Abstract
Reinforcement occurs when natural selection strengthens behavioral discrimination to prevent costly interspecies matings, such as when matings produce sterile hybrids. This evolutionary process can complete speciation, thereby providing a direct link between Darwin's theory of natural selection and the origin of new species. Here, by examining a case of speciation by reinforcement in Drosophila, we present the first high-resolution genetic study of variation within species for female mating discrimination that is enhanced by natural selection. We show that reinforced mating discrimination is inherited as a dominant trait, exhibits variability within species, and may be influenced by a known set of candidate genes involved in olfaction. Our results show that the genetics of reinforced mating discrimination is different from the genetics of mating discrimination between species, suggesting that overall mating discrimination might be a composite phenomenon, which in Drosophila could involve both auditory and olfactory cues. Examining the genetics of reinforcement provides a unique opportunity for both understanding the origin of new species in the face of gene flow and identifying the genetic basis of adaptive female species preferences, two major gaps in our understanding of speciation.
Highlights
During reinforcement, mating discrimination is strengthened by natural selection in response to maladaptive hybridization between closely related taxa (Dobzhansky 1940; Fisher 1958)
Alleles conferring mating discrimination spread if they become genetically correlated with alleles reducing hybrid fitness
We have provided the first genetic dissection of an adaptive female preference involved in speciation by developing a quantitative trait locus (QTL) map for discrimination variation in Drosophila pseudoobscura
Summary
During reinforcement, mating discrimination is strengthened by natural selection in response to maladaptive hybridization between closely related taxa (Dobzhansky 1940; Fisher 1958). Theoretical work on reinforcement shows that reproductive isolation may be strengthened when either the same (one) or different (two) alleles conferring mating discrimination spread in the emerging species (Felsenstein 1981). Alleles conferring mating discrimination spread if they become genetically correlated with alleles reducing hybrid fitness. One-allele models are not opposed by recombination because alleles conferring mating discrimination reduce hybridization in the genetic background of both species (Kelly and Noor 1996; Servedio 2000) and so may be more conducive to reinforcement. Empirical data concerning these two models of speciation are lacking (see Ortız-Barrientos et al 2002; Servedio and Noor 2003)
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