Conservation and divergence of sex-biased gene expression across 50 million years of Drosophila evolution

Abstract

In sexually dimorphic species, sex-biased gene expression plays an important role in driving morphological, physiological, and behavioral differences between males and females. Here, we examined patterns of sex-biased gene expression within and among 6 Drosophila species with divergence times ranging from 2-50 million years. We detected contrasting patterns of sex bias conservation and turnover between heads and bodies, with more extensive sex-biased expression and greater conservation of sex-biased expression in the body, but more species-specific turnover of sex-biased expression in the head, where conserved, unbiased expression was common. Interestingly, lineage-specific gains of sex-biased expression occurred most often via concordant expression changes in both sexes that differed only in their magnitude, with this pattern being particularly strong in the head, suggesting that the majority of lineage-specific sex bias gains do not represent a resolution of sexual antagonism, but instead reflect regulatory changes shared between the sexes. We detected an enrichment of putatively positively selected expression changes among sex-biased genes in both body parts. Altogether, our findings suggest that sex-biased expression changes are often facilitated by selection, including selection acting on the sex with lower expression, which is especially common for male expression of female-biased genes. We also detected differences in the proportion of sex-biased genes located on the X chromosome depending on sex bias and body part. Overall, our results provide novel insights into the dynamics of sex-biased gene expression, as well as the molecular mechanisms and selective forces underlying its turnover, across short and long evolutionary timescales.