The Genetic Basis of Rapidly Evolving Male Genital Morphology inDrosophila

Abstract

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. M ORPHOLOGICAL evolution is an important mechanism for generating biodiversity. One of the goals of evolutionary developmental biology is to identify genes that specify morphology and understand how genetic variation at those loci directs development to give rise to intra-and interspecific differences in morphology. Two different approaches have been primarily used to identify genes important for specifying morphological differences between species. One approach has been to identify genes that are important for development of morphological structures in one species and study their developmental roles in closely related species.The second approach has been to genetically map regions of the genome that have large morphological effects between species that produce viable, fertile hybrid offspring to identify the causative loci. Both approaches have been successful in identifying genes, genetic pathways, and regulatory differences underlying species-specific morphologies in a variety of taxa including plants (Luo et al. 1996;Doebley et al.

Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

“…Epandrial posterior lobes provide the strongest discriminatory characters between species of the melanogaster complex (Fig. 1B–C, E–F, H–I, K–L) and have been subject to extensive investigations aiming at identifying the genetic basis of morphological divergence [45]–[50]. We found that average female pouch area correlates with average male lobe area in the melanogaster complex species (Spearman’s rank correlation: r  = 1.00, P <0.157; Fig.…”

Revision of Drusinae subfamily (Trichoptera, Limnephilidae): divergence by paraproct and paramere: speciation in isolation by integration

“…Unfortunately the molecular mechanisms of shape divergences is poorly studied. A limited knowledge is slowly accumulating on genomic processes of the subtle shape divergences, pertaining exclusively to some reference elite organisms like Drosophila, but highly deteriorated by virtuality (Franco et al 2006, Masly et al 2011, Mc Neil et al 2011, Schafer et al 2011.…”

Eat to reproduce: a key role for the insulin signaling pathway in adult insects

“…Besides directly inducing maintenance and proliferation of germ line stem cells in relation to nutrient availability, the ISP also affected spermatocyte growth in testes of male D. melanogaster (Ueishi et al, 2009; McLeod et al, 2010; Wang et al, 2011). A study in other Drosophila species suggested that the ISP also influences the growth of male external genitalia (Masly et al, 2011). Studies on different species of horned beetles suggested that the ISP also mediates the growth of the horns that are used by males of these species for competing with rival males, when protecting female mating partners (Emlen et al, 2012; Lavine et al, 2013).…”