachia – induced incompatibility precedes other Irbid incompatibilities in Nasonia. Nature 409: 707‐ 710. 3‐ ¿La especiación infecciosa es un evento especiogénico dirigido por el hospedador o por el parásito? ¿Cuáles serían las implicancias evolutivas de cada caso? 4‐ ¿Considera que la incompatibilidad citoplasmática unidireccional podría conducir al aislamiento reproductivo? 5‐ ¿Cuáles son las diferencias entre el modelo génico y el infeccioso planteado en la figura 2 del trabajo de Wade? 6‐ ¿Cuáles son las hipótesis de trabajo de Bordenstein y colaboradores? Exprese su respuesta en términos de hipótesis nula y alternativa. 7‐ ¿Qué concepto de especie las sustentan? 8‐ Analice la figura 1. A partir de estos resultados obtenidos ¿es posible refutar la hipótesis nula? 9‐ ¿Qué aproximaciones experimentales utilizaron posteriormente los autores para sostener su argumento? ¿Qué tipos de MARs analizaron a través de ellas y cómo incidieron los resultados en las hipótesis de trabajo (i.e. nula y altenativa)? 10‐ ¿Qué crítica podría realizar al sistema bajo estudio? 77
Modelo II: Especiación simpátrica • Linn C., Feder J.L., Nojima S., Dambroski S.H., Berlocher S.H. & Roelofs W (2003) Fruit odor discrimination and sypatric host formaion in Rhagoletis. PNAS 100: 11490‐11493. 11‐ ¿Cuáles son los rasgos de Rhagoletis pomonella que la señalan como una especie adecuada para el estudio de la especiación simpátrica? 12‐ Desde el punto de vista aislacionista propugnado por Mayr y Dobzhansky ¿qué tipo de MARs esperaría que tuvieran mayor incidencia en la especiación simpátrica? Señale los supuestos del modelo. 13‐ ¿Qué tipo de estímulo podrían utilizar las razas de R. pomonella para distinguir a su hospedador? Vincule esta respuesta a los supuestos enunciados anteriormente. 14‐ Analice cuidadosamente la figura 1. ¿Qué conclusión extrae ante cada estímulo presentado a las razas bajo estudio? 15‐ ¿Existe consenso entre los resultados obtenidos bajo condiciones de laboratorio y los obtenidos a partir de condiciones naturales? 16‐ ¿La capacidad de discriminación de la especie hospedadora por parte de la raza de la manzana sería una característica derivada o primitiva? ¿Cómo arribaron los investigadores a este resultado? Preguntas unificadoras 17‐ ¿Cómo describiría un modelo de especiación por aislamiento geográfico? Suponiendo que antes de completarse el aislamiento reproductivo se restableciera el flujo génico y que los grupos previamente aislados produjeran una F1... ¿qué ocurriría si esa F1 tuviera menor fitness que ambos parentales? ¿Qué pasaría si esa F1 tuviera mayor fitness que sus parentales? 18‐ ¿Considera posible revertir la aparición de los MARs? ¿Por qué? 78
Coyne, J. A. & Orr, H. A. 2004. Speciation. Sinauer, Sunderland, MA. Clasificación
de los mecanismos de aislamiento reproductivo (MARs)
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Ridley, M. 2004. Evolution. 3rd Edition. Blackwell Publishing. Malden, MA.
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PART 4 / Evolution and Diversity
14.1 How can one species split into two reproductively
isolated groups of organisms?
Reproductive isolation is the main
topic in research on speciation
The crucial event for the origin of a new species is reproductive isolation. As we saw in
Chapter 13, the members of a species usually differ genetically, ecologically, and in their
behavior and morphology (that is, phenetically) from other species, as well as in who
they will interbreed with. Some biologists prefer to define species not by reproductive
isolation but by other properties, such as genetic or ecological differences. Probably no
single property can provide a universal species definition, applicable to all animals,
plants, and microorganisms. However, many species do differ by being reproductively
isolated, and even if the evolution of reproductive isolation is not always the crucial
event in speciation, it is certainly the key event in research on speciation. The topic of
this chapter is the evolution of reproductive isolation. The aim is to understand how a
barrier to interbreeding can evolve between two populations, such that one species
evolves into two.
Reproductive isolation can be caused by many features of organisms (see Table 13.1,
p. 356). However, for most of the research in this chapter, we only need a distinction
between prezygotic and postzygotic isolation. Prezygotic isolation exists when, for
instance, two species have different courtship or mate choices, or different breeding
seasons. Postzygotic isolation exists when two species do interbreed, but their hybrid
offspring have low viability or fertility. Some of the theories of speciation apply only to
prezygotic isolation, some only to postzygotic isolation, and some to both.
14.2 A newly evolving species could theoretically have an
allopatric, parapatric, or sympatric geographic relation
with its ancestor
Speciating populations can have
various kinds of geographic
relations
We can start with a distinction between different geographic conditions in the speciating populations. If a new species evolves in geographic isolation from its ancestor, the
process is called allopatric speciation. If the new species evolves in a geographically contiguous population, it is called parapatric speciation. If the new species evolves within
the geographic range of its ancestor, it is called sympatric speciation (Figure 14.1). The
distinctions between these three kinds of speciation can blur, but we shall begin the
chapter with the most important of the three processes: allopatric speciation. Almost
all biologists accept that allopatric speciation occurs. The importance of parapatric and
sympatric speciation are more in doubt, and we shall come on to them later.
In allopatric speciation, new species evolve when one (or more) population of a
species becomes separated from the other populations of the species, in the manner of
Figure 14.1a. This kind of event often happens in nature. For example, a species could
split into two separate populations if a physical barrier divided its geographic range.
The barrier could be something like a new mountain range, or river, cutting through
the formerly continuous population. Or the intermediate populations of a species
may be driven extinct, perhaps by a local disease outbreak, leaving the geographically
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CHAPTER 14 / Speciation
383
Space
(a)
Time
(b)
Figure 14.1
Three main theoretical types of speciation can be distinguished
according to the geographic relations of the ancestral species
and the newly evolving species. (a) In allopatric speciation the
new species forms geographically apart from its ancestor;
(b) in parapatric speciation the new species forms in a contiguous
population; and (c) in sympatric speciation a new species emerges
from within the geographic range of its ancestor.
(c)
Geographic separation alone is not
reproductive isolation
extreme populations cut off from each other. Or a subpopulation may migrate (actively
or passively) to a new place, outside the range of the ancestral species, such as when a
few individuals colonize an island away from the mainland. Such a population, at the
edge of the main range of a species, is called a “peripheral isolate.”
One way or another, a species can become geographically subdivided, consisting of a
number of populations between which gene flow has been cut off. This is not, in itself,
an isolating barrier in the sense of Table 13.1 (p. 356). An isolating barrier is an evolved
property of a species that prevents interbreeding. When two populations are geographically cut off, gene flow ceases but only because members of the population do not
meet. The two populations have not yet evolved a genetic difference. The evolution of
an isolating barrier requires some new character, such as a new courtship song, to
evolve in at least one of the populations a a new character that has the effect of preventing gene flow. In the theory of allopatric speciation, the cessation of gene flow between
allopatric populations leads, over time, to the evolution of intrinsic isolating barriers
between the populations. Let us see what happens to the reproductive isolation
between these populations over evolutionary time.
14.3 Reproductive isolation can evolve as a by-product of
divergence in allopatric populations
We have two main kinds of evidence that reproductive isolation evolves when
geographically separate populations are evolving apart. One comes from laboratory
experiments and the other comes from biogeographic observations.
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Reinforcement works in sympatry
409
populations. Within one population, natural selection will not favor a genetic change
that is incompatible with genes at other loci.
Prezygotic isolation, however, does not require incompatible genetic change at several loci. Prezygotic isolation can evolve as a by-product of divergence if the characters
that have diverged between populations are genetically correlated with characters causing prezygotic isolation. This theory is less strongly tied to the theory of allopatric speciation. The process can indeed occur between populations that are separately evolving
in different places. But adaptive divergence can also occur within one population, as we
shall see, and that at least raises the possibility that speciation could occur nonallopatrically.
The other theory was reinforcement. Reinforcement only occurs in sympatry.
Natural selection only favors discrimination among potential mates for the range of
mates that are present in a particular place. The theory of reinforcement is only weakly
tied to the theory of allopatric speciation. Indeed, it is hardly an allopatric theory of
speciation at all. Reinforcement was only used in the allopatric theory to “finish off ”
speciation that was incomplete in allopatry.
Thus, in the theories we have met so far, speciation in non-allopatric populations
is relatively unlikely. One well supported theory, the Dobzhansky–Muller theory, is
allopatric. Reinforcement is a sympatric process, but (as we saw) little supported by
evidence and problematic in theory. However, non-allopatric speciation has not been
ruled out, and in the next two sections we shall look some more at whether speciation
could occur parapatrically or sympatrically.
14.9 Parapatric speciation
14.9.1
European crows provide an
example of a hybrid zone
Parapatric speciation begins with the evolution of a
stepped cline
In parapatric speciation, the new species evolve from contiguous populations, rather
than completely separate ones, as in allopatric speciation (see Figure 14.1). The full
process could occur as follows. Initially, one species is distributed in space. The species
evolves a “stepped cline” pattern of geographic variation (Section 13.4.3, p. 363). The
stepped cline could exist because of an abrupt environmental change: one form of the
species would be adapted to the conditions on one side of the boundary, the other form
to the conditions on the other side of the boundary.
A hybrid zone is a stepped cline in which the forms on either side of the boundary are
sufficiently different that they can easily be recognized. The two forms may have been
given different taxonomic names, as subspecies or races, or they may be different
enough to have been classified as separate species.
The carrion crow (Corvus corone) and hooded crow (C. cornix) in Europe are a
classic example of species round a hybrid zone (Figure 14.13). The hooded crow is
distributed more to the east, the carrion crow to the west, with the two species meeting along a line in central Europe. At that line a the hybrid zone a they interbreed and
produce hybrids. The hybrid zone for the crows was first recognized phenotypically,
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410
C. cornix
C. corone
Figure 14.13
Hybrid zone between the carrion crow (Cornix corone) and
hooded crow (C. cornix) in Europe. Here the two crows are
shown as two separate species, but some taxonomists classify
them as subspecies. Redrawn, by permission of the publisher,
from Mayr (1963). © 1963 President and Fellows of Harvard
College.
Many hybrid zones are tension
zones . . .
. . . in which reinforcement may
operate
because the hooded crow is gray with a black head and tail, whereas the carrion crow is
black all over. The two species (or near species) are now known to differ in many other
respects too. The fact that the crows interbreed in the hybrid zone means that speciation between them is incomplete. We shall meet some more examples of hybrid zones
in Section 17.4 (p. 497).
The conditions in a hybrid zone (or a stepped cline) are particularly ripe for
speciation if it is a tension zone. A tension zone exists when the hybrids between the
forms on either side of the boundary are selectively disadvantageous. (A hybrid zone
is not a tension zone if the hybrids have intermediate, or superior, fitness to the
pure forms.) For instance, if one homozygote (AA) is adapted to one environment,
and another homozygote (aa) to another environment, heterozygotes (Aa) will be
produced where the two environments meet up. If the heterozygotes are disadvantageous, the meeting place is an example of a tension zone. Most known hybrid zones
are in fact tension zones (see, for example, Barton & Hewitt’s (1985) review of
170 hybrid zones).
In a tension zone, the conditions are exactly the preconditions for reinforcement
(Section 14.6.1). Matings within a type are advantageous, and matings between types
produce disadvantageous hybrids. Natural selection favors assortative mating. We can
therefore imagine a sequence where a stepped cline initially evolves, and then becomes
distinct enough to count as a hybrid zone. We are near the border of the origin of a new
species. Reinforcement could then finish speciation off, eliminating hybridization
from the hybrid zone. That sequence of events constitutes parapatric speciation.
The strong point of the theory of parapatric speciation is that the environment
“stabilizes” the preconditions for reinforcement. We saw that these conditions are
liable to autodestruct, as the two forms interbreed, or as one eliminates the other. But
if the environment varies in space, the clinal variation will be maintained. Parapatric
speciation could work, in theory.
83
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14.9.2
Most hybrid zones are due to
secondary contact
411
Evidence for the theory of parapatric speciation is
relatively weak
The theory of parapatric speciation has two main weak points in the evidence. One is
the evolutionary history of hybrid zones. Hybrid zones can be “primary” or “secondary.” A hybrid zone is primary if it evolved while the species had approximately
their current geographic distribution. It is secondary if in the past the species was subdivided into separate populations, where the differences between the forms evolved,
and the populations later expanded and met up at what is now the hybrid zone. Real
hybrid zones only illustrate a stage in parapatric speciation if they are primary. The
abundance of hybrid zones in nature would only be evidence that parapatric speciation
is a plausible process if those hybrid zones are mainly primary. If most hybrid zones are
secondary, the difference between the forms evolved allopatrically not parapatrically.
In fact the evidence suggests that most hybrid zones are secondary. Hooded and carrion
crows, for instance, have met up after their ranges expanded following the most recent
ice age. Indeed, range expansion following the ice age is a common explanation of
hybrid zones (Section 17.4, p. 497). Hybrid zones provide little support for the theory
of parapatric speciation.
Secondly, if reinforcement operates in hybrid zones, we predict that prezygotic
isolation will be stronger in the hybrid zone than between the two forms away from
the hybrid zone. The prediction is a special case of the general biogeographic test of
reinforcement (Section 14.6.3). The evidence does not support the prediction: we have
little good evidence that prezygotic isolation is reinforced in hybrid zones.
Thus, the process of parapatric speciation is possible in theory. The theory solves one
key problem in reinforcement. Most (but not all) stages of parapatric speciation can be
illustrated by evidence. But parapatric speciation lacks the solid weight of supporting
evidence and the theoretical near inevitability of allopatric speciation. Parapatric speciation cannot be ruled out, and probably operates in some cases. But the case that it is
important has still to be made.
14.10 Sympatric speciation
14.10.1 Sympatric speciation is theoretically possible
In sympatric speciation, a species splits into two without any separation of the ancestral
species’ geographic range (see Figure 14.1). Sympatric speciation has been a source of
recurrent controversy for a century or so. Mayr (1942, 1963) particularly cast doubt on
it, and in doing so has stimulated others to look for evidence and to work out the theoretical conditions under which it may be possible.
In the theory of parapatric speciation, the initial stage in speciation is a spatial
polymorphism (or stepped cline). In sympatric speciation, the initial stage is a polymorphism that does not depend on space within a population. For instance, two forms
of a species may be adapted to eat different foods. If matings between the two are disadvantageous, because hybrids have low fitness, reinforcement will operate between
84
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412
them. Most models of sympatric speciation suppose that natural selection initially
establishes a polymorphism, and then selection favors prezygotic isolation between
the polymorphic forms. “Host shifts” in a fly called Rhagoletis pomonella provide a case
study that may illustrate part of the process.
14.10.2 Phytophagous insects may split sympatrically by host shifts
The apple maggot fly has only
recently moved on to apples
The races on apples show some
isolation from the ancestral races
on hawthorn
But the example is incomplete
Rhagoletis pomonella is a tephritid fly and a pest of apples. It lays its eggs in apples
and the maggot then ruins the fruit, but this was not always so. In North America,
R. pomonella’s native larval resource is the hawthorn. Only in 1864 were these species
first found on apples. Since then it has expanded through the orchards of North
America, and has also started to exploit cherries, pears, and roses. These moves to new
food plants are called host shifts. In the host shift of R. pomonella, speciation may be
happening before our eyes.
The R. pomonella on the different hosts are currently different genetic races. Females
prefer to lay their eggs in the kind of fruit they grew up in: females isolated as they
emerge from apples will later choose to lay eggs in apples, given a choice in the laboratory. Likewise, adult males tend to wait on the host species that they grew up in, and
mating takes place on the fruit before the females oviposit. Thus there is assortative
mating: male flies from apples mate with females from apples, males from hawthorn
with females from hawthorn.
The races are presumably about 140 generations old (given that they first moved on
to apples nearly one and a half centuries ago). Is this long enough for genetic differences
between the races to have built up? Gel electrophoresis shows that the two races have
evolved extensive differences in their enzymes. They also differ genetically in their
development time: maggots in apples develop in about 40 days, whereas hawthorn
maggots develop in 55–60 days. This difference also acts to increase the reproductive
isolation between the races, because the adults of the two races are not active at the
same time.
Apples and hawthorns differ and selection will therefore probably favor different
characters in each race; this may be the reason for their divergence. If it is, selection may
also favor prezygotic isolation and speciation. If flies from the different races are put
together in the lab, however, they mate together indiscriminately. Either reinforcement
has not operated when it might have been expected, or, alternatively, the differences in
behavior and development time in the field may be enough to reduce interbreeding
to the level natural selection favors. Selection would then not be acting to reinforce
the degree of prezygotic isolation. We do not know which interpretation is correct;
we need to know more about the forces maintaining the genetic differences between
the races. Once again, the evidence for reinforcement is the weak point in a theory of
speciation.
In the case of host shifts, we can be practically certain that the initial host shift, and
formation of a new race, has happened in sympatry. The shift took place in historic
time. However, it is not a full example of sympatric speciation because the races have
not fully speciated. Indeed, we do not know whether they will, or whether the current
situation, with incomplete speciation, is stable.
85
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news and views
the relative production of thorium to uranium because these elements are separated by
only two atomic numbers. And the different
decay rates of 232Th and 238U ensure that the
abundance ratio of these two elements will
be a sensitive function of their age. Cayrel et
al.1 propose that the neutron-capture material in the atmosphere of CS31082-001 has
an age of 12.5 Gyr with an uncertainty of 3.3
Gyr, a more accurate estimate of the age of
the Universe. Further analysis of the whole
range of neutron-capture elements in this
star will refine this age estimate, narrowing
the uncertainty.
We now know of a handful of stars born
early in our Galaxy’s history that are anomalously enriched in radioactive thorium, and
at least one with uranium. We may expect
to find more examples of such stars, as our
surveys of the Galactic halo with the new
generation of very large telescopes is just
beginning. With new discoveries, more age
estimates will be found, further nailing down
the exact age of the Universe.
■
Christopher Sneden is in the Department of
Astronomy, University of Texas at Austin, Austin,
Texas 78712, USA.
1. Cayrel, R. et al. Nature 409, 691–692 (2001).
2. Chaboyer, B. Phys. Rep. 307, 23–30 (1998).
3. Beers, T. C., Preston, G. W. & Schectman, S. Astron. J. 103,
1987–2034 (1992).
4. Butcher, H. R. Nature 328, 127–131 (1987).
5. Sneden, C. et al. Astrophys. J. 533, L139–L142 (2000).
6. Westin, J., Sneden, C., Gustafsson, B. & Cowan, J. J. Astrophys. J.
530, 783–799 (2000).
7. Cowan, J. J. et al. Astrophys. J. 521, 194–205 (1999).
8. Goriely, S. & Clerbaux, B. Astron. Astrophys. 346, 798–804 (1999).
Evolution
Infectious speciation
Michael J. Wade
The bacterium Wolbachia has strange and wonderful effects on
reproduction in its many invertebrate host species. In effect, the creation
of new species can now be added to the list.
or a new species to arise, a single population must somehow be split into two
reproductively isolated populations
that cannot interbreed. Such reproductive
isolation usually stems from genetic incompatibility. It is easy to see how that arises
when a geographical barrier divides one
population of an organism into two, which
then diverge genetically. On page 707 of this
issue, however, Bordenstein, O’Hara and
Werren1 show that in two species of parasitoid wasp it is microbial infection that is the
barrier to gene exchange.
The microbe concerned, Wolbachia pipientis, is a member of a highly diverse group of
bacteria that is thought to include the ancestor of the mitochondrion — the powerhouse
of multicellular organisms that was originally
free-living. Wolbachia are endosymbionts,
living inside the cells of certain host organisms, and like mitochondria they are almost
always inherited through the maternal line.
Their host range is broad, for the bacteria are
found in association with about 20–75% of
the insects, crustaceans, mites and nematode
worms that have been surveyed with molecular markers2,3. Such is the range of effects
of the microbe on its host — positive and
negative — that it is not always possible to
characterize Wolbachia simply as a mutualist, symbiont or pathogen.
Among the variety of reproductive
anomalies caused by Wolbachia is the
phenomenon of cytoplasmic incompatibility (Fig. 1), which results in the failure
of infected host males and uninfected host
females to produce offspring. Wolbachia
F
NATURE | VOL 409 | 8 FEBRUARY 2001 | www.nature.com
Females
Males
W+
W-
No
offspring
X
W-
X
Offspring
W+
Offspring
X
W+
W-
W+
Offspring
X
W-
Figure 1 Wolbachia and cytoplasmic
incompatibility. Cytoplasmic incompatibility
means that when a male host infected with
Wolbachia (W& ) mates with an uninfected
female (W1 ), no offspring are produced. All
other matings are fully compatible and result in
the production of offspring. The consequence
of this system is that the maternally transmitted
Wolbachia tend to spread through the host
species.
residing in host males are not typically
transmitted to offspring, but they eliminate
competing uninfected maternal lineages
from the host population by their incompat© 2001 Macmillan Magazines Ltd
86
100 YEARS AGO
Dr. R. A. Daly, of the Department of Geology
and Geography of Harvard University, is
endeavouring to organise a geological and
geographical excursion in the North Atlantic
for the summer of 1901. Conditionally on the
formation of a sufficiently large party, a
steamer of about 1000 tons, specially
adapted for ice navigation, and capable of
accommodating sixty persons, will leave
Boston on or about June 26… The main object
of the voyage will be to offer to the members
of the excursion party opportunity of studying
the volcanic cones and lava-fields, the
geysers, ice-caves and glaciers of Iceland,
the fiords and glaciers of the west coast of
Greenland, and the mountains and fiords of
Northern Labrador… A hunting party may
take part in the expedition; it could be landed
for a fortnight or three weeks in Greenland
and for about the same period in Labrador.
From Nature 7 February 1901.
50 YEARS AGO
Surprisingly little of the information obtained
with microscopes has been quantitative; most
observers are content to sit at the microscope
and regard the image, or to photograph it.
Theoretically, it is possible to scan the image
or its photograph mechanically; but this has
seldom been done in practice. The whole
method of obtaining resolution by lenses
involves so much loss of light, lack of control
of contrast, and other difficulties, that it is
difficult to provide a good display or method
of scanning. Some of these difficulties can be
avoided by using a wholly different means of
obtaining resolution and amplification. The
essence of the problem of resolution is to
separate in some way the light passing
through very close regions of an object. The
conventional microscope does this by using
refraction by lenses to separate the light
from neighbouring regions. An alternative
method is to use the lens system the other
way round, namely, to produce a minute
spot of light. Discrimination between
neighbouring points is then produced by
passing the light through them at different
times by making the spot scan it. After
passing through the preparation, the spot is
made to fall on a photocell, with subsequent
amplifcation and display as required. Such a
flying-spot microscope depends on scanning
different parts at different times, and will
only give accurate information about objects
that are stationary or moving only at a rate of
a different order from that of the spot.
From Nature 10 February 1951.
675
news and views
ible matings. So the bacteria in males are
essential to the spread of their maternally
transmitted relatives through the host
population.
Typical cytoplasmic incompatibility falls
short of speciation because the barrier to
reproduction between infected and uninfected populations works only in one direction, not reciprocally. Although females
of the uninfected host population cannot
interbreed with males of the infected host
population, the reciprocal cross is fully
fertile. But there is evidence4,5 that different
genetic strains of Wolbachia can cause
reciprocal, two-way reproductive isolation
between host populations in some parasitoid
wasps, mosquitoes and fruit flies6. This
observation has led some evolutionary biologists to speculate that Wolbachia might
be an agent of infectious speciation6,7.
Such speculation is controversial, for two
reasons. First, it is widely accepted that,
when two host populations become reproductively isolated, so do the populations of
their respective endosymbionts. Hence, in a
process called co-speciation, a host may
cause subsequent speciation of its endosymbionts, an explanation suggested for the
genetic divergence of strains of Wolbachia8.
The hypothesis of infectious speciation
turns this view on its head. Second, so the
theory goes, speciation occurs when reproductive isolation arises as the incidental
by-product of the gradualistic, genetic
divergence of two populations. Microbial
speciation, in contrast, might be comparatively rapid (as seen for instance in polyploid
or hybrid speciation in some plants9), and
could occur without any genetic evolution
of the host. Polyploid speciation occurs
through a doubling, or more, of chromosome number.
Bordenstein and colleagues1 provide evidence that microbes have acted faster than
genes in producing reproductive isolation
between the wasps Nasonia giraulti and N.
longicornis; this can be taken as the first stage
of speciation. First, the authors showed that
each wasp harbours a genetically distinct
strain of Wolbachia that causes cytoplasmic
incompatibility with the other uninfected
host species. They then used antibiotics to
create an uninfected strain of each host
species and demonstrated that in Wolbachiafree wasps there are no genetic barriers in
first- or second-generation hybrids to free
interbreeding between the two wasps.
How might these findings fit into a standard genetic model of speciation, as shown
in Fig. 2a? In this model, incompatible gene
combinations (such as A1B1) cause sterility
or inviability of offspring, and so speciation.
