Chemosensation drives divergent social behavior in Drosophila

The social environment can have a considerable impact on animal behavior. However, the molecular signals that drive socially sensitive behaviors are not completely defined. Using the model organism, Drosophila melanogaster, we investigated behavioral responses to housing status. Group housing of male flies induces robust social interactions--composed of chasing and touching--in the Dahomey strain, but not in other commonly used parental lines. Testing mixed-strain groups revealed that strain-specific variation in chemosensation, rather than in the generation of chemosignals, likely underlies the divergent group behaviors. Using locomotor activity as a higher throughput readout for increased social interactions, we found that manipulations that decrease or ablate olfaction--through surgical removal of olfactory organs, silencing of olfactory neurons, or mutations in odorant receptor co-receptor (Orco)--decrease Dahomey social sensitivity. Females of all tested strains, including Dahomey, show no evidence of increased group activity. These results demonstrate that Dahomey social sensitivity is a sexually dimorphic, olfaction-dependent group behavior. The OR43a receptor, as well as signaling through Or43a+ neurons, contributes to Dahomey group hyperactivity. Additional studies also suggest that strain-specific single nucleotide polymorphisms (SNPs) in the Or43a gene are associated with Dahomey social sensitivity. Our studies reveal insights on the mechanisms that regulate sensory recognition and behavioral responses to the social environment, and how divergent strategies may have evolved within the same species.