Divergent visual ecology of Drosophila species drives object-tracking strategies matched to landscape sparsity

Maintaining stable gaze while tracking moving objects is commonplace across animal taxa, yet how diverse ecological needs impact these processes is poorly understood. During flight, the fruit-eating fly Drosophila melanogaster maintains course by making smooth steering adjustments to fixate the image of the distant visual background on the retina, while executing body saccades to investigate nearby objects such as food sources. Cactophilic Drosophila mojavensis live where there is no canopy; rather, the flora forming visual "background" and "objects" are one and the same. We tested whether D. mojavensis have adapted their flight control strategies for a visually sparse landscape. We used a magnetic tether that allows free movement in the yaw axis. In response to a textured bar moving across a similarly textured stationary background, D. melanogaster fixates the background, thereby stabilizing gaze while integrating bar dynamics to trigger tracking saccades. By contrast, two mojavensis subspecies in the repleta subgroup and one species in the melanogaster subgroup steer to smoothly fixate the bar, seemingly ignoring the stationary surround. Desert flies execute frequent bar-tracking saccades, but theirs are triggered when rotational velocity lags the bar. Thus, D. melanogaster, which lives in visually cluttered cosmopolitan habitats, leverages the optical disparities between nearby objects and distant foliage for a hybrid control strategy: "ground-fixate, object-saccade." Flies in distant phylogenetic subgroups with similar visual ecology use a "fixate-and-saccade" strategy, which would be adaptive in a visually sparse environment where individual landscape features are both approached and used to maintain a straight course.