Failure to mate enhances investment in behaviors that may promote mating reward and impairs the ability to cope with stressors via a subpopulation of Neuropeptide F receptor neurons

Abstract

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.

Sexual deprivation induces a CRF independent stress response and decreases resistance to stressors inDrosophilavia a subpopulation of Neuropeptide F receptor-expressing neurons

“…Similar responses to social stress and reward-seeking behaviors can be seen in a variety of animals, suggesting that the central systems facilitating survival and reproduction originated early in evolution, and that similar ancient basic building blocks, biological processes and genes are inherently involved in these processes 7,39 . In agreement with this concept, we and others showed that Drosophila melanogaster display the ability to adjust their behavior and physiology to various changes in their social environment [40][41][42][43][44][45][46][47][48][49][50][51][52] . Moreover, recent studies provided evidence that the brains of mammals and fruit flies share similar principles when it comes to encoding stress and reward 40,[53][54][55] .…”

“…In response to repeated failures to mate, rejected males exhibit features characteristic of a frustrationlike state, such as persistent mating actions (some of which are elongated), increased arousal, increased aggression, as well as long mating duration upon successful mating encounters, all of which are reminiscent of high motivational state 47 . While this motivational state may serve to increase their fitness, it is perceived as a stressful experience manifested by the appearance of displacement-like behavior and accompanied by temporal costs in the form of sensitivity to acute stressors.…”

“…We previously documented increased aggression, increased social avoidance and longer mating duration (LMD) following repeated sexual deprivation 47 . These actions can be interpreted as a result of a frustration-like state caused by stressful encounters with unreceptive females.…”

“…The latter is augmented by increased expression of certain seminal fluid genes that facilitate stronger postmating responses in female flies 47 . While certain types of social challenges in mammals are considered stressors, affecting health and lifespan, it is not known whether this occurs in fruit flies, and more specifically, whether failure to mate in Drosophila male flies is an acute stressor imposing certain costs to male flies, or simply a lack of reward.…”

“…Successful mating and sexual deprivation bi-directionally regulate the level of NPF, which in turn regulates the motivation to consume ethanol as a drug reward 40,78 . We recently discovered that male flies that experience repeated events of sexual deprivation respond to this social challenge by increasing their competitive behaviors in the form of increased arousal when interacting with rival male flies in a group, elevated aggression, and prolonged copulation time with receptive female flies (known as mate guarding) 47 . The latter is augmented by increased expression of certain seminal fluid genes that facilitate stronger postmating responses in female flies 47 .…”