Trends in Ecology & Evolution
OpinionThe genes underlying the process of speciation
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
References (82)
What does Drosophila genetics tell us about speciation?
Trends Ecol. Evol.
(2006)Recent advances in assessing gene flow between diverging populations and species
Curr. Opin. Genet. Dev.
(2006)Sympatric speciation in animals: the ugly duckling grows up
Trends Ecol. Evol.
(2001)Speciation genetics: epistasis, conflict and the origin of species
Curr. Biol.
(2007)Hybrid incompatibility genes: remnants of a genomic battlefield?
Trends Genet.
(2010)Speciation genes
Curr. Opin. Genet. Dev.
(2004)- et al.
Speciation
(2004) The genetic basis of reproductive isolation: insights from Drosophila
Proc. Natl. Acad. Sci. U.S.A.
(2005)- et al.
Speciation genetics: evolving approaches
Nat. Rev. Genet.
(2006) Evidence for ecological speciation and its alternative
Science
(2009)
Skepticism towards Santa Rosalia, or why are there so few kinds of animals?
Evolution
Speciation genes in plants
Ann. Bot.
Doomed lovers: mechanisms of Isolation and Incompatibility in plants
Annu. Rev. Plant Biol.
Natural selection in action during speciation
Proc. Natl. Acad. Sci. U.S.A.
Fitness Landscapes and the Origin of Species
A fine-scale genetic analysis of hybrid incompatibilities in Drosophila
Genetics
Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae)
Evolution
Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats
Evolution
The strength and genetic basis of reproductive isolating barriers in flowering plants
Philos. Trans. R. Soc. B: Biol. Sci.
Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila
Science
A single gene causes both male sterility and segregation distortion in Drosophila hybrids
Science
Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities
Science
Genes and speciation
Nat. Rev. Genet.
Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones
Nature
Reproductive protein evolution
Annu. Rev. Ecol. Syst.
Reproductive isolation between species of sea urchins
Bull. Mar. Sci.
Plant speciation
Science
Speciation and the evolution of gamete recognition genes: pattern and process
Heredity
A genetic interpretation of ecologically dependent isolation
Evolution
Ecological speciation
Ecol. Lett.
A rapidly evolving homeobox at the site of a hybrid sterility gene
Science
The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus
Proc. Natl. Acad. Sci. U.S.A.
The normal function of a speciation gene, Odysseus, and its hybrid sterility effect
Science
A rapidly evolving MYB-related protein causes species isolation in Drosophila
Proc. Natl. Acad. Sci. U.S.A.
Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus
PLoS Biol.
Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila
Nature
Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless
Proc. Natl. Acad. Sci. U.S.A.
Consequences of reproductive barriers for genealogical discordance in the European corn borer
Proc. Natl. Acad. Sci. U.S.A.
A simple genetic incompatibility causes hybrid male sterility in Mimulus
Genetics
The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat (PPR) genes
Genetics
Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species
New Phytologist
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