Wind history shapes olfactory search response in free-flying Drosophila melanogaster

The ability of flying insects to locate distant food and mates by tracking odor plumes through turbulent and unsteady flow represents a remarkable feat of sensorimotor integration. Successful navigation requires not only extracting a reliable directional estimate from an intermittent olfactory signal, but also contending with the challenging dynamics of variable winds. Whereas prior work has established that insects integrate the history of odor encounters to shape search decisions, whether they also retain a history of recently experienced wind conditions has remained unknown. Here, we used optogenetics combined with controlled wind perturbations in a free-flight wind tunnel to investigate how wind history modulates the olfactory search behavior of Drosophila melanogaster. By introducing lateral 'gust' flow via auxiliary fans and independently delivering olfactory stimuli, we show that the wind experienced during an olfactory stimulus shapes both the immediate surge response and the subsequent spatial search. Flies that received an olfactory stimulus while being displaced by a crosswind gust were significantly more likely to return to the gust zone during the post-stimulus search phase compared with flies that received the same odor cue in steady laminar flow. Meanwhile, surge responses and course directions exhibited during search indicate that moment-to-moment flight kinematics may be driven more by instantaneous flow. These results reveal that wind experience is tracked in addition to olfactory experience, and provide evidence that D. melanogaster maintain a short-term history of ambient wind conditions to guide olfactory navigation.