Neuromuscular mechanisms of an elaborate wing display in the golden-collared manakin (Manacus vitellinus)

Abstract

Many species perform elaborate physical displays to court mates and compete with rivals, but the biomechanical mechanisms underlying such behavior are poorly understood. We address this issue by studying the neuromuscular origins of display behavior in a small tropical passerine bird, the golden-collared manakin (). Males of this species court females by dancing around the forest floor and rapidly snapping their wings together above their back. Using radio-telemetry, we collected electromyographic (EMG) recordings from the three main muscles that control avian forelimb movement, and found how these different muscles are activated to generate various aspects of display behavior. The muscle that raises the wing (supracoracoideus, SC) and the primary muscle that retracts the wing (scapulohumeralis caudalis, SH) were activated during the wing-snap, whereas the pectoralis (PEC), the main wing depressor, was not. SC activation began before wing elevation commenced, with further activation occurring gradually. By contrast, SH activation was swift, starting soon after wing elevation and peaking shortly after the snap. The intensity of this SH activation was comparable to that which occurs during flapping, whereas the SC activation was much lower. Thus, light activation of the SC likely helps position the wings above the back, so that quick, robust SH activation can drive these appendages together to generate the firecracker-like snap sonation. This is one of the first looks at the neuromuscular mechanisms that underlie the actuation of a dynamic courtship display, and it demonstrates that even complex, whole-body display movements can be studied with transmitter-aided EMG techniques.

Physiological constraint on acrobatic courtship behavior underlies rapid sympatric speciation in bearded manakins

“…For the roll-snap, skeletal muscle performance may be one of the limiting factors, considering that muscle tissue itself is thought to be the origin of the speed-endurance trade-off ( Vanhooydonck et al, 2014 ; Wilson et al, 2002 ; Bottinelli et al, 1994 ). In bearded manakins, the scapulohumeralis caudalis muscle (SH, Figure 4a ) is the primary actuator of the roll-snap—it contracts when a male’s wings are raised vertically above its back, causing the wrists to collide (snap) over the axial mid-line ( Fuxjager et al, 2017a ). Otherwise, the SH is a flight muscle, acting as a ‘strut’ during powered locomotion by rotating and retracting the wing ( Dial, 1992 ).…”

“…Skeletal muscle performance is a prime example of this phenomenon: its design entails performance traits that are inversely related to each other, such as between speed and endurance ( Vanhooydonck et al, 2014 ; Wilson et al, 2002 ). At the same time, skeletal muscle also actuates many sexually-selected behaviors that act as the basis for mate choice ( Goller and Suthers, 1996 ; Garcia et al, 2012 ; Fuxjager et al, 2017a ). This suggests that performance trade-offs inherent to muscle itself can impede the formation of reproductive barriers, particularly in cases where behavioral divergence should mediate speciation.…”

“…We specifically examine how disruptive selection operates on one of the bird’s main courtship signals—the roll-snap—to generate phenotypic divergence sufficient to facilitate assortative mating ( Servedio, 2016 ). Males produce this behavior by rapidly hitting their wings together over their back, generating a mechanical trill-like sound ( Fuxjager et al, 2017a ). The result is a repetitive rhythmic signal, which is a common signal type in animal courtship ( Mowles and Ord, 2012 ).…”

Proposing a neural framework for the evolution of elaborate courtship displays

“…In this same vein, researchers should begin to investigate the role of the PAG in other species’ display maneuvers that rely on complex body movement. This is a challenging task, but advances in the ability to manipulate and monitor neural circuits is making it more possible to do so ( Fuxjager et al, 2017 ; Spool et al, 2021 ). In the spirit of this goal, there are also several core approaches to studying the PAG and display that biologists can leverage; for example, comparisons of sex differences in PAG structure and function are possible and easy to do, especially when species show clear sex differences in courtship behavior.…”