WalkingDrosophilanavigate complex plumes using stochastic decisions biased by the timing of odor encounters

Abstract

Insects find food, mates, and egg-laying sites by tracking odor plumes swept by complex wind patterns. Previous studies have shown that moths and flies localize plumes by surging upwind at odor onset and turning cross-or downwind at odor offset. Less clear is how, once within the expanding cone of the odor plume, insects use their brief encounters with individual odor packets, whose location and timing are random, to progress towards the source. Experiments and theory have suggested that the timing of odor encounters might assist navigation, but connecting behaviors to individual encounters has been challenging. Here, we imaged complex odor plumes simultaneous with freely-walking flies, allowing us to quantify how behavior is shaped by individual odor encounters. Combining measurements, dynamical models, and statistical inference, we found that within the plume cone, individual encounters did not trigger reflexive surging, casting, or counterturning. Instead, flies turned stochastically with stereotyped saccades, whose direction was biased upwind by the timing of prior odor encounters, while the magnitude and rate of saccades remained constant. Odor encounters did not strongly affect walking speed. Instead, flies used encounter timing to modulate the rate of transitions between walks and stops. When stopped, flies initiated walks using information from multiple odor encounters, suggesting that integrating evidence without losing position was part of the strategy. These results indicate that once within the complex odor plume, where odor location and timing are unpredictable, animals navigate with biased random walks shaped by the entire sequence of encounters.

Inter-species comparison of the orientation algorithm directing larval chemotaxis in the genus Drosophila

“…In absence of turn bias toward the gradient, chemotaxis is generally impaired (see for instance Figure 9B-D). Interestingly, the ability of larvae and adult flies to turn toward the odor gradient emerges as essential to achieve strong chemotaxis in computational simulations (Davies, Louis et al 2015, Demir, Kadakia et al 2020. By contrast, the case study of Figure 7 illustrates that the ability to modulate the run speed (Figure 1Bi) and the turn rate (when-to-turn, Figure 1Bii) as function of the bearing is not necessary to ensure strong chemotaxis.…”

“…On the other hand, E-2-hexenal induces an increase in the overall run speed that is not observed for ethyl acetate (Figure 7B). The where-to-turn-to and weathervaning routines are common to the response elicited by both odors, underscoring the importance of biasing turns toward the gradient for flies to perform strong chemotaxis (Demir, Kadakia et al 2020).…”

Odor motion sensing enables complex plume navigation

“…The fly walking assay is identical to the one used in a previous study (Demir et al, 2020). All experiments were done in a behavioral room held at 21-23 o C and 50% humidity.…”

“…We re-analyzed behavioral data previously extracted from Drosophila navigating an imaged complex plume of smoke (Demir et al, 2020) in the same walking assay used throughout this study. The signal in the virtual antenna was quantified as described previously; briefly, the virtual antenna is defined as an ellipse perpendicular to the body axis with the long axis given by the size of the fly (1.72 ± 0.24 mm) and the small axis equal to one-fifth the minor axis of the fly (0.46 ± 0.24 mm).…”

Tempo is the key

“…Now, in eLife, Thierry Emonet and co-workers from Yale University – including Mahmut Demir and Nirag Kadakia as first authors – report how the fruit fly Drosophila melanogaster behaves in response to an attractive smell while walking ( Demir et al, 2020 ). Quite serendipitously, they discovered that starved flies are attracted to smoke, which can be easily visualized.…”