Social interaction and network structure in groups of Drosophila males are shaped by prior social experience and group composition

Abstract

SummaryLiving 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 experience. We simplified the complexity of interactions 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 inter-individual and inter-group variance, high inter-individual coordination, and stable social clusters. Using environmental and genetic manipulations, we show that this structure requires visual and pheromonal cues, and that cVA sensing neurons are necessary for the expression of different aspects of social interaction in a group. Finally, we explored the formation of group behavior and structure in heterogenous groups composed of flies with distinct internal states, and discovered evidence suggesting that group structure and dynamics reflect a level of complexity that cannot be explained as a simple average of the individuals that constitute it. 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 social environments.