Select forelimb muscles have evolved superfast contractile speed to support acrobatic social displays

Abstract

Many species perform rapid limb movements as part of their elaborate courtship displays. However, because muscle performance is constrained by trade-offs between contraction speed and force, it is unclear how animals evolve the ability to produce both unusually fast appendage movement and limb force needed for locomotion. To address this issue, we compare the twitch speeds of forelimb muscles in a group of volant passerine birds, which produce different courtship displays. Our results show that the two taxa that perform exceptionally fast wing displays have evolved 'superfast' contractile kinetics in their main humeral retractor muscle. By contrast, the two muscles that generate the majority of aerodynamic force for flight show unmodified contractile kinetics. Altogether, these results suggest that muscle-specific adaptations in contractile speed allow certain birds to circumvent the intrinsic trade-off between muscular speed and force, and thereby use their forelimbs for both rapid gestural displays and powered locomotion.

Keywords: behavioral evoltuion; birds; courtship and social displays; ecology; manakins; muscle twitch speed; neuroscience.

Figure 1.. Species and muscles examined in this study.

(A) Species included in our study, with common names in boldface typesetting and scientific names in italic typesetting. A brief description of each species’ display and reason for inclusion in the study is described. Photos with permission from Nick Athanas. (B) Illustration of the three main wing muscles in a golden-collared manakin that are involved in the production of the roll-snap. These include (i) the supracoracoideus (SC), which raises the wing by elevating the humerus; (ii) the pectoralis (PEC), which lowers the wing by depressing the humerus, and (iii) the scapulohumeralis caudalis (SH), which retracts the wing via the humerus (Biewener, 2011; Dial, 1992; Dial et al., 1991). Note that the SC is a darker shade of pink, compared to the PEC and SH, because the SC lies deep to the PEC. Scientific illustrations of these muscles can be found elsewhere (Welch and Altshuler, 2009; George and Berger, 1966). This schematic is modified with permission from Schlinger, et al. (Schlinger et al., 2013). DOI: http://dx.doi.org/10.7554/eLife.13544.003

Figure 2.. Experimental design.

(A) Schematic of the work flow and procedural design. Muscles were prepared in situ (see methods) and stimulated at frequencies ranging from 10 Hz to 100 Hz, increasing at increments of 10 Hz. Stimulation trains were spaced 1 min apart. After the 100 Hz stimulation train, we administered a second 20 Hz stimulation train (shown underlined and in boldface typesetting). Percent recoveries were compared between this 20 Hz stimulation train and the first 20 Hz stimulation train to validate that the procedure did not exhaust/damage muscle. (B) Representative twitch recordings from a red-capped manakin (10 Hz from the SC and 100 Hz from the SH; note the differences in time scale). For each individual, percent recovery at a given stimulation frequency was calculated by averaging the percent recoveries of the first eight stimulations within the administered train. This corresponds to reasonable numbers of wing oscillations that golden-collared and red-capped manakins incorporate into their respective roll-snap or clap displays. DOI: http://dx.doi.org/10.7554/eLife.13544.004

Figure 3.. Muscle twitch speed dynamics in the (A, D) pectoralis, (B, E) supracoracoideus, and (C, F) scapulohumeralis of the five avian species included in our study.

(A–C) Non-linear models generated to depict the relationship between mean muscle relaxations in response to different muscle stimulation frequencies. In each graph, muscle relaxation at a given stimulation frequency represents the mean (± 1 SEM) among individuals of a given species. (D–F) Half-relaxation frequencies of the different forelimb muscles across the five species in our analysis. Data represent mean (± 1 SEM) half-relaxation frequency for the given species. (F) For the SH, differences in the letters atop each bar denote statistically significant differences in mean half-relaxation values, according to post-hoc analyses (SNK tests, p<0.05). In all graphs, GCM = golden-collared manakin (orange); RCM = red-capped manakin (red); BCM = blue-crowned manakin (blue); DAB = dusky antbird (black); and HW = house wren (brown). DOI: http://dx.doi.org/10.7554/eLife.13544.006

Figure 4.. Schematic representation of the experimental set up used to record muscle twitch in situ.

Birds were deeply anesthetized with isoflurane; their muscles were exposed, attached to the force transducer, and implanted with silver electrode wires. Data were collected on a nearby laptop computer. Note that the elements in this figure are not drawn to scale. DOI: http://dx.doi.org/10.7554/eLife.13544.009