Female × male and male × male interactions have limited influence on competitive fertilization in <i>Drosophila melanogaster</i>

Abstract How males and females contribute to joint reproductive success has been a long-standing question in sexual selection. Under postcopulatory sexual selection (PSS), paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within- and between-sex interactions in Drosophila melanogaster using isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We found surprisingly few genotypic interaction effects on various stages of PSS such as female remating interval, copulation duration, sperm transfer, or sperm storage. Only the timing of female sperm ejection depended on female × male genotypic interactions. By contrast, several reproductive events, including sperm transfer, female sperm ejection and sperm storage, were explained by two- and three-way interactions among sex-specific phenotypes. We also documented complex interactions between the lengths of competing males’ sperm and the female seminal receptacle, which are known to have experienced rapid female-male co-diversification. Our results highlight the non-independence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection. Significance statement For species with internal fertilization and female promiscuity, postcopulatory sexual selection (PSS) is believed to depend, in part, on complex interactions between rival males and between the sexes. Although little investigated, clarifying such interactions is critical as they may limit the efficacy of PSS in the diversification of reproductive traits (e.g., ejaculate biochemistry and sperm, genitalia and female reproductive tract morphology). Here, we resolve how sex-specific traits and their interactions contribute to key reproductive events and outcomes related to competitive fertilization success, including traits known to have experienced rapid diversification. Our results provide novel insights into the operation and complexity of PSS and demonstrate that the processes of sperm competition and cryptic female choice are not independent selective forces.