The genetic basis of rapidly evolving male genital morphology in Drosophila

The external genitalia are some of the most rapidly evolving morphological structures in insects. The posterior lobe of the male genital arch shows striking differences in both size and shape among closely related species of the Drosophila melanogaster species subgroup. Here, we dissect the genetic basis of posterior lobe morphology between D. mauritiana and D. sechellia, two island endemic species that last shared a common ancestor ∼300,000 years ago. We test a large collection of genome-wide homozygous D. mauritiana genetic introgressions, which collectively cover ∼50% of the genome, for their morphological effects when placed in a D. sechellia genetic background. We find several introgressions that have large effects on posterior lobe morphology and that posterior lobe size and posterior lobe shape can be separated genetically for some of the loci that specify morphology. Using next generation sequencing technology, we perform whole transcriptome gene expression analyses of the larval genital imaginal disc of D. mauritiana, D. sechellia, and two D. mauritiana-D. sechellia hybrid introgression genotypes that each have large effects on either posterior lobe size or posterior lobe shape. Many of the genes we identify as differentially expressed are expressed at levels similar to D. mauritiana in one introgression hybrid, but are expressed at levels similar to D. sechellia in the other introgression hybrid. However, we also find that both introgression hybrids express some of the same genes at levels similar to D. mauritiana, and notably, that both introgression hybrids possess genes in the insulin receptor signaling pathway, which are expressed at D. mauritiana expression levels. These results suggest the possibility that the insulin signaling pathway might integrate size and shape genetic inputs to establish differences in overall posterior lobe morphology between D. mauritiana and D. sechellia.