Social challenge or opportunity result in unique cell type specific transcriptome and modulate reproductive related behaviors and physiology

Living in a social environment involves diverse types of interactions between members of the same species that are essential for the health, survival, and reproduction of animals. The intricate nature of social interaction requires the ability to recognize other members of the group in the right context, season, sex, age, and reproductive state, and to respond appropriately to different social encounters. Here we explored the behavioral responses of male Drosophila melanogaster exposed to challenge or opportunity (i.e. repeated sexual rejection, or to multiple successful mating events) on their behavioral responses when interacting with other male flies in a group. We discovered that rejected male flies and mated male flies respond differently when they encounter other male flies. Rejected males show increased activity and engage in fewer touch behaviors while maintaining large distances between flies. In contrast, mated males exhibit long periods of quiescence-like behavior, short distances between flies, an increased aggregation behavior. We find that rejected males exhibit significantly higher aggressive displays in comparison to mated male flies, and when allowed to mate with virgin females, they expand the duration of copulation events. These behavioral changes are associated with changes in the expression of several accessory gland proteins and with a unique transcriptional profile within different neuronal populations in the brain that regulate both metabolic aspects and reproductive success. Our results provide an insight into how social behavior is influenced by sexual competition and demonstrate that Drosophila males employ a plastic mating strategy that is regulated by sexual experience.