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

Abstract

Animals differ in their appearances and behaviors. While many genetic studies have addressed the origins of phenotypic differences between fly species, we are still lacking a quantitative assessment of the variability in the way different fly species behave. We tackled this question in one of the most robust behaviors displayed by Drosophila: chemotaxis. At the larval stage, Drosophila melanogaster navigate odor gradients by combining four sensorimotor routines in a multilayered algorithm: a modulation of the overall locomotor speed and turn rate; a bias in turning during down-gradient motion; a bias in turning toward the gradient; the local curl of trajectories toward the gradient ("weathervaning"). Using high-resolution tracking and behavioral quantification, we characterized the olfactory behavior of eight closely related species of the Drosophila group in response to 19 ecologically-relevant odors. Significant changes are observed in the receptive field of each species, which is consistent with the rapid evolution of the peripheral olfactory system. Our results reveal substantial inter-species variability in the algorithms directing larval chemotaxis. While the basic sensorimotor routines are shared, their parametric arrangements can vary dramatically across species. The present analysis sets the stage for deciphering the evolutionary relationships between the structure and function of neural circuits directing orientation behaviors in Drosophila.