Out of the testis, into the ovary: biased outcomes of gene duplication and deletion in Drosophila.

Abstract

Gene turnover is a key source of adaptive variation. Yet most evolutionary studies have focused on gene duplication, dismissing gene deletion as a mechanism that simply eradicates redundancy. Here, I use genome-scale sequence and multi-tissue expression data from Drosophila melanogaster and Drosophila pseudoobscura to simultaneously assess the evolutionary outcomes of gene duplication and deletion in Drosophila. I find that gene duplication is more frequent than gene deletion in both species, indicating that it may play a more important role in Drosophila evolution. However, examination of several genic properties reveals that genes likely possess distinct functions after duplication that diverge further before deletion, suggesting that loss of redundancy cannot explain a majority of gene deletion events in Drosophila. Moreover, in addition to providing support for the well-known "out of the testis" origin of young duplicate genes, analyses of gene expression profiles uncover a preferential bias against deletion of old ovary-expressed genes. Therefore, I propose a novel "into the ovary" hypothesis for gene deletion in Drosophila, in which gene deletion may promote adaptation by salvaging genes that contribute to the evolution of female reproductive phenotypes. Under this combined "out of the testis, into the ovary" evolutionary model, gene duplication and deletion work in concert to generate and maintain a balanced repertoire of genes that promote sex-specific adaptation in Drosophila.