Wind gates olfaction-driven search states in free flight

For organisms tracking a chemical cue to its source, the motion of their surrounding fluid provides crucial information for success. Swimming and flying animals engaged in olfaction-driven search often start by turning into the direction of an oncoming wind or water current. However, it is unclear how organisms adjust their strategies when directional cues are absent or unreliable, as is often the case in nature. Here, we use the genetic toolkit of Drosophila melanogaster to develop an optogenetic paradigm to deliver temporally precise "virtual" olfactory experiences for free-flying animals in either laminar wind or still air. We first confirm that in laminar wind flies turn upwind. Furthermore, we show that they achieve this using a rapid (∼100 ms) turn, implying that flies estimate the ambient wind direction prior to "surging" upwind. In still air, flies adopt a remarkably stereotyped "sink and circle" search state characterized by ∼60° turns at 3-4 Hz, biased in a consistent direction. Together, our results show that Drosophila melanogaster assesses the presence and direction of ambient wind prior to deploying a distinct search strategy. In both laminar wind and still air, immediately after odor onset, flies decelerate and often perform a rapid turn. Both maneuvers are consistent with predictions from recent control theoretic analyses for how insects may estimate properties of wind while in flight. We suggest that flies may use their deceleration and "anemometric" turn as active sensing maneuvers to rapidly gauge properties of their wind environment before initiating a proximal or upwind search routine.