Ecological cues orchestrate concerted courtship in a Drosophila host specialist
Mating decisions are often attributed to the sensory signaling between prospective sexual partners. Yet these interactions are also shaped by the broader environmental context in which they unfold, to appropriately align sexual arousal with reproductive opportunities. Here we show that in the host specialist Drosophila erecta mating is strictly contingent on the ecological and social environment generated as flies densely aggregate in groups on a food patch. We find that food volatiles directly promote male sexual arousal, triggering individuals to sample and pursue potential mates, giving rise to dynamic interactions across the group. The ensuing visual motion transforms each males visual field, which in turn further amplifies his arousal, generating a multisensory feedback loop that coordinately promotes courtship across individuals. D. erectas strict dependence on environmental cues appears latent in related species, such as D. melanogaster, where food odor can promote arousal but is dispensable for vigorous courtship. Comparative circuit analyses reveal that species-specific thresholds for sexual arousal reflect variation in how olfactory input modulates conserved nodes controlling courtship drive, rendering food volatiles a strict sensory gate only in D. erecta. Together, our findings highlight how ecological cues not directly tied to sexual signaling can profoundly influence reproductive behavior and reorganize the social landscape to ensure mating occurs in contexts where reproductive opportunities are abundant.