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Flying Drosophila melanogaster maintain arbitrary but stable headings relative to the angle of polarized light

ABSTRACT Animals must use external cues to maintain a straight course over long distances. In this study, we investigated how the fruit fly Drosophila melanogaster selects and maintains a flight heading relative to the axis of linearly polarized light, a visual cue produced by the atmospheric scattering of sunlight. To track flies' headings over extended periods, we used a flight simulator that coupled the angular velocity of dorsally presented polarized light to the stroke amplitude difference of the animals’ wings. In the simulator, most flies actively maintained a stable heading relative to the axis of polarized light for the duration of 15 min flights. We found that individuals selected arbitrary, unpredictable headings relative to the polarization axis, which demonstrates that D. melanogaster can perform proportional navigation using a polarized light pattern. When flies flew in two consecutive bouts separated by a 5 min gap, the two flight headings were correlated, suggesting individuals retain a memory of their chosen heading. We found that adding a polarized light pattern to a light intensity gradient enhanced flies' orientation ability, suggesting D. melanogaster use a combination of cues to navigate. For both polarized light and intensity cues, flies' capacity to maintain a stable heading gradually increased over several minutes from the onset of flight. Our findings are consistent with a model in which each individual initially orients haphazardly but then settles on a heading which is maintained via a self-reinforcing process. This may be a general dispersal strategy for animals with no target destination. Summary: Relative to celestial cues, fruit flies select unpredictable flight headings and maintain them with gradually increasing fidelity. This may be a general dispersal strategy for animals with no target destination.