Wind Gates Search States in Free Flight.

For any organism tracking a chemical cue to its source, the motion of its surrounding fluid provides crucial information for success. For both swimming and flying animals engaged in olfaction driven search, turning into the direction of oncoming wind or water current is often a critical first step 1, 2 . However, in nature, wind and water currents may not always provide a reliable directional cue 3, 4, 5 . It is unclear how organisms adjust their search strategies accordingly due to the challenges of separately controlling flow and chemical encounters. Here, we use the genetic toolkit of Drosophila melanogaster , a model organism for olfaction 6 , to develop an optogenetic paradigm to deliver temporally precise "virtual" olfactory experiences in free-flying animals while independently manipulating the wind conditions. We show that in free flight, Drosophila melanogaster adopt distinct search routines that are gated by whether they are flying in laminar wind or in still air. We first confirm that in laminar wind flies turn upwind, and further, we show that they achieve this using a rapid turn. In still air, flies adopt remarkably stereotyped "sink and circle" search state characterized by ∼60°turns at 3-4 Hz, biased in a consistent direction. 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 7, 8 . 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.

Sensory neuron population expansion enhances odor tracking without sensitizing projection neurons.

The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous neural pathways of Drosophila melanogaster and its close relative Drosophila sechellia , an extreme specialist for Morinda citrifolia noni fruit. D. sechellia has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN population increases contribute to stronger, more persistent, noni-odor tracking behavior. These sensory neuron expansions result in increased synaptic connections with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odor-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron expansions to explain ecologically-relevant, species-specific behavior.