Events begin with an ancestral species,
A0A0B0B0, that becomes split by geological
events into two geographically isolated
daughter populations. The evolutionary
forces of mutation, random genetic drift
676
a
Ancestral
population
Geographically
isolated
daughter
populations
Different
mutations
become fixed
in the genomes
A 0 A 0 B0 B0
A 0 A 0 B0 B0
A 0 A 0 B0 B0
A 1 A 1 B0 B0
A 0 A 0 B1 B1
Reproductive
isolation and
speciation because
of the incompatible
gene combination A1B1
Mating results
in inviable or
infertile hybrids
b
Uninfected (W-)
ancestral
population
Geographically
isolated
daughter
populations
Independent
infection and
spread of
Wolbachia
Reproductive
isolation due to
Wolbachia
infection
A 0 A 0 B0 B0
WA 0 A 0 B0 B0
W-
A 0 A 0 B0 B0
W-
A 0 A 0 B0 B0
WA
A 0 A 0 B0 B0
WB
Reciprocal
incompatibility
and natural selection operate independently
on each daughter population. Eventually,
one gene undergoes mutation to allele A1,
and becomes fixed in one daughter population, while a second mutation, to allele B1
at the other gene, becomes fixed in the second daughter population. The two daughter
populations become reproductively isolated
because matings between them result in the
A1B1 deleterious gene combination. In this
classic model, genetic barriers to reproduction and genetic exchange, and so speciation, arise as a by-product of local, gradual
evolution.
Microbially driven speciation could
occur in much the same way, stemming from
cytoplasmic incompatibility between two
different strains of Wolbachia infecting the
same host species (Fig. 2b). Here, however,
infectious transmission of incompatible
Wolbachia strains, one in each daughter population, replaces the incompatible gene
combinations. Predatory mites and parasitoid wasps are the most likely candidates
for spreading Wolbachia between different
species of host. Previous cases of reciprocal
cytoplasmic incompatibility have been
between species pairs, which also exhibited
evidence of genetic barriers to gene
exchange. Whenever both are present, it is
difficult to determine which — the incompatible gene combinations or the microbes
— came first. The report by Bordenstein
et al. provides evidence that, at least in this
case, microbially induced reproductive isolation preceded genetic isolation.
© 2001 Macmillan Magazines Ltd
87
Figure 2 Genetic and infectious models of
speciation. a, A standard genetic model in which
the initial state is an ancestral population of a
species that is homozygous at both of two gene
loci, and so is A0A0B0B0. Following geographical
isolation, each of two daughter populations is
gradually modified as new alleles (A1 and B1)
arise by mutation and then become fixed in the
genome by random genetic drift and natural
selection. Because the A1B1 gene combination
causes complete inviability or sterility in
hybrids, the daughter populations are new,
descendant species. b, Infectious speciation,
which parallels the genetic model. The initial
state is an ancestral species, W1 , not infected
with Wolbachia. Two daughter populations
arise which have become infected by different
strains of Wolbachia (A and B) after
transmission from a parasite or parasitoid. The
different strains then become fixed in each
genome by cytoplasmic incompatibility.
Reciprocal cytoplasmic incompatibility between
WA males and WB females, and WB males and WA
females, prevents hybridization, so in effect the
daughter populations are new species even
though they remain genetically identical to one
another and to the ancestor.
How common might infectious speciation be? It is not possible to draw a conclusion from this single example — which
has of course to be contrasted with the many
examples of genetic speciation10. But there
are several reasons why it is unlikely to
happen often. First, incomplete cytoplasmic
incompatibility (where incompatible crosses produce some progeny instead of none)
seems to be more common than complete
cytoplasmic incompatibility. Reciprocal but
incomplete incompatibility is not a barrier
to gene flow. Second, genetic models of
Wolbachia–host coevolution indicate that
the favoured trajectory is from complete
to incomplete cytoplasmic incompatibility.
Finally, we know little of the initial stages of
Wolbachia infection in natural populations.
When artificially introduced into new hosts,
Wolbachia can be difficult to transmit11.
So the experimental results are consistent
with the scheme outlined in Fig. 2b, but may
not reflect the actual historical sequence
of events.
Nevertheless, with the paper by Bordenstein et al., host speciation can now be
added to the list of modifications to reproduction caused by Wolbachia infection.
Given the ubiquity of Wolbachia, infectious
barriers to gene exchange may be much
more common in the early stages of speciation than we realize.
■
Michael J. Wade is in the Department of Biology,
Indiana University, Bloomington, Indiana 47405,
USA.
news and views
1. Bordenstein, S. R., O’Hara, F. P. & Werren, J. H. Nature 409,
707–710 (2001).
2. Werren, J. H., Windsor, D. & Gao, L. Proc. R. Soc. Lond. B 262,
197–204 (1995).
3. Jeyaprakash, A. & Hoy, M. A. Insect Mol. Biol. 9, 393–405 (2000).
4. Wade, M. J., Chang, N. W. & McNaughton, M. Heredity 75,
453–459 (1995).
5. Shoemaker, D. D., Katju, V. & Jaenike, J. Evolution 53,
1157–1164 (1999).
6. Hurst, G. D. D. & Schilthuizen, M. Heredity 80, 2–8 (1998).
7. Thompson, J. N. Biol. J. Linn. Soc. 32, 385–393 (1987).
8. Futuyma, D. J. Evolutionary Biology 541 (Sinauer, Sunderland,
MA, 1998).
9. Reiseberg, L. H. Annu. Rev. Ecol. Syst. 28, 359–389 (1997).
10. Wu, C. I. & Palopoli, M. F. Annu. Rev. Genet. 28, 283–308
(1994).
11. Clancy D. J. & Hoffmann, A. A. Am. Nat. 149, 975–988
(1997).
Astronomy
The day the solar wind nearly died
Mike Lockwood
On 11 May 1999, the density of the solar wind dropped almost to zero.
Space scientists are now giving their first reports of this rare opportunity to
study the complex relationship between the Sun and Earth.
he study of space is generally passive, as
the input factors to an environment
cannot be adjusted in a controlled manner to study one isolated mechanism, as they
can in a laboratory. Instead scientists have to
monitor all the inputs and try to disentangle
the various effects that are taking place
simultaneously. For instance, the Sun emits a
continuous stream of ionized gas (containing mostly protons and electrons) called the
T
solar wind, which varies in concentration,
flux, speed, temperature and composition.
All of these factors affect the magnetosphere
— the cavity formed by the Earth’s magnetic
field in the solar wind — and separating their
various effects is difficult. This is why rare
events such as the one centred around 11
May 1999 are so valuable. In this period, the
solar wind remained completely normal
except that its density plummeted to 5% of
a
Strahl
IMF field lines
from the Sun
Open
field lines
(XLN)
XS
To Sun
Closed
field lines
Tail
Magnetosphere
Solar
wind
Open
field lines
Cusp
Bow shock
Magnetopause
Field lines to outer
heliosphere
b
XLN
(XS)
Open field lines
Closed field line
Magnetosphere
To Sun
Tail
Solar
wind
typical values. The first studies from this
period are now published in a special issue of
Geophysical Research Letters1.
When the density dropped, many aspects
of the magnetosphere’s behaviour were as
scientists had predicted, which was a satisfying triumph for current theories. But the
event also had some puzzling characteristics.
Some of these are apparent in the data presented in these initial papers, although not
all are commented on. Others aspects are so
intriguing that further study is required.
Earth’s magnetic field is confined to the
low-density, high-field magnetosphere by
the dynamic pressure of the solar wind on the
side of the Earth facing the Sun, and by thermal pressure on the long tail that trails away
from the Sun (Fig. 1). Both these pressures
depend on the concentration of the solar
wind, so the magnetosphere grew to exceptionally large dimensions (100 times its typical volume) as the solar wind decayed.
Another feature was the appearance of highly energetic flows of electrons parallel to the
direction of the magnetic field in the vicinity
of Earth. These so-called ‘strahl’ electrons
(red arrows in Fig. 1) are continuously emitted by the Sun but their flow is usually disrupted by the solar wind, making their fluxes
Figure 1 Earth’s magnetosphere and the solar
wind. a and b show two possible ways in which
the interplanetary magnetic field (IMF) can
interconnect with Earth’s magnetospheric field.
a, New open field lines (red lines) are produced
at a reconnection site XS and solar wind energy is
directly deposited in the inner magnetosphere
and upper atmosphere, as well as being stored in
the tail of the magnetosphere because open field
lines accumulate there. b, Field lines that are
already open are reconfigured by reconnection
at XLN, in this example in the Northern
Hemisphere. In this instance, solar-wind energy
is not added to the tail because no new open flux
is produced. Closed field lines are shown in blue;
unconnected IMF lines are yellow; strahl
electrons are represented by red arrows. The
magnetopause is the boundary between the
magnetosphere and the solar wind, and the bow
shock is the edge where the supersonic solar
wind abruptly drops in velocity. The solar wind
behind the bow shock (dark blue) is denser than
the incoming solar wind (medium blue),
whereas the magnetosphere (grey) is the least
dense of the three regions. A study of Earth’s
magnetosphere during a period of exceptionally
low solar-wind flux promises to explain the
complex interplay between these
two situations1.
Overdraped
open field line
88
677
letters to nature
for the separation of the moa, which was consistent with the estimated emu/cassowary
split at 30±35 Myr. The analysis was a simple extension of a described method29 to allow
more than four taxa. The assumption of rate constancy among the ratites was tested using
a likelihood ratio test of the molecular clock model30. With a likelihood ratio of 12.68, rate
constancy can be rejected (P , 0.01). However, Fig. 2 suggests that the ostrich may have an
elevated rate of substitution, so the test was repeated with the ostrich allowed a different
rate from those of other ratites. The resulting likelihood ratio of 0.449 (P = 0.92) shows
that this two-rate model is consistent with clock-like behaviour. The two-rate model has
little effect on the divergence estimates (Table 2), with ostrich dates becoming younger by
5% of the largest change.
Received 12 July; accepted 26 October 2000.
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2. Sibley, C. G. & Ahlquist, J. E. Phylogeny and Classi®cation of Birds (Yale Univ. Press, London, 1990).
3. Cooper, A. et al. Independent origins of the New Zealand moas and kiwis. Proc. Natl Acad. Sci. USA
89, 8741±8744 (1992).
4. Cooper, A. & Penny, D. Mass survival of birds across the Cretaceous±Tertiary: Molecular evidence.
Science 275, 1109±1113 (1997).
5. Feduccia, A. The Origin and Evolution of Birds (Harvard Univ. Press, Cambridge, Massachusetts, 1997).
6. Van Tuinen, M., Sibley, C. & Hedges, S. B. Phylogeny and biogeography of ratite birds inferred from
DNA sequences of the mitochondrial ribosomal genes. Mol. Biol. Evol. 15, 370±376 (1998).
7. Olson, S. L. in Avian Biology Vol. VIII (eds Farner, D. S., King, J. R. & Parkes, K. C.) 79±238 (Academic,
Orlando, 1985).
8. Lee, K., Feinstein, J. & Cracraft, J. in Avian Molecular Evolution and Molecular Systematics (ed. Mindell,
D.) 173±208 (Academic, New York, 1997).
9. Houde, P. Ostrich ancestors found in the Northern Hemisphere suggest new hypothesis of ratite
origins. Nature 324, 563±565 (1986).
10. Bledsoe, A. H. A phylogenetic analysis of postcranial skeletal characters of the ratite birds. Ann.
Carnegie Mus. 57, 73±90 (1988).
11. Cooper, A. in Avian Molecular Evolution and Molecular Systematics (ed. Mindell, D.) 345±373
(Academic, New York, 1997).
12. Handt, O., Krings, M., Ward, R. H. & PaÈaÈbo, S. The retrieval of ancient human DNA sequences. Am. J.
Hum. Genet. 59, 368±376 (1996).
13. Krings, M. et al. Neandertal DNA sequence and the origin of modern humans. Cell 90, 19±30 (1997).
14. Cooper, A. in Ancient DNA (eds Herrmann, B. & Hummel, S.) 149±165 (Springer, New York, 1993).
15. Boles, W. E. Hindlimb proportions and locomotion of Emuarius gidju (Patterson & Rich, 1987) (Aves:
Casuariidae). Memoirs of the Queensland Museum 41, 235±240 (1997).
16. Lawver, L. A., Royer, J-Y., Sandwell, D. T. & Scotese, C. R. in Geological Evolution of Antarctica (eds
Thomson, M. R. A., Crame, J. A. & Thomson, J. W.) 533±539 (Cambridge Univ. Press, Cambridge,
1991).
17. Cooper, R. A. & Millener, P. R. The New Zealand biota: Historical background and new research.
Trends Ecol. Evol. 8, 429±433 (1993).
18. Fleming, C. A. The Geological History of New Zealand and its Life (Univ. Auckland Press, Auckland,
1979).
19. Stevens, G. R. Lands in collision. N. Z. Dept Sci. Ind. Res. Inf. Serv. 161 (1985).
20. Storch, G. in The Africa±South America Connection (eds George, W. & Lavocat, R.) 76±86 (Clarendon,
Oxford, 1993).
21. Martin, P. G. & Dowd, J. M. Using sequences of rbcL to study phylogeny and biogeography of
Nothofagus species. Aust. Syst. Bot. 6, 441±447 (1993).
22. Herzer, R. et al. Reinga Basin and its margins. N. Z. J. Geol. Geophys. 40, 425±451 (1997).
23. Sauer, E. G. F. Ratite eggshells and phylogenetic questions. Bonn Zool. Beitr. 23, 3±48 (1972).
24. Krause, D. W., Prasad, G. V. R., von Koenigswald, W., Sahni, A. & Grine, F. E. Cosmopolitanism
among Gondwanan Late Cretaceous mammals. Nature 390, 504±507 (1997).
25. Sampson, S. D. et al. Predatory dinosaur remains from Madagascar: Implications for the Cretaceous
biogeography of Gondwana. Science, 280, 1048±1051 (1998).
26. Cooper, A. & Poinar, H. Ancient DNA: Do it right or not at all. Science 289, 1139 (2000).
27. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) (Sinauer,
Sunderland, Massachusetts, 1999).
28. Huelsenbeck, J. P., Hillis, D. M. & Jones R. in Molecular Zoology: Strategies and Protocols (eds Ferraris,
J. & Palumbi, S.) 19±45 (Wiley, New York, 1996).
29. Rambaut, A. & Bromham, L. Estimating divergence dates from molecular sequences. Mol. Biol. Evol.
15, 442±448 (1998).
30. Felsenstein, J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol.
17, 368±376 (1981).
Supplementary information, including clone and primer sequences is
available on Nature's World-Wide Web site (http://www.nature.com), or on
http://evolve.zoo.ox.ac.uk/data/Ratites/, or as paper copy from the London editorial of®ce
of Nature.
Acknowledgements
We thank W. Boles, R. Cooper, R. Herzer, P. Houde, C. Mourer-ChauvireÂ, D. Penny and
T. Worthy for valuable comments, and M. Sorenson for allowing us access to unpublished
rhea and ostrich sequences. We are grateful to T. Worthy and the staff of the Museum of
New Zealand for the moa samples. Modern samples were kindly provided by A. C. Wilson
(deceased), M. Potter and M. Braun, and laboratory space by R. Thomas, J. Bertranpetit
and the Oxford University Museum. A.C. was supported by the NERC, the Leverhulme
Fund, the New Zealand Marsden Fund and the Royal Society. C.L.F. was supported by the
Comissionat per a Universitats i Recerca (Catalan Autonomous Government), and A.R.
was supported by the Wellcome Trust.
Correspondence and requests for materials should be addressed to A.C. (e-mail:
[email protected]). Software is available at http://evolve.zoo.ox.ac.uk/software.
89
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Wolbachia-induced incompatibility
precedes other hybrid
incompatibilities in Nasonia
Seth R. Bordenstein, F. Patrick O'Hara & John H. Werren
Department of Biology, The University of Rochester, Rochester, New York 14627,
USA
..............................................................................................................................................
Wolbachia are cytoplasmically inherited bacteria that cause a
number of reproductive alterations in insects, including cytoplasmic incompatibility1,2, an incompatibility between sperm and egg
that results in loss of sperm chromosomes following fertilization.
Wolbachia are estimated to infect 15±20% of all insect species3,
and also are common in arachnids, isopods and nematodes3,4.
Therefore, Wolbachia-induced cytoplasmic incompatibility could
be an important factor promoting rapid speciation in
invertebrates5, although this contention is controversial6,7. Here
we show that high levels of bidirectional cytoplasmic incompatibility between two closely related species of insects (the parasitic
wasps Nasonia giraulti and Nasonia longicornis) preceded the
evolution of other postmating reproductive barriers. The presence of Wolbachia severely reduces the frequency of hybrid
offspring in interspecies crosses. However, antibiotic curing of
the insects results in production of hybrids. Furthermore, F1 and
F2 hybrids are completely viable and fertile, indicating the absence
of F1 and F2 hybrid breakdown. Partial interspeci®c sexual isolation occurs, yet it is asymmetric and incomplete. Our results
indicate that Wolbachia-induced reproductive isolation occurred
in the early stages of speciation in this system, before the evolution of other postmating isolating mechanisms (for example,
hybrid inviability and hybrid sterility).
Symbiotic microorganisms are widespread in nature and often
have intimate associations with their hosts, ranging from mutualistic to parasitic relationships. It has been suggested that these
associations may act as a source of evolutionary innovation for their
hosts, leading to differentiation between host populations and
ultimately to the evolution of new species8. Wolbachia are particularly good candidates for symbiont-induced speciation, because
these bacteria can modify compatibility between eggs and sperm of
hosts, and thus directly cause reproductive isolation without longterm coevolution of the host and symbiont5. There is some empirical evidence for a role of Wolbachia in speciation in mushroomfeeding Drosophila9, the ¯our beetle Tribolium10, and parasitic
wasps11. However, the view that Wolbachia are involved in invertebrate speciation is still controversial5±7. Here we present evidence
that Wolbachia-induced reproductive isolation precedes the evolution of other postmating isolating mechanisms in Nasonia. The
®nding supports the view that Wolbachia can play a role in
reproductive isolation and speciation.
Nasonia is a complex of three closely related species of haplodiploid parasitic wasps. Nasonia vitripennis is found worldwide, and is
a generalist that parasitizes a variety of ¯y species. Nasonia giraulti
occurs in eastern North America and N. longicornis in western
North America, where they parasitize the pupae of blow¯ies in
birds' nests12. Genetic and molecular evidence shows that N. giraulti
and N. longicornis are more closely related sister species. Estimates
place the divergence of these two species at around 0.250 Myr ago
and their divergence from N. vitripennis at around 0.800 Myr13.
All three species are infected with Wolbachia, and individuals of
each species are typically infected with two different bacterial types,
each belonging to the two major subgroups of arthropod Wolbachia
(A and B)14. Furthermore, phylogenetic analysis (data not shown)
indicates that the A group bacteria of each species are not closely
707
letters to nature
708
their own species or males of the other species (N. giraulti female ´
N. giraulti male, 100.2 6 5.6 versus N. giraulti female ´ N. longicornis
male, 99.0 6 4.0; and N. longicornis female ´ N. longicornis
male, 68.5 6 4.1 versus N. longicornis female ´ N. giraulti male,
78.5 6 4.8). As only females are hybrids in a haplodiploid insect, we
also compared the number of female offspring produced in intraand interspeci®c crosses (Fig. 1). There was no reduction in the
number of F1 hybrid females relative to intraspeci®c controls.
Finally, we compared the number of eggs laid during a 6-h
oviposition period to the number of adult offspring emerging in
hybrid crosses. No signi®cant differences were found (N. giraulti
female ´ N. longicornis male, 22.5 6 6.4 eggs versus 20.7 6 7.1
adults; reciprocal cross, 25.0 6 9.2 eggs versus 24.3 6 3.2 adults).
Therefore, results clearly indicate that there is no signi®cant F1
hybrid inviability. They also show that there is no reduction in
fertilization of eggs based on whether the sperm came from heterospeci®c or homospeci®c males, indicating no incompatibilities in
the fertilization mechanism between these species.
The level of F1 hybrid female fertility was measured by counting
eggs laid by females during a time-limited oviposition period. F1
hybrid females did not show reduced fertility relative to non-hybrid
control females (Fig. 2). In fact, hybrid females with the N. longicornis cytoplasm laid signi®cantly more eggs than non-hybrid
N. longicornis females (Mann±Whitney U-test (U), P , 0.001).
Sterility and/or mortality of F2 progeny (hybrid breakdown) is
one of the earlier manifestations of genetic incompatibility between
recently evolved species20,21. This is believed to be due to the general
recessivity of genes involved in hybrid inviability and infertility20±22.
The haploidy of males in Nasonia offers an advantage to the study of
recessive incompatibility factors, as such factors will be readily
expressed in haploid males15,22. We investigated inviability by
comparing the number of F2 eggs laid by F1 virgin females to the
Number of hybrid (female) offspring
a
100
90
80
70
60
50
40
30
20
10
0
GxG
GxL
LxG
LxL
Cross (female x male)
b
Number of hybrid (female) offspring
related to each other, and therefore have been independently
acquired by horizontal transmission. Thus, the Nasonia system
appears to be prone to the acquisition of Wolbachia, and is a
promising system for studying the role of these bacteria in reproductive isolation.
Previous studies have shown Wolbachia-induced bidirectional
incompatibility between two diverged species, N. vitripennis and
N. giraulti11. F1 hybrids are not formed unless Wolbachia are
removed by antibiotic curing. However, several other isolating
barriers exist between these species, including high levels of F2
hybrid lethality, abnormal courtship behaviours in F2 hybrid
males (behavioural sterility), and partial premating (sexual) isolation (refs 15, 16, and F.P.O'H., A C. Chawla and J.H.W., manuscript
in preparation). It is therefore unclear whether Wolbachia-induced
cytoplasmic incompatibility (CI) evolved before the evolution of
other isolating barriers or after the divergence of the species. If
Wolbachia play a causal role in speciation, cases where Wolbachiainduced CI evolved before other mechanisms of reproductive
isolation should exist.
Here we investigate the role of Wolbachia in reproductive incompatibility in a younger species pair, using the more closely related
species N. giraulti and N. longicornis. First, we screened ®eldcollected insects to determine the frequencies of infections in
natural populations of the three species. A polymerase chain
reaction (PCR) method was employed using previously published
speci®c primers17. In all three species, 100% of the individuals from
various geographical areas were found to be infected (N. giraulti,
n = 29; N. longicornis, n = 31; N. vitripennis, n = 31). All samples
were doubly infected with A and B, except for one N. longicornis
strain with a single A infection. Sequence analysis of PCR-ampli®ed
products of the wsp gene18 from a subset con®rms that the species
are infected with species-speci®c Wolbachia, and that the Wolbachia
from different intraspeci®c strains form monophyletic groups (data
not shown), with little sequence variation within a host species.
We undertook experiments to determine whether Wolbachia
cause reproductive incompatibility between the `young' species
pair, N. giraulti and N. longicornis. Wild-type infected strains and
antibiotically cured strains derived from those infected strains were
crossed in all pairwise combinations. Results show that bidirectional
CI occurs between infected N. giraulti and N. longicornis (Fig. 1).
When Wolbachia are present, no F1 hybrid (female) offspring are
produced in the N. giraulti male ´ N. longicornis female cross and
29.7 6 2.6 (mean 6 s.e., and hereafter) hybrid offspring are
produced in the reciprocal N. longicornis male ´ N. giraulti female
cross. In contrast, crosses using antibiotically cured strains produce
63.9 6 4.1 hybrid offspring and 82.9 6 5.1 hybrid offspring,
respectively. Thus, presence of Wolbachia causes a 100% reduction
in F1 hybrids in one direction and 62.8% reduction in the other
direction. In N. giraulti and N. longicornis, CI results in both a
paternal genome loss19 and offspring lethality (data not shown).
These results show that Wolbachia-induced CI is a signi®cant
component of reproductive incompatibility between N. giraulti
and N. longicornis.
To assess whether Wolbachia-induced incompatibility between
N. giraulti and N. longicornis is one of the ®rst incompatibilities to
evolve in the divergence of these species, we tested for several other
hybrid incompatibilities. Speci®cally, we investigated (1) interspeci®c sperm±egg compatibility, (2) inviability and sterility among F1
hybrid females and (3) inviability and sterility of F2 hybrid males.
Both spermatogenic and behavioural sterility of F2 males was
examined. All the experiments described below were performed
with uninfected individuals to exclude the effects of Wolbachia on
compatibility and viability.
To investigate viability of F1 females, we compared the number
of progeny produced by females mated to intra- and interspeci®c
males. Crosses with uninfected females show that they produce
the same number of F1 progeny whether they mate with males of
100
90
80
70
60
50
40
30
20
10
0
GxG
GxL
LxG
LxL
Cross (female x male)
Figure 1 Number of hybrid (female) offspring produced from intra- and interspeci®c
crosses. Results are shown for infected individuals (a) and uninfected individuals (b). Data
are the mean number 6 s.e. of F1 progeny. G and L denote N. giraulti and N. longicornis,
respectively.
90
letters to nature
number of F2 males that survived to adulthood. (Virgin females
produce haploid male progeny from unfertilized eggs in this
haplodiploid insect.) There are no signi®cant differences in mortality levels among the F2 hybrid males relative to the non-hybrid
controls (Fig. 2). Mortality was found among F2 males of hybrid
females from the N. longicornis male ´ N. giraulti female cross
(mean 6 s.d. = 19.3 6 0.4% (ref. 23) mortality; U, egg versus adult
number, p = 0.002). However, a similar level of mortality was also
observed among non-hybrid N. giraulti males (F2 males from the
N. giraulti male ´ N. giraulti female cross; 14.3 6 0.3% mortality, P
= 0.009). No signi®cant differences were found between these
crosses in the number of F2 eggs (U, P = 0.595) or F2 surviving
adults (U, P = 0.862). Therefore, there is not elevated mortality
among hybrids. This ®nding is quite different from what is found in
the older species pair (N. giraulti ´ N. vitripennis), which has high
levels (70±85%) of F2 hybrid male mortality15. Such recessive
genetic incompatibilities have apparently not yet evolved between
N. giraulti and N. longicornis.
We assessed the fertility of F2 hybrid and non-hybrid males by
dissecting testes and categorizing sperm motility into three groups:
normal, reduced or absent. All males possessed some motile sperm.
