Trends in Ecology & Evolution
ReviewEcological explanations for (incomplete) speciation
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
References (72)
A species definition for the modern synthesis
Trends Ecol. Evol.
(1995)- et al.
Bimodal hybrid zones and speciation
Trends Ecol. Evol.
(2000) Disruptive selection and then what?
Trends Ecol. Evol.
(2006)Sympatric speciation in animals: the ugly duckling grows up
Trends Ecol. Evol.
(2001)Chromosomal rearrangements and speciation
Trends Ecol. Evol.
(2001)- et al.
Adaptation from standing genetic variation
Trends Ecol. Evol.
(2008) Hybridization and adaptive radiation
Trends Ecol. Evol.
(2004)Recent advances in assessing gene flow between diverging populations and species
Curr. Opin. Genet. Dev.
(2006)- et al.
Rapid speciation via parallel, directional selection on regulatory genetic pathways
J. Theor. Biol.
(2000) Herbivorous insects: model systems for the comparative study of speciation ecology
Genetica
(2002)
Comparative analyses and the study of ecological speciation in herbivorous insects
The Ecology of Adaptive Radiation
Speciation
Fitness Landscapes and the Origin of Species
Ecological speciation
Ecol. Lett.
Speciation in Birds
Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles
Evolution
Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa
Proc. Natl. Acad. Sci. U. S. A.
Divergent host-plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking-sticks
Am. Nat.
Reproductive isolation caused by colour pattern mimicry
Nature
Speciation through sensory drive in cichlid fish
Nature
Host races in plant-feeding insects and their importance in sympatric speciation
Philos. Trans. R. Soc. Lond. B Biol. Sci.
Natural hybridization in heliconiine butterflies: the species boundary as a continuum
BMC Evol. Biol.
Progressive levels of trait divergence along a ‘speciation transect’ in the Lake Victoria cichlid fish Pundamilia
Patterns of speciation in Drosophila
Evolution Int. J. Org. Evolution
Perspective: Reproductive isolation caused by natural selection against immigrants from divergent habitats
Evolution Int. J. Org. Evolution
How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles
Mol. Ecol.
Geographic Variation, Speciation and Clines
Consequences of reproductive barriers for genealogical discordance in the European corn borer
Proc. Natl. Acad. Sci. U. S. A.
Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA
Annu. Rev. Ecol. Evol. Syst.
The genic view of the process of speciation
J. Evol. Biol.
Ernst Mayr and the modern concept of species
Proc. Natl. Acad. Sci. U. S. A.
The relative influence of natural selection and geography on gene flow in guppies
Mol. Ecol.
Cichlid fish diversity threatened by eutrophication that curbs sexual selection
Science
Speciation reversal and biodiversity dynamics with hybridization in changing environments
Mol. Ecol.
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