The evolutionary trajectory of drosophilid walking

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 execute precise individual movements in one species and simultaneously support rapid evolutionary changes in the temporal ordering of these modular elements across clades. •Unconstrained locomotor behavior measured in more than one thousand individual flies•Drosophilid walking can be captured by a universal low-dimensional behavior space•Hierarchical evolution and varying dynamics among behavioral components•Behaviors evolve more rapidly than other traits within Drosophila York et al. study the evolutionary dynamics of the Drosophila walking repertoire over 40 million years. They find that the kinematic structure of walking is deeply conserved, although the occurrence and sequencing of specific movement patterns have evolved rapidly. This study opens new pathways for the macroevolutionary study of behavioral traits.