Gene protein sequence evolution can predict the rapid divergence of ovariole numbers inDrosophila

Abstract

AbstractOvaries play key roles in fitness and evolution: they are essential female reproductive structures that develop and house the eggs in sexually reproducing animals. InDrosophila, the mature ovary contains multiple tubular egg-producing structures known as ovarioles. Ovarioles arise from somatic cellular structures in the larval ovary called terminal filaments, formed by terminal filament cells and subsequently enclosed by sheath cells. As in many other insects, ovariole number per female varies extensively inDrosophila. At present however, there is a striking gap of information on genetic mechanisms and evolutionary forces that shape the well-documented rapid interspecies divergence of ovariole numbers. To address this gap, here we studied genes associated withD. melanogasterovariole number or functions based on recent experimental and transcriptional datasets from larval ovaries, including terminal filaments and sheath cells, and assessed their rates and patterns of molecular evolution in five closely related species of themelanogastersubgroup that exhibit species-specific differences in ovariole numbers. From comprehensive analyses of protein sequence evolution (dN/dS), branch-site positive selection, expression specificity (tau) and phylogenetic regressions (PGLS), we report evidence of 42 genes that showed signs of playing roles in the genetic basis of interspecies evolutionary change ofDrosophilaovariole number. These included the signalling genesupd2andIlp5and extracellular matrix genesvkgandCol4a1, whose dN/dS predicted ovariole numbers among species. Together, we propose a model whereby a set of ovariole-involved gene proteins have an enhanced evolvability, including adaptive evolution, facilitating rapid shifts in ovariole number amongDrosophilaspecies.Significance StatementOvaries inDrosophila, like in other insects, contain egg producing structures, known as ovarioles. The number of ovarioles per female varies amongDrosophilaspecies, but little is known about the genes and evolutionary dynamics that may shape interspecies changes in ovariole numbers. Here, useda prioriexperimental and transcriptome data fromD. melanogasterto identify genes involved in ovariole formation and functions, and studied their molecular evolution among its closely related species within themelanogastersubgroup. Using a multi-layered analysis consisting of protein sequence divergence (dN/dS), adaptive evolution, expression breadth, and phylogenetic regressions, we identified 42 genes whose molecular evolution patterns were well linked to ovariole numbers divergence. Further, gene protein sequence divergence was often predictive of species ovariole numbers.