The percentage of males with normal quantities of motile sperm was
94.7% (n = 19) and 95.0% (n = 20) for the two hybrid genotypes and
95.0% (n = 20) and 100% (n = 19) for non-hybrids. Additionally, we
tested the ability of hybrid and non-hybrid sperm to fertilize both
N. giraulti and N. longicornis eggs. Of 69 males that copulated, only
one failed to produce female offspring, but this occurred in an
intraspeci®c cross. Thus, hybrid sperm is completely functional.
This contrasts to many studies in Drosophila, which indicate a
prevalence of hybrid male sterility loci24,25 and that spermiogenic
sterility evolves rapidly in the divergence between species20,21.
F2 hybrid breakdown can also affect courtship behaviour, due to a
general `sickness' of hybrid males or to speci®c negative interactions
in genes involved in courtship behaviour26. We assessed the ability of
hybrid and non-hybrid males to (1) locate and mount females, (2)
perform the ritualized courtship display, and (3) copulate with
females. The type of female did not in¯uence probabilities of
initiating courtship and no differences were found among males
in their ability to locate and mount females (hybrids, 93.7%
(n = 187); N. longicornis, 97.8% (n = 46); N. giraulti, 95.7% (n = 46);
X2 = 1.42, 2 degrees of freedom (d.f.), P = 0.49). Among males who
successfully mount females, there was a small and nearly signi®cant
difference in the proportion of males performing the courtship
display (hybrids, 94.2% (n = 172); N. longicornis, 100% (n = 45);
N. giraulti, 100% (n = 45); X2 = 5.44, 2 d.f., P = 0.07). Among those
males who courted N. giraulti females, no differences were found in
the proportion of males copulating (hybrids, 91.5% (n = 94);
30
Offspring number
25
20
15
10
N. longicornis, 95.8% (n = 24); N. giraulti, 96.0% (n = 25);
X2 = 0.97, 2 d.f., P = 0.62). However, males did differ in their ability
to copulate with N. longicornis females (hybrids, 52.9% (n = 68);
N. longicornis, 95.2% (n = 21); N. giraulti, 21.2% (n = 19);
X2 = 22.74, 2 d.f., P , 0.001). This difference cannot be attributed
to hybrid breakdown, because hybrid males with N. longicornis
females copulate at signi®cantly higher rates than do N. giraulti
males (X2 = 6.08, 1 d.f., P = 0.014).
The above results are therefore best explained as mate discrimination of N. longicornis females against F2 hybrid males, rather than
to F2 hybrid `sickness'. In contrast, our ®ndings with F2 hybrid males
from the older species pair (N. giraulti and N. vitripennis) indicate
high levels of reproductive incompetence throughout the various
stages of courtship and mating. For example in the older species
cross, 27.6% of F2 hybrid males failed to locate and mount females,
and of those that did mount females, 26.8% failed to perform the
ritualized courtship display. As a result, a total of 53.2% of F2 hybrid
males in the older species cross fail to successfully mount females
and perform the courtship display (compared to only 13.8% who
fail to do so in the younger species cross, not signi®cantly different
from controls). We conclude that the genetic incompatibilities
responsible for these problems have not arisen since the more
recent divergence of N. giraulti and N. longicornis.
Finally, we investigated the level of premating isolation between
the two species in single pair-mating situations. During a 30-min
mating period, N. giraulti females show no mate discrimination
towards N. longicornis males, mating at similar frequencies as they
do to homospeci®c males (94.5% mating, n = 200 versus 95.6%,
n = 159, P = 0.32). In contrast, N. longicornis females show
partial mate discrimination towards N. giraulti males relative to
homospeci®c males (46.9% mating, n = 113 versus 89.9%, n = 178,
P , 0.0001).
The experiments presented here clearly indicate that the species
pair N. giraulti and N. longicornis do not show signi®cant levels of F1
or F2 lethality, F1 or F2 reproductive sterility, or F2 `hybrid sickness'
as manifested by competence in courtship behaviour. In contrast,
high levels of Wolbachia-induced reproductive incompatibility are
present in this species pair. Therefore, we conclude that interspecies
bidirectional CI has preceded the evolution of these other isolating
mechanisms in this system. In addition to Wolbachia-induced
reproductive incompatibility, there is partial premating isolation
in one direction between these species. The strength of premating
isolation, at least under the conditions tested here, is weaker than
the postmating reproductive incompatibilities caused by Wolbachia.
The role of Wolbachia in speciation is a matter of current
debate5±7 and so far, there is limited empirical support for it9±11.
We do not claim that Wolbachia are currently causing reproductive
isolation between N. giraulti and N. longicornis in nature. Other
factors, such as geographical isolation (allopatry) are likely to be
more important. However, our results do show that Wolbachiainduced bidirectional CI has preceded the evolution of other
intrinsic, postmating reproductive isolation barriers in these
newly evolving species. The present work therefore provides further
support for the argument that the cytoplasmic bacterium Wolbachia
M
could promote host speciation.
Methods
5
0
Crosses for assay of CI and copulation frequencies
G[G]
LG[G]
GL[L]
L[L]
F1 female genotype
Figure 2 F2 egg and adult offspring number produced from F1 hybrid and non-hybrid
females. Data are the mean number 6 s.e. of eggs (black bar) and surviving adults (white
bar). The term in brackets denotes the cytotype, while the term before the brackets
denotes nuclear genotype. For instance, LG[G] hybrid females are derived from the cross,
L male ´ G female.
91
Single pairs of male and female virgins were observed for 30 min in a 12 ´ 75-mm vial. We
only collected data on incompatibility relationships from crosses with an observed
copulation. After 24 h, the male was discarded from the vial, and each mated female was
hosted with two Sarcophaga bullata blow¯y pupal hosts for egg laying. F1 progeny were
scored for sex ratio and family size upon death. RV2, RV2R, IV7 and IV7R2 are the N.
giraulti and N. longicornis infected and uninfected strains, respectively. Uninfected strains
were generated from the corresponding infected strains in 1996 through antibiotic
treatment of 1% Rifadin (10% sugar water) for three successive generations. Infection
status of these strains was con®rmed by PCR before the experiments.
709
letters to nature
F2 hybrid viability
F1 hybrid and non-hybrid virgin adult females (1±2-d old) were placed on four hosts for
roughly 48 h for host feeding and egg laying. Females were immediately transferred to one
host for a 6-h laying period, after which females were removed from the vial. We limited
the ovipositioning period to prevent wasps from becoming resource-limited. Half of these
replicates were immediately scored for the number of F2 eggs laid in 6 h and the remaining
half were scored later for the number of adults.
Dissections for sperm motility assay
Testes and seminal vesicles were viewed under a microscope at ´400 magni®cation for the
presence of motile sperm. Tested males were dissected on the day they emerged in a drop of
phosphate-buffered saline. At least one testis and one seminal vesicle from each male were
viewed. Males were scored as fully fertile if motile sperm were observed in all testes and
seminal vesicles observed. Males were scored as partially fertile if a reduced number of
motile sperm were observed in any organs viewed.
F2 hybrid male behavioural and spermiogenic fertility
Single males, aged 18±48 h, were placed in clear 12 ´ 75-mm vials with ®ve virgin females,
no more than four days old. Behaviour of each male was observed for 15 min. After
courtship observation, males were left in the vial with females for an additional 105 min
(2 h total) and then removed. Females were then given ®ve hosts for feeding and egg laying.
On death of their F1 progeny, each vial was inspected for the presence of female offspring,
indicating successful fertilization of at least one female by the tester male. Behavioural
fertility data were not signi®cantly different for F2 hybrid males from the two reciprocal
crosses (F2 males from N. giraulti males ´ N. longicornis females and from N. giraulti
females ´ N. longicornis males), and therefore the data were pooled for statistical
analysis.
Received 22 September; accepted 30 November 2000.
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Acknowledgements
We thank R. Billings, M. Vaughn and B. J. Velthuis for technical assistance, and J. Bartos, A.
Betancourt, J. Jaenike, J. P. Masly, T. van Opijnen and D. Presgraves for critical reading of
the manuscript. This work was supported by the NSF (J.H.W.).
Correspondence and requests for materials should be addressed to S.R.B.
(e-mail: [email protected]).
.................................................................
Evolutionary radiations
and convergences in
the structural
organization of mammalian brains
Willem de Winter & Charles E. Oxnard
Department of Anatomy and Human Biology, The University of Western
Australia, Perth, Western Australia 6907, Australia
..............................................................................................................................................
The sizes of mammalian brain components seem to be mostly
related to the sizes of the whole brain (and body), suggesting a
one-dimensional scale of encephalization1±3. Previous multivariate study of such data concludes that evolutionary selection for
enlargement of any one brain part is constrained to selection for a
concerted enlargement of the whole brain4. However, interactions
between structurally related pairs of brain parts5 con®rm reports
of differential change in brain nuclei6, and imply mosaic rather
than concerted evolution. Here we analyse a large number of
variables simultaneously using multi-dimensional methods7. We
show that the relative proportions of different systems of functionally integrated brain structures vary independently between
different mammalian orders, demonstrating separate evolutionary radiations in mammalian brain organization8. Within each
major order we identify clusters of unrelated species that occupy
similar behavioural niches and have convergently evolved similar
brain proportions. We conclude that within orders, mosaic brain
organization is caused by selective adaptation, whereas between
orders it suggests an interplay between selection and constraints.
We use data from the same source9,10 as the previous studies4,5. In
ref. 4 a small subset of these data was analysed multivariately to
study species separations, but in a context where size outweighed
most other information; an even smaller subset of the same data was
used to study bivariate relationships between pairs of brain parts in
ref. 5. Here we examine the complete set of specimen measurements
underlying these data by relating the various brain structures in
proportion to two reference structures. We explore the detailed
structure of the resulting 19-dimensional data space in two
stages, and combine the strategies of the previous studies4,5 by
looking for species relationships as well as associations between
variables.
The ®rst stage in this study explores species separations in the
subspace spanned by the ®rst three principal components (85% of
the information). Figures 1 and 2 show that all orders are clearly
differentiated; this shows that they differ uniquely in their internal
brain proportions. The three large ordersÐprimates, insectivores
and batsÐare especially different, being dispersed in nearly orthogonal directions (although not along the orthogonal principal
components of the analysis). The primate and insectivore dispersions are separate, but are linked together via some bats. The two
92
Fruit odor discrimination and sympatric host race
formation in Rhagoletis
Charles Linn, Jr.*, Jeffrey L. Feder†, Satoshi Nojima*, Hattie R. Dambroski†, Stewart H. Berlocher‡,
and Wendell Roelofs*§
*Department of Entomology, New York State Agricultural Experimental Station, Cornell University, Geneva, NY 14456; †Department of Biological Sciences,
University of Notre Dame, Notre Dame, IN 46556-0369; and ‡Department of Entomology, University of Illinois, 320 Morrill Hall, 505 South Goodwin
Avenue, Urbana, IL 61801
Contributed by Wendell Roelofs, August 7, 2003
standing sympatric host race formation and speciation in Rhagoletis, and potentially several other insect specialists, therefore
requires elucidating the mechanistic basis for differential host
choice. Here we show that host fruit odor plays a key role in this
process.
Precisely how R. pomonella distinguishes among potential
hosts is not known. However, studies have discerned several cues
that apple flies use to recognize apple trees. The major longrange stimulus drawing flies to apple trees appears to be volatile
compounds emanating from ripening apple fruit (13). In the
field, apple flies oriented upwind toward a point source of butyl
hexanoate, a key component of the identified apple volatile
blend (Table 1), at a distance of 12 m (14). At shorter distances
of ⬍1 m, visual cues become important for finding fruit within
the tree canopy (13, 15). Other visual characteristics of trees
(e.g., color, shape, and size), although used by flies for distinguishing trees from other objects (16), are not host-specific (13).
The literature on host recognition in the R. pomonella apple race
therefore suggests that differences in fruit volatiles may be
critical for host discrimination.
To determine whether apple and hawthorn flies use fruit odor
as an olfactory cue to help distinguish between their host plants,
we prepared synthetic blends of apple and hawthorn volatiles
that contained the biologically active chemical components of
fruit odors (Table 1; refs. 17 and 18). We then used these blends
in flight-tunnel assays and field trials to test whether apple- and
hawthorn-origin flies preferentially oriented to, or were captured with, their natal fruit volatiles. We report results implying
that the historically derived apple fly race has evolved an
increased preference for apple fruit volatiles and decreased
response to hawthorn volatiles.
Rhagoletis pomonella is a model for incipient sympatric speciation
(divergence without geographic isolation) by host-plant shifts.
Here, we show that historically derived apple- and ancestral
hawthorn-infesting host races of the fly use fruit odor as a key
olfactory cue to help distinguish between their respective plants.
In flight-tunnel assays and field tests, apple and hawthorn flies
preferentially oriented to, and were captured with, chemical
blends of their natal fruit volatiles. Because R. pomonella rendezvous on or near the unabscised fruit of their hosts to mate, the
behavioral preference for apple vs. hawthorn fruit odor translates
directly into premating reproductive isolation between the fly
races. We have therefore identified a key and recently evolved
(<150 years) mechanism responsible for host choice in R.
pomonella bearing directly on sympatric host race formation and
speciation.
S
peciation in sexual organisms occurs as inherent barriers to
gene flow evolve between previously interbreeding populations. To elucidate the origins of species therefore requires
understanding how and why new traits arise that reproductively
isolate taxa (1). Proponents of sympatric or ecological speciation
posit that divergence is often initiated as a result of natural
selection differentially adapting populations to alternative habitats (2, 3). Habitat-specific mating is an ecological adaptation
central to many models of divergence-with-gene-flow speciation
(4, 5). When organisms mate in preferred environments, a
system of positive assortative mating is established that helps
generate disequilibrium between habitat preference and performance genes. This disequilibrium lessens the ‘‘selectionrecombination antagonism’’ (5, 6), making it potentially possible
for divergence to occur without geographic isolation in the face
of gene flow (i.e., in sympatry).
The Rhagoletis pomonella sibling species complex is a model
for sympatric speciation by host-plant shifts (7). The recently
derived apple (Malus pumila)-infesting population of R.
pomonella, which originated by a shift from hawthorn (Crataegus
spp.) in the mid-1800s, represents an example of host race
formation in action, the hypothesized initial stage of sympatric
speciation (2, 7). Host-specific mating is a key feature of
Rhagoletis biology, as it is for many phytophagous insect specialists (2). Because Rhagoletis flies mate exclusively on or near
the unabscised fruit of its host plants (8, 9), differences in host
preference translate directly into mate choice and premating
reproductive isolation (10). Rhagoletis is a vagile insect; most
flies visit multiple trees in their lifetimes searching for food,
mates, and fruit oviposition sites (10, 11). The potential therefore exists for substantial mixing between sympatric fly populations. Despite this potential, fly migration has been estimated
to be 4–6% per generation per year (Rhagoletis is univoltine)
between apple and hawthorn trees based on a mark-recapture
experiment conducted at a field site with interspersed host trees
(10, 11). Studies on related sibling species in the R. pomonella
group have implied that ‘‘host fidelity’’ can potentially cause
complete premating isolation between fly taxa (12). Under-
11490 –11493 兩 PNAS 兩 September 30, 2003 兩 vol. 100 兩 no. 20
Materials and Methods
Insects. Apple and hawthorn flies were collected as larvae from
infested fruit in Grant, MI, Fennville, MI, and Urbana, IL,
during the 1999–2003 field seasons, and reared to adulthood in
the laboratory by using standard protocols (19). Apple and
hawthorn populations at these three sites have been the subject
of previous ecological and genetic studies and have been shown
to differ significantly from one another in allozyme frequencies
(20–24). Eclosing adults were kept in cages in an environmental
chamber at 23–24°C, 16 h light兾8 h dark photoperiod, 60–70%
relative humidity, and fed an artificial diet containing water,
sugar, vitamins, casein hydrolysate, and a salt mixture (25).
Sexually mature, odor-naive adults between 10 and 21 days
posteclosion were tested in the flight tunnel. Roughly equal
numbers of males and females were tested, and no behavioral
difference between the sexes was apparent in the flight tunnel.
Fruit Volatile Blends. Synthetic apple and hawthorn fruit volatile
blends were tested in the study (Table 1). The biologically active
§To
whom correspondence should be addressed. E-mail: [email protected].
© 2003 by The National Academy of Sciences of the USA
93
www.pnas.org兾cgi兾doi兾10.1073兾pnas.1635049100
3-methylbutan-1-ol with the other components added in the
proportions shown in Table 1. Blends were prepared 60 min
before the tests, with fresh sources and spheres used for each test.
Three treatments were tested: (i) a blank red sphere with a
control solvent-treated rubber septum, (ii) the apple blend, and
(iii) the hawthorn blend.
Table 1. Volatile blends for apple and hawthorn fruit
Apple blend
Butyl hexanoate (0.37)
Pentyl hexanoate (0.05)
Propyl hexanoate (0.04)
Butyl butanoate (0.1)
Hexyl butanoate (0.44)
Hawthorn blend
Butyl hexanoate (0.01)
3-Methylbutan-1-ol (1.0)
Isoamyl acetate (0.4)
4,8-Dimethyl-1,3(E),7-nonatriene (0.02)
Ethyl acetate (20.0)
Dihydro-␤-ionone (0.02)
Field Trials. Field trapping studies were conducted in mixedvariety apple orchards and hawthorn copses from August 27 to
September 9, 2002, at the Experiment Station in Geneva, NY,
and from July 25 to September 5, 2002, at the Trevor Nichols
Research Complex near Fennville, MI. Red sphere traps (7.5-cm
diameter) coated with ‘‘Tanglefoot’’ stickum were used in New
York, whereas clear glass spheres (5.5-cm diameter) were used
at the Michigan site to remove any visual cue provided by the red
sphere. (Fig. 2 shows the spheres used in the study.) Three-way
choice experiments were performed to assess the relative preferences of the host races for fruit odors. For the three-way tests,
rubber septa lures containing 2 mg of apple, hawthorn, or no
blend were separately attached to the tops of three spheres
triangulated 2 m apart in host trees. Three replicate tests were
conducted at each site in a trial period, with a trial period lasting
from 1 to 2 days. Traps were checked after each trial period, with
captured flies counted and removed, lures replaced, and traps
rotated to new positions. Statistical analyses were performed by
using the total number of flies captured across the three
replicates during trial periods. Paired field trials of only the apple
blend vs. blank controls on clear spheres were also performed at
the Fennville, MI, site to assess host race attraction to apple odor
in the absence of the visual cue provided by the red sphere. For
the paired experiments, the apple blend was released from
scintillation vials prepared by Great Lakes IPM. Release rate of
odor from these vials was estimated at 1 mg兾h at 25°C. Baited,
clear spheres were hung 1 m from blank clear spheres fitted with
empty vials. Six pairs of replicate traps were monitored and
rotated every 5 days for the paired trials. The same design was
used to test the apple blend in flowering dogwood (Cornus
florida) stands in Cassopolis, MI, and Granger, IN, from September 16 to October 13, 2002.
The numbers in parentheses are microgram amounts per microliter of the
solution applied to the septum.
chemical components of apple and hawthorn fruit volatiles were
first identified by using solid-phase microextraction, coupled gas
chromatography兾electroantennogram detection, mass spectrometry, and a sustained-flight tunnel assay (17, 18). The
compositions of the blends were determined through reiterative
testing such that equivalent amounts of whole-fruit extracts and
the synthetic mixes elicited similar levels of behavioral activity
from natal fly races in the flight tunnel (17, 18).
Flight Tunnel. The response of flies to fruit volatiles was measured
EVOLUTION
in a 183-cm-long, 61 ⫻ 61-cm-square flight tunnel (see refs. 17
and 18 for details of tunnel and flight conditions). Solutions of
the synthetic blends prepared in hexane were applied to acetonewashed, rubber septa (Thomas Scientific, Swedesboro, NJ). A
septum was attached to a 7.5-cm-diameter red plastic sphere
(Great Lakes IPM, Vestaburg, MI) hung at the upwind end of
the tunnel. Individual flies were transferred to a screen cage,
which was then placed on a screen stand 1 m downwind of the
sphere, and their behaviors were recorded (see Fig. 1 legend for
description of fly behaviors). Field experiments have shown that
apple flies can orient upwind to a point source of butyl hexanoate, a key volatile of the apple odor blend, at a distance of at least
12 m (14). Fruit volatiles are therefore not just short-range
attractants. For all flight-tunnel tests, 200-␮g sources of a
particular fruit blend were used. For the apple blend, the 200-␮g
dosage refers to the complete five-component mix (Table 1). For
the hawthorn blend, the 200-␮g dose reflects the amount of
Fig. 1. Percentages of tested apple- (open symbols) and hawthorn-origin flies (filled symbols) displaying the indicated or greater behavioral acceptance of apple
blend (A) and hawthorn (Haw) blend (B) in flight-tunnel assays. Behavioral responses in order of increasing blend acceptance are as follows: walk and groom
(fly remaining in release cage), take flight (flight from the release cage), upwind (oriented flight toward sphere), and reach sphere. The percentage of flies
displaying walk-and-groom behavior ⫽ 100% ⫺ % take flight. Populations tested were ‚, Urbana, IL; ƒ, Urbana, IL, hawthorn flies reared on apple for two
generations; E, Grant, MI; 䊐, Fennville, MI; and 〫, Geneva, NY, apple fly colony. P ⬍ 1 ⫻ 10⫺7 for every test of behavioral difference between races at a site,
as determined by Fisher’s exact test. Populations within a race did not differ significantly from each other in their responses to their natal fruit blend. However,
significant heterogeneity occurred among apple-fly populations in their responses to hawthorn blend (G test reaching sphere ⫽ 11.3, P ⫽ 0.158, 3 df) and among
hawthorn fly populations to apple blend (G test ⫽ 15.8, P ⫽ 0.0006, 2 df).
Linn et al.
94
PNAS 兩 September 30, 2003 兩 vol. 100 兩 no. 20 兩 11491
Fig. 2. Tanglefoot-coated spheres used for field trials. (A) Clear sphere with
septum used to release volatiles for three-way choice tests at Fennville, MI. (B)
Clear sphere with scintillation vial used to release volatiles for paired appleblend vs. blank tests. (C) Red sphere used in New York field trials and flight
tunnel. Background is a hawthorn tree with red fruits visible.
Results and Discussion
Flight Tunnel. In control flight-tunnel experiments, no fly of either
host race flew upwind toward a ‘‘blank’’ red sphere fitted with
an odorless septum. The sphere and septum used as a release
point for the blends in the tunnel therefore held no intrinsic
attractive value from the 1-m distance at which flies were
released.
Significant differences were observed, however, in the behavioral responses of the host races to red spheres with apple vs.
hawthorn volatiles. Virtually every apple-origin fly tested took
flight when the septum attached to the sphere contained the
apple blend. A majority of these apple flies (⬎70%) displayed
upwind anemotactic flight, tracking the apple-odor plume in the
tunnel to reach the source sphere (Fig. 1 A). The finding of
anemotactic flight, not previously reported for Rhagoletis, is
important because it implies that these flies have the capacity to
locate an olfactory source from a considerable distance in the
field. Hawthorn-origin flies responded similarly when the sphere
contained the hawthorn blend (Fig. 1B). However, both fly races
displayed a significantly reduced response to their nonnatal
blend. Less than 25% of apple flies flew upwind and reached the
sphere when hawthorn volatiles were present (Fig. 1B), and
fewer hawthorn flies reached apple-blend spheres (Fig. 1 A). The
results were similar for three pairs of apple and hawthorn fly
populations tested from Grant, MI, Fennville, MI, and Urbana,
IL, and for a laboratory colony of Geneva, NY, apple flies
established from the wild in the 1970s (Fig. 1). Thus, the host
races showed a consistent pattern of preference for their natal vs.
nonnatal blend across their geographic range of overlap. Moreover, Urbana, IL, hawthorn flies reared for two generations in
the laboratory on apple displayed the same behavioral responses
as hawthorn flies reared directly from field-collected hawthorns
(Fig. 1). This finding discounts an effect of the larval-host fruit
environment on adult fly behavior. Genetic crosses between
apple and hawthorn flies are expected to allow mapping of
quantitative trait loci for host odor preference.
Fig. 3. Total percentages of resident Rhagoletis flies captured across replicate trapping periods on baited spheres (red in New York, clear in Michigan
and Indiana) in apple orchards, hawthorn copses, and dogwood-tree stands in
Geneva, NY, Fennville, MI (FMI), Cassopolis, MI (CMI), and Granger, IN. (A)
Results for three-way choice study of apple blend, hawthorn blend, and blank
spheres. P ⬍ 1 ⫻ 10⫺12 for all pairwise comparisons of difference in fly capture
on sphere types between apple orchard and hawthorn tree copses, as determined by G contingency tests. (B) Results for paired field study of apple blend
vs. blank, clear spheres in apple, hawthorn, and dogwood tree stands. P ⬍ 1 ⫻
10⫺15 for all comparisons of difference in capture on sphere types between
apple vs. hawthorn or dogwood stands, as determined by two-tailed Fisher’s
exact test. Sample n ⫽ total number of flies trapped on all spheres in a given
tree stand.
