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University of Groningen
What do we need to know about speciation?
Butlin, Roger; Debelle, Allan; Kerth, Claudius; Snook, Rhonda R.; Beukeboom, Leonardus;
Castillo Cajas, Ruth; Diao, Wenwen; Maan, Martine; Paolucci, Silvia; Weissing, Franz
Published in:
Trends in Ecology and Evolution
DOI:
10.1016/j.tree.2011.09.002
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Publication date:
2012
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Citation for published version (APA):
Butlin, R., Debelle, A., Kerth, C., Snook, R. R., Beukeboom, L. W., Castillo Cajas, R., ... Marie Curie
SPECIATION Network (2012). What do we need to know about speciation? Trends in Ecology and
Evolution, 27(1), 27-39. DOI: 10.1016/j.tree.2011.09.002
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Online Supplementary Material
What do we need to know about speciation?
The Marie Curie SPECIATION Network*
Corresponding author: Butlin, R. ([email protected]).
*Members of the Marie Curie Initial Training Network ‘SPECIATION’ contributing to this paper were: Roger Butlin, Allan Debelle, Claudius Kerth and Rhonda
R. Snook (Animal and Plant Sciences, The University of Sheffield, Sheffield, UK, S10 2TN); Leo W. Beukeboom, Ruth F. Castillo Cajas, Wenwen Diao,
Martine E. Maan, Silvia Paolucci, Franz J. Weissing and Louis van de Zande (Centre for Ecological and Evolutionary Studies, University of Groningen, PO
Box 11103, 9700 CC Groningen, the Netherlands); Anneli Hoikkala, Elzemiek Geuverink, Jackson Jennings, Maaria Kankare, K. Emily Knott, Venera I.
Tyukmaeva and Christos Zoumadakis (Centre of Excellence in Evolutionary Research, Department of Biological and Environmental Science, PO Box 35,
40014 University of Jyväskylä, Finland); Michael G. Ritchie, Daniel Barker and Elina Immonen (School of Biology, Centre for Evolution, Genes and Genomics,
University of St Andrews, St Andrews, UK, KY16 9TH); Mark Kirkpatrick (Section of Integrative Biology, University of Texas at Austin, Austin, TX 78712,
USA); Mohamed Noor (Biology Department, Duke University, Durham, NC 27708, USA); Constantino Macias Garcia (Instituto de Ecologia, Universidad
Nacional Autonoma de Mexico, Apartado Postal 70-275 Ciudad Universitaria, UNAM 04510 México); Thomas Schmitt (Biology I, University Freiburg,
Hauptstr. 1, D-79104 Freiburg, Germany); Menno Schilthuizen (Netherlands Centre for Biodiversity 'Naturalis', PO Box 9517, 2300 RA Leiden, the
Netherlands).
Arriving at the most important speciation questions
The Marie Curie Initial Training Network ‘SPECIATION’ includes 10 graduate students in four European institutions, 11 group
leaders involved in their supervision, two senior scientific advisers from outside Europe and three collaborating specialists. This
group represents a substantial cross-section of the speciation research community but it is biased in various ways: there is a
predominance of genetic and behavioural approaches, for example, with limited representation of systematists. Most, but not all of
our study organisms are insects and most, but not all of us are empiricists rather than theorists.
We generated an initial list of speciation questions by asking each group member to propose five questions. We did this with
minimal guidance in order to allow the widest possible interpretation of the problem. We did not aim to ask novel questions: many
long-standing issues still need work while others should, perhaps, have less attention in future (Box 6). The initial list contained
duplicates, of course, so it was refined to the list of 102 questions presented in Table S1. We voted on this set in order to provide a
prioritised list. Only then did we seek to structure the list. The three broad themes and 13 topics used in the article emerged from
the priority list rather than being imposed at the start. Topics were selected to ensure that coverage was as broad as possible,
rather than simply reflecting votes. Some questions were allocated to Boxes since we considered them to be background issues
rather than research priorities. Small groups then drafted text for each topic, taking into account the set of questions included and
their perceived importance, and all of us commented on these initial drafts.
