Sexual deprivation modulates social interaction and reproductive physiology

In highly polyandrous species, where females mate with multiple males within a single fertility period, there is typically a high level of sperm competition. To cope with this challenge, males apply various behavioral and physiological strategies to maximize their paternity rates. Previous studies in Drosophila melanogaster established a link between the composition of the social environment and the reproductive success of individual male flies. While most studies until now focused on the adaptive responses of male flies to the presence of rival males, little is known about whether the outcomes of sexual interactions with female partners affect male-male social interactions in a competitive environment such as the social group. Here we show that repeated failures to mate promote a coordinated physiological and behavioral responses that can serve to increase paternity chances over mating rivals. We exposed male flies to sexual deprivation or successful mating and analyzed the behavioral repertoires of individuals within groups and the structure of their emerging social networks. We discovered that failures to mate and successful mating generate distinct emergent group interactions and structures, where sexually deprived males form low density social networks and actively minimize their encounters with other group members, while increasing their aggressive behavior. In addition, sexually deprived male flies elevate the production of seminal fluid proteins (known to facilitate post-mating responses in females) and extend mating duration upon mating with receptive females, altogether leading to reduced re-mating rates. Our results demonstrate the existence of a flexible mating strategy that may provide a short-term fitness advantage over competing rivals and pave the path for using simple model organisms to dissect the neurobiology of social plasticity as coping strategy to living in a highly dynamic environment as the social domain.