Female Drosophila melanogaster gene expression and mate choice: candidate genes underlying sexual isolation

Background The evolution of female choice mechanisms favouring males of their own kind is considered as crucial step during the early stages of speciation. However, although the genomics of mate choice may influence both the likelihood and speed of speciation, the identity and location of genes underlying assortative mating remain largely unknown. Methods and Findings We used mate choice experiments and gene expression analysis of female D. melanogaster to examine three key components influencing speciation. We show that the 1,498 genes in Zimbabwean female Drosophila melanogaster whose expression levels differ when mating with more (Zimbabwean) versus less (Cosmopolitan strain) preferred males include many with high expression in the central nervous system and ovaries, are disproportionately X-linked and form a number of clusters with low recombination distance. Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations. Conclusion Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized. We measured gene expression of adult female Drosophila melanogaster from a composite Zimbabwe (Z) strain population named SZ, produced by mixing the genomes of six Z strain isofemale lines, shortly after mating them with either SZ strain or cosmopolitan (M strain) males. Data from four replicates of each of the two treatments (SZ mated with SZ; SZ mated with M) are presented, giving a total of eight arrays.