The resulting text is something that we all accept, although each of us alone might have argued differently and dropped or
included other topics. We fully appreciate that other speciation biologists will disagree with some ideas we have included and would
wish to highlight other issues.
Table S1. Original questions provided by members of the Marie Curie Initial Training Network SPECIATION, grouped according to the
broader questions highlighted in the main text
Group
Question
1. Which barriers contribute to
What is the significance of microbial symbionts [not just Wolbachia] for speciation?
reproductive isolation?
Is pre-mating isolation sufficient to maintain species separate. Is something else needed to consolidate a new
species (local adaptation, post-mating isolation)?
How important are differences in mating preferences in driving speciation compared to other causes of premating isolation?
How important are the, often neglected and hard to study, gametic (post-mating pre-zygotic) reproductive
barriers?
How often do we observe post-zygotic isolation in the absence of pre-zygotic isolation?
What are the first incompatibilities to arise among divergent populations?
How can we test whether speciation is a by-product of divergence between populations in ecological or other
traits or the divergence between populations is a by-product of reproductive isolation (speciation)?
How important is reproductive isolation as a driver of speciation or is it just a consequence of speciation?
What is the importance of temporal (allochronic) isolation in the speciation process?
Species are separated by pre- or post-zygotic hybridisation barriers or by both. Are there differences in their
significance for the speciation process?
How does the stability of species boundaries depend on the type of isolating barrier and its underlying
molecular basis?
2. When does drift play a
What are the roles of natural selection and genetic drift in speciation? [While drift is currently thought to be a
significant role?
weak force, current human impacts on populations (e.g. reducing population sizes, restricting migration) may
increase the effectiveness of drift in driving speciation]
Speciation caused by drift and speciation caused by selection: can we generalize about the circumstances in
which speciation might be driven by one or the other? There may be too much emphasis on selection at
present.
Is speciation adaptive (i.e., is speciation initiated and driven by directional processes like natural and sexual
selection)? How can one test this hypothesis?
What is the relative importance (and/or plausibility) of parapatric speciation, as opposed to divergence in strict
allopatry, in generating patterns of biodiversity?
How many hybrid zones are primary in origin? [Geographic zones of sharp genetic change can be the result
of a change in selection pressure (parapatric speciation; primary zones) or of secondary contact between
previously isolated populations. The patterns themselves are virtually indistinguishable, making it almost
impossible to get a good estimate of the frequency of parapatric speciation.]
3. What are the relative roles of
What is the relative importance of natural and sexual selection in speciation?
natural and sexual selection?
What is the empirical evidence for different selective mechanisms that underlie mating preference divergence
and what is their relative importance? How often do preferences differ at the phenotypic level due to
pleiotropic effects of natural selection causing sensory biases, female responses to sexual conflict or heritable
phenotypic plasticity?
Ecological speciation, as a process, is dominating current speciation literature. Is such a focus justified? What
benefits are to be realized and costs incurred by such a focus?
Is natural selection involved in the origin or in the maintenance of species?
To what extent does intraspecific sexual conflict influence divergence of populations and ultimately,
speciation?
When /how often does sexual selection drive speciation without involving natural selection/ecological factors?
How often does sensory drive contribute to sexual isolation between species?
Where are we, and where do we need to be, in documenting that sexual selection is a driver of speciation?
Is speciation triggered by co-evolutionary interactions (‘biodiversity begets biodiversity’)? What is the relative
importance of co-evolutionary interactions (mutualistic-antagonistic, host-parasite, predator-prey) in speciation
relative to abiotic influences of the environment and/or sexual selection?
4. What is the role of
What makes the difference between stable local adaptation and progress towards complete reproductive
reinforcement?
isolation?
