Androgens Support Male Acrobatic Courtship Behavior by Enhancing Muscle Speed and Easing the Severity of Its Tradeoff With Force

Steroid hormone action in the brain regulates many animals' elaborate social displays used for courtship and competition, but it is increasingly recognized that the periphery may also be a site for potent steroidal modulation of complex behavior. However, the mechanisms of such bottom-up regulation of behavioral outflow are largely unclear. To study this problem, we examined how androgenic sex hormones act through the skeletal muscular system to mediate elaborate courtship acrobatics in a tropical bird called the golden-collared manakin. As part of their display, males snap their wings together above their backs at rates that are at least 2xfaster than the normal wing-beat frequency used for flight. This behavior, called the roll-snap, is actuated by repeatedly activating a humeral retractor muscle-the scapulohumeralis caudalis (SH)-which produces contraction-relaxation cycling speeds similar to the superfast muscles of other taxa. We report that endogenous androgenic activation of androgen receptor (AR) sustains this muscle's exceptionally rapid contractile kinetics, allowing the tissue to generate distinct wing movements at oscillation frequencies > 100 Hz. We also show that these effects are rooted in an AR-dependent increase to contractile velocity, which incurs no detectable cost to force generation. Thus, AR enhances SH speed necessary for courtship display performance while avoiding the expected tradeoff with strength that could otherwise negatively influence aspects of flight. Peripheral AR therefore not only sets up the muscular system to perform a complex wing display, but does so in a way that balances the functional requirements of this muscle for other life-sustaining behavior.