Neural Control of Coordinated Wing and Leg Movements During a Terrestrial Threat Display

Author: Cao, Shuo

Year: 2027

Degree: Dissertation (Ph.D.)

Advisor: Anderson, David J.

Committee Members: Hong, Elizabeth J.; Dickinson, Michael H.; Prober, David A.; Anderson, David J.

Option: Biology

DOI: 10.7907/ts9b-rx94

Abstract

Social displays are a widespread form of animal communication used to signal intent and are central to survival and reproduction. These displays are often multi-modal, engage multiple body parts, and follow characteristic, species-specific patterns. Although their behavioral diversity is well described in the ethological and evolutionary literatures, the neural circuits that generate and coordinate them remain largely uncharacterized. The Drosophila male wing threat display offers a tractable system for addressing this gap: it is an intrinsic aggressive behavior built from coordinated wing and leg actions, including wing elevation, wing pump, turning, and charging, that can occur in both flexible and coordinated combinations. Prior work in the Anderson lab identified AIP, a small cluster of interneurons that is both necessary and sufficient for this display and dispensable for other aggressive behaviors such as lunging and tussling, suggesting that AIP functions as a command-like node specifically for wing threat. This thesis uses AIP as an entry point to determine how various wing and leg actions are controlled and coordinated by the neural circuits in wing threat display. By mapping AIP neurons onto an electron-microscopy connectome of the Drosophila brain, I identified its major downstream targets. For four of these, I generated sparse, specific genetic drivers and characterized their individual and combined contributions to behavior. Contrary to the expectation that each downstream neuron type would drive a single, dedicated action, this work shows that AIP targets are organized into two appendage-specific modules — one for the wings, one for the legs — each governed by its own combinatorial logic. Wing movements are controlled by two descending neurons, DNpe050 and DNp60, which act synergistically: activating either alone produces only weak effects but simultaneous co-activation of both drives robust wing actions. Leg movements, in contrast, are governed by two interneurons with antagonistic effects on locomotion; their patterned co-activation produces the characteristic locomotion features of the wing threat, likely by recruiting and coordinating a broader population of downstream descending neurons. Together, these findings reveal a circuit-level logic by which different appendages are repurposed and coordinated to build specialized, structured actions during social display. This work provides a mechanistic framework for future studies of how animals select actions in real time during social interactions by integrating external sensory inputs and internal states.

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