Three-Way Choice Study. Field trials indicated that the preferences
spheres across 12 replicate block periods; ␹2r for the Michigan
apple orchard was 6.0; P ⫽ 0.05, three replicate periods). The
pattern was reversed at hawthorn tree stands in New York and
Michigan ⬍1 km away from the apple orchards (Fig. 3A). Here,
significantly more flies were trapped on the hawthorn blend than
the other spheres (␹2r New York hawthorn stand was 12.7, P ⬍
0.001, 12 replicate periods; ␹2r for the Michigan hawthorn stand
was 6.0, P ⫽ 0.05, 3 replicate periods).
displayed by the host races in the flight tunnel were relevant in
nature. In three-way choice experiments conducted in unsprayed
apple orchards near Geneva, NY, and Fennville, MI, resident
flies were captured significantly more often on sticky spheres
(red in New York, clear in Michigan) baited with the apple-blend
than on hawthorn-blend or blank spheres (Figs. 2 and 3A; ␹2r
Friedman’s test for the New York apple orchard was 21.1; P ⬍
0.0001 for significantly higher rank order capture on apple-blend
11492 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.1635049100
95
Linn et al.
volatiles from apple fruit, and decreased response to hawthorn
volatiles, during the course of its ⬇150 years of existence.
Because mate choice in R. pomonella is directly tied to host
choice, the difference in host odor preference results in premating reproductive isolation between apple and hawthorn flies. We
have therefore identified a key host-related adaptation underlying host race formation and incipient sympatric speciation in R.
pomonella.
In conclusion, investigations of the apple maggot fly are
adding to a growing list of systems demonstrating a role for
ecological adaptation in incipient population divergence and
speciation (3, 27–29). What makes the R. pomonella story
compelling is that the known history and geography of race
formation allows us to directly connect host adaptation (e.g.,
fruit-odor preference) and reproductive isolation in real-time
ecological experiments in nature.
Paired Field Trials. The flight-tunnel and three-way choice experiments imply that the historically derived apple race has evolved
an increased preference for apple volatiles. To further test this
hypothesis, we performed paired field trails of just the apple
blend vs. blank clear spheres at the Fennville, MI, site (Fig. 2B),
and a study of R. pomonella’s sister species, the undescribed
flowering dogwood fly (26). In the Fennville apple orchard,
significantly more resident flies were captured on the apple
blend than blank spheres (Fig. 3B; Z ⫽ 2.93, P ⫽ 0.003,
two-tailed Wilcoxon sign-rank test for greater capture on apple
blend spheres across 11 replicate periods). In the hawthorn tree
copse, in contrast, significantly more flies were captured on
blank spheres than on apple-blend spheres (Fig. 3B; Z ⫽ 2.52,
P ⫽ 0.012, eight replicate periods). The results in flowering
dogwood stands were similar to those for hawthorn trees (Fig.
3B). At two stands of C. florida trees near Granger, IN, and
Cassopolis, MI, a total of 58 resident flies were captured on
apple-blend vs. 175 on blank spheres (Z ⫽ 2.52, P ⫽ 0.012, eight
replicate periods in Indiana; Z ⫽ 2.02, P ⫽ 0.043, five replicate
periods in Michigan). The reduced capture of both the ancestral
hawthorn race and immediate outgroup dogwood fly on appleblend vs. blank clear spheres supports the hypothesis that the
increased preference of apple flies for apple odor is a derived
characteristic of the population. The results also suggest that
hawthorn and dogwood flies may avoid the odor of apples.
Conclusion. Our results imply that the apple race of R. pomonella
has evolved an increased preference for a specific blend of
We thank K. Catropia, K. Filchak, R. Harrison, C. Musto, R. Oakleaf,
K. Pelz, K. Poole, H. Reissig, J. Roethele, C. Smith, L. Stelinski, U. Stolz,
B. Westrate, J. Wise, the Niles, MI, U.S. Department of Agriculture
facility, the Trevor Nichols Research Complex, and the New York State
Agricultural Experimental Station at Geneva Fly Rearing Center. This
work was supported by grants from the National Science Foundation
Integrated Research Challenges (to all authors) and the U.S. Department of Agriculture National Research Initiative (to J.L.F. and S.H.B.)
and by the state of Indiana 21st Century Fund (to J.L.F.).
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PNAS 兩 September 30, 2003 兩 vol. 100 兩 no. 20 兩 11493
SEMINARIO III: GENÉTICA DE LA ESPECIACIÓN Marcela Rodriguero & Abel Carcagno En este seminario se discutirán dos trabajos que tratan acerca de la genética de la especiación y de la diferentes escuelas relacionadas con los mecanismos subyacentes al proceso especiogénico. Nota: Se recomienda especialmente la lectura crítica del trabajo “Dualism and conflicts in understanding speciation”, de Menno Schilthuizen (Bioessays 22(12): 1134‐1141, 2000) disponible en http://www.ege.fcen.uba.ar/materias/evolucion/material.htm Genética del proceso especiogénico: dos escuelas teóricas Punto de partida de la especiación Fuerzas evolutivas preponderantes durante el progreso de la especiación Resultado último de la especiación Velocidad del proceso especiogénico en relación a la escala geográfica Escuela Aislacionista Escuela Seleccionista Interrupción del flujo génico Deriva genética y/o selección natural Adaptación a ambientes diferentes Selección natural Aislamiento reproductivo pre y/o postcigótico Más rápido en focos periféricos aislados, aunque puede darse en otra configuración geográfica Diferentes acervos génicos adaptados Más rápido en simpatría, aunque puede darse en otra configuración geográfica Escuela Aislacionista • Schemske D.W. & Bradshaw H.D. (1999) Pollinator preference and the evolution of floral traits in mokeyflowers (Mimulus). PNAS 96: 11910‐11915. 1‐ ¿Existen los genes de la especiación? 2‐ ¿Cuántos genes requiere un proceso especiogénico? 3‐ ¿Qué son los QTLs y qué relevancia tienen para el estudio de la especiación? 4‐ ¿Cuál es la hipótesis de trabajo de Schemske & Bradshaw (1999) y qué antecedentes la sustentan? 5‐ ¿Qué aproximación experimental utilizaría para dilucidar la arquitectura genética del aislamiento reproductivo mediado por polinizadores? 6‐ ¿Cómo se confeccionó la figura 2? Indique el tratamiento estadístico de los datos. 97
7‐ ¿Qué conclusión puede extraer de la figura 2 respecto de las preferencias de cada polinizador? 8‐ Explique cómo se obtuvieron los resultados graficados en las figuras 3 y 4. Compárelos con los de la figura 2. ¿Dichos resultados se contradicen? 9‐ A partir de estos datos, ¿cuál es la arquitectura genética del aislamiento reproductivo de estas especies? 10‐ ¿Se puede establecer inequívocamente que los cuatro caracteres analizados son los responsables absolutos del aislamiento reproductivo? Escuela Seleccionista • Fontaneto D., Ermiou E.A., Boschetti C., Caprioli M., Melone G., Ricci C., Barraclough T.G. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biology 5(4): 914‐ 921. 11‐ Si existen los genes de la especiación... ¿cuáles serían en este caso? 12‐ ¿Qué particularidad presenta la clase Bdelloidea? ¿Qué concepto de especie utilizaría? ¿Qué modelo de especiación? 13‐ ¿Cuáles son las hipótesis del trabajo de Fontaneto et al. (2007)? ¿Cuáles son las predicciones de cada escenario? 14‐ Este taxón presenta una particularidad que podría oscurecer el análisis. Menciónelo y fundamente su respuesta. A partir de dicha conclusión, ¿qué carácter emerge como la mejor opción para contrastar las hipótesis de trabajo y cuál podría ser su valor adaptativo? ¿Siente que la utilización de dicha característica podría llevar a circularidad en el contraste de la hipótesis? 15‐ Una vez seleccionado el carácter morfológico a estudiar, mencione los fundamentos teóricos y las herramientas metodológicas utilizadas para abordar la hipótesis de evolución independiente. 16‐ ¿Cuántas entidades evolutivas se pueden distinguir en Bdelloidea? ¿Son realmente independientes? ¿Existe congruencia entre las unidades evolutivas y las reconocidas por los taxónomos? ¿Cómo explicaría las discrepancias? 17‐ Mencione la aproximación metodológica y teórica utilizada para el contraste de la hipótesis de divergencia adaptativa (relacione esto con lo aprendido en la unidad de Neutralismo). 18‐ A partir de los resultados obtenidos, ¿qué fuerza evolutiva operó en la acumulación de cambio evolutivo dentro de Bdelloidea? ¿Qué factores apoyan este resultado? 19‐ ¿Qué unidades evidencian la acumulación de divergencia adaptativa? ¿Se le ocurre alguna manera de reconciliar estos resultados con los derivados del contraste de la hipótesis de evolución independiente? 20‐ Una vez comprendidos los objetivos y resultados del trabajo, ¿cuántos conceptos de especie diferentes podría aplicar a los rotíferos de la clase Bdelloidea? 98
Preguntas unificadoras 21‐ Comparando ambos trabajos... ¿En qué caso la selección natural desarrolla un papel principal en el proceso especiogénico? ¿Qué papel juega entonces en el otro caso de estudio durante el proceso de especiación? 22‐ ¿Por qué cree que la teoría de especiación por selección natural tuvo menos adeptos en el pasado y actualmente está resurgiendo? 99
Pollinator preference and the evolution of floral traits
in monkeyflowers (Mimulus)
Douglas W. Schemske*† and H. D. Bradshaw, Jr.‡
*Department of Botany and ‡College of Forest Resources, University of Washington, Seattle, WA 98195
Edited by Barbara Anna Schaal, Washington University, St. Louis, MO, and approved August 11, 1999 (received for review June 10, 1999)
A paradigm of evolutionary biology is that adaptation and reproductive isolation are caused by a nearly infinite number of mutations of individually small effect. Here, we test this hypothesis by
investigating the genetic basis of pollinator discrimination in two
closely related species of monkeyflowers that differ in their major
pollinators. This system provides a unique opportunity to investigate the genetic architecture of adaptation and speciation because
floral traits that confer pollinator specificity also contribute to
premating reproductive isolation. We asked: (i) What floral traits
cause pollinator discrimination among plant species? and (ii) What
is the genetic basis of these traits? We examined these questions
by using data obtained from a large-scale field experiment where
genetic markers were employed to determine the genetic basis of
pollinator visitation. Observations of F2 hybrids produced by crossing bee-pollinated Mimulus lewisii with hummingbird-pollinated
Mimulus cardinalis revealed that bees preferred large flowers low
in anthocyanin and carotenoid pigments, whereas hummingbirds
favored nectar-rich flowers high in anthocyanins. An allele that
increases petal carotenoid concentration reduced bee visitation by
80%, whereas an allele that increases nectar production doubled
hummingbird visitation. These results suggest that genes of large
effect on pollinator preference have contributed to floral evolution
and premating reproductive isolation in these monkeyflowers. This
work contributes to growing evidence that adaptation and reproductive isolation may often involve major genes.
reproductive isolation 兩 adaptation 兩 speciation 兩 natural
selection 兩 pollination
O
ne of the principal goals of evolutionary biology is to
discover the genetic architecture of adaptation. Fisher’s
‘‘infinitesimal’’ model of evolution proposes that adaptation is
due to the fixation of many genes with small individual effects,
and is based on the assumption that large-effect mutations move
a population farther from, rather than closer to, its phenotypic
optimum (1). This micromutationist view of ‘‘adaptive geometry’’ (2) has had widespread support, but was challenged recently
by a theory suggesting that mutations of large effect can often be
beneficial during the early stages of adaptation as populations
move toward their optimum phenotype (3). There have been too
few empirical studies to resolve the debate, and it is therefore
important to identify systems in which both the genetic basis and
ecological significance of adaptive traits can be identified (4, 5).
Adaptations that reduce the frequency of mating among
neighboring populations are of special interest, as these may
contribute to the origin of new species. Although evidence from
Drosophila suggests that premating isolation may evolve quickly
(6), and can have a simple genetic basis (7, 8), there are few
comparable data from other organisms and no studies investigating the genetics of premating reproductive isolation in natural
populations (9, 10).
Pollinator-mediated selection on floral traits is widely regarded as a common mechanism of adaptation and speciation in
plants (11–19). The traditional view is that adaptation to the
most abundant or efficient pollinators in geographically isolated
populations results in floral divergence, and that pollinator
preference prevents intercrossing if populations come into sec-
11910ⴚ11915 兩 PNAS 兩 October 12, 1999 兩 vol. 96 兩 no. 21
100
ondary contact. Two species that show this pattern of secondary
contact are the predominantly bee-pollinated Mimulus lewisii
and its hummingbird-pollinated congener Mimulus cardinalis. M.
lewisii has pink flowers, a wide corolla with inserted anthers and
stigma, a small volume of nectar, petals thrust forward to provide
a landing platform for bees, and two yellow ridges of brushy hairs
presumed to be nectar guides (Fig. 1A). M. cardinalis has red
flowers, a narrow tubular corolla, reflexed petals, a large nectar
reward, and exserted anthers and stigma to contact the forehead
of hummingbirds (Fig. 1C). Neither species has an odor detectable by humans, and our observations suggest that pollinator
visitation is influenced primarily by flower color, size, shape, and
nectar reward.
Despite striking morphological differences, these two monkeyflowers are very closely related. A phylogeny based on DNA
sequence from the internal transcribed spacer of nuclear ribosomal RNA places M. cardinalis and the Sierra Nevada form of
M. lewisii together and distinct from Rocky Mountain and
Cascade Range populations of M. lewisii and other members of
the section Erythranthe (A. Yen, R. G. Olmstead, H.D.B. and
D.W.S., unpublished work). Crosses between these two species
produce fertile hybrids (20). Their geographic distributions are
largely nonoverlapping, with M. lewisii found principally from
mid-to-high elevation, and M. cardinalis found from low-to-mid
elevation. The two species co-occur in a narrow altitudinal zone
at 1400 m in the Sierra Nevada.
In 1998, we conducted observations (⬎80 hr) in a sympatric
area along the South Fork of the Tuolumne River, California,
and found that bees were the only visitors to M. lewisii (100% of
233 visits), and that hummingbirds were the primary visitors to
M. cardinalis (97% of 146 visits). Only once did we observe a
pollinator visit both Mimulus species in succession. These results
show that pollinator discrimination results in strong premating
reproductive isolation in the zone of sympatry.
Two experiments are required to elucidate the genetic architecture of reproductive isolation by pollinator-mediated selection. First, the genetic basis of traits such as flower color, size,
shape, and nectar reward must be determined for plant species
with different pollinators. Second, the response of wild pollinators to each floral trait must be evaluated in a geographic region
where the plant species co-occur. We have completed the first
experiment, using linkage mapping with molecular markers to
identify quantitative trait loci (QTL) that control complex floral
traits in M. lewisii and M. cardinalis. We found that most floral
traits had at least one QTL of large effect (explaining ⬎25% of
the F2 phenotypic variance), suggesting that pollinator-mediated
selection in this system could involve ‘‘major’’ genes (21, 22).
Here, we report results from the second experiment, identifying
the ecological significance of floral traits and the effect of simple
genetic changes on pollinator visitation in nature.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviation: QTL, quantitative trait loci.
†To
whom reprint requests should be addressed. E-mail: [email protected].
The publication costs of this article were defrayed in part by page charge payment. This
article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C.
§1734 solely to indicate this fact.
EVOLUTION
Fig. 1.
M. lewisii (A), an F1 hybrid (B), M. cardinalis (C), and examples of variation in floral traits found in F2 hybrids (D–L).
Seed of both parental species was collected in Yosemite National
Park. We crossed M. lewisii (Fig. 1 A) with M. cardinalis (Fig. 1C)
to produce F1 hybrids, then mated unrelated F1s to produce an
Schemske and Bradshaw
101
outcrossed F2 population. The F1 hybrids have pink flowers and
moderately reflexed petals, with nectar guides similar to those of
M. lewisii, but lacking hairs (Fig. 1B), whereas the F2 generation
displays a wide range of flower colors and morphologies (Fig. 1
D–L).
PNAS 兩 October 12, 1999 兩 vol. 96 兩 no. 21 兩 11911
11912 兩 www.pnas.org
102
Standardized regression coefficient
A 0.2
Proportion of visits by bees
*
0.1
0
-0.1
-0.2
**
-0.3
***
****
anthocyanins
carotenoidsnectar
projected area
B 0.4
Standardized regression coefficient
We examined the visitation by bees and hummingbirds to the
parental species and hybrids in an experimental population. We
grew parental, F1, and F2 individuals to flowering in the University of Washington greenhouses as part of our QTL studies
(22), and transported a subset of these plants to the study site
(Wawona Ranger Station, Yosemite National Park, elevation
1300 m) where the two species co-occur. We arranged plants
randomly in a 5 x 15 m plot, with 0.5-m spacing (n ⫽ 24 for each
of the parents and the F1, and n ⫽ 228 for the F2 generation).
We used fewer parentals and F1s than F2s to reduce the
likelihood that pollinators would develop a preference for F2s
that resembled the parental species. Our observation period
(June 1996) preceded the flowering time of natural populations
of M. lewisii and M. cardinalis. This schedule prevented gene flow
from our study population and ensured that pollinators had not
yet encountered the study species in natural populations in 1996.
We conducted observations of bee and hummingbird visitation from dawn to dusk in separate 30-min periods, three to four
times a day (mean ⫽ 3.7 periods per day for each pollinator type)
on 7 days from June 18 to June 27, for a total of 26 hr. Three to
five observers watched the plot during each observation period,
using tape recorders to record flower visits by bees and hummingbirds. We recorded the number of open flowers for each
plant on each day of observation. To obtain a daily ‘‘rate’’ of
pollinator visitation (visits per flower per day), we divided the
daily total number of visits for each pollinator by flower number.
There were more bees than could be recorded during some
observation periods, but this is likely to result in only a slight
underestimate of the relative frequency of bee visitation, so we
did not attempt to correct for the unobserved bee visits. Voucher
specimens of the most common bees were identified by E.
Sugden (Department of Zoology, University of Washington).
Four floral traits were chosen for analysis: (i) petal anthocyanin concentration (purple pigments), (ii) petal carotenoid
concentration (yellow pigments), (iii) nectar volume, and (iv)
projected area (a composite measure of the petal surface
exposed to pollinators). These traits are highly diverged in the
two parental species (21–23), and were expected to affect
pollinator visitation rates because of their contribution to pollinator attraction and reward. We cannot exclude the possibility
that other, unmeasured traits may contribute to pollinator
visitation, and that these may be linked to the traits included in
our study, or have pleiotropic effects on those traits.
We used the mean of two randomly drawn flowers per plant
to estimate the phenotypic value of each trait. Petal anthocyanin
concentration was estimated by punching 6-mm disks from the
lateral petals, extracting the anthocyanins with 0.5 ml of methanol/0.1% HCl, and determining the absorbance at 510 nm. Petal
carotenoid concentration was estimated similarly, using methylene chloride for extraction and measuring absorbance at 450
nm. To estimate projected area of the corolla, we recorded video
images of flowers from the perspective of approaching pollinators, i.e., in a plane perpendicular to the long axis of the corolla
tube, and analyzed these with image analysis software (National
Institutes of Health IMAGE; http://rsb.info.nih.gov/nih-image).
Nectar volume was measured with a graduated pipette tip. For
practical reasons, all measurements were conducted while the
study plants were growing in the University of Washington
greenhouse. We remeasured a subset of plants in the field plot,
and found that the greenhouse and field values were positively
correlated for all morphological traits (P ⬍ 0.01, n ⫽ 56) and for
nectar volume (P ⬍ 0.0001, n ⫽ 31).
To examine the relationship between pollinator visitation and
floral traits in the F2 population, we treated the proportion of
bee visits and the daily visitation rates of bees and hummingbirds
as dependent variables in separate multiple regressions, with the
four floral traits as independent variables. Analyzing the proportion of bee visits evaluates the effects of floral characters on
Visitation rates
0.2
****
****
*
0
-0.2
*
****
-0.4
antho.
carot.
bees
hummingbirds
nectar proj. area
Fig. 2. Contribution of floral traits to pollinator visitation, as determined by
multiple regression analysis (antho., petal anthocyanin concentration; carot.,
petal carotenoid concentration; nectar, nectar volume per flower; proj. area,
projected area of petals). Bars give the standardized regression coefficients; 多,
P ⬍ 0.05; **, P ⬍ 0.01; ***, P ⬍ 0.001; ****, P ⬍ 0.0001. n ⫽ 228 F2 plants for
all analyses. (A) Multiple regression of floral traits on the proportion of visits
by bees (F ⫽ 24.2, P ⬍ 0.0001, R2 ⫽ 0.31). (B) Multiple regression of floral traits
on the mean daily visitation rates by bees (F ⫽ 22.1, P ⬍ 0.0001, R2 ⫽ 0.28) and
hummingbirds (F ⫽ 13.7, P ⬍ 0.0001, R2 ⫽ 0.20).
the composition of the pollinator assemblage, whereas analyzing
daily visitation rates by bees and hummingbirds identifies the
mechanisms responsible for differences in pollinator composition, i.e., increasing bee visitation vs. decreasing hummingbird
visitation. We performed an angular transformation on the
proportion of visits by bees and a square-root transformation on
all floral traits. The transformed variables were then standardized (mean ⫽ 0, SD ⫽ 1) to provide a direct comparison of the
magnitudes of the regression coefficients for different analyses.
Results and Discussion
We observed a total of 12,567 pollinator visits in the experimental population. The non-native honeybee Apis mellifera
comprised ⬍5% of the total visits to F2s and was excluded from
our analyses. We combined all other bee species to form a single
category. The bumblebee Bombus vosnesenski was responsible
for ⬎95% of all bee visits, with the remaining visitation by Osmia
(Monilosmia) sp. and an unknown bumblebee. Bumblebees
generally visited flowers for nectar and made only passive
contact with the anthers, whereas Osmia (Monilosmia) sp.
actively collected pollen during its foraging bouts. Pollencollecting bumblebees were observed most often on plants with
red or orange flowers. Anna’s hummingbird (Calypte anna) was
the only species of hummingbird observed. Although we did not
mark hummingbirds, chases between individuals with different
plumage were common, suggesting that several different hummingbirds were visiting the experimental plants.
M. lewisii was visited primarily by bees (82% of 78 visits), and
M. cardinalis was visited by hummingbirds (99.6% of 2,097
visits), establishing that pollinator behavior in our experimental
plots is similar to that observed in natural populations. The
composition of the visitors to F1 hybrids (59% bees; 1,744 visits)
was exactly intermediate to that of the parental species, indiSchemske and Bradshaw
103
EVOLUTION
Fig. 3. Effect of allelic differences at the yup locus on the visitation rate (visits
per flower per day) of hummingbirds (A) and bees (B). Heterozygous individuals (LC) or those homozygous for the M. lewisii allele (LL) lack carotenoids in
their upper petals and are pink-flowered (n ⫽ 165), whereas individuals
homozygous for the M. cardinalis allele (CC) have petal carotenoids and vary
in color from light orange to red (n ⫽ 63). Bars denote the mean ⫹ 2 SE.
Significance levels were determined by Mann–Whitney U tests.
Fig. 4. Effect of marker genotype for the major nectar QTL (RAPD marker
L04co; ref. 22) on nectar volume per flower (A), and the visitation rate (visits
per flower per day) of hummingbirds (B) and bees (C). Genotypes are: LL,
individuals homozygous for the M. lewisii allele (n ⫽ 61); LC, heterozygotes
(n ⫽ 130); CC, individuals homozygous for the M. cardinalis allele (n ⫽ 36). Bars
denote the mean ⫹ 2 SE, and bars with different letters identify means that are
significantly different (P ⬍ 0.01) based on Mann–Whitney U tests corrected for
multiple comparisons (31).
cating a strong genetic component to visitation. The composition
of pollinators visiting the F2s (8648 visits) varied widely, from
plants visited only by bees to those visited only by hummingbirds,
with a mean of 38% bee visitation per plant.
Increased petal anthocyanins, petal carotenoids, and nectar
volume significantly reduced the proportion of bee visitation,
whereas greater projected area increased the proportion of bee
visitation (Fig. 2A). These results provide clear evidence that
f lower color contributes to reproductive isolation in this
system, despite recent statements to the contrary (24, 25).
Petal anthocyanin concentration significantly affected both
bee and hummingbird visitation rates, but with opposite
effects, whereas each of the other f loral traits had a significant
effect on one pollinator, but not on the other (Fig. 2B). Bee
visitation rate was negatively associated with petal anthocyanin and carotenoid concentration and positively associated
with projected area, whereas hummingbird visitation rate was
positively associated with both petal anthocyanin concentration and nectar volume (Fig. 2B).
We tested the hypothesis that adaptation to different pollinators may involve genes with large phenotypic effects by
comparing visitation rates as a function of QTL marker genotype
for petal carotenoid concentration and nectar volume, the two
traits with the greatest impact on bee and hummingbird visitation, respectively (Fig. 2B). A single Mendelian locus controls
the distribution of carotenoid pigments in the petals (20). F2
plants homozygous for the recessive M. cardinalis allele at the yup
locus (yellow upper; ref. 20) have carotenoids distributed
throughout the petals, and are orange- or red-flowered (Fig. 1
D, E, K, and L), whereas F2s carrying the dominant M. lewisii
allele are pink-flowered (Fig. 1 F–J). There was no effect of yup
genotype on hummingbird visitation rate (Fig. 3A), but bee
visitation was 80% lower in plants homozygous for the M.
cardinalis allele (Fig. 3B). This clearly shows that genetic
variation for petal carotenoid concentration affects bee visitation and supports earlier findings that bees visiting Mimulus
species in the section Erythranthe strongly prefer pink over red
f lowers (26).
