Sexual rejection modulates social interaction and reproductive physiology

Abstract

In highly polyandrous species, in which 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 reproductive success. 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 alter male-male social interactions. Here we show that repeated failures to mate promote coordinated physiological and behavioral responses that can serve to increase reproductive success over mating rivals in the future competition. We exposed male flies to sexual rejection, successful mating or no sexual experience, and analyzed the behavioral repertoires of individuals within groups and the structure of their emerging social networks. We discovered that failures to mate promote the formation of distinct emergent group interactions and structures, where rejected male flies form low density social networks and actively minimize their encounters with other group members, while increasing their aggressive behavior. In addition, sexually rejected male flies elevate the production of seminal fluid proteins and extend mating duration with receptive females, altogether leading to reduced re-mating rates. Our results demonstrate the existence of a flexible mating response as possible coping strategy for living in a highly dynamic and competitive environment as the social domain.