Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless
Marcus R. Kronforst, Laura G. Young, Durrell D. Kapan, Camille McNeely, Rachel J. O'Neill, and Lawrence E. Gilbert
PNAS April 25, 2006; 103:6575-6580
Abstract: Sexual isolation is a critical form of reproductive isolation in the early stages of animal speciation, yet little is known about the genetic basis of divergent mate preferences and preference cues in young species. Heliconius butterflies, well known for their diversity of wing color patterns, mate assortatively as a result of divergence in male preference for wing patterns. Here we show that the specific cue used by Heliconius cydno and Heliconius pachinus males to recognize conspecific females is the color of patches on the wings. In addition, male mate preference segregates with forewing color in hybrids, indicating a genetic association between the loci responsible for preference and preference cue. Quantitative trait locus mapping places a preference locus coincident with the locus that determines forewing color, which itself is perfectly linked to the wing patterning candidate gene, wingless. Furthermore, yellow-colored males of the polymorphic race H. cydno alithea prefer to court yellow females, indicating that wing color and color preference are controlled by loci that are located in an inversion or are pleiotropic effects of a single locus. Tight genetic associations between preference and preference cue, although rare, make divergence and speciation particularly likely because the effects of natural and sexual selection on one trait are transferred to the other, leading to the coordinated evolution of mate recognition. This effect of linkage on divergence is especially important in Heliconius because differentiation of wing color patterns in the genus has been driven and maintained by natural selection for Müllerian mimicry.
The last paragraph gives insight into the overall mechanism:
"Regardless of the specific nature of the association, the fact that wing color and color preference are very tightly linked genetically has important evolutionary consequences. Wing pattern diversification in the genus Heliconius has been driven by natural selection for Müllerian mimicry (33, 46, 47). Because wing color serves as a critical cue in mate recognition, and male preference for wing color is linked to color, natural selection on wing patterns that is imposed by predators will simultaneously drive the divergence of both mate recognition signal and signal preference. This scenario, which provides a direct link between disruptive natural selection and divergence at loci mediating conspecific recognition and mate choice, facilitates the rapid evolution of sexual isolation. Furthermore, the association between color and preference limits recombination between the two components of mate recognition when species and color pattern races hybridize, a common phenomenon in the genus Heliconius, thus allowing phenotypic differentiation to persist in the face of hybridization. Given the effects of this association on the origin and maintenance of diversity, it has undoubtedly played a significant role in facilitating the explosive adaptive radiation of Heliconius butterflies."