Although hummingbirds have been shown to exert strong
selection for red coloration (27), we found only a weak relationship between hummingbird visitation and flower color.
Hummingbirds had a slight, but significant preference for flowers with high petal anthocyanin concentration (Fig. 2B), but
exhibited no preference for flowers high in petal carotenoids.
That petal carotenoids significantly decrease bee visitation but
have no effect on hummingbirds suggests that the high concentration of these pigments in the flowers of M. cardinalis (22) may
function primarily to discourage bee visitation. The hypothesis
that the red coloration of many hummingbird flowers functions
primarily to reduce visitation by insects (28) is consistent with
the finding that hummingbirds do not have an innate preference
for red (29, 30).
To examine the effect of nectar reward on pollinator
visitation, we compared hummingbird and bee visitation rates
for the three F2 genotypic classes at the major nectar QTL (22).
Our previous genetic mapping study found that this QTL
explains 41% of the difference in nectar volume between the
two parental species and has an additive mode of action, with
the M. cardinalis allele causing an increase in nectar (22).
Segregation of the parental alleles at this locus produced a
nearly 3-fold range in mean nectar volume per f lower in our
F2 field population (Fig. 4A). The average nectar volume of the
heterozygous genotypic class was intermediate to that of the
two homozygous classes (Fig. 4 A), and the visitation rate of
hummingbirds closely matched this distribution of nectar
volume (Fig. 4B). Plants homozygous for the M. cardinalis
allele had twice the rate of hummingbird visitation as M. lewisii
homozygotes, whereas heterozygotes had an intermediate
value (Fig. 4B). These results demonstrate that despite the
bewildering array of f loral variation in the F2 population (Fig.
1 D–L), hummingbirds have the remarkable ability to distinguish the phenotypic effects of allele substitutions at the major
nectar QTL. In contrast, there was no relationship between
bee visitation rate and marker genotype at the nectar QTL
(Fig. 4C). The ability of hummingbirds to quickly find rich
nectar sources, and to return to them often, has also been
documented in experiments on spatial learning (29, 32, 33) and
suggests that hummingbirds are capable of exerting strong
selection on the nectar rewards of f lowers.
Taken together, our results provide evidence of striking
differences in the floral preferences of bees and hummingbirds,
and considerable opportunity for the adaptive divergence of
floral traits through pollinator-mediated selection. This stands in
contrast to recent suggestions that pollinators typically have
broad preferences, and are therefore unlikely to contribute to
floral evolution or the reproductive isolation of sympatric taxa
(25, 34, 35). Floral traits associated with bumblebee and hummingbird pollination, such as petal carotenoid pigments and
nectar volume, appear to be under relatively simple genetic
control, with major QTLs responsible for pollinator discrimination and reproductive isolation in nature. This work contributes
to the growing body of evidence that adaptation may often
involve genes of large effect (3, 5, 36–39). Further studies are
needed to determine whether our results can be generalized to
other plant taxa where closely related species differ in their
major pollinators.
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11914 兩 www.pnas.org
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We thank B. Best, J. Coyne, and two anonymous reviewers for
thoughtful comments on the manuscript; B. Best, D. Ewing, B. Frewen,
J. McKay, K. Otto, Y. Sam, and K. Ward for technical assistance; E.
Sugden for identifying the bees; and J. van Wagtendonk, P. Moore, and
the staff of Yosemite National Park for permission to conduct our
research. This work was supported by the Royalty Research Fund of
the University of Washington and National Science Foundation Grant
DEB 9616522.
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EVOLUTION
32.
33.
34.
35.
105
PLoS BIOLOGY
Independently Evolving Species
in Asexual Bdelloid Rotifers
Diego Fontaneto1[, Elisabeth A. Herniou2,3[, Chiara Boschetti4, Manuela Caprioli1, Giulio Melone1, Claudia Ricci1,
Timothy G. Barraclough2,3,5*
1 Dipartimento di Biologia, Università di Milano, Milan, Italy, 2 Division of Biology, Imperial College London, Ascot, United Kingdom, 3 Natural Environment Research Council
Centre for Population Biology, Imperial College London, Ascot, United Kingdom, 4 Institute of Biotechnology, University of Cambridge, Cambridge, United Kingdom,
5 Jodrell Laboratory, Royal Botanic Gardens, Kew, United Kingdom
Asexuals are an important test case for theories of why species exist. If asexual clades displayed the same pattern of
discrete variation as sexual clades, this would challenge the traditional view that sex is necessary for diversification
into species. However, critical evidence has been lacking: all putative examples have involved organisms with recent or
ongoing histories of recombination and have relied on visual interpretation of patterns of genetic and phenotypic
variation rather than on formal tests of alternative evolutionary scenarios. Here we show that a classic asexual clade,
the bdelloid rotifers, has diversified into distinct evolutionary species. Intensive sampling of the genus Rotaria reveals
the presence of well-separated genetic clusters indicative of independent evolution. Moreover, combined genetic and
morphological analyses reveal divergent selection in feeding morphology, indicative of niche divergence. Some of the
morphologically coherent groups experiencing divergent selection contain several genetic clusters, in common with
findings of cryptic species in sexual organisms. Our results show that the main causes of speciation in sexual
organisms, population isolation and divergent selection, have the same qualitative effects in an asexual clade. The
study also demonstrates how combined molecular and morphological analyses can shed new light on the evolutionary
nature of species.
Citation: Fontaneto D, Herniou EA, Boschetti C, Caprioli M, Melone G, et al. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biol 5(4): e87. doi:10.1371/
journal.pbio.0050087
Although horizontal gene transfer can occur between
distantly related bacteria, homologous recombination occurs
only at appreciable frequency between closely related strains
[20,21]. Therefore, clusters in these bacteria could arise from
similar processes to interbreeding and reproductive isolation
in sexual eukaryotes [20]. Aside from issues of sexuality,
previous studies looking for distinct clusters have been
descriptive, relying on visual interpretation of plots of
genetic or phenotypic variation rather than on formal tests
of predictions under null and alternative evolutionary
scenarios [1].
Here, we demonstrate that a classic asexual clade, the
bdelloid rotifers, has diversified into independently evolving
and distinct entities arguably equivalent to species. Bdelloids
are abundant animals in aquatic or occasionally wet
terrestrial habitats and represent one of the best-supported
clades of ancient asexuals [22–24]. They reproduce solely via
parthenogenetic eggs, and no males or traces of meiosis have
ever been observed. Molecular evidence that bdelloid
Introduction
Species are fundamental units of biology, but there remains
uncertainty on both the pattern and processes of species
existence. Are species real evolutionary entities or convenient
figments of taxonomists’ imagination [1–3]? If they exist, what
are the main processes causing organisms to diversify [1,4]?
Despite considerable debate, surprisingly few studies have
formally tested the evolutionary status of species [1,5,6].
One central question concerning the nature of species has
been whether asexual organisms diversify into species [1]. The
traditional view is that species in sexual clades arise mainly
because interbreeding maintains cohesion within species,
whereas reproductive isolation causes divergence between
species [7]. If so, asexuals might not diversify into distinct
species, because there is no interbreeding to maintain
cohesive units above the level of the individual. However, if
other processes were more important for maintaining
cohesion and causing divergence, for example, specialization
into distinct niches, then asexuals should diversify in a
manner similar to sexuals, although the rate and magnitude
of divergence might differ [8–11].
Empirical evidence to test these ideas has been rare. Most
asexual animal and plant lineages are of recent origin [9,12].
The diffuse patterns of variation typical of such taxa [13]
could simply reflect their failure to survive long enough for
speciation to occur or the effects of ongoing gene flow from
their sexual ancestors [9,12]. Distinct genetic and phenotypic
clusters have been demonstrated in bacteria [14–17] and
discussed as possible evidence for clonal speciation [1].
However, all the study clades engage in rare or even frequent
recombination as well as clonal reproduction [14,18,19].
Academic Editor: Mohamed A. F. Noor, Duke University, United States of America
Received September 11, 2006; Accepted January 26, 2007; Published March 20,
2007
Copyright: Ó 2007 Fontaneto e al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author
and source are credited.
Abbreviations: GTR, general transition rate; PC, principal component; SEM,
scanning electron microscopy
* To whom correspondence should be addressed. E-mail: t.barraclough@imperial.
ac.uk
[ These authors contributed equally to this work.
0914
106
Speciation in Asexual Rotifers
Author Summary
branches from other such clusters (H1, Figure 2A; and [9]).
Coalescent models can be used to distinguish the two
scenarios [30]. Failure to reject the null model would indicate
a lack of evidence for the existence of independently evolving
entities.
Next, to investigate the role of adaptation to different
niches in generating and maintaining diversity within the
clade, we extend classic methods from population genetics to
test directly for adaptive divergence of ecomorphological
traits. If trait diversity evolves solely by neutral divergence in
geographic isolation, we expect morphological variation
within and between entities to be proportional to levels of
neutral genetic variation (H0, Figure 2B, Materials and
Methods). If, instead, different entities experience divergent
selection on their morphology, we expect greater morphological variation between clusters than within them, relative
to neutral expectations (H1, Figure 2B; and [31]). Past work
has often discussed sympatry of clusters as evidence for niche
divergence [1], but, in theory, coexistence can occur without
niche differences [32]; hence, we introduce an alternative,
more direct approach.
Our results demonstrate that bdelloids have diversified not
only into distinct genetic clusters, indicative of independent
evolution, but also into entities experiencing divergent
selection on feeding morphology, indicative of niche divergence. In common with findings of cryptic species in sexual
organisms [33,34], the morphologically coherent groups
experiencing divergent selection often include several genetic clusters: this introduces difficulties in deciding which units
to call species, but this problem is shared with sexual
organisms [3,33]. In short, bdelloids have diversified into
entities equivalent to sexual species in all respects except that
individuals do not interbreed. The results demonstrate the
benefits of statistical analyses of combined molecular and
morphological data for exploring the evolutionary nature of
species.
The evolution of distinct species has often been considered a
property solely of sexually reproducing organisms. In fact, however,
there is little evidence as to whether asexual groups do or do not
diversify into species. We show that a famous group of asexual
animals, the bdelloid rotifers, has diversified into distinct species
broadly equivalent to those found in sexual groups. We surveyed
diversity within a single clade, the genus Rotaria, from a range of
habitats worldwide, using DNA sequences and measurements of jaw
morphology from scanning electron microscopy. New statistical
methods for the combined analysis of morphology and DNA
sequence data confirmed two fundamental properties of species,
namely, independent evolution and ecological divergence by
natural selection. The two properties did not always coincide to
define unambiguous species groups, but this finding is common in
sexual groups as well. The results show that sex is not a necessary
condition for speciation. The methods offer the potential for
increasing our understanding of the nature of species boundaries
across a wide range of organisms.
genomes contain only divergent copies of nuclear genes
present as two similar copies (alleles) in diploid sexual
organisms rules out anything but extremely rare recombination [25–27]. Yet, bdelloids have survived for more than 100
million y and comprise more than 380 morphologically
recognizable species and 20 genera [28]. The diversity of the
strictly asexual bdelloids poses a challenge to the idea that sex
is essential for long-term survival and diversification [29].
However, taxonomy does not constitute strong evidence for
evolutionary species: the species could simply be arbitrary
labels summarizing morphological variation among a swarm
of clones [7]. We adopt a general evolutionary species
concept, namely, that species are independently evolving
and distinct entities, and then break the species problem into
a series of testable hypotheses derived from population
genetic predictions [3]. We use the word ‘‘entity’’ to refer to a
set of individuals comprising a unit of diversity according to a
given criterion or test: the question of whether to call those
entities ‘‘species’’ will be returned to below.
Focusing on the genus Rotaria (Figure 1), one of the bestcharacterized genera of bdelloids, we use combined molecular and morphological analyses to distinguish alternative
scenarios for bdelloid diversification (Figure 2). First, the
entire clade might represent a single species, that is, a swarm
of clones with no diversification into independently evolving
subsets of individuals. Second, the clade may have diversified
into a series of independently evolving entities. By ‘‘independently evolving,’’ we mean that the evolutionary processes
of selection and drift operate separately in different entities
[8,9], such that genotypes can only spread within a single
entity. Possible causes of independence include geographical
isolation or adaptation to different ecological niches [10,17].
The expected outcome is cohesion within entities but genetic
and phenotypic divergence between them [9–11].
We first test for the presence of independently evolving
entities. Under the null scenario of no diversification, genetic
relationships should conform to those expected for a sample
of individuals from a single asexual population (H0, Figure
2A). Under the alternative scenario that independently
evolving entities are present, we expect to observe distinct
clusters of closely related individuals separated by long
Results/Discussion
We collected all individuals of Rotaria encountered during
3 y searching rivers, standing water, dry mosses, and lichens,
centered on Italy and the United Kingdom but also globally
[35]. Individuals were identified to belong to nine taxonomic
species (Tables S1 and S2). Most of the described species of
Rotaria missing from our sample are known from only one
record or are very rarely encountered (Protocol S1). Bayesian
and maximum parsimony analyses of mitochondrial cytochrome oxidase I (cox1) and nuclear 28S ribosomal DNA
sequences provide strong support for the monophyly of
taxonomic species (Figures 3, S1, S2, and S3 and Text S1),
with the sole exception of R. rotatoria, which was already
suspected to comprise a species complex based on disagreements among authors [36,37].
Morphometric analyses further support the distinctness of
taxonomic species. Bdelloid morphology is hard to measure
because of their shape-changing abilities; hence, we used
geometric morphometrics [38] to measure the only suitable
trait, their hard jaws, called trophi [39] (Figures 1 and S4).
Trophi size and shape are not characters that have been used
in the traditional taxonomy of the genus (Table S2). Trophi
scale weakly with rough measures of body size of each species
(mean trophi size against log body length from [37]: r¼0.55, p¼
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107
Figure 2. Scheme Showing the Predicted Patterns of Genetic and
Morphological Variation Underlying Our Tests of Alternative Scenarios of
Diversification
(A) Hypothetical trees showing expected genetic relationships among a
sample of individuals under the null model that the sample is drawn
from a single asexual population (H0) and under the alternative model
that the clade has diversified into a set of independently evolving
entities (H1).
(B) Expected variation in two ecomorphological traits evolving either
neutrally (H0) or by adaptive divergence (H1) in a genus that has
diversified into six genetic clusters. Note that a mixed pattern is possible:
Some genetic clusters may have experienced divergent selection on
morphology, whereas others have not.
Figure 1. SEM Pictures of Some Species of the Genus Rotaria
(A) R. neptunia, lateral view; (B) R. macrura, ventral view; (C) R. tardigrada,
dorsal view; (D) R. sordida, lateral view; and (E) trophi of R. tardigrada
with open circles showing the location of landmarks used for the shape
analysis. Scale bars: 100 lm for animals, 10 lm for trophi.
sordida, and R. tardigrada (Table S3). The remaining species
overlapped in shape but could be discriminated by size
(Figures 4 and S5). Related species on the DNA trees tend to
have similar morphology: for example, R. magnacalcarata, R.
socialis, and R. rotatoria FR.2.1 and IT.5 overlap in shape, but are
more distant from R. rotatoria UK.2.2. Only two of the
traditional species found to be monophyletic in the DNA tree
displayed significant variation in size or shape among
populations: R. sordida and R. tardigrada. In both cases, the
populations that differed were deeply divergent in the DNA
tree as well.
Congruence between molecules and morphology confirms
0.2, Spearman’s rank test), and both the size and shape of
trophi likely reflect different types or sizes of particulate food
consumed, although the details of how food is processed
remain unclear [28]. Discriminant analysis of the first five
principal components (PCs) describing trophi shape (cumulative explained variance, 97.1%; Materials and Methods)
produced a correct classification with respect to traditional
taxonomy of most specimens of R. macrura, R. neptunia, R.
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108
Figure 3. Phylogenetic Relationships in the Genus Rotaria
The consensus of 80,000 sampled trees from Bayesian analysis of the combined cox1 and 28S rDNA data sets is shown, displaying all compatible
groupings and with average branch lengths proportional to numbers of substitutions per site under a separate GTR þ invgamma substitution model for
the cox1 and 28S partitions. Posterior probabilities above 0.5 and bootstrap support above 50% from a maximum parsimony bootstrap analysis are
shown above and below each branch, respectively. Support values for within-species relationships are not shown for very short branches but are shown
in Figures S1 through S3. Closed circles indicate clusters identified by the clustering analysis. Colors represent traditional species memberships.
Diamonds indicate taxonomic species and monophyletic groups of Rotaria. Names refer to the species, the country, the number of site within that
country for that species, and the number of individual from that site if several were isolated; for example, R.macr.IT.1.1 refers to the first individual from
site 1 in Italy for R. macrura. Pictures of trophi from one individual from each cluster are shown to scale: Representatives of all sampled populations are
shown in Figure S4. A full list of names and localities of samples is available in Table S1.
0917
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are present in bdelloids but at a lower level than taxonomic
species, that is, cryptic taxa within the taxonomic species.
However, the nature of independent evolution remains
unclear. Clusters might simply represent geographically
isolated, or even partially geographically isolated, populations
evolving neutrally [32,44]. Alternatively, the clade might have
diversified into ecologically distinct species experiencing
divergent selection pressures. To resolve these alternatives,
we test directly for divergent selection between different
lineages, adapting classic methods from molecular population
genetics [31,45]. If rotifers have experienced divergent
selection on trophi morphology between species, for example, adapting to changes in habitat or resource use, we expect
low variation within species and high variation between
species, relative to the same ratio for neutral changes.
To explore the level at which divergent selection acts on
morphology, we compared rates of morphological change
within clusters, between clusters within taxonomic species,
and between taxonomic species, in each case relative to silent
substitution rates in cox1, assumed to reflect neutral changes
(see Materials and Methods). The test is robust to sampling
issues and differences in mutational mechanism between
morphology and cox1 (see Materials and Methods). The results
reveal significant evidence for divergent selection on trophi
size and PC2 (Figure 5; Table S5). However, divergent selection
occurs between taxonomic species, not between clusters; both
traits are conserved within taxonomic species but diverge
rapidly between species, relative to neutral expectations.
Changes in PC1 are more complex, being lower between
clusters either than within clusters or between taxonomic
species. However, overall the results demonstrate divergent
selection on the size and some aspects of shape of the trophi.
Our results show that Rotaria has undergone adaptive
diversification in feeding morphology, presumably associated
with specialization to different habitats. The finding is
supported by observations of ecological differences among
the traditional species. For example, R. socialis and R.
magnacalcarata live externally on the body of the water louse
Asellus aquaticus but partition their use of the host, with the
former living around the leg bases and the latter on the
anterior, ventral surface. Our analyses show that these
traditional species, which are found living together on single
louse individuals, are evolutionarily independent and distinct
entities. Another traditional species, R. sordida, is found in
more terrestrial habitats than the other species, although it
sometimes co-occurs with R. tardigrada, which is generally
more aquatic (Table S2). Therefore, informal observations of
habitat partitioning and coexistence at local scales add
further support to the role of niche partitioning.
Not all of the entities identified as genetic clusters display
evidence of divergent selection on feeding morphology: the
signature of divergent selection was detected at a broader
level than that of independently evolving clusters. One
possible explanation is that some clusters arose solely from
neutral divergence in complete or partial geographical
isolation [32,44]. Some of the clusters do comprise geographically localized sets of samples, but at least one traditional species, R. macrura, contains two clusters without
obvious geographical separation. Alternatively, divergent
selection might act at different hierarchical levels on different traits [17]: clusters might have diverged in unmeasured
traits such as behavior, gross body morphology, or life history.
Figure 4. Plot of the Size and Shape (the First Two PCs, PC1 and PC2,
from the Generalized Procrustes Analysis) of Trophi across Species
The directions of shape variation along each axis are shown for PC1 and
PC2, respectively, using 32 and 34 magnification of the observed
variation for emphasis. PC1 represents a continuum from oval to rounder
trophi and from parallel to converging major teeth. PC2 represents a
trend in the distance of the major teeth from the attachment point
between the two halves of the trophi.
that most traditional Rotaria species are monophyletic clades
but does not rule out the possibility that taxa reflect variation
within a single asexual species or swarm of evolutionarily
interacting clones. Under the alternative scenario that
independently evolving entities are present, we expect to
observe clusters of closely related individuals separated from
other such clusters by longer internal branches on a DNA tree
[9,30,40]. We therefore tested for significant clustering by
comparing two models describing the likelihood of the
branching pattern of the DNA trees: first, a null model that
the entire sample derives from a single population following
a neutral coalescent [41], and, second, a model assuming a set
of independently evolving populations joined by branching
that reflects the timing of divergence events between them,
that is, cladogenesis [9,30,42]. The models allow departures
from strict assumptions of constant population size and rates
of cladogenesis (see Materials and Methods).
The results indicate significant clustering within Rotaria, as
expected if several independently evolving entities are
present and consistent with patterns of mtDNA diversity
from a broad sample of bdelloids [43]. The maximum
likelihood solution for the independent evolution model on
the combined tree infers 13 isolated clusters, with the
remaining individuals inferred to be singletons (Figure 3;
Table S4). Two monophyletic taxonomic species contained
two separate clusters: R. magnacalcarata has two clusters
corresponding to the U.K. and Italian samples, whereas R.
macrura has two clusters not matching sampling locality.
Uncorrected pairwise distances of cox1 within clusters ranged
from 0% to 3.3% (mean, 1.5%), and those between clusters
ranged from 4.1% to 23.1% (mean, 16.0%). The null model
that the entire lineage represents a single cluster can be
rejected (log likelihood ratio test, 2 3 ratio ¼ 30.8, v2 test,
three degrees of freedom, p , 0.0001).
Our results indicate that independently evolving entities
0918
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model of reproductive isolation and neutral divergence
[32,47,48]? In addition, clades differing in levels of recombination could be compared to determine how sexual reproduction affects the strength and rate of diversification. Does
the requirement for reproductive isolation limit opportunities for speciation in sexuals, or do their faster adaptive rates
promote stronger patterns of diversification than in asexuals
[9,49]? Microbial eukaryotes, prokaryotes, and fungi could
provide additional study clades for such studies [12], linked to
genetic studies verifying the presumed lack of recombination
[50].
Our study highlights the advantages of statistical analyses
of combined morphological and molecular data. Recent work
delimiting or identifying species from DNA barcode data
[34,51] has been criticized for relying on organelle genome
markers, which may not reveal recent divergences or reflect
the history of nuclear genes [52,53]. Morphology provides a
ready window on adaptive differences between populations,
often the first sign of divergence and at the present easier to
sample than the genes underlying important traits [54,55], but
has lacked the theoretical framework of DNA. Combined
analyses, sampling at the population level across entire clades,
offer new potential to uncover the nature of species and
biological diversity. Our methods could be readily applied to
sexual clades and to other cases presenting challenges to
current theories, such as groups in which barriers to
interbreeding appear to be weak or nonexistent [1].
Figure 5. Evolutionary Rates of Changes in Trophi Size and Shape
Rates are expressed as the variance in each trait per unit branch length.
Branch lengths are in units of the number of silent substitution per
codon of cox1. Estimates from the maximum model with three rate
classes are shown: within clusters, between clusters within taxonomic
species, and between taxonomic species. Error bars show confidence
limits within 2 log likelihood units of the maximum likelihood solution.
Hierarchical likelihood ratio tests indicated that the model for size could
be simplified to assume a joint rate for within cluster and between
cluster branches (Table S5).
DNA analyses. DNA was isolated either from clonal samples of five
to 25 individuals grown in the laboratory from a single wild-caught
individual or from single wild-caught individuals using a chelex
preparation (InstaGene Matrix; Bio-Rad, http://www.bio-rad.com).
The 28S rDNA and cox1 mtDNA were amplified and sequenced by
PCR as described in Protocol S1. Trees were reconstructed from the
cox1 and 28S rDNA matrices separately and from a combined matrix
for all individuals with at least one gene sequenced. Bayesian analyses
were run in Mr Bayes (http://mrbayes.csit.fsu.edu) 3.1.1 for 5 million
generations with two parallel searches, using a general transition rate
(GTR) þ invgamma model [56]. The combined analysis implemented a
partition model with a separate GTR þ invgamma model and rate
parameter for the two partitions. Maximum parsimony support was
assessed using 100 bootstrap replicates, searching each heuristically
with 100 random addition replicates and TBR branch swapping in
Paup*4.10. Eight individuals from the related genus Dissotrocha were
included as outgroups. Comparisons of the two genes are described in
Protocol S1 and Text S1.
Morphometric analyses. Trophi were prepared for scanning
electron microscopy (SEM) by dissolving soft tissues on a cover slide
with sodium hypochloride (NaOCl 4%), rinsing with deionized water,
dehydrating at room temperature, and sputter-coating a thin layer of
gold. Shape was measured by Generalized Procrustes Analysis (GPA)
[57] of six landmarks on digitized pictures of the cephalic (ventral)
view (Figure 1). GPA coordinates were used for PC analysis after
projection onto an Euclidean space tangent to the shape space (see
Protocol S1). Size was expressed as centroid size of the landmark
configuration. We attempted to culture all individuals, to allow
morphometrics and sequencing on individuals from the same clone.
However, not all clones survived in the laboratory; for these, we used
replicate individuals from the same wild population where possible.
