The female nervous system contributes to postcopulatory sexual selection in Drosophila melanogaster

Abstract

Postcopulatory sexual selection is prolonged in internally fertilizing species in which a female mates with multiple males throughout her lifetime. Sperm from rival males compete for fertilization opportunities, and females can bias sperm usage toward a certain male. Multiple studies have demonstrated that the female’s genotype, the male’s genotype, and female × male genotypic interactions all influence differential paternity proportion, but the genetic factors and mechanistic basis acting in the female remain largely elusive. A previous genome-wide association study of the female genotype’s role in influencing the proportion of first-male progeny (P1) across the Drosophila Genetic Reference Panel (DGRP) identified 33 top-associated candidate genes. My colleagues and I functionally tested these genes using ubiquitous, pan-neuronal, and neuron-type specific gene knockdown, and identified eight genes that regulated P1 through different neurons and reproductive tract tissues. In particular, our results suggested the involvement of octopaminergic/tyraminergic Tdc2 neurons, proprioceptive pickpocket (ppk) neurons, and the female sperm storage organ spermathecae in regulating P1. Tdc2 neurons have critical functions in female reproduction and mediate the transition of unmated to mated state in the female reproductive tract. Further investigation showed that inhibiting Tdc2 neuronal activity in females increased P1. Control females exhibited bias for using second-male sperm to produce progeny, but the bias was suppressed when Tdc2 neurons were inhibited. Tdc2 neuronal activity was not required for other aspects of differential sperm handling. Taken together, these results contribute to our understanding of the mechanisms by which the female acts in postcopulatory sexual selection by identifying specific genes and tissues, and a physiological mechanism, that contribute to differential paternity proportions.