Whole-limb scaling of muscle mass and force-generating capacity in amniotes

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Zoological Science
This might at first seem at odds with the finding that, for example, mammals exhibit positive allometry whereas reptiles do not show a significant departure from isometry. The apparent contradiction can be reconciled by noting that these comparisons are testing two different things in isolation of one another, whereas in reality there is a gradation across successively overlapping exponents and CIs—the statistical analogue of a ‘ring species’.

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Introduction

  1. The muscles collectively share a common volume, whereby changes in the size of one muscle may affect the size of adjacent muscles (Fig. 1A). For example, in order for the limb to avoid becoming too heavy (or having too high a rotational inertia), increase in the size of one muscle may necessitate a decrease in the size of another.

  2. Architectural specialization of muscles can limit their ability to effectively contribute to a diverse range of tasks (Wilson & Lichtwark, 2011), and hence specialization in one muscle may necessitate concomitant change in another so that limb functionality is not compromised. For example, a muscle with short fascicles will have a high PCSA but a reduced working range, which may require another muscle to compensate by having longer fascicles, but with reduced PCSA (Fig. 1B).

Materials & methods

Dataset

Published data

  1. All or almost all of the muscles of the limb had been measured and reported (save the manual and pedal muscles, as noted above), since the overarching aim of the present study is considering the whole limb. Studies in which a few small muscles (e.g., deep muscles such as the gemellus, quadratus femoris or popliteus) were not reported were still included, since the omission of such small muscles is expected to have minimal effect on the overall results. Studies that measured multiple muscles under a single name (e.g., multiple heads of the flexor carpi radialis as a single muscle) were also included, since this nevertheless accounts for all the muscle mass present. In contrast, studies that did not report one or more major muscles were excluded from consideration. All datasets ultimately selected for use in the present study included all major extensor and adductor (antigravity) muscles of the limb. The specific muscles included (and which, if any, were excluded) in a given source study are outlined in Table S1.

  2. Each of the architectural parameters listed in Eq. (1) were either explicitly reported, or their values able to be back-calculated from reported values, the latter either as PCSA (e.g., Cuff et al., 2016a, 2016b; back-calculated via Eq. (1)) or mass-scaled values (e.g., Dick & Clemente, 2017; Cieri, Dick & Clemente, 2020; back-calculated by unscaling according to reported body mass). A few previous studies had neglected to measure (or at least report) pennation angle, but to maximize consistency across the present dataset these studies were excluded. Studies that reported dry muscle mass only were also excluded.

  3. The data reported were for adult or large-sized individuals, to reduce potential confounding effects of ontogenetic variation (Table S1). In approximately two-fifths of species sampled, multiple similarly-sized individuals had been investigated, but the data reported by the relevant studies were only presented as a species mean, wherein a given architectural parameter for a given muscle had already been averaged across the individuals studied; in these cases, the mean body mass of that sample was used. For all other species, architectural and body mass data were reported for separate individuals. When data for multiple individuals of a given species had been reported separately (e.g., Lamas, Main & Hutchinson, 2014; Allen et al., 2015; Martin et al., 2019), those for the largest individual were used, to reduce possible ontogenetic effects. This approach was deemed more appropriate than computing a species average across all individuals, because in several instances the sample of individuals investigated by prior studies (especially those focused on ontogeny) exhibited high disparity in body sizes, undermining the value of a species mean; moreover, such an arithmetic mean would not account for ontogenetic allometry within the species, and hence could introduce further error into the analyses. Ultimately, each species contributed only a single datapoint to the analyses.

New data

Anatomical comparisons

#1—Total muscle mass (Σmmuscle) v. body mass (mbody)

#2—Mean size-normalized isometric strength v. mbody

#2b—Median Fmax* v. mbody

#2c—Total Fmax* v. mbody

#3—Characteristic fascicle length v. mbody

#4—ΣPCSA v. Σmmuscle

Statistical analyses

Results

Total muscle mass v. body mass

Mean size-normalized isometric strength ( Fmax*) v. body mass

Characteristic fascicle length (L*) v. body mass

Total PCSA v. total muscle mass

Pan-amniote regression

Discussion

Mass and force-generating capacity scaling across terrestrial amniotes

Fascicle packing

Considerations for future studies

Conclusion

Supplemental Information

Supplemental figures and tables, and description of the supplemental code.

DOI: 10.7717/peerj.12574/supp-1

The raw architectural data used in this study.

Raw hindlimb data, raw forelimb data, hindlimb data collated into the parameters investigated in the study, and forelimb data collated into the parameters investigated in the study.

DOI: 10.7717/peerj.12574/supp-2

Supplemental code and data.

This contains R computer code used to perform all analyses in the study, along with necessary input data files (muscle data in .csv format, phylogenetic tree in .nwk format). The code also allows for estimation of a particular variable via the pan-amniote regression given some user-supplied input (e.g., body mass estimate for an extinct species), along with 95% prediction intervals.

DOI: 10.7717/peerj.12574/supp-3

Additional Information and Declarations

Competing Interests

Stephanie E. Pierce is an Academic Editor for PeerJ.

Author Contributions

Peter J. Bishop conceived and designed the experiments, performed the experiments, analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the paper, and approved the final draft.

Mark A. Wright performed the experiments, analyzed the data, authored or reviewed drafts of the paper, and approved the final draft.

Stephanie E. Pierce conceived and designed the experiments, authored or reviewed drafts of the paper, and approved the final draft.

Data Availability

The following information was supplied regarding data availability:

All data and R code used in the present study and additional figures and tables providing a further break-down of results reported in the article are available in the Supplemental Files.

Funding

This work was supported by the William F. Milton Fund (Harvard University, to Stephanie E. Pierce) and United States National Science Foundation grants DEB-1754459 and EAR-2122115 (to Stephanie E. Pierce), and is published with the assistance of a grant from the Wetmore Colles Fund (Harvard University, to Mark A. Wright). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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