Adult male red-capped manakin, which produces wing claps by rapidly retracting its wings toward its body. Credit: Matthew Fuxjager

Studies in a group of tropical birds have revealed one of the fastest limb muscles on record for any animal with a backbone. The muscle, which can move the wing at more than twice the speeds required for flying, has evolved in association with extravagant courtship displays that involve rapid limb movements, according to a paper to be published in the journal eLife.

The 'superfast' wing movements of male red-capped and golden-crowned manakins are undetectable to the human eye, and are about six to eight times faster than the 8-hertz (Hz) speed at which a sprinter, such as Olympian athlete Usain Bolt, moves their legs through the air in a 100-metre run.

"The discovery of the superfast wing muscle in these birds paves the way for further studies into what has to change, or what can change, in a muscle to make it drive faster movements," says first author Matthew Fuxjager, from Wake Forest University.

"This could be important for developing therapies for motor disorders, particularly those characterized by decreases in muscle performance that result from diseases such as cancer and HIV."

Many different species perform rapid limb movements as part of their courtship displays, from certain birds running across lake surfaces, to the unusual boxing displays of hares in March.

However, because muscle performance is limited by trade-offs between speed and force, it is unclear how animals develop the ability to generate both the swift movements involved in showy physical displays and the force needed to drive these movements.

High-speed video of a golden-collared manakin performing a roll-snap. Credit: Barney Schlinger. As published in: Fuxjager, M.J., Longpre, K.M., Chew, J.G, Fusani, L. and Schlinger, B.A. (2013). Peripheral androgen receptors sustain the acrobatics and fine motor skill of elaborate male courtship. Endocrinology, 154: 3168-3177.)

To address this question, Fuxjager and his team compared the twitch speeds of forelimb muscles from wild-caught golden-collared and red-capped manakins to those of three other related species: the blue-crowned manakin, the dusky antbird, and the house wren.

"Of the species studied, the golden-collared and red-capped manakins produce exceptionally rapid wing movements as part of their acrobatic courtship displays," Fuxjager explains.

"For example, the golden-collared manakins perform 'roll-snaps', whereby they hit their wings together above the back at around 60 Hz to produce a loud mechanical sound. Likewise, red-capped manakins produce a similar wing sonation called a 'clap', in which the wings are extended slightly above the body and immediately retracted back to the sides in quick succession, at around 45 Hz."

To explain these birds' abilities to move their limbs rapidly during courtship performances, the researchers investigated the differences in muscle contraction speeds by comparing the half-relaxation frequency among the five different species. This represents the frequency at which each wing muscle is stimulated to contract, while still being able to relax to half their length following stimulation, thereby showing an accurate measure of how quickly they can contract.

For two of the three wing muscles, the half-relaxation frequencies averaged around 50 Hz and were indistinguishable among species. By contrast, the frequency measures in the main muscle that retracts the humerus were significantly higher in both the golden-collared and red-capped manakins. Estimates of their half-relaxation frequencies in this muscle were exceptionally high, and the frequencies between the two birds were indistinguishable.

These results show that only the golden-collared and red-capped manakins have evolved superfast contractile movements in their main humeral retractor muscle. The other two muscles that generate the majority of aerodynamic force for flight are no different from those of other birds, suggesting that they have been preserved to produce the strength needed for flying.

The team also found that the humeral retractor muscle in golden-collared and red-capped manakins is more than capable of driving the natural wing oscillations that make up their impressive displays.

Taken together, the results suggest that muscle-specific adaptations in contractile speed allow certain birds to avoid the trade-off between muscular speed and force, thereby using their forelimbs for both rapid gestural displays and powered locomotion.

"Further studies could now explore how this one muscle can create such superfast wing movements and whether male hormones, such as testosterone, play a role in regulating the muscle's speed," Fuxjager adds.

"If we discover whether steroids regulate the muscle's ability to contract at superfast speed, we would be uncovering how hormones can 'turn on' or 'turn off' its extraordinary ability. This would open the door to understanding how rapid limb movements are regulated in accordance with the animals' reproductive environment."

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More information: Matthew J Fuxjager et al. Select forelimb muscles have evolved superfast contractile speed to support acrobatic social displays, eLife (2016). Journal information: eLife Matthew J Fuxjager et al. Select forelimb muscles have evolved superfast contractile speed to support acrobatic social displays,(2016). DOI: 10.7554/eLife.13544

Provided by eLife