The evolutionary trajectory of drosophilid walking

Abstract

Neural circuits must both execute the behavioral repertoire of individuals and account for behavioral variation across species. Understanding how this variation emerges over evolutionary time requires large-scale phylogenetic comparisons of behavioral repertoires. Here, we describe the evolution of walking in fruit flies by capturing high-resolution, unconstrained movement from 13 species and 15 strains of drosophilids. We find that walking can be captured in a universal behavior space, the structure of which is evolutionarily conserved. However, the occurrence of, and transitions between, specific movements have evolved rapidly, resulting in repeated convergent evolution in the temporal structure of locomotion. Moreover, a meta-analysis demonstrates that many behaviors evolve more rapidly than other traits. Thus, the architecture and physiology of locomotor circuits can both execute precise individual movements in one species and simultaneously support rapid evolutionary changes in the temporal ordering of these modular elements across clades.

Long-timescale anti-directional rotation in Drosophila optomotor behavior

“…Individual strains of D. melanogaster , and other drosophilid species, display significant variation in their locomotor patterns during walking ( York et al, 2022 ). Indeed, when we tested a Canton-S D. melanogaster strain, we observed milder but significant anti-directional turning at long timescales ( Figure 1—figure supplement 2b ).…”

Long timescale anti-directional rotation inDrosophilaoptomotor behavior

“…Individual strains of D. melanogaster , and other drosophilid species, display significant variation in their locomotor patterns during walking (York et al, 2022). Indeed, when we tested a Canton-S D. melanogaster strain, we observed mild but significant anti-directional turning at long timescales ( Supp.…”

Visual and motor signatures of locomotion dynamically shape a population code for feature detection in Drosophila

“…To do this, we examined walking trajectories from our open behavioral arena (See Fig. 6 and York et al, 2022) (Fig. S4A).…”

“…To simulate the visual input that would be generated from Drosophila walking through such an environment, we moved the camera through the scene according to measured fly walking trajectories. Trajectories of female flies walking in the dark were measured in a 1 square meter arena with automatic locomotion tracking, as described previously (York et al, 2022). 20 second snippets from measured trajectories were selected to include periods of locomotor movement, and to exclude long stationary periods.…”

“…6A). To move this scene, we measured fly walking trajectories using a 1m 2 arena with automated tracking, as described previously (York et al, 2022), and applied short segments of these walking trajectories to the camera location and heading in our visual environment, creating an open loop "play-back" stimulus (Fig. 6B).…”