Is the strength of assortative mating (= a correlation between mates for the value of a trait expressed in both
sexes) typically an adaptation or is it more often a by-product of other processes, such as habitat choice?
Does reinforcement commonly play a part in speciation? Specifically, are we overrating reinforcement
because of a publication bias towards studies that do find evidence for reinforcement?
The conditions for speciation to take place by reinforcement are complex. How can we adequately test for
reinforcement experimentally? [Previous experiments have used a “kill the hybrids” approach which effectively
makes the two populations good species already]
How often do sympatric species show higher pre-zygotic isolation than allopatric species of comparable age?
Pre-mating hybridization barriers often evolve by disrupting and/or diversifying an existing intraspecific
communication channel (e.g. sex pheromones, mating calls). On the other hand, there should be stabilizing
selection on an already functioning communication channel. How can the stabilizing selection be overcome?
How important is a broad range of recognition criteria in the receiving sex for the evolution of pre-mating
barriers? Do receivers always "follow" the sender of these cues and/or signals? Are traits, cues or signals
used for mate finding and species discrimination selected by the receiver?
5. How important is hybridisation
What is the role of hybridisation in generating new species? [It is important in plants, but its relative
in speciation?
contribution in animals is still debated.]
6. What are the environmental
Can we distinguish common scenarios in the dynamics of the appearance of reproductive barriers due to
and genetic conditions that
genotypic architecture, developmental pathways, etc?
promote speciation?
What is the role of standing genetic variance in generating new species? [Some variation is essential, but
perhaps too much variance would impede fixation of characters related to isolation.]
Does seasonal variation slow down adaptation/speciation processes? [Seasonal variation (changing selection
pressures) maintains genetic variation in adaptively important life-history traits and this may work against
population divergence in these traits.]
How stable are species boundaries?
Is there any strong relationship between geographic context and process in speciation?
Is speciation inevitable? Is it anything more than the evolution of differences? [Modelling shows that genotypic
clusters (“species”) tend to form under a broad range of circumstances. Does this mean that speciation is
inevitable or is it possible to conceive of a world where genetic variation remains continuously distributed
among individuals and no discrete species form?]
Can we predict the conditions under which speciation will occur and how speciation will occur? Can we make
a list of factors which, individually or in combination, make speciation a more likely outcome in any particular
system?
Are there general rules of speciation?
7. What is the nature of speciation How often does meiotic drive or gene transposition (or other such forces) contribute to hybrid male sterility?
genes? Can speciation be due to
What is the role of transposable elements in speciation?
specific genes?
Gene networks are phenotypes. Different species have different phenotypes. How does gene network
architecture reflect speciation?
To what extent is speciation linked with changes in genes, as opposed to changes in interactions among
genes? [Are these changes important in their own right, e.g. changing affinity of an enzyme for its substrate?
Or are they important due to the effect they have on protein-protein or protein-DNA interactions (e.g.
signalling cascades and regulation of transcription)?]
Can changes in sex determination mechanisms lead to speciation?
Do genetic changes involved in speciation preferentially involve a certain class of genes? That is, do
speciation genes group into specific gene ontologies?
What kind of genes are involved in different forms or reproductive isolation (e.g. behavioural isolation or
hybrid sterility?
What genetic changes underlie reproductive isolation? Can any gene be a speciation gene, or are there
specific classes of genes involved in speciation?
Why do we not see rampant positive selection in speciation gene families? Chemosensory genes may be an
example, with less positive selection than sperm-egg recognition proteins. Are expression or copy-number
changes more important than sequence-level evolution?
Do speciation genes exist? [What is known about the genes involved in speciation? How many speciation
genes are known?]
Are taxonomically-restricted genes (i.e. so called orphan genes) important in evolution and eventually in
speciation? For example, in basal metazoans such as Nematostella, Acropora and Hydra “orphan genes” are
involved in important species-specific adaptive processes.
