Genetic analysis of mate sorting in females and its association with host fruit specialization in interbreeding species of Drosophila

Abstract Physical linkage between alleles that confer mate choice and alleles that confer adaptive traits can drive speciation and maintain species despite gene flow. Theoretical models predict that tight linkage is not necessary for ecological speciation to occur but there are few empirical examples to illustrate this idea. Drosophila simulans and D. sechellia are two nascent species of vinegar fly that are still able to interbreed. D. sechellia is an island endemic that has adapted to the fruit of Morinda citrifolia, which is toxic to D. simulans. The two species prefer to mate with their own species, and crosses between D. simulans males and D. sechellia females are rarely successful. Here, we have applied HT-seq based QTL mapping to identify loci that contribute to mate sorting in females and ask if those alleles are linked to genomic regions that confer adaptation to M. citrifola fruit. We find that mate choice in females is determined by two major effect loci, one on each arm of the third chromosome that interact through epistasis and are found roughly in the same location in both backcrosses. Some female mate sorting loci are found tightly linked to major effect loci that confer male mate sorting and M. citrifolia toxin resistance, but others are more loosely clustered in a ~12 Mbp segment. We suggest that this entangled genetic architecture could have been a factor in the initial divergence between species as well as maintenance of species boundaries during ongoing hybridization between wild D. simulans and D. sechellia.