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The reward system is a collection of circuits that reinforce behaviors necessary for survival [1, 2]. Given the importance of reproduction for survival, actions that promote successful mating induce pleasurable feeling and are positively reinforced [3, 4]. This principle is conserved in Drosophila, where successful copulation is naturally rewarding to male flies, induces long-term appetitive memories [5], increases brain levels of neuropeptide F (NPF, the fly homolog of neuropeptide Y), and prevents ethanol, known otherwise as rewarding to flies [6, 7], from being rewarding [5]. It is not clear which of the multiple sensory and motor responses performed during mating induces perception of reward. Sexual interactions with female flies that do not reach copulation are not sufficient to reduce ethanol consumption [5], suggesting that only successful mating encounters are rewarding. Here, we uncoupled the initial steps of mating from its final steps and tested the ability of ejaculation to mimic the rewarding value of full copulation. We induced ejaculation by activating neurons that express the neuropeptide corazonin (CRZ) [8] and subsequently measured different aspects of reward. We show that activating Crz-expressing neurons is rewarding to male flies, as they choose to reside in a zone that triggers optogenetic stimulation of Crz neurons and display conditioned preference for an odor paired with the activation. Reminiscent of successful mating, repeated activation of Crz neurons increases npf levels and reduces ethanol consumption. Our results demonstrate that ejaculation stimulated by Crz/Crz-receptor signaling serves as an essential part of the mating reward mechanism in Drosophila. VIDEO ABSTRACT.

Living in a social environment requires the ability to respond to specific social stimuli and to incorporate information obtained from prior interactions into future ones. One of the mechanisms that facilitates social interaction is pheromone-based communication. In Drosophila melanogaster, the male-specific pheromone cis-vaccenyl acetate (cVA) elicits different responses in male and female flies, and functions to modulate behavior in a context and experience-dependent manner. Although it is the most studied pheromone in flies, the mechanisms that determine the complexity of the response, its intensity and final output with respect to social context, sex and prior interaction, are still not well understood. Here we explored the functional link between social interaction and pheromone-based communication and discovered an odorant binding protein that links social interaction to sex specific changes in cVA related responses. Odorant binding protein 69a (Obp69a) is expressed in auxiliary cells and secreted into the olfactory sensilla. Its expression is inversely regulated in male and female flies by social interactions: cVA exposure reduces its levels in male flies and increases its levels in female flies. Increasing or decreasing Obp69a levels by genetic means establishes a functional link between Obp69a levels and the extent of male aggression and female receptivity. We show that activation of cVA-sensing neurons is sufficeint to regulate Obp69a levels in the absence of cVA, and requires active neurotransmission between the sensory neuron to the second order olfactory neuron. The cross-talk between sensory neurons and non-neuronal auxiliary cells at the olfactory sensilla, represents an additional component in the machinery that promotes behavioral plasticity to the same sensory stimuli in male and female flies.

As a result of an author oversight in the originally published version of this article, an error was introduced in the author list. The name Jennifer I.C. Benichou was mistakenly written as Jennifer Benishou. This error has now been corrected online.

Social behaviors are mediated by the activity of highly complex neuronal networks, the function of which is shaped by their transcriptomic and proteomic content. Contemporary advances in neurogenetics, genomics, and tools for automated behavior analysis make it possible to functionally connect the transcriptome profile of candidate neurons to their role in regulating behavior. In this study we used Drosophila melanogaster to explore the molecular signature of neurons expressing receptor for neuropeptide F (NPF), the fly homolog of neuropeptide Y (NPY). By comparing the transcription profile of NPFR neurons to those of nine other populations of neurons, we discovered that NPFR neurons exhibit a unique transcriptome, enriched with receptors for various neuropeptides and neuromodulators, as well as with genes known to regulate behavioral processes, such as learning and memory. By manipulating RNA editing and protein ubiquitination programs specifically in NPFR neurons, we demonstrate that the proper expression of their unique transcriptome and proteome is required to suppress male courtship and certain features of social group interaction. Our results highlight the importance of transcriptome and proteome diversity in the regulation of complex behaviors and pave the path for future dissection of the spatiotemporal regulation of genes within highly complex tissues, such as the brain.

Living in a group creates a complex and dynamic environment in which the behavior of the individual is influenced by and affects the behavior of others. Although social interactions and group living are fundamental adaptations exhibited by many organisms, relatively little is known about how prior social experience, internal states and group composition shape behavior in a group, and the neuronal and molecular mechanisms that mediate it. Here we present a practical framework for studying the interplay between social experience and group interaction in Drosophila melanogaster and show that the structure of social networks and group interactions are sensitive to group composition and individuals' social history. We simplified the complexity of interaction in a group using a series of experiments in which we controlled the social experience and motivational states of individuals to dissect patterns that represent distinct structures and behavioral responses of groups under different social conditions. Using high-resolution data capture, machine learning and graph theory, we analyzed 60 distinct behavioral and social network features, generating a comprehensive representation ("group signature") for each condition. We show that social enrichment promotes the formation of a distinct group structure that is characterized by high network modularity, high interindividual and inter-group variance, high inter-individual synchrony, and stable social clusters. Using environmental and genetic manipulations, we show that this structure requires visual and pheromonal cues. Particularly, the male specific pheromone cVA and Or65a sensory neurons are necessary for the expression of different aspects of social interaction in a group. Finally, we explored social interactions in heterogenous groups and identified clusters of features that are sensitive to increasing ratios of aggressive flies, some of which reveal that inter-individual synchronization depends on group composition. Our results demonstrate that fruit flies exhibit complex and dynamic social structures that are modulated by the experience and composition of different individuals within the group.This paves the path for using simple model organisms to dissect the neurobiology of behavior in complex environments associated with living in a group.Many species have adapted to living in groups, from simple organisms, such as nematodes, to humans. Group living takes different forms with various levels of complexity, from almost random interactions to fully synchronized collective behavior 1-5 , and can be described by measuring the behavior of individuals, the interaction between individuals and the resulting social network, altogether defined here as "group behavior". When individuals interact in a group, their internal motivational state, previous memories and other physiological processes affect their action selection, giving rise to diverse activity levels, behavioral responses, and engagement with others 6 . This results in a highly complex and continuously changing envi...

No 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.