There is now a lot of evidence from genomic studies that loci related to sperm development are under strong
positive selection. How and how often do these changes contribute to reproductive isolation?
8. What is the role of changes in
What is the importance of gene expression differences vs. coding sequences differences in population
gene expression and in genomic
divergence and in the evolution of reproductive isolation?
processes?
To what degree are the differences in mating behaviour (or any isolating trait) due to changes in gene
regulation versus variation in coding region? How important are epigenetic changes and how stable are they?
What is the role of gene regulation in speciation? More specifically, does the redundancy of regulatory
networks keep differentiation from occurring or is it precisely this redundancy that allows for some variation
which might be subjected to differential selection?
Gene expression patterns are phenotypes. Different species have different phenotypes. How do gene
expression patterns reflect speciation?
We are very concerned with the genetic basis of variation in adaptive traits. Where do we have to look for this
genetic variation? Are differences in regulatory genomic regions more or less important than differences in
coding sequences? Do these differences lead to speciation?
What is the relative importance of changes in regulatory versus coding regions of the genome in promoting
reproductive isolation?
How important is epigenetic inheritance in the evolution of species?
9. What is the role of plasticity?
What role do gene-environment interactions play in speciation? Especially phenotypic plasticity: it can
generate phenotypic variation, is heritable and it may contribute to the evolution of reproductive isolation. Can
plasticity play a part in speciation events involving sexual selection?
Can phenotypic plasticity slow down speciation processes? [Plasticity of life-history traits may dampen the
effects of natural selection by, for example, allowing individuals to rapidly adapt to new environmental
conditions resulting in reduced genetic divergence.]
Does plasticity pre-dispose populations to divergence? If the answer is ‘Yes and No’; then when is it ‘Yes’ and
when is it ‘No’? Can any generalizations or predictions be made?
How can the contribution of phenotypic plasticity (reaction norms) to speciation be validated?
Why are there so many different species rather than a few species with highly phenotypically plastic forms?
Does phenotypic plasticity constrain speciation?
Can adaptation to local conditions lead to speciation through plastic changes in male mating signals? [Male
mating signals are often sensitive to male condition. Can the females get information through these signals on
how well the males have adapted to local conditions and can mate choice favouring locally adapted
individuals finally lead to speciation?]
10. What are the genomic
How frequently do chromosomal rearrangements contribute to speciation? When chromosomal
patterns of reproductive isolation? rearrangements do contribute to speciation, how frequently is it because of their genic content and how
frequently because of the structural effects of the rearrangements?
Are there genetic constraints to speciation?
How many loci in the genome need to diverge in order to cause appreciable reproductive isolation between
populations? Are those loci physically linked and concentrated on the X chromosome?
What is the pattern of differentiation across the genome and how does it vary among modes of speciation or
over time?
Where in the genome do changes that cause reproductive isolation preferentially occur? [Do they occur in
regulatory parts of DNA that code for where in the body and when during development genes are activated, or
do they influence properties of the genes themselves, like where within a cell a certain enzyme will be located
and what reaction it catalyzes?]
Are there certain genomic regions that accumulate differences at faster rates than others? Do traits become
isolating barriers due to their genomic location (i.e. can any trait in a certain location become a barrier), or do
certain traits have inherent properties that make them more likely to diverge regardless of their location?
The role of introns in the genome is poorly known. Exon/intron structures of genes differ greatly across
species and the effects of intron gains and losses are not entirely known. Latest studies have shown that
intron function could be far more important in the evolution of genomes (and eventually in speciation) than
previously thought (i.e. exonization where an intron becomes an exon).
Is genome sequencing any use in positively resolving questions in speciation research? [If genome
sequences do contain the answers to important questions, how many genomes are needed and how do we
find the answers in the mass of data?]
Can ‘next generation’ methods help to find new speciation genes? Whole genomes of different organisms can
be compared with the aid of next generation methods – will this start a new era in speciation research?
