Two major-effect loci influence assortative mating in females of the sibling species, Drosophila simulans and D. sechellia

Abstract

Secondary contact between incompletely isolated species can produce a wide variety of outcomes, including production of new species and adaptive radiations. The vinegar flies Drosophila simulans and D. sechellia diverged on islands in the Indian Ocean and are currently separated by partial pre- and postzygotic barriers. The recent discovery of hybridization between D. simulans and D. sechellia in the wild presents an opportunity to monitor the prevalence of alleles that influence introgression between these species. We therefore sought to identify those loci that affect assortative mating, and we adapted a two-choice assay to test behavioral isolation in females. Using high-resolution seq-based QTL mapping, we found two major effect loci on the third chromosome that have a profound effect upon assortative mating of females. Each major QTL accounts for 32-37% of the difference in phenotype on its own, which is highly significant for a behavioral trait. The two major QTL of both backcrosses co-localize in one-dimensional analyses, suggesting that they may be alternate alleles of the same loci. The major-effect loci also co-localize with genes that encode enzymes required for female- and species-specific production of the pheromone, 7,11-heptacosadiene, emphasizing the importance of female attractiveness to males in separation of these species. Moreover, the genetic architecture of female assortative mating may be a factor in species separation, since alleles that influence assortative mating in females are linked to major-effect loci that influence assortative mating in males, and to loci that contribute to host fruit adaptation in D. sechellia.