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Comparison of Hindlimb Muscle Architecture Properties in Small-Bodied, Generalist Mammals Suggests Similarity in Soft Tissue Anatomy

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Abstract

For the first 100+ million years of their evolutionary history, the majority of mammals were very small, and many exhibited relatively generalized locomotor ecologies. Among extant mammals, small-bodied, generalist species share similar hindlimb bone morphology and locomotor mechanics, but details of their musculature have not been investigated. To examine whether hindlimb muscle architecture properties are also similar, we dissected hindlimb muscles of the gray short-tailed opossum (Monodelphis domestica) and aggregated muscle properties from the literature for three other small-bodied mammals (Mus musculus, Rattus norvegicus, Cavia porcellus). We then studied hindlimb musculature from a whole-limb perspective and by separating the limb into nine anatomical regions. The region analysis explained substantially more variance in the data (r2: 0.601 > 0.074) but only detected six statistically significant pairwise species differences in muscle architecture properties. This finding suggests either deep conservation of therian hindlimb muscle properties or, more likely, a biomechanical constraint imposed by small body size. In addition, we find specialization for either large force production (i.e., PCSA) or longer active working ranges (i.e. long muscle fascicles) in proximal limb regions but neither specialization in more distal limb regions. This functional pattern may be key for small mammals to traverse across uneven and shifting substrates, regardless of environment. These findings are particularly relevant for researchers seeking to reconstruct and model soft tissue properties of extinct mammals during the early evolutionary history of the clade.

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All data generated or analyzed for this study are included in this published article and its supplementary information files.

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Acknowledgements

The study was conceived and designed by S.E.P. and M.A.W.; and K.E.S. sourced and provided the opossum cadavers upon which measurements were made. M.A.W. performed the muscle dissections, 3D muscle segmentation, and statistical analyses. The manuscript was prepared by M.A.W. and S.E.P., and all authors contributed to editing the manuscript. We thank the Pierce Lab for valuable discussion and feedback throughout the project (especially Katrina Jones, Blake Dickson, and Peter Bishop).

Funding

Funding for this project was partially provided by Harvard University and the National Science Foundation grants EAR-1