Neural coordination of wing and leg movements during a terrestrial threat display

In most flying species, legs and wings mediate earthbound vs. aerial locomotion, respectively. During terrestrial social displays such as threat or courtship, however, species-typical movements of these appendages are coordinated in a stereotyped manner. How such appendicular control is integrated is poorly understood. Threat behavior in Drosophila consists of four types of leg and wing actions, which can be performed singly or in combination. Using a large-scale functional screen, we previously identified a cluster of 4–5 AIP (CL062) neurons whose optogenetic activation can evoke all threat actions and which are essential for natural threat displays. To understand how this threat command module functions, we have mapped AIP neurons into the male fly connectome and identified split-GAL4 drivers for four major downstream targets, whose functional connectivity and behavioral roles we have tested. Surprisingly, we find that distinct threat-specific actions are not controlled by parallel connections from different subsets of AIP cells to different action-specific descending neurons (DNs), a parsimonious circuit architecture. Rather, AIP neurons collectively activate two parallel downstream modules comprising pairs of neurons that control wing vs. leg movements, respectively. Wing movements are controlled via direct projections to two specialist DNs that act synergistically, while leg movements are controlled indirectly via two interneurons that act antagonistically to pattern the activity of multiple DNs, which are likely used in other locomotor contexts. These data elucidate a hierarchical circuit for appendicular coordination during a terrestrial social display and provide insight into how the brain has repurposed appendage-specific locomotor control for social communication, a form of exaptation.