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The genes underlying the process of speciation

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The long-standing goal of finding genes causing reproductive isolation is being achieved. To better link the genetics with the process of speciation, we propose that ‘speciation gene’ be defined as any gene contributing to the evolution of reproductive isolation. Characterizing a speciation gene involves establishing that the gene affects a component of reproductive isolation; demonstrating that divergence at the locus occurred before completion of speciation; and quantifying the effect size of the gene (i.e. the increase in total reproductive isolation caused by its divergence). Review of a sample of candidate speciation genes found that few meet these criteria. Improved characterization of speciation genes will clarify how numerous they are, their properties and how they affect genome-wide patterns of divergence.

Section snippets

What are speciation genes and why study them?

Understanding the genetic basis of speciation is a long-standing goal in evolutionary biology, but many questions remain unanswered or debated 1, 2, 3. For example, how many genes contributed to speciation? What are their effect sizes? Are the same genes involved repeatedly in independent speciation events? Did mutations involved in speciation arise de novo or from older standing genetic variation? How prevalent are Dobzhansky-Muller incompatibilities (see Glossary) compared with additive

Criteria for speciation genes

We propose that identifying a speciation gene involves the following steps: (i) demonstrating that the gene has an effect on a component of reproductive isolation today; (ii) demonstrating that divergence at the locus occurred before speciation was complete; and (iii) quantifying the ‘effect size’ of the gene at the time it diverged; that is, the degree to which divergence at the locus increased total reproductive isolation.

Past definitions of speciation genes invoke criterion (i) above. By our

Candidate speciation genes

It is only with technological advances made during the past decade or so that numerous genes underlying reproductive isolation have been robustly identified and analyzed at the DNA-sequence level 1, 14, 15, 16. How strong is the evidence that they are speciation genes? To answer this, we compared examples from the literature against our criteria (Tables S1 and S2 in the supplementary material online). Our goal was to illustrate the application of our criteria using a sample of candidate genes,

Speciation genes and the mechanisms of speciation

Candidate speciation genes have already provided information about the speciation process. Particularly in animal taxa, there is evidence that genes causing reproductive isolation were influenced by natural selection. First, an increasing number of genes are being discovered whose alternative alleles affect phenotypic traits that are adapted to contrasting environments. These genes might contribute to extrinsic reproductive isolation. In some cases, the mechanism of selection affecting the gene

Conclusions and future directions

Genes causing reproductive isolation have been called ‘speciation genes’. Here, we outlined a modified definition and the criteria to meet it. Our survey of examples highlights the work that remains to be done to better characterize speciation genes. For example, some genes expected to lead to extrinsic isolation have been identified, but their effects on reproductive isolation have yet to be measured. For candidate speciation genes affecting all types of reproductive isolation, future studies

Acknowledgments

J. Galindo, S. Pavey, J. Mallet, H. Collin, J. Feder and A. Meyer provided useful discussion concerning the genetics of speciation. J. Feder, R. Barrett, S. Rogers, L. Rieseberg, and four anonymous reviewers provided comments on an earlier draft of the article. During the writing of this article, P.N. was funded by the Institute for Advanced Study Berlin (Wissenschaftskolleg) and D.S. by the Natural Sciences and Engineering Council of Canada.

Glossary

Divergent natural selection
selection that either acts in contrasting directions between two populations, usually with reference to ecological differences between their environments (e.g. large body size confers high survival in one environment and low survival in the other), or that favors opposite extremes of a trait within a single population (i.e. disruptive selection).
Dobzhansky-Muller incompatibilities
hybrid dysfunction arising from negative interactions (epistasis) between alleles at two

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