Will the current inflow of genomic data change the concept(s) of species definition?
11. How are biodiversity patterns
Do cryptic species result from a particular type of speciation mechanism more so than any other?
related to speciation
How can phylogenies be used to infer the mechanisms underlying speciation?
mechanisms?
How can the patterning of present-day biodiversity be used to infer the mechanisms underlying speciation?
How do current patterns of diversity reflect different mechanisms of speciation? Can we relate patterns of
diversity to processes of speciation and diversification?
How can the theories of micro-evolution and speciation be integrated to achieve a synthetic theory of macroevolution?
12. What causes variation in
How can we compare gradual and quantum speciation? Do they have anything in common?
speciation rate and duration?
What are the causes of the natural biodiversity patterns on a global scale, especially the latitudinal cline in
species richness.
Why is it that, although species are far more numerous in terrestrial/freshwater environments, there is a
greater diversity of phyla in the marine environment?
What is the explanation for “Punctuated Equilibria?” [Why do species appear to remain unchanged for long
periods of time, even when the environment changes drastically? E.g. many species from Pleistocene
deposits are morphologically identical to current-day populations and only seem to have suffered
biogeographic effects from the glaciations. Given our knowledge on the potentially rapid evolutionary
response to changes in environment, these patterns are no less puzzling now than they were 40 years ago.]
What determines the evolutionary success of a species? Is radiation an evolutionary success strategy, or are
those clades that are widespread and able to adapt to local conditions more resistant against extinction?
What kind of genetic changes (gene gains and losses, changes in the function and splicing of regulatory
genes and the rate of non-synonymous mutations) underlie rapid evolution in island ecosystems and why do
founder events to new islands so often lead to the evolution of new species?
The timescale of speciation: how rapidly can speciation occur and how rapidly does it usually occur?
What makes certain taxa speciate at much faster rates than others? Are there certain elements (molecular,
ecological) that are shared between the taxa that show rapid speciation rates, and can we use these to
predict the future patterns of biodiversity?
What factors limit speciation rates in "living fossils" (lung fish, horseshoe crabs, etc.)?
Why is diversification faster in some clades than others? How can we explain the fact that some clades have
remained constant in the number of species while other clades exhibit enormous radiation? Is this due to
inherent characteristics of these groups or can we discover a universal law that explains this?
How do phylogenetic constraints have an impact on the evolvability of pre-mating barriers?
Does speciation really take millions of years to occur?
13. What is the impact of
What are the human impacts on speciation rates and patterns? Has our destruction of biodiversity allowed for
anthropogenic change?
increased speciation by freeing up niche-space for example?
Are mass extinction events (comet/meteor collisions, disease, etc.) and/or anthropogenic disturbances (global
warming, oil spills, pollution, ect.) actually “good” for the process of speciation in the long run (for instance, by
opening up vast new niches, which in turn may promote new evolutionary radiations)? In other words, is
species conservation GOOD for speciation?
Is anthropogenic activity slowing-down or accelerating speciation. It may be that both are true in different
systems, yet it would be useful to know the main effect
What is the importance of speciation in a rapidly changing world? If extinction rates increase (as they are
doing now), can we expect some groups of species to radiate faster and occupy the available niches?
Box 1
Does genomics allow for a universal species concept? [Gene-centred views of species are beginning to allow
a convergence between species concepts in eukaryotes and prokaryotes, with rates of genetic exchange
across the genome the common denominator: insect species differences are sometimes restricted to a
relatively small genome region where recombination does not occur and the same may be true for bacteria.]
Does the term “species” refer to a real evolutionary unit or is it just a concept “made up” by scientists in order
to have a common reference unit?
How do we know when speciation is finished and a new species is formed?
Box 4
What questions about speciation have been decisively answered in the last 150 years?
Will we answer the open questions in speciation research by focusing on the established model species or is
there more of a role for non-model organisms (due to the decreased sequencing costs)?