Chemosensation drives divergent social behavior in Drosophila

Abstract

Social interactions play a key role in animal survival and reproduction, shaping mating success, cooperation, competition, and the transmission of information and disease. Across species, the social environment not only influences behavior but also feeds back on physiology, stress responses, and evolutionary trajectories. Despite this central importance, the molecular signals that control how animals sense and respond to one another remain incompletely understood. Drosophila melanogaster provides a powerful model to probe these mechanisms, as it combines a rich repertoire of social behaviors with unparalleled genetic tools, highly accessible neural circuits, and evolutionary conservation of key molecular pathways underlying sensory processing. Using this system, we investigated behavioral responses to housing status. While group housing elicits interactions such as chasing and touching, Dahomey males uniquely exhibit a collective increase in social behaviors that is absent in other commonly studied lines and in females. Testing mixed-strain populations revealed that strain-specific differences in sensing other flies underlie the divergent group behaviors. Olfactory signaling through Or43a is necessary but not sufficient for Dahomey social sensitivity. Furthermore, specific single nucleotide polymorphisms (SNPs) in Or43a are associated with the social phenotype. These results demonstrate that social sensitivity is a sexually dimorphic, olfaction-dependent group behavior. Our studies reveal insights on the mechanisms that drive behavioral responses to social enrichment, and demonstrate how divergent strategies for regulating social behavior may evolve within a species. (Figure presented.)