Review
Ecological explanations for (incomplete) speciation

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Divergent natural selection has been shown to promote speciation in many taxa. However, although divergent selection often initiates the process of speciation, it often fails to complete it. Several time-based, geographic and genetic factors have been recognized to explain this variability in how far speciation proceeds. We review here recent evidence indicating that variability in the completeness of speciation can also be associated with the nature of divergent selection itself, with speciation being greatly promoted by (i) stronger selection on a given, single trait (the ‘stronger selection’ hypothesis) and (ii) selection on a greater number of traits (the ‘multifarious selection’ hypothesis). However, evidence for each selective hypothesis is still scarce, and further work is required to determine their relative importance.

Section snippets

Variability in the completeness of ecological speciation

The causes of speciation have received much attention from biologists 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13. One hypothesis posits that divergent selection between ecological niches drives the evolution of reproductive incompatibility (see Glossary). This process of ‘ecological speciation’ occurs because traits under divergent natural selection, or those genetically correlated with them, affect reproductive compatibility 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, and includes the special

Non-ecological factors promoting speciation

Much theoretical and empirical work on the completeness of speciation has focused on time-based, geographic or genetic factors (Figure 2). Speciation can be promoted by increased time since beginning of divergence 4, 16 and by geographic barriers to gene flow 4, 5. Speciation can also be promoted by pleiotropic effects on reproductive isolation of genes under selection 4, 5, 8, 37 and by physical linkage of genes under selection and those conferring reproductive isolation, perhaps facilitated

A unified framework for testing ecological speciation

The study of ecological speciation involves isolating the association between ecological divergence and the completeness of speciation, independent from the other factors discussed above (Box 1) 1, 2, 8, 9, 10. Examples of measures of ecological divergence are the extent of divergence between taxa along one niche dimension (we hereafter use the term ‘niche dimension’ to refer to an ecological axis, such as habitat use 3, 32, 36), the number of niche dimensions that differ between taxa, the

The nature of ecological shifts and the completeness of speciation

The nature of ecological shifts can affect the completeness of speciation (Box 1). Under one scenario, slight shifts along a single niche dimension initiate speciation, but more extreme shifts along that same dimension are required to complete speciation 5, 7, 9. This idea has seen few tests, because most speciation studies consider only two categories of ecological divergence (ecologically similar and ecologically divergent), precluding a test of how reproductive isolation varies with the

Mechanisms strongly promoting speciation: stronger versus multifarious selection

We consider two mechanisms by which extreme or highly dimensional ecological shifts promote speciation (Figure 3). First, under the stronger selection hypothesis, the completeness of speciation is positively related to the strength of selection on a single trait, with very strong selection on one or a few traits driving the completion of speciation 3, 4, 5, 6. Second, under a multifarious selection hypothesis, the completeness of speciation is positively related to the number of genetically

Probability of speciation under stronger versus multifarious selection

The probability of speciation under stronger versus multifarious selection can vary according to the total strength of divergent selection, per-trait selection coefficients and the nature of correlations between selected traits and other traits.

Support for the stronger selection hypothesis

Support for the stronger selection hypothesis stems from Ref. [9], a study which, in addition to the niche dimensions of diet and habitat, also reports on divergence in one phenotypic trait (body size). In some cases, body size divergence was positively correlated with reproductive isolation, independent from time. Assuming that greater divergence in size arises via stronger divergent selection on size, the results support the stronger selection hypothesis. Similar results stem from positive

Support for the multifarious selection hypothesis

This hypothesis most clearly traces its roots to a review of experimental evolution studies in Drosophila that concluded that ‘laboratory experiments collectively indicate that multifarious…divergent selection can readily lead to complete reproductive isolation, but that single-factor…divergent selection will typically lead to only incomplete reproductive isolation’ ([33], p. 1647). Despite being intuitive, there are almost no tests of this hypothesis in nature, perhaps due to the difficulty of

Integration of different factors affecting speciation

The selective hypotheses reviewed here are refinements of the ecological speciation hypothesis. Nonetheless, such refinements are important, given the abundant unexplained variability in the stage of speciation achieved (Table 1). Similar refinement has been important for understanding the specific role of geographic, genetic and time-based factors in speciation 4, 5, 71. For example, it would be overly crude to classify levels of gene flow during divergence as present versus absent; a

Conclusions and future directions

We have outlined a framework for testing the role of ecology in the completeness of speciation, reviewed how speciation can be strongly promoted by extreme or highly dimensional ecological shifts and outlined two hypotheses for why such shifts drive speciation: the stronger and multifarious selection hypotheses. Each hypothesis has seen some limited and relatively indirect support, and certainly one hypothesis does not appear more strongly supported than the other. Thus, further tests are

Acknowledgements

We thank D. Schluter, R. Butlin, J. Bridle, A. Hendry, J. Galindo, S. Egan, J. Lee-Yaw, D. Funk, S. Rogers, C.P. Sandoval, B.J. Crespi, J. Mallet, J. Losos, T. Price, K. Young, H. Collin and the members of the Schluter and Seehausen laboratories for discussions about speciation. D. Schluter, J. Mallet, B.J. Crespi, R. Barrett, M. Maan and D. Funk provided constructive criticism on previous versions of the manuscript. P.N. was funded by a postdoctoral fellowship from the Natural Sciences and

Glossary

Correlated evolutionary response
divergence of a trait, which itself might not be under selection, which occurs because it is correlated with another trait that is under divergent selection. Here we use this term primarily to refer to reproductive isolation that evolves as a correlated response to selection on other traits.
Divergent natural selection
selection arising from environmental differences or ecological interactions (e.g. competition) that acts in contrasting directions on two

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