In total, we measured 326 SEM pictures of trophi from 23
populations belonging to eight species (see Table S1b). For species
with both laboratory-cultured and wild-caught measures, we found
no evidence that sample type influenced either the mean or variance
of size and shape measures (Table S6), indicating respectively that
species differences are genetically based (not environmental) and that
there appears to be little genetic variation for morphology within
populations. Statistical analyses were performed using the R
statistical programming language [58] and routines in the Tps series
of programs [59].
Future work sampling additional genetic markers and
phenotypic traits for the identified clusters might distinguish
these alternatives.
So which level should we call ‘‘species’’? As increasingly
recognized in reviews of species concepts, the answer will
depend on which aspect of diversity is of most interest and on
the intended use of the delimitation [3,46]. For evolutionary
studies, for example, into how bdelloids might adapt to
changing environments, the genetic clusters provide statistical evidence of independent evolution within the traditionally recognized species that needs to be taken into account.
For ecological studies, the traditional species conform closely
to units that are ecologically distinct in terms of feeding
morphology. Perhaps surprisingly for a poorly studied group
of microscopic animals, traditional species limits appear to
be robust for many purposes with the exception of the
paraphyletic R. rotatoria. However, the important point here
is that the same issues apply to studies of sexual organisms.
Genetic surveys often reveal cryptic species within morphologically coherent sexual species and elicit the same arguments over their interpretation [3,33,34].
We conclude that bdelloids display the same qualitative
pattern of genetic and morphological clusters, indicative of
diversification into independently evolving and distinct
entities, as found in sexual clades. This refutes the idea that
sex is necessary for diversification into evolutionary species.
Similar approaches could be used to explore the nature of
species in sexual clades—for example, how often is speciation
accompanied by ecological divergence compared to a null
0919
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Clustering test for independent evolution. Under the null model
that the entire sample derives from a single population obeying a
single coalescent process, we calculated the likelihood of waiting
times, xi, between successive branching events on the DNA tree as
Lðxi Þ ¼ b eb
x
i
to each node. Below the branch are bootstrap percentages from a
maximum parsimony search with 100 bootstrap replicates each using
a heuristic search with 100 random addition replicates, TBR branch
swapping, and saving only one tree per addition replicate.
Found at doi:10.1371/journal.pbio.0050087.sg001 (21 KB PDF).
ð1Þ
Figure S2. Phylogenetic Relationships from Bayesian Analysis of cox1
Posterior probabilities are indicated above each branch; parsimony
bootstrap values are indicated below each branch.
with
p
b ¼ kðni ðni 1ÞÞ
ð2Þ
where ni is the number of lineages in waiting interval i, k is the
branching rate for the coalescent (the inverse of twice the effective
population size in a neutral coalescent), and p is a scaling parameter
that allows the apparent rate of branching to increase or decrease
through time, fitting a range of qualitative departures from the strict
assumptions of a neutral coalescent, for example, growing (p , 1)
or declining (p . 1) population size [30]. Under the alternative model
that the sample derives from a set of independently evolving
populations, each one evolving similarly to the null case, we
calculated the likelihood of waiting times as Equation 6 from Pons
et al. [30]. The alternative model optimizes a threshold age, T, such
that nodes before the threshold are considered to be diversification
events with branching rate kD and scaling parameter pD. Branches
crossing the threshold define k clusters each obeying a separate
coalescent process but with branching rate, kC, and scaling
parameter, pC, assumed to be constant across clusters. The
alternative model thus has three additional parameters. Models were
fitted using an R script available from T.G.B. to an ultrametric tree
obtained by rate smoothing the combined analysis DNA tree using
penalized likelihood in r8s (http://ginger.ucdavis.edu/r8s) and crossvalidation to choose the optimal smoothing parameter for each tree
[60].
Test for divergent selection. In an asexual clade, all genes have the
same underlying genealogy: the entire genome is inherited as a single
unit. Assuming that silent substitutions are neutral, the expected
number of silent mtDNA substitutions on a branch of the genealogy
is lt, where t is the branch length in units of time and l is the
mutation rate of the gene. Assuming a neutral morphological trait
evolving by Brownian motion, the expected squared change
(variance) along a branch is r2m t, where r2m is the mutational rate of
increase of variance [61]. The expectations are the same for branches
within populations or between them. Therefore, the average rate of
change of a neutral trait expressed as variance per silent substitution
should be the same within populations as between them, that is,
r2m =l : This prediction holds even if mutation rates vary across the
tree, providing they do so without a systematic bias between the
branch classes being compared, a reasonable assumption shared with
widely used molecular versions of the test [31].
We reconstructed evolutionary changes in trophi size and shape
(PC1 and PC2) onto the DNA tree using the Brownian motion model
by Schluter et al. [62] implemented in the Ape library for R [63].
Branch lengths were optimized as the proportion of silent substitutions per codon using PAML software [64]. The null model
assumes a constant rate of morphological change across the entire
tree. The alternative model labels branches as between taxonomic
species, within species and within clusters, and estimates different
rates for each class. Under a three rate-class model, the likelihood of
the reconstruction, Equation 3 of [62] becomes the product of the
equivalent likelihood for each class of branches.
3
1
Qð~
lk Þ
ð3Þ
Lð~
l1:k ; b1:k Þ} P N1 exp
k¼1 b
2bk
k
Figure S3. Phylogenetic Relationships from Bayesian Analysis of 28S
rDNA
Posterior probabilities are indicated above each branch; parsimony
bootstrap values are indicated below each branch.
Figure S4. SEM Pictures of Trophi from Each Study Population
(A) R. macrura macrIT2; (B) R. macrura macrIT1; (C) R. macrura
macrIT3; (D) R. macrura R.macr.UK.1; (E) R. magnacalcarata magnIT1;
(F) R. magnacalcarata magnIT3; (G) R. magnacalcarata magnIT2; (H) R.
magnacalcarata R.magn.UK.2.1; (I) R. socialis sociIT1; (J) R. socialis
sociIT2; (K) R. socialis sociIT3; (L) R. socialis R.soci.UK, (M) R. rotatoria
R.rota.IT.5; (N) R. rotatoria R.rota.FR.2.1; (O) R. rotatoria R.rota.UK.2.2;
(P) R. sordida sordIT1; (Q) R. sordida sordIT2; (R) R. sordida sordAU; (S)
R. neptunoida noidIT; (T) R. neptunia R.nept.IT, (U) R. tardigrada
tardIT1; (V) R. tardigrada tardIT3; (W) R. tardigrada R.tard.US; and (X)
landmarks and links used for shape analysis.
Figure S5. Box Plot of the Size of Trophi for Each Study Population
Analysis of variance test, ln CS: F22,303 ¼ 684.17, p , 0.0001.
Protocol S1. Sampling, Molecular Analyses, and Morphometrics
Found at doi:10.1371/journal.pbio.0050087.sd001 (87 KB PDF).
Protocol S2. Test for Divergent Selection on Morphology
Table S1. Locality Records for DNA Sequences and Morphometric
Measurements
Found at doi:10.1371/journal.pbio.0050087.st001 (78 KB PDF).
Table S2. Traditional Taxonomy of Rotaria Species
Table S3. Discriminant Analysis of Trophi Shape
Table S4. Comparison of Models of Single versus Multiple Independently Evolving Entities
Table S5. Comparison of Alternative Models for Rates of Changes in
Trophi Size and Shape within and between Clusters and Species
Table S6. The Effects of Sampling Type (Clonal versus Population
Sample) on the Mean and Variance of Size and Shape of Trophi
where k indicates the branch classes from 1 to 3, bk is the rate
parameter for each class of branches, Nk is the number of nodes
ancestral to each class of branch, and Q(ũk) is the sum of the scaled
variance of changes across branches [62] of class k. Optimization was
implemented in a modified version of the ‘‘ace’’ function of Ape,
available from T. G. B. Divergent selection between taxonomic
species, for example, would be indicated by a significantly lower rate
within cluster and within species branches (classes 1 and 2) than
between species branches (class 3). Assumptions and robustness of the
test are discussed further in Protocol S2.
Text S1. Comparison of cox1 and 28S rDNA Results
Accession Numbers
DNA sequences have been deposited at GenBank (http://www.ncbi.
nlm.nih.gov/Genbank) under accession numbers DQ656756 to
DQ656882.
Acknowledgments
Supporting Information
We thank Bill Birky, Jr., Austin Burt, Andrea Cardini, Fred Cohan,
Brian O’Meara, Ian Owens, Andy Purvis, Vincent Savolainen, Michael
Turelli, and two anonymous reviewers for their help.
Author contributions. DF, EAH, GM, CR, and TGB conceived and
Figure S1. Phylogenetic Relationships from Bayesian Analysis of the
Combined Data
Posterior probabilities from the Bayesian analysis are indicated next
0920
112
designed the experiments. DF, EAH, CB, and MC performed the
experiments. DF, EAH, CB, and TGB analyzed the data. GM, CR, and
TGB contributed reagents/materials/analysis tools. DF, EAH, CR, and
TGB wrote the paper.
Funding. This research was supported by Natural Environment
Research Council UK grant NER/A/S/2001/01133, a Systematics
Association and The Linnean Society of London Systematics Fund
travel grant to DF, a Royal Society University Research Fellowship to
TGB, a Royal Society Dorothy Hodgkin Fellowship to EAH, and a
Royal Society International Joint Project grant to CR and TGB.
Competing interests. The authors have declared that no competing
interests exist.
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Problems and paradigms
Dualism and conflicts in
understanding speciation
Menno Schilthuizen
Summary
Speciation is a central but elusive issue in evolutionary
biology. Over the past sixty years, the subject has been
studied within a framework conceived by Ernst Mayr and
Theodosius Dobzhansky and subsequently developed
further by numerous other workers. In this `ìsolation''
theory, the evolution of reproductive isolation is a key
element of speciation; natural selection is given only
secondary importance while gene flow is considered
prohibitive to the process. In this paper, I argue that
certain elements in this approach have produced confusion and irreconcilability among students of speciation.
The more prominent debates in speciation (i.e., the
species definition, sympatry/allopatry, and the role of
reinforcement) all derive from an inherent conflict
between the `ìsolation'' theory and Darwin's ``selection''
view on species and speciation (in which disruptive
selection is crucial). New data, mainly from field ecology,
molecular population genetics, laboratory studies with
Drosophila and computer analysis, all suggest that the
isolation theory may no longer be the most desirable
vantage point from which to explore speciation. Instead,
environmental selection in large populations, often
unimpeded by ongoing gene flow, appears to be the
decisive element. The traditional preoccupation with
reproductive isolation has created gaps in our knowledge
of several crucial issues, mainly regarding the role of
environmental selection and its connection with mate
selection. BioEssays 22:1134±1141, 2000.
ß 2000 John Wiley & Sons, Inc.
Introduction
Speciation, the evolution of new species, is a central but unresolved issue in evolutionary biology.(1) What is the essence
of speciation? What geographical conditions are required for it
to happen? What evolutionary forces are crucial? Many
answers have been given to these questions and often appear
irreconcilable.(2) This has given rise to the conviction that
speciation is a very multifarious phenomenon, which defies
any generalisation. As I will argue in this paper, this confusion
stems largely from a conflict between two theories on speciation that have existed side-by-side for the past sixty years. The
Laboratory of Genetics, Wageningen University, Wageningen, The
Netherlands. Present address: Institute for Tropical Biology and
Conservation, Universiti Malaysia Sabah, Locked Bag 2073, 88999
Kota Kinabalu, Sabah, Malaysia. E-mail: [email protected]
1134
BioEssays 22.12
first of these theories is the one put forward by Charles Darwin
in 1859.(3) The second is the theory developed as part of the
Modern Synthesis in the 1930s and 1940s. Since the theories
differ chiefly in their emphasis on which factor drives populations apart, I will refer to them as the ``selection theory'' and the
`ìsolation theory'', respectively.
I will first recapitulate some aspects of the historical development of speciation theory, outline the basic tenets of both
views, and highlight the conflicts between them. Then I will
review three prominent debates related to speciation and
argue that all are reflections of those conflicts. At the same
time, I will describe recent data from field ecology, molecular
population genetics, laboratory experiments with Drosophila
and computer analysis, which suggest that a modernised
version of Darwin's view is more likely to bring progress in the
field than an emphasis only on the isolation theory.
The conflict
Species and speciation form the basis of one of the longeststanding debates in biology. Dedicated attempts to define
species were made as early as the 17th century.(4± 6) No single
early author, however, devoted as much time to it as Darwin,
whose expertise in taxonomy made him the foremost authority
on species in the mid-19th century. In On the Origin of Species
by Means of Natural Selection, he elaborated the point that
species are no more than ``well-marked varieties'', and that the
term was `àrbitrarily given for the sake of convenience to a set
of individuals closely resembling each other''.(3) He added that
the ``search for the undiscovered and undiscoverable essence
of the term species'' was in vain, as it was an attempt at
``defining the undefinable''.(7)
Most present day biologists consider Darwin's opinion
outdated and mainly accept the ``biological species concept''
(BSC). The BSC, which was developed during the 1930s by
Ernst Mayr and Theodosius Dobzhansky, hinges (unlike
Darwin's concept) primarily on reproductive barriers. Mayr
defined species as ``groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups''.(8) Dobzhansky consequently
applied the BSC to define the process by which species arise
(i.e., speciation) as ``that stage of the evolutionary process at
which the once actually or potentially interbreeding array of
forms becomes segregated into two or more separate arrays
which are physiologically incapable of breeding''.(9)
BioEssays 22:1134±1141, ß 2000 John Wiley & Sons, Inc.
114
It is important to realise that the BSC was not primarily
intended as a convenient criterion for sorting taxa. Instead, it
was an essential part of a multidisciplinary theory of speciation. This theory developed in a number of logical steps. Mayr's
vast ornithological experience with geographic variation and
endemism in New Guinea and Polynesia, and similar data from
other groups of organisms, had convinced him that geographical isolation (allopatry) was cardinal to the speciation
process. His 1942 book Systematics and the Origin of
Species, was intended to show that the ``crucial process in
speciation is not selection [ . . . ], but isolation''.(10) The fact that
isolation was crucial meant that the processes responsible
for allopatric differentiation would break down under gene
flow. So, sympatry would only be possible once reproductive
isolation had evolved. In the absence of reproductive isolation,
two differentiated populations would fuse again upon secondary contact. Therefore, reproductive isolation needed to be
the decisive criterion for what constitutes a species, and the
evolution of reproductive isolation would define the point
where speciation has been completed.
The processes responsible for generating reproductive
isolation among populations were considered to be a subtle
combination of genetic drift, natural selection, and epistasis,
acting in small ``peripherally isolated'' populations. Mayr
proved (1954, 1963) that, under the right circumstances, the
combined effects of these forces could produce new coadapted gene complexes with reconstituted reproductive
systems, i.e., new species under the BSC.(4,11) So, the theory
of speciation developed by Mayr and Dobzhansky relies
almost exclusively on the evolution of reproductive isolation
for explaining the origin and maintenance of species. To
many biologists, the development of this theory was an
improvement on Darwin, who had not realised the importance
of reproductive isolation and hence lacked a clear theory on
speciation.
Both these claims about Darwin, however, are not entirely
correct. Contrary to popular belief, Darwin was well-aware of
reproductive isolation between species. For example, he
starts chapter 8 of On the Origin of Species with: ``The view
generally entertained by naturalists is that species, when
intercrossed, have been specially endowed with the quality of
sterility, in order to prevent the confusion of all organic
forms''.(3) Darwin, however, knew that hybridisation is common among many groups of animals and plants, without
affecting the distinctness of species. This was one of the
reasons why he did not consider reproductive isolation of
crucial importance, writing that ``neither sterility nor fertility
affords any clear distinction between species or varieties''.(3)
To Darwin, then, speciation (or, as he called it, ``divergence of
character'') was not brought about by the evolution of
reproductive barriers, but by a mechanism that would force a
single species in two directions, reproductively isolated or not.
This mechanism was natural selection, which would not just be
able to make a single species change by adaptation, but also to
make a single species split in two.
Darwin observed that an assemblage of species is more
efficient at exploiting a patch of habitat than a single species.
By analogy, he reasoned that, under conditions of severe
competition, natural selection will favour those individuals
within a population that have the most extreme phenotypes,
and therefore suffer the least from competition with relatives.
``Consequently, I cannot doubt that in the course of many
thousands of generations, the most distinct varieties of any
one species [ . . . ] would always have the best chance of
succeeding and of increasing in numbers, and thus of supplanting the less distinct varieties; and varieties, when
rendered very distinct from each other, take the rank of
species''.(3)
The main difference between Darwin's view and the one
elaborated by Mayr and Dobzhansky, then, is the role of
natural selection. To Darwin, natural selection could make a
single population change to suit a changing environment
(adaptation) or it could force a single population in two, to
better exploit the available niches (speciation). Mayr and
Dobzhansky, in contrast, decoupled adaptation from speciation; environmental selection is a causative agent only in
adaptation. As I hope the following paragraphs will show, much
of the confusion about speciation is the result of the fact that
the isolation theory has become embedded in the selectionbased neodarwinian school. Three conflicts in evolutionary
biology are probably the direct result from this irreconcilability.
These are the species definition, the allopatry/sympatry, and
the reinforcement debates.
The species definition debate
In Mayr's writings, two views on species appear. The first is
that all individuals of a species share the same well-integrated
complex of epistatically and pleiotropically interacting genes.
This is the species concept, and Mayr writes that the evolution
of two well-integrated gene complexes from a single ancestral
one is ``the essence of speciation''.(4) At the same time,
however, the biological species definition makes no mention
of gene complexes, but rather of devices for reproductive
isolation. Consequently, Mayr can also be found writing that
``speciation is characterized by the acquisition of these
devices''.(4) What transpires is that Mayr did not claim that
reproductive isolation per se was essential, but that new
gene complexes can not evolve nor persist before such
barriers to gene flow were in place: ``Reproductive isolation
refers to the protective devices of a harmoniously coadapted
gene pool against destruction by genotypes from other gene
pools''.(4)
The contrast between Mayr's species concept (coadapted
gene complexes) and his species definition (reproductive
isolation) is illustrated by his discussion of cytoplasmic incompatibility in insects. This phenomenon, which is now known to
BioEssays 22.12
115
1135
be caused by the bacterium Wolbachia,(12,13) can produce full
reproductive isolation between populations infected by different strains of the symbiont. Hence, Laven(14) suggested that
cytoplasmic incompatibility could be a mechanism for instantaneous speciation. Mayr,(4) however, objected that two
cytoplasmically incompatible populations `ànswer the definition of [...] species, yet there is serious doubt whether it would
be legitimate to label as species allopatric strains that may
differ by only a single genetic factor.'' Apparently, even though
this single factor conveyed complete intersterility, Mayr hesitated to apply the BSC, because the evolution of two different,
coadapted gene complexes had not taken place.(15)
Recent molecular population genetic data, however, suggest that the BSC with its reproductive-isolation criterion does
not automatically follow from a concept of a species as a coadapted gene complex, because the latter can persist in spite
of the absence of reproductive barriers. In the fruit fly species
complex Rhagoletis pomonella, for example, an estimated
gene flow of 6% does not negate the effects of disruptive
selection for an apple- and a hawthorn-feeding species.(16)
Another example comes from microsatellite studies of two
European oak species. In spite of pervasive interspecific
hybridization and gene flow, the two sympatric species remain
morphologically, ecologically and genetically distinct.(17)
Furthermore, based on mtDNA and microsatellite data,
vertebrate species(18,19) have been shown to exhibit considerable gene flow across ecotones. Nevertheless, this has not
prevented the divergent environmental selection pressures
on either side of the ecotones resulting in the build-up of
differently coadapted gene complexes.(20)
These new data suggest that species differences can
persist in the face of gene flow. Therefore, the importance of
``protective devices'' in the form of reproductive isolation
mechanisms may have been overstated. Consequently, since
the relevant characteristics of species can also be attained
without the protection of complete reproductive isolation, the
case for using this property as a sine qua non for characterising
species has been considerably weakened. What remains is
the valuable insight that species are stable coadapted gene
complexes. Disconnected from reproductive isolation, it is not
possible or desirable to formalise this notion into a strict
species definition. In evolutionary biology, it should be sufficient to study the evolution of such gene complexes, without
any reference to the category assigned to them. In taxonomy,
the BSC has only incidentally been used as a standard to test
systematic revisions against and Darwin's motto that ``the
opinion of naturalists having sound judgement and wide
experience seems the only guide to follow'',(3) has never
ceased to be important.
The sympatry/allopatry debate
The single most conspicuous conflict in speciation undoubtedly is the sympatry/allopatry debate.(1,4,21) Can speciation
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BioEssays 22.12
116
occur without geographic isolation? If so, how easily, how
quickly and under what circumstances does it occur? In
Darwin's theory of speciation (see above), sympatry is an
implied prerequisite. Here, speciation is fueled by intraspecific
competition. The most extreme phenotypes are selected,
since they suffer least from mutual exclusion. By necessity,
this process takes place only in full sympatry. In the isolation
theory, on the contrary, there is no place for sympatry. Since in
this framework any gene flow is expected to disrupt the
evolution of new coadapted gene complexes, it is inconceivable that two different gene complexes could diverge within
the same population, without any prior reproductive isolation.
Dobzhansky wrote: ``Species are distinct because they carry
different constellations of genes. Interbreeding [ . . . ] results in
a breakdown of these systems [ . . . ]. Hence, the maintenance
of species as discrete units is contingent on their isolation.
Species formation without isolation is impossible''.(9)
Empirical data exist for both allopatric and sympatric
speciation, however. On the one hand, Mayr's work remains
one of the most comprehensive enumerations of evidence for
allopatric speciation, listing numerous instances where populations isolated by geographic barriers have genetically
diverged to a small or large extent.(4) On the other hand,
evidence for speciation in sympatry has also been accumulating steadily, especially in the past two decades. Some of this
evidence is indirect: molecular phylogenetics of sympatric
groups of freshwater fish in constricted environments (small
lakes, the waters around rocky islands or a single stream
system) has revealed monophyly.(22± 24) Other evidence is
more direct: observed host shifts in several groups of insects
have led to the origin and maintenance of genetically differentiated host-specialists.(25± 29)
These conflicting observations have produced a consensus among many evolutionary biologists that speciation is
multifarious. It can be allopatric, when it is caused by isolation,
or sympatric, when selection is the driving force. Differences of
opinion revolve primarily about the prevalence of either mode.
The two modes may not be so different, however, and, instead,
they could be two ends of a continuum of gene-flow opportunities, with selection as the driving factor across the range. To
assess the merits of this view, it may be worthwhile to investigate in more detail the respective roles of selection and isolation in allopatry.
To begin with the latter, indications exist that even in
classical cases of allopatry (populations isolated in caves, on
islands, or in habitat fragments) residual gene flow remains
among the supposedly isolated populations. Populations of
cave organisms, for example, have been shown to be interconnected by subterranean populations living in minute rock
crevices,(30) while land snail populations on isolated limestone
hills probably exchange genes via low-density populations on
non-calciferous soils.(31) The degree of isolation, then, may
often have been overestimated.
The role of selection, in contrast, may have been undervalued in models of allopatric speciation. In the basic allopatry
model, a species' range becomes bisected by a physical
barrier, producing two very large daughter populations. With
this model, since selective differences are likely to be small,
and the populations so large that genetic drift is close to zero,
speciation will proceed slowly, if at all. Stebbins,(32) for
example, pointed out that American and Asian sycamore
trees, after millions of years of isolation, have failed to evolve
reproductive isolation. According to Mayr,(33) the rise of the
Isthmus of Panama, which partitioned entire marine biotas into
a Pacific and a Caribbean portion 3.5 million years ago, had
produced ``two collossal gene pools'', and ``differences are still
either nonexistent or they are so slight that one doesn't really
like to rank these as species.''
In the isolation framework, where founder effects and
genetic drift play an important role, large isolated populations
are not expected to be the ideal situation for the evolution
of new coadapted gene complexes. Stebbins's sycamore
enigma, for example, was explained by Mayr(4) by arguing that
the two populations had been too large to be genetically
restructured and hence continued to share the same balancing
systems. An alternative for basic allopatry is the bottleneck
model, in which geographically isolated populations are
founded by a very small number of colonists. In such a small
population, random changes in gene frequencies and the
ensuing changes in epistasis could, theoretically at least,
cause a genetic revolution, leading to a new coadapted gene
complex, which subsequently could possibly shift into a new
niche.
Little evidence for bottleneck speciation exists, however.
Five small-scale(34) and three large-scale(35 ±37) laboratory
studies have largely yielded negative results. Molecular data
from field populations also do not support the idea. Ancient
allele polymorphisms in island species flocks, long regarded
as prime examples of speciation by founder effects, were discovered to be high. Enzyme polymorphisms in the Hawaiian
Drosophilas are just as high as those in their mainland
counterparts,(38) and in the GalaÂpagos finches, 21 ancient
allele variants were found at an Mhc locus.(39) The persistence
of high numbers of ancient haplotypes is inconsistent with very
small numbers of colonists. In the case of the GalaÂpagos
finches, the founding populations must at least have been as
large as forty birds, and probably several hundred.
At the same time, new data tend to favour the basic
allopatry model. The Panama Isthmus, regarded by Mayr as
ineffective in producing allopatric speciation, is now known
to have caused the evolution of numerous reproductively
isolated species in various groups of marine organisms.(40)
Knowlton and co-workers(41,42) for example, have shown that
the isthmus separates almost twenty pairs of sister species of
snapping shrimp. All species pairs are reproductively isolated
while morphologically very similar, and their mtDNA diver-
gence corresponds well with the geological age of the barrier.
