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

Abstract

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...

Drosophila melanogaster behaviour changes in different social environments based on group size and density

“…Previous studies on groups of 12 flies failed to show effects of vision or sound on group-level structure 35 . However, recent research indicates that both vision and the cVA receptor, Or65a, are required to regulate social group interactions in groups of 10 flies 36 and groups of 50 flies' social clustering is impacted by various sensory modalities, including olfaction, vision and touch 17 . Further studies on smaller group sizes are required to fully dissect how flies detect their social environment.…”

Indirect genetic effects for social network structure in Drosophila melanogaster

“…The social interactions that individuals engage in, and the emergent structure of the social groups they are a part of, can shape individuals' entire lives in important ways [1–3]. One of the many factors contributing to social interactions and emergent social group structure is the genotypes of individuals comprising a group [3–6]. From an evolutionary perspective, the quantitative genetics of social interactions are particularly interesting: when the genotype of one individual affects the phenotype of an interacting partner—a phenomenon termed indirect genetic effects (IGEs)—this genetic component of the social environment indicates that the social environment itself can respond to selective pressures and evolve [7–9].…”

“…To move beyond studying IGEs in dyadic contexts, social network analysis provides a promising opportunity, as it allows us to measure how the effects of social group members cascade through networks of direct and indirect interactions [4–6,17]. Social network analysis has emerged as a widely used tool for describing how individuals' direct and indirect social interactions are nested within the emergent social structure of their group [1,2,31–34], but has only rarely been deployed in genetically informative samples that would allow estimation of IGEs [4,5,17].…”

“…Numerous studies have found that behavioural variation shapes the positions that individuals hold in their networks of social interactions (e.g. movement and exploratory behaviour [35,36]; aggression and policing behaviours [19,37,38]; group size preference and experience [6,29,39]). However, it remains unclear whether these behavioural effects on network structure have an underlying quantitative genetic basis, and if so, how genetic variation acts through direct genetic effects (DGEs) and IGEs to produce variation in network structure [4–6,40].…”

“…movement and exploratory behaviour [35,36]; aggression and policing behaviours [19,37,38]; group size preference and experience [6,29,39]). However, it remains unclear whether these behavioural effects on network structure have an underlying quantitative genetic basis, and if so, how genetic variation acts through direct genetic effects (DGEs) and IGEs to produce variation in network structure [4–6,40]. Extending our knowledge of how the genetic effects of social group members affect the structure and dynamics of networks of social interactions—i.e.…”