Sox21bunderlies the rapid diversification of a novel male genital structure betweenDrosophilaspecies

Abstract

SummaryThe emergence and subsequent diversification of morphological novelties is a major feature of animal evolution1–9. However, in most cases little is known about the molecular basis of the evolution of novel structures and the genetic mechanisms underlying their diversification. The epandrial posterior lobes of the male genital arch is a novelty of some species of theDrosophila melanogastersubgroup10–13. The posterior lobes grasp the ovipositor of the female and then integrate between her abdominal tergites, and therefore these structures are important for copulation and species-recognition10–12,14–17. The posterior lobes evolved from co-option of a Hox regulated gene network from the posterior spiracles10and have since diversified in shape and size in theD. simulansclade in particular over the last 240,000 years driven by sexual selection18–21. The genetic basis of this diversification is highly polygenic but to the best of our knowledge none of the causative genes have yet been identified despite extensive mapping22–30. Identifying the genes underlying the diversification of these secondary sexual structures is essential to understanding the basis of changes in their morphology and the evolutionary impact on copulation and species recognition. Here, we show that the transcription factor encoded bySox21bnegatively regulates posterior lobe size during development. This is consistent with higher and expanded expression ofSox21binD. mauritiana, which develops smaller posterior lobes compared toD. simulans. We tested this by generating reciprocal hemizygotes and confirmed that changes inSox21bunderlie posterior lobe evolution between these two species. Furthermore, we found that differences in posterior lobe size caused by the species-specific allele ofSox21bsignificantly affect the duration of copulation. Taken together, our study reveals the genetic basis for the sexual selection driven diversification of a novel morphological structure and its functional impact on copulatory behaviour.HighlightsSox21bregulates the development of the epandrial posterior lobes, a recently evolved novel structure of some species of theDrosophila melanogastersubgroup, which has subsequently rapidly diversified in size and shape.D. mauritianahas smaller posterior lobes thanD. simulansand more expansive expression ofSox21bin the developing genitalia. Using a reciprocal hemizygosity test, we show that variation inSox21bunderlies the diversification of epandrial posterior lobe size and shape betweenD. simulansandD. mauritiana.Behavioural tests show that the species allele ofSox21bcauses differences in the duration of copulation in otherwise genetically identical backgrounds.Sox21bhas evolved betweenD. simulansandD. mauritiana, and contributed to the divergence of a morphological novelty and copulatory behaviour between these two species.