Nevertheless, there can be no doubt that the populations have
always been very large, which rules out any bottleneck effects
or genetic drift. In contrast, transisthmian environmental
differences are considerable, including tidal influence, nutrient
content and temperature fluctuations, which might better
explain the genetic differentiation.
Laboratory studies, too, have shown that reproductive
isolation can build up in `àllopatric'' populations exposed to
different selection regimes. Rice and Hostert(34) cite numerous
experiments using Drosophila that resulted in prezygotic
reproductive isolation. Some experimenters(43,44) also tested
the development of reproductive isolation between allopatric
populations that experienced the same selection pressure,
and obtained negative results. These developments indicate
that in both allopatric speciation and sympatric speciation,
adaptation to different niches is the driving force, although
stronger selection pressures are required to produce speciation in the latter. This selection pressure will often be met
because of strong competition in sympatry.
The reinforcement debate
The reinforcement model of speciation says that populations
that have attained a certain degree of postzygotic reproductive
isolation in allopatry (as shown by reduced hybrid fitness),
are expected to improve prezygotic reproductive isolation
on secondary contact, given natural selection for assortative
mating.(9,45± 47) In view of its reliance on reproductive isolation
alone, reinforcement can thus be seen as fully consistent with
the `ìsolation'' view of speciation.
To better define the role of reinforcement in speciation,
Butlin distinguished between the processes of reproductive
character displacement (namely, the adaptive increase of
assortative mating between populations that have already
experienced full postzygotic reproductive isolation) and
reinforcement (that is, adaptive increase of assortative mating
between populations that have experienced only partial
postzygotic reproductive isolation).(45,46) With this distinction
in mind, we see that reproductive character displacement is
not a speciation process under the isolation theory, whereas
reinforcement is. Nevertheless, the basic evolutionary mechanism (selection for assortative mating) is identical in both
processes.
Butlin's papers, which also carried criticism against the
probability of reinforcement actually operating in nature, were
followed by a number of theoretical,(47 ±49) comparative(50,51)
and empirical(52,53) studies. Liou and Price(49) showed that,
under conditions of low hybrid fitness and considerable initial
genetic divergence between the two hybridising populations,
reinforcement could indeed reduce gene flow to zero. The
empirical studies, which were done on flycatchers(53) and
Drosophila,(52) supported this, as they showed an increase in
assortative mating in sympatry, whereas hybrid fitness was
BioEssays 22.12
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low but not zero. The comparative studies on Drosophila,
finally, showed that sympatric species have relatively stronger
prezygotic isolation than allopatric species, which also lends
support to reinforcement as a relevant speciation mode in this
group.
From the viewpoint of the isolation theory, then, these
recent data suggest that reinforcement can and does indeed
produce new species. From the viewpoint of the selection
theory, however, the relevance of reinforcement is reduced.
As the process acts only on pairs of populations that are
already genetically and ecologically diverged and that have a
strong (though not complete) degree of reproductive isolation,
it can be argued that reinforcement is not a speciation mode
because it is not instrumental in the populations' divergence.
It only serves to reduce gene flow to zero. If the selection
viewpoint is adopted, reinforcement represents the same
phenomenon as reproductive character displacement: it is
adaptation within two populations that have already speciated.
Redefining the role of reproductive isolation
In the previous paragraphs, I have argued that the selection
view may eventually be a preferable platform for discussing
species and speciation than the isolation view. Selection,
rather than reproductive isolation, appears to be what drives
and keeps species apart, both in allopatric and in sympatric
situations. It will be interesting, however, to examine in more
detail the precise role of reproductive isolation, for two
reasons. (1) Models and observations exist where full prezygotic and/or postzygotic isolation evolves between populations without any obvious environmental selection. (2)
Reproductive isolation is still important, as it will act as a
catalyst of speciation processes that are initiated by selection.
Two types of ``non-environmental'' reproductive isolation,
i.e., without any direct connection to environmental selection,
can be envisaged. First, there are situations of the `ìnstantaneous kind, where a single trait becomes fixed in a population,
rendering it reproductively isolated from other populations.
Examples include bidirectional cytoplasmic incompatibility
in arthropods due to infection by the bacterial symbiont
Wolbachia, as mentioned above,(14,15,54,55) coil reversal in
globular snails, which causes mechanical incompatibility of
the genitalia,(56± 58) and polyploidy in plants, which leads to
inviability of hybrids due to aneuploidy.(4) Second, recent
advances in the field of sexual selection suggest that isolated
populations can easily diverge in their systems for sexual
signalling. Computer analysis of ``runaway'' sexual selection
has shown that this process exhibits unpredictable, cyclical
behaviour, which is likely to run out of phase in allopatric
populations.(59) This means that, soon after geographic
separation, male signals in one population may no longer
coincide with a preference in females of the other population,
leading to prezygotic isolation. Moreover, allopatric populations are likely to diverge in the complicated sets of traits that
1138
BioEssays 22.12
118
are involved in male±male sperm competition, sexual
manipulation of females by males, and the female prevention
of the latterÐa set of selective pressures referred to as
sexually antagonistic selection.(60) Again, if males and females
do not coevolve (as in allopatric populations), their compatibility will decrease, resulting eventually in both prezygotic and
postzygotic isolation.
All the situations mentioned above should result in a
situation where isolation is attained first, unrelated to environmental selection, after which the resultant genetic partitioning
would allow for independent adaptation in both daughter
populations. Will the latter actually happen? Two facts make
subsequent niche shifts unlikely in the `ìnstantaneous'' situations. First, the reproductive isolation trait will usually be the
only genetic difference between populations that are incompatible due to Wolbachia infection, coil reversal, or polyploidy.
Second, the environment will remain unaltered. In coil reversal
and Wolbachia infection, respectively, the conditions for the
establishment(61) and maintenance(15) of the isolation are
restrictive, and empirical evidence is rare.(54,58,62) Allopolyploid (rather than autopolyploid) plants, however, are an
exception. The combination of two different genomes may
allow the new polyploid to be preadapted to a niche that is
intermediate between those of its parents. In fact, studies of
recently originated allopolyploids show that these establish
successfully in such intermediate habitats (e.g., Tragopogon
in North America see Refs. 63,64). Possibly, allopolyploid
speciation may be a case where the isolation view is more
appropriate than the selection view. However, the same may
not be true for situations where isolation is attained through
sexual selection and/or sexually antagonistic selection.
On the one hand, there is no doubt that speciation is often
associated with strong divergence in traits for assortative
mating and/or postzygotic isolation. For example, Odysseus, a
gene responsible for hybrid male sterility between Drosophila
simulans and D. mauritiana has turned out to be a homeobox
gene, expressed in the testes, which evolves extremely rapidly
due to an unknown selection pressure.(65,66) (See the article
by Orr and Presgraves, this issue.) The fact that molecular
phylogenies of the Drosophila simulans clade using this gene
show better resolution than those using other genetic markers,
suggests that it has been important in the speciation process
from a very early stage onwards.(67) Many other genes involved in reproduction show similar evidence for strong
selection, although usually it is not known if these genes are
responsible for reproductive isolation between species.(68 ± 70)
Other evidence comes from comparative studies of speciation
rates in birds, which generally show that polygamous clades
(where ``runaway'' sexual selection will be more prevalent),
show higher speciation rates.(71,72) In effect, sexual selection
can play a major role in incipient isolation.
On the other hand, however, sexual selection and sexually
antagonistic selection may often be chanelled by natural
Box 1. Two concepts of speciation
`Ìsolation'' concept
Speciation initiated by:
``Selection'' concept
Speciation progresses by:
Disruption of gene flow due to geographical, temporal, ecological,
or any other type of gene-pool segregation; most rapid in
peripheral isolates, but also possible in other geographic settings
Genetic drift and founder effects, natural selection or both
Speciation completed when:
Pre- and/or postmating reproductive isolation has evolved
Accompanying species
concept:
Geographic setting:
Biological species concept
Natural selection and superimposed sexual
selection
Differently adapted gene pools have
evolved
Darwin's species definition
Most rapid in peripheral isolates, but also possible in other
geographic settings
Most-rapid in sympatry, but also possible in
other geographic settings
selection. Colour variation in male guppies(73) and possibly
also cichlids,(74) for example, is influenced by the presence or
absence of predatory birds, and mate selection in fishes is
often by body size, which is also an environmentally selected
trait.(75) In addition, many types of reproductive isolation have
been shown to be caused secondarily by environmental
selection. For example, flowering time in monkeyflowers has
diverged due to water regimes of the soil(76) and diurnal mating
rhythms in melon flies have been shown to diverge as a
correlated response to larval development time.(77) Therefore,
possibly, even in cases where species appear to have formed
primarily due to the evolution of reproductive isolation, this
reproductive isolation may have been actually superimposed
on an underlying environmental selection.
In general, then, the role for reproductive isolation may be
seen as catalytic, rather than instrumental in speciation. The
buildup of differently adapted gene pools will be disrupted by
recombination. Because assortative mating and postzygotic
isolation can prevent this, selection and reproductive isolation
are probably best viewed as mutually reinforcing, as has been
pointed out by Rice and Hostert: once an initial episode of
strong environmental selection causes partial reproductive
isolation as a by-product, weaker selection (which otherwise
would have been hampered by gene flow) will then be able to
differentiate the two populations further, which in turn causes
further reproductive isolation, and so on.(34)
Conclusions
In this paper, I have attempted to argue that many of the
debates concerning speciation are the result of conflicts
between the ``selection'' and `ìsolation'' views on species and
speciation. The biological species concept, the scepticism
towards sympatric speciation, the emphasis on genetic drift,
and the popularity of reinforcement are all features of the
isolation theory, which views speciation as a process that
begins and ends with the acquisition of reproductive isolation.
Recent data, however, allow a re-appreciation of the role of
Adaptation to different environments
natural selection. Reproductive isolation is then seen to take a
catalytic, rather than an instrumental role. This view on species
and speciation is surprisingly compatible with Darwin's ideas
on the subject.
Future work on the role of environmental selection should
fill conspicuous gaps in our knowledge of speciation. The
experiments by Kilias and co-workers(43) and Dodd,(44) which
showed that prezygotic and weak postzygotic isolation
evolved in `àllopatric'' laboratory populations of Drosophila
under conditions of different selection regimes, but not under
identical selection, urgently need a detailed follow-up. These
studies indicate that reproductive isolation may often be a
by-product of selection, whereas theory(59,60) suggests that
it might also build up independently. We may only have
scratched the surface of the full extent of interactions between
natural and sexual selection.
Acknowledgements
For the development of the ideas presented in this paper, I am
indebted to several people who have helped shape my viewpoints, namely, John Endler, Jeffrey Feder, Arne Mooers, Bill
Rice, Michael Rosenzweig, Ulrich Schliewen, Dolph Schluter,
and Chung-I Wu. The constructive comments by Jacques van
Alphen, Jeroen Roelfsema, Jeffrey Feder, Ole Seehausen,
Chung-I Wu and two anonymous reviewers on an earlier
version of the manuscript are also gratefully acknowledged.
For the contents of this paper, however, only I am responsible.
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MÓDULO V: BIOGEOGRAFÍA HISTÓRICA 5
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INTRODUCCIÓN GENERAL Ana Liza Tropea El trabajo práctico a continuación constituye el inicio del segundo bloque temático de la materia en el que se estudiarán los procesos que modelaron la diversidad biológica por encima del nivel poblacional. Para ello, no sólo se requieren los conceptos estudiados anteriormente (procesos microevolutivos) sino que también es necesario introducir nuevos elementos para lograr comprender el surgimiento de las especies, sus patrones de variabilidad genética, su distribución geográfica y temporal y, sus relaciones de parentesco (nivel macroevolutivo) como resultados de un largo proceso histórico, único pero a la vez contingente. En particular, el concepto de tiempo geológico es de vital importancia para el estudio de la historia de la vida en la Tierra, muy diferente a la escala temporal generacional en la que se enmarcan los estudios microevolutivos. En este nuevo contexto, es interesante destacar cómo, para inferir aquellos procesos que ocurrieron en el pasado y construir escenarios evolutivos, se deben estudiar los correspondientes patrones observables en el presente. Como una primera aproximación a esta nueva mirada del mundo vivo, y previo a la lectura del módulo, le proponemos la lectura del siguiente material y lo invitamos a reflexionar sobre las preguntas a continuación: S.J. Gould. “Los signos insensatos de la historia” en El pulgar del Panda (capítulo 2). Ed. Crítica. 1994. Pp.24‐30. 1. ¿Por qué la evolución es una ciencia histórica? ¿Cuáles son las preguntas que se formula? ¿Qué metodología/s utiliza? ¿Cuál es el estatus epistemológico de las inferencias sobre el pasado evolutivo? 2. ¿Qué son los patrones y los procesos en el marco de la biología evolutiva? ¿A qué hace referencia el autor con la frase “Las rarezas, en términos del presente, son las señas de identidad de la historia”? Sintetice el ejemplo de las tortugas presentado por el autor. 3. ¿Qué tipo de información, distinta a la conocida por ud. hasta el momento, se utiliza para inferir el pasado evolutivo de las especies, familias u otros clados? 4. ¿Por qué se suele afirmar que la historia evolutiva ocurrida es “uno de muchos caminos posibles”? 7
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INTRODUCCIÓN A LA BIOGEOGRAFÍA HISTÓRICA Alexandra M. Gottlieb Objetivos 1‐ Conocer el desarrollo histórico de las ideas en Biogeografía. 2‐ Familiarizarse con los conceptos utilizados por esta disciplina. 3‐ Aplicar los conocimientos adquiridos en el planteo de hipótesis que expliquen a través de procesos evolutivos, los patrones de distribución geográfica observados. Introducción La Biogeografía es una disciplina histórica que estudia la distribución de los seres vivos en el tiempo y el espacio, e incluye temáticas como Geología, Geografía y Biología. El padre de la nomenclatura binomial, C. Linneo (1707‐1778), intentó explicar las causas de la distribución geográfica de los organismos siguiendo, en su tradición creacionista y fijista, el relato bíblico del Jardín del Edén. Ciertos autores reconocen en el Conde de Buffon (1707‐1788), opositor al sistema linneano, los comienzos de la Biogeografía. Fue su sistema alternativo de clasificación lo que le permitió a Buffon agrupar los animales de acuerdo a su geografía y organizarlos en faunas. Además, fue Buffon quien introdujo el concepto de centros de origen aunque asociado al creacionismo. El botánico A. P. de Candolle (1778‐1841), en 1820 reconoció dos enfoques en la investigación biogeográfica: el ecológico y el histórico. Si bien antiguamente estos eran dos enfoques excluyentes, en la actualidad se reconoce que todo patrón biogeográfico es el resultado de la combinación de ambos tipos de procesos. La Biogeografía Ecológica analiza patrones de distribución a nivel local, de poblaciones o de especies, teniendo en cuenta procesos de adaptación al ambiente y las relaciones entre dichas poblaciones o especies. La Biogeografía Histórica se ocupa de estudiar a escala global, cómo los procesos históricos que suceden a través de millones de años (v.g.: la tectónica de placas, los movimientos orogénicos, los procesos macroevolutivos, etc.) afectan los patrones de distribución de especies y de taxones superiores. Los datos biogeográficos fueron muy importantes en el desarrollo de las ideas evolutivas de C. R. Darwin (1809‐1882) y de A. R. Wallace (1823‐1913). En su libro “Viaje de un naturalista alrededor del mundo” (1831‐1835), Darwin se cuestiona acerca de los patrones de distribución de plantas y animales, e interpreta los fósiles como restos de los antecesores de los organismos vivos. Para Darwin, el clima y las barreras geográficas condicionan y limitan la distribución actual de los seres vivos. Más tarde, Darwin dedicó un capítulo de su “Origen…” (1859) a explicar muchos hechos biogeográficos (como por ejemplo el aislamiento de Australia y la evolución de los marsupiales), al mismo tiempo que el pasado fósil de los organismos actuales fue tratado en otro capítulo de dicha obra. Wallace, gran naturalista inglés contemporáneo a Darwin, contribuyó significativamente a la Biogeografía con su libro “La Distribución Geográfica de los Animales” (1876). Darwin y Wallace consideraban que las especies se originaban en un centro a partir del cual algunos individuos se dispersaban al azar y posteriormente evolucionaban por selección natural. Esta visión fue rebatida por Lyell y Hooker, entre otros, ya que consideraban poco probable la dispersión a larga distancia a través de barreras amplias. En cambio, sostenían que las especies se habrían distribuido a través de grandes puentes terrestres y continentes, ahora 13
sumergidos. La tradición de Darwin –Wallace tuvo sus defensores más prominentes en el genetista E. Mayr (1904‐2005) y el paleontólogo G. G. Simpson (1902‐1984), entre muchos otros. Entre las décadas de 1950 y 1960, el paradigma dominante en Biogeografía era el paradigma dispersalista debido principalmente a la influencia de Simpson, y a que muchos biólogos ignoraban conceptos geológicos como el de Deriva Continental (luego la Tectónica de Placas). Justamente fue esta teoría la que dio sustento a la visión vicariante de la distribución biológica, opuesta al dispersalismo, antes mencionado. No obstante, Simpson distinguió la dispersión por medio de corredores, puentes filtro y rutas al azar (o “sweepstakes”). Así, los animales pueden desplazarse libremente en ambas direcciones a través de corredores, y en consecuencia, las regiones conectadas tendrían una gran similitud faunística. Los puentes filtro constituían un medio más selectivo para la dispersión, ya que sólo ciertas clases de animales podría atravesarlo y en una dirección. Las rutas al azar son aquellas que son cruzadas fortuitamente por algunos organismos al ser arrastrados por las corrientes, o al estar adheridos a otros organismos, o simplemente al estar sobre un tronco flotante. En 1958 el botánico L. Croizat (1894–1982) planteó que las barreras geográficas evolucionaron conjuntamente con las biotas 1 , y que las áreas disyuntas 2 constituyen relictos de las distribuciones ancestrales. Croizat desarrolló el método denominado panbiogeografía para reconstruir biotas ancestrales, poniendo énfasis en el análisis de los patrones de distribución comunes de taxones animales y vegetales, y no en la capacidad de dispersión de cada uno de ellos. Este fue uno de los primeros enfoques que consideró a la vicarianza como un proceso fundamental en la Biogeografía Histórica (ver más adelante). Por su parte, W. Hennig (1913‐1976) postuló la existencia de una relación estrecha entre las especies y el espacio que ocupa cada una de ellas. Con el desarrollo de la Cladística y su aplicación a la Biogeografía, surgió la disciplina conocida como Biogeografía Cladística. Este enfoque emplea cladogramas para inferir la historia biogeográfica de un grupo, en particular, el interés de esta corriente reside en el estudio de la historia de grupos monofiléticos en el tiempo y el espacio. Deriva Continental y Tectónica de Placas El meteorólogo A. Wegener (1880‐1930) propuso en 1915 su teoría de la Deriva Continental, la cual sostenía que los continentes se deslizaban lentamente sobre la superficie de la corteza terrestre debido a la fuerza de las mareas. Si bien Wegener no fue el primero en notar que muchas líneas de la costa (como América del Sur y África) parecieran encajar juntas como un rompecabezas, fue uno de los primeros en proponer que los continentes pudieron haber estado ensamblados juntos en algún punto en el pasado formando el supercontinente Pangea (ver Fig. 1). Esta propuesta fue apoyada por paleontólogos que encontraron fósiles de especies muy similares entre continentes ahora separados por una gran distancia geográfica (v.g.: restos de la planta fósil Glossopterys en África, Sudamérica, Australia e India; restos de fósiles de un reptil del Paleozoico, Mesosaurus, en Brasil y África). Las ideas de Wegener fueron muy polémicas porque carecían de una explicación mecánica para el movimiento o deriva de los continentes. Muchos geólogos anti‐movilistas creían que el planeta pasaba por ciclos de calentamiento y enfriamiento, lo que causaba la dilatación y contracción de las masas de la tierra. Los movilistas, en cambio, apoyaban las ideas de Wegener. Aunque la teoría de la Deriva Continental fue posteriormente refutada, sentó las bases para el desarrollo de la Tectónica de Placas. 1
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Biotas: conjuntos de taxones que habitan un área geográfica determinada. Areas disyuntas: áreas sin continuidad geográfica. 14
FIGURA 1. Esquema cronológico en el que se muestran las masas de tierra emergidas en el Pérmico, Triásico, Jurásico, Cretácico y en la época actual, producto del movimiento de las placas tectónicas. En los años 1960 una serie de sismómetros instalados para vigilar una prueba nuclear, reveló que los terremotos, los volcanes, y otros procesos geológicos activos, se alineaban a lo largo de cinturones alrededor del mundo, definiendo los bordes de placas tectónicas. Los estudios paleomagnéticos mostraron que el Polo Norte Magnético vagó aparentemente sobre todo el globo. Esto fue interpretado como que, o bien las placas se movían, o bien el Polo Norte era móvil. Excepto los períodos de revocaciones magnéticas en los cuales los Polos Norte y Sur se invierten, el Polo Norte se encuentra fijo. Los geólogos y los geofísicos descubrieron que la corteza terrestre en el fondo oceánico, tenía registro de estas revocaciones, lo que constituiría una prueba de que la litosfera 3 tuvo que estar en movimiento. La evidencia geológica, geofísica y sismológica fortaleció la idea de la tectónica de placas. Hacia finales de la década de 1960, la comunidad científica aceptó a la Tectónica de Placas como un paradigma explicativo coherente acerca de la dinámica del planeta y su interacción con los ecosistemas. Esta teoría explicó por ejemplo, la existencia de marsupiales en Sudamérica y Australia considerando que durante el Eoceno (hace 40 millones de años, Ma) (ver Fig. 2) estas regiones se encontraban cercanas entre sí y con la Antártica, que para aquel entonces poseía un clima cálido. 3
Litosfera: capa superficial de la Tierra sólida formada por corteza y manto. 15
La ruptura y separación (es decir, el cambio de posición) de las masas de tierra hace que esas regiones estén sometidas a cambios de clima y aislamiento y, en consecuencia, a cambios de presión de selección sobre los organismos y divergencia. Contrariamente, las fusiones de continentes y las migraciones bidireccionales homogeneizan áreas y producen un aumento en la competencia por el espacio y los recursos. La disposición de las tierras continentales, el surgimiento de islas, la apertura y cierre de plataformas marinas y oceánicas, etc., afectaron profundamente la distribución y la historia de los seres vivos. FIGURA 2. Esquema cronológico de los Eones, Eras, Períodos y Épocas geológicas de la Tierra (escala cronoestratrigráfica). Áreas de distribución, áreas de endemismo y centros de origen Desde sus orígenes la Biogeografía intenta comprender por ejemplo, por qué algunos taxones poseen distribución más amplia que otros; o cómo explicar las distribuciones disyuntas de los miembros de un mismo taxón; o por qué un taxón es más diverso en ciertas regiones, etc. Por distribución disyunta se entiende aquella donde los miembros de un mismo taxón habitan localidades muy distantes, sin una continuidad geográfica entre ellas. Responder estas preguntas requiere delimitar las áreas de estudio; y para ello se emplean dos conceptos fundamentales: área de distribución y área de endemismo. El área de distribución es la región total dentro de la cual se distribuye una unidad taxonómica cualquiera. Se relaciona con factores como el clima, el hábitat, la competencia intra e interespecífica, etc. Un parámetro importante del área de distribución es su carácter continuo o discontinuo (área disyunta). La 16
distribución de una especie evolutivamente “nueva” es naturalmente continua, pero los cambios climáticos estocásticos, las epidemias y/o la competencia ecológica pueden conducir a la fragmentación de su distribución y a la posterior divergencia de las poblaciones aisladas (especiación alopátrica). La delimitación de las áreas de distribución de un taxón suele ser una simplificación de la distribución de los organismos en la naturaleza debido a que, muchas veces éstas representan las localidades donde el taxón ha sido encontrado o coleccionado. Los mapas de distribución pueden elaborarse a partir de las áreas de distribución para cualquier nivel de la jerarquía linneana (v.g.: especies, familias, órdenes, etc.). Mediante la elaboración de mapas de distribución, la Tierra fue dividida en ocho regiones biogeográficas para la fauna y otras seis regiones para la flora. Por otro lado, los límites a la distribución están determinados por los atributos ecológicos (nicho fundamental, nicho realizado) e históricos de un taxón. Así una especie puede ser ecológicamente apta para vivir en un lugar pero estar ausente porque nunca migró y/o logró establecerse. Los cambios climáticos ocurridos en el pasado, como las glaciaciones, trajeron como consecuencia que el rango de distribución de muchas especies del Hemisferio Norte se desplazara más hacia el sur por migración. Alternativamente, también pudo haber ocurrido que el rango de distribución se contrajera y se desplazara más hacia el sur por la muerte de los individuos que habitaban las zonas más frías (sin migración). Más controvertida es la delimitación del área de endemismo ya que existe cierta dependencia de la escala de estudio y, a su vez, no existe un consenso en la comunidad científica acerca de su definición. Nelson y Platnick (1981) definieron áreas de endemismo como áreas relativamente pequeñas que presentan un número significativo de especies que no están presentes en ninguna otra área. Más tarde, Platnick (1991) la definió como aquella área delimitada por las distribuciones congruentes de dos o más especies. Una especie es endémica (es un endemismo) cuando se presenta en un área muy restringida. Un endemismo puede encontrase en el área donde se originó, en cuyo caso decimos que es un neoendemismo. Un paleoendemismo es una especie cuya distribución restringida representa sólo una pequeña parte de otra distribución anterior más amplia, generalmente lejos del área en la que surgió evolutivamente. Decimos en este caso que la especie ocupa un área relicta o relictual. Los organismos se dispersan desde su centro de origen tanto como se lo permitan sus habilidades y las condiciones del medio. Los datos del registro fósil son esenciales para determinar los centros de origen, si bien existen numerosos criterios para su delimitación. Entre los criterios más empleados se pueden mencionar: (i) aquel donde actualmente se encuentra la mayor diversidad del taxón; (ii) la mayor cantidad de individuos; (iii) los individuos de mayor tamaño; (iv) la mayoría de los genes dominantes, etc. Extinción, dispersión y vicarianza La Tierra ha permanecido en un estado de flujo durante 4.000 Ma. A lo largo del tiempo, la abundancia y diversidad de linajes varió abruptamente. Los linajes evolucionan y radian empujando a otros linajes hacia la extinción, o hacia una existencia relictual en refugios protegidos (o microhábitats adecuados). Se han distinguido tres procesos principales en el tiempo‐espacio que pueden modificar la distribución espacial de los organismos: las extinciones, las dispersiones y la vicarianza. La extinción biológica es la desaparición de un taxón y representa la terminación de su linaje o clado. La transformación de una especie ancestral en otra derivada se denomina pseudoextinción. 17
En términos generales, la diversidad ha aumentado desde el comienzo de la vida. Sin embargo, el aumento se ha interrumpido numerosas veces por las extinciones en masa. Estas implican una reducción de la diversidad biológica debida a la muerte de todos los individuos de una población local, especie o taxón de rango superior, aproximadamente al mismo tiempo. Las extinciones masivas están seguidas de periodos de radiación en los que evolucionan nuevas especies que ocupan los nichos vacantes. Por tanto las extinciones moldean el patrón general de la macroevolución. Muchos investigadores consideran que sobrevivir a una extinción en masa es, mayormente, una cuestión de suerte o una lotería, y que las reglas que rigen estos periodos son diferentes a las de los tiempos “normales”. Es así que la contingencia jugaría un gran papel en los patrones de la macroevolución. En clases posteriores veremos cómo la modificación ambiental puede ser el impulsor de más cambio evolutivo. El vulcanismo, el impacto de asteroides o cometas, o una reacción en cadena de estos procesos, originaron el colapso de los ecosistemas y el consecuente cambio climático (v.g.: glaciaciones, descenso o aumento de temperaturas, oscilaciones en el nivel de los mares, etc.). Se supone que estos procesos han participado como causas de muchas extinciones. Los datos paleontológicos indican que las extinciones masivas han sido periódicas, algunas más extensas que otras. Son eventos “rápidos” en términos geológicos, es decir, se encuentran en el orden de miles a decenas de miles de años. Como ejemplo, podemos mencionar que la biota del Mesozoico tuvo su declive y caída durante 1 o 2 Ma, esta cifra representa tan sólo el 0,55% de los 180 Ma que duró el Mesozoico. Se han registrado numerosas extinciones, aunque cinco de ellas son las más destacadas debido a su intensidad en exterminación. La primera extinción (hace unos 440 Ma) marca el final del Período Ordovícico (ver Fig. 2). El cambio climático se caracterizó por ser severo y acompañado de un enfriamiento global repentino, constituyéndose como la causa próxima de esta extinción que ocasionó cambios profundos principalmente en la vida marina, pues en ese tiempo no existen evidencias de vida terrestre. Se calcula que aproximadamente el 25% de las familias de organismos marinos desapareció. La segunda extinción (hace unos 370 Ma) cerca del final del Período Devónico, podría haber sido el resultado de cambios climáticos globales. Aquí, llegaron a su fin el 19% de las familias. La tercera extinción (hace unos 245 Ma) se produjo hacia el final del Período Pérmico (ver Figs. 1 y 2) y se la considera la mayor extinción de la historia de la vida en la Tierra (por lo menos hasta ahora!). Evidencias recientes sugieren que el impacto de un asteroide, similar al evento ocurrido al final del Cretácico, puede haber sido la causa de esta extinción. En esa época también se produjo un descenso mundial del nivel del mar. Se estima que desapareció el 96% de todas las especies existentes (50‐54% de todas las familias). La cuarta extinción (hace unos 210 Ma), al final del Período Triásico, tuvo lugar poco después de la evolución de los dinosaurios y los primeros mamíferos; sus causas aún son desconocidas. Se estima que el 23% de las familias de organismos vivientes desapareció. La quinta extinción (hace unos 65 Ma) al final del Período Cretácico (en el límite entre los periodos Cretácico y Terciario o Límite K/T), es quizás la más famosa y la más reciente de las extinciones. Se ha llegado al consenso de que este evento fue causado por una colisión (o múltiples) entre la Tierra y un asteroide, generando un desequilibrio ambiental. Sin embargo, algunos geólogos apuntan a una cadena de eventos físicos que perturbaron severamente los ecosistemas. Aquí, se perdió el 17% de las familias, y marcó el fin de todos los linajes de dinosaurios, excepto el de las aves, y la desaparición de los amonites marinos, así como de muchas otras especies del espectro filogenético y de todos los hábitats. Con la erradicación de los dinosaurios, los mamíferos, confinados principalmente a nichos insectívoros nocturnos, radiaron ocupando los nichos vacantes. Actualmente, la alteración humana de la ecósfera está provocando una extinción en masa global, considerada por algunos científicos como la sexta extinción. 18
Como mencionamos, la dispersión y la vicarianza (ver Fig. 3) fueron originalmente consideradas como dos explicaciones mutuamente excluyentes para dar cuenta de la distribución disyunta de los grupos de organismos. Actualmente se acepta que ambos procesos ocurren en la naturaleza. DISPERSION
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FIGURA 3. Explicación de la distribución disyunta. Diferencias en el marco de la Biogeografía Histórica entre los procesos de dispersión y vicarianza. Modificado de Crisci et al. (2000) y Avise (2000). NOTA: las letras mayúsculas indican áreas de distribución; las letras minúsculas indican taxones. La explicación por dispersión señala que el/los ancestro/s común/es de los taxones con distribución disyunta se dispersaron por migración a partir de centros de origen atravesando barreras geográficas preexistentes, hacia donde se encuentran hoy los descendientes. Por lo tanto, la barrera geográfica debería ser más antigua que la disyunción. 19
La explicación por vicarianza sostiene que el ancestro común de los taxones con distribución disyunta, se encontraba ampliamente distribuido en un área que comprendía las áreas actualmente disyuntas, las cuales representan restos o relictos de una distribución ancestral. La población ancestral se divide en subpoblaciones por el surgimiento de una barrera geográfica infranqueable (v.g.: el levantamiento de una cadena montañosa, la ruptura de continentes, la subdivisión de cuerpos de agua, etc.). Por lo tanto, la barrera no podría ser más antigua que la disyunción. Los eventos de vicarianza afectan conjuntamente a todos los taxones que se distribuyen en un área, mientras que la dispersión afecta por lo general, a uno o a unos pocos taxones. En general, cuando distintos grupos taxonómicos muestran distribuciones correlativas o congruentes, éstas fueron probablemente producidas por vicarianza. En cambio, si las diversas especies se dispersaron independientemente de su centro de origen entonces no tendrán una distribución congruente. Bajo vicarianza, la filogenia de los taxones se corresponde con el orden de separación de las áreas, mientras que bajo la hipótesis de dispersión las áreas y los taxones pueden mostrar relaciones históricas más variadas (Fig. 3). Métodos de la Biogeografía La reconstrucción que la Biogeografía Histórica hace de los eventos del pasado puede abordarse desde tres perspectivas diferentes: (i) desde los grupos individuales (taxones); (ii) desde las áreas de endemismo y; (iii) desde las biotas. La mayoría de los métodos biogeográficos emplean cladogramas como herramienta básica de inferencia de relaciones históricas. Los biogeógrafos testean sus ideas mediante el estudio de los patrones de división (cladogénesis) de un grupo de organismos y su correspondencia, o no, con la historia geológica y geográfica de la región en la que vivía dicho grupo. Para esto, construyen un cladograma de áreas (ver Fig. 3) reemplazando los nombres de los taxones terminales por las áreas de endemismo donde se distribuyen. Este procedimiento es simple si cada taxón es endémico de un único área o si cada área posee un único taxón. Cuando este no es el caso, es decir cuando los taxones están ampliamente distribuidos o cuando existen distribuciones redundantes y/o hay áreas ausentes, deben aplicarse ciertas reglas metodológicas para resolver los cladogramas. Como mencionamos anteriormente, si la cladogénesis fue causada por procesos geológicos (vicarianza), la filogenia del grupo reflejará la secuencia definida de eventos tectónicos. Al examinar cladogramas de otros taxones de las mismas áreas, éstos deberían ser congruentes (deberían coincidir en el orden de ramificación). Este análisis sólo es válido cuando se trabaja con grupos monofiléticos, lo que implica que la Biogeografía se sustenta en clasificaciones naturales. La metodología general puede resumirse como sigue: 1. obtención del cladograma del grupo en estudio; 2. proyección del cladograma sobre un mapa de áreas de distribución; 3. individualización del centro de origen del grupo mediante la aplicación de reglas específicas; 4. formulación de una hipótesis sobre la biogeografía del grupo; 5. confrontación de la hipótesis con la geología del área y otras fuentes de datos independientes. 20
Existen al menos nueve metodologías básicas. Algunos de estos métodos asumen que sólo operó el proceso de dispersión, mientras que otros métodos consideran también a la vicarianza como proceso que modeló el patrón de distribución observado. Al mismo tiempo, ciertos métodos reconstruyen la historia de biotas; otros reconstruyen la distribución de biotas individuales o la historia de las áreas; mientras que otros trabajan sobre biotas y áreas conjuntamente. Respecto al rango taxonómico de aplicación, la Filogeografía es la única metodología que se aplica al nivel poblacional. Las metodologías restantes trabajan a nivel de especies o de taxones de rango superior. La Biogeografía Cladística basa sus inferencias en el supuesto que establece que los miembros más primitivos de un taxón se hallan más cercanos al centro de origen. A su vez, la hipótesis nula contra la cual se testean los resultados es que la distribución de grupos taxonómicos es determinada por eventos de vicarianza dentro del rango de la especie ancestral; mientras que generalmente la hipótesis alternativa propone que la distribución observada está determinada por dispersión. Lectura adicional (optativa) En la página de la materia encontrará los siguientes trabajos: 1‐ Webb DS (2006) The Great American Biotic Interchange: patterns and processes. Ann. Missouri Bot. Gard. 93: 245–257. 2‐ Marshall LG, Webb DS, JJ Sepkoski Jr, Raup DM (1982) Mammalian evolution and the Great American Interchange. Science 215: 1351‐1357. Bibliografía Consultada Avise JC. (2000). Phylogeography. The history and formation of species. Harvard Univ. Press. London England. Beardsley PM, Getty SR & P Numedahl (2009) Explaining Biogeographic data: Evidence for Evolution. The American Biology Teacher 71 (2): 5‐9. Crisci JV, Katinas L, Posadas P. (2000). Introducción a la teoría y práctica de la Biogeografía Histórica. Sociedad Argentina de Botánica. Pp.169 Damborenea MC & Cigliano MM. (2006). Cladística y sus aplicaciones en Biogeografía Histórica y co‐
evolución (capítulo 13). En: Sistemática Biológica: fundamentos teóricos y ejercitaciones. Lanteri AA, Cigliano MM Eds. 203‐219. Universidad Nacional de La Plata. Eldregde N. (1989) Life Pulse: Episodes from the story of the fossil record. FOF Publication. NY, UK, pp. 246. Fernández‐López SR (2000). La naturaleza del registro fósil y el análisis de las extinciones. Coloquios de Paleontología 51: 267‐280. Nelson GJ, Platnick NI (1981) Systematics and biogeography: cladistics and vicariance. Columbia Univ. Press, NY. Platnick NI (1991) On areas of endemism. Australian Systematic Botany 4: 11‐12. Ridley M. (2004). Evolutionary Biogeography (Capítulo 17). En: Evolution. 3rd Ed. Blackwell Publishing. 21
DESARROLLO DEL TRABAJO PRÁCTICO PRIMERA PARTE Como se mencionó anteriormente, la noción de “profundidad del tiempo geológico” constituye un eje fundamental sobre el que se articulan las inferencias o reconstrucciones del pasado evolutivo de las especies o, taxones de orden superior. Sin embargo, resulta muy difícil incorporar dicha escala de tiempo dado que excede ampliamente los rangos temporales compatibles con la historia humana y, más aun, con la esperanza de vida de nuestra especie. En un esfuerzo por hacer comprender la velocidad relativa con que se sucedieron las diversas etapas desde que se formó el Universo, Carl Sagan, el conocido astrónomo de la Universidad de Cornell, en su libro Los Dragones del Edén, ha incluido lo que él llama "El Calendario Cósmico": supongamos que pudiéramos comprimir los quince mil millones de años que han transcurrido desde la Gran Explosión hasta nuestros días en un sólo año. Así, cada mil millones de años corresponderían a 24 días del Calendario Cósmico, en tanto que un segundo del año cósmico equivaldría a 475 vueltas de la Tierra alrededor del Sol. A esta escala, la evolución del universo transcurre a una gran velocidad. Sin embargo, para poder completar la historia de la vida en nuestro planeta y el desarrollo de la historia en esta perspectiva, Sagan dividió este calendario en tres etapas, las fechas precámbricas, el mes de diciembre y finalmente el último día del año cósmico (ver figura 4). El Calendario Cósmico fue elaborado a partir de la información más confiable con que contamos hoy en día y es posible sin lugar a duda que admita modificaciones a medida que se profundice el conocimiento científico. Sin embargo, no cambiará la conclusión de que somos parte de un proceso de evolución que se inició con el origen mismo del Universo, además, como dice Sagan, la conciencia de que las grandes hazañas del hombre ocupan apenas unos cuantos segundos de este primer año. 1.1. A partir de la figura 4, destaque los principales hechos de interés para la biología evolutiva. ¿En qué porción del tiempo han ocurrido dichos eventos? 1.2. ¿En qué momento surge la vida? ¿Y nuestra especie? 22
Figura 4: Calendario Cósmico, Carl Sagan
23
SEGUNDA PARTE Usted es un investigador interesado en realizar un estudio biogeográfico de las faunas de mamíferos de América del Norte y del Sur de los últimos 12 millones de años. 2.1. ¿En qué período geológico se enmarca este estudio? ¿Cómo se ubicaban las placas continentales de la actual América en dicho período? Utilice las figuras 1 y 2 de la introducción teórica y la figura 5 de la parte práctica. 2.2. A partir del esquema de la figura 6, complete la tabla 1 con: ‐ el número de registros de fósiles de los linajes indicados en cada uno de los 6 sitios; ‐ la sumatoria del número de registros y la datación aproximada del fósil más antiguo, para cada una de las dos regiones, tanto América del Norte como América del Sur. 3. Responda el siguiente cuestionario: 3.1. Considerando el rango de 11 a 4 millones de años antes del presente (AP), indique las familias de mamíferos endémicas para Norteamérica y Sudamérica. 3.2. Indique el tiempo aproximado de arribo, o introducción, de animales endémicos de Sudamérica en Norteamérica y el tiempo de arribo de los linajes endémicos sudamericanos en Norteamérica. ¿En qué datos se basó? 3.3. ¿Cómo explicaría el arribo de animales endémicos sudamericanos a América del Norte (y viceversa)? 3.4. Examine el registro del linaje de los rinocerontes. ¿En qué rango de tiempo hay evidencias de estos organismos? ¿Qué inferencias puede hacer acerca de la historia de los rinocerontes? Proponga hipótesis alternativas. 3.5. ¿Cuál es la evidencia fósil más temprana del linaje de los mamuts? ¿Cómo explicaría la ocurrencia repentina de mamuts en el registro fósil? ¿Hay evidencias de estos organismos en Sudamérica? 3.6. Para un tiempo geológico dado, ¿considera que cada sitio muestra todos los animales que se desarrollaron allí? Justifique. FIGURA 5. Formación del istmo de Panamá. 24
FIGURA 6. Esquema de registros paleontológicos de seis secciones geológicas. Los fósiles de 12 familias de mamíferos identificados por sus
iniciales, se presentan en función de la edad geológica (Ma, millones de años).
Ma
0
2
4
Florida
ESTADOS UNIDOS
Arizona
Nuevo Méjico
O M
F Cm
M P
Gl
Pu
A
F
C
O Pu
P
M A
E P
Cp
F
Cm
MÉJICO
F E
Cm
P
E
E
M
C
E
F
F
Cm
E
E
E
E
F
6
R
E
C
F
E
8
Cm
R
A
M
Gl A
Cp P
P
C
P
C
E
Cm
R
E
R
Cm
F
R
F R
C
Cm
Cm
C
C
R
E
R
E
E
E
C
10
F
F
12
25
COLOMBIA
P
ARGENTINA
Gl
F
O
Cm
Cp E
O P
P Cp
Pu
A O
A P Cp
O
Cp Pu
Gl
P
Cp
P
P
O
Gl
O Cp
Cm
P
F
E
C P Cp
Gl
O
A
Cp
Cp Pu
O
Pu
P
P A
O
P
A
Pu
A Gl
Pu
Pu
P
O
Cp
A
C
Gl
O
TABLA 1.
ESTADOS UNIDOS
Florida
Arizona Nuevo
Méjico
Registros Registros Registros
Organismos
Armadillo (A)
MÉJICO
COLOMBIA ARGENTINA
NORTEAMÉRICA
Registros
Registros
totales
Camélido (Cm)
Cánido (C)
Capibara (Cp)
Equido (E)
Félido (F)
Gliptodonte (Gl)
Mamut (M)
Opósum (O)
Perezoso (P)
Puercoespín (Pu)
Rinoceronte (R)
26
Datación
(Ma)
SUDAMÉRICA
Registros
Registros
Registros
totales
Datación
(Ma)
Concepción diagramática de Simpson (1940) sobre la migración a través de puentes. (Traducción: Los puentes NO: 1) permiten que solo pase un tipo de animal, 2) permiten viajar en una única dirección y 3) transportan fauna completamente desbalanceada.) 27
Ejercitación adicional Entre la fauna del archipiélago de Los Cocos se encuentran los caracoles terrestres del género Gouldiana. Estos caracoles están presentes en casi la totalidad de las islas que conforman el archipiélago pero se discute cómo llegaron a poblarlas. Sabiendo: ‐ Que la distribución de las especies reconocidas en el archipiélago es la informada en la Figura 1. ‐ Que algunas especies de caracoles presentan bandas coloreadas es su concha. ‐ Que todas las especies de caracoles son vegetarianos. ‐ Que la filogenia más reciente y completa del grupo es la informada en la Figura 2. ‐ Que durante la última glaciación el nivel del mar estaba 100 metros por debajo del nivel actual, y todas las islas conformaban una masa terrestre denominada Antiguos Cocos. Responda: a. ¿Qué proceso biogeográfico considera compatible con el patrón de distribución de especies entre islas? Justifique. b. ¿Qué evidencia o prueba adicional aportaría mayor soporte a su hipótesis? c. ¿Cuál es el modelo geográfico de especiación que explicaría la evolución de las diferentes especies de caracoles entre las distintas islas? Justifique brevemente. d. Utilice un modelo alternativo para explicar la divergencia y especiación dentro de las islas y enuncie las condiciones necesarias para que este modelo pueda aplicarse. e. Bajo el modelo que Ud. postuló en c): ¿cómo ocurrió la divergencia genética entre las especies? ¿Cuántos genes y qué tipo de caracteres fueron los involucrados? 28
Figura 1: Archipiélago de Los Cocos Figura 2: Reconstrucción filogenética a partir de secuencias de genes nucleares y mitocondriales. 29
30
EJERCICIOS de REPASO Problema 1.El Dr. H. estudia dos “variedades” de angiospermas (plantas con flores) que habitan en una pradera y un bosque de una misma región geográfica. A lo largo de varios años ha colectado la siguiente información: i) En el año 2006 el investigador realizó un estudio con plantas de la pradera y del bosque analizando los caracteres: largo del tallo, número de hojas, concentración de carotenos en las flores, largo de los estambres y número de estomas por cm3. Combinó toda esta información en dos variables nuevas y obtuvo el siguiente gráfico: ii) En el año 2007, realizó cruzamientos de plantas de ambas poblaciones cortando los estambres de las flores y fecundando las mismas artificialmente en el laboratorio. Sembró las semillas producidas en el invernadero y obtuvo los siguientes resultados: Flores pradera x polen pradera: 200 plantas Flores pradera x polen bosque: 150 plantas Flores bosque x polen bosque: 150 plantas Flores bosque x polen pradera: 185 plantas iii) Al año siguiente decidió transplantar individuos a los que les había cortado los estam bres desde la población del bosque a la pradera y viceversa. Cuando analizó la cantidad de semillas en las flores de cada población, encontró los siguientes valores promedio: Pradera: Individuos originarios de la pradera: 5 ± 1 semillas/flor Individuos originarios del bosque: 0,2 ± 0,1 semillas/flor Bosque: Individuos originarios de la pradera: 1 ± 0,2 semillas/flor Individuos originarios del bosque: 20 ± 4 semillas/flor a. Interprete la información de los tres estudios y explique los resultados obtenidos. b. Especifique cuántas especies podrían definirse para estas dos variedades de angiospermas deacuerdo a los conceptos de especie morfológico, ecológico, biológico y cohesivo. Justifiqueclaramente sus respuestas. c. Para el concepto de especie que corresponda, indique el/los mecanismo/s de aislamientoreproductivo existentes. d. ¿En cuál de las dos escuelas teóricas sobre el proceso de especiación (aislacionista o seleccionista) cree Ud. que se encuadra el trabajo del Dr. H.? Justifique. e. Compare ambas escuelas con respecto a: el concepto de especie utilizado, cuáles serían los“genes de especiación”, el papel de la selección natural y la deriva génica en el proceso especiogénico y el modelo geográfico paradigmático. Problema 2. La mosca sudamericana de la fruta, Anastrepha fraterculus es una plaga muy destructiva que
infecta a más de 80 plantas huésped e impacta negativamente en la producción de muchos
cultivos de frutales. Habita en la mayoría de los países de América, desde Estados Unidos (Texas)
hasta Argentina. Si bien todas las poblaciones de A. fraterculus son similares morfológicamente, se
han descriptos 4 morfotipos (M, en base a caracteres morfométricos) que se distribuyen de forma
clinal con la latitud (MI se encuentra en EEUU y México, MII en Colombia, MIII en Perú y MIV en
sur de Brasil y Argentina; En Brasil también se encuentran presentes los morfotipos II y III). Dicha
variación intraespecífica junto a otras evidencias genéticas ha llevado a proponer que se trata de
un complejo de especies crípticas en lugar de una sola entidad biológica. Un estudio reciente,
evaluó varios aspectos del comportamiento reproductivo entre poblaciones peruanas y argentinas
de A. fraterculus. Los resultados se muestran a continuación.
Información previa con la que contaban los autores del trabajo:
-
-
Los machos de A. fraterculus se congregan en zonas comunes (leks) para atraer a las
hembras mediante la liberación de feromonas sexuales.
Los machos despliegan un elaborado comportamiento de cortejo que incluye movimiento
de las alas y señales visuales y acústicas.
Las hembras de la especie evalúan a los machos y eligen la pareja con la que van a
aparearse.
Durante el apareamiento se realiza la transferencia de esperma, cuya efectividad está
relacionada con la duración de la cópula (una cópula exitosa es de 1h aproximadamente)
Tabla 1. Porcentaje de apareamiento y duración de la cópula registrado
en jaulas de campo entre machos y hembras de las poblaciones de Perú y
Argentina. A y B difieren significativamente de C y D (P < 0.05) para ambas
variables.
A
B
C
D
Perú x Perú
Arg x Arg
Arg x Perú
Perú x Arg
% de apareamiento Duración de la cópula (min)
90
67
85
68
52
28
48
25
Tabla 2. Porcentaje de viabilidad larvaria (VL) y emergencia de adultos (EA) F1
descendientes de los 4 tipos de cruzamientos realizados en el laboratorio. Para
VL: A y B difieren significativamente de C y D; para EA: no se encontraron
diferencias significativas entre los 4 grupos.
A
B
C
D
Perú x Perú
Arg x Arg
Arg x Perú
Perú x Arg
% viabilidad larvaria F1
70
75
12
15
% emergencia de adultos F1
95
99
95
96
Figura 1. Composición
cualitativa y cuantitativa de
los compuestos que forman
las feromonas sexuales de
los machos de la población
argentina (A) y de la
población peruana (B). Cada
número corresponde a un
compuesto diferente; la
altura del pico corresponde
a la cantidad relativa del
compuesto. El perfil de la
feromona sexual
difiere
significativamente entre las
poblaciones.
En función de los resultados mostrados responda brevemente:
1) ¿Están aisladas reproductivamente la población peruana de la población argentina de A.
fraterculus? Justifique.
…...............................................................................................................................................
…...............................................................................................................................................
2) Si este fuera el caso, ¿qué tipo de mecanismo/s de aislamiento presentan? Explique
brevemente.
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................
3) ¿Qué concepto/s de especie le parece que es/son aplicable/s en este caso? Justifique.
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................
4) ¿Los resultados obtenidos apoyan la hipótesis de que A. fraterculus es un complejo de
especies? Justifique.
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................
5) ¿Con qué modelo de especiación geográfica considera que podría ser compatible este
caso? Justifique.
…...............................................................................................................................................
…...............................................................................................................................................
…...............................................................................................................................................

seminario i: realidad y conceptos de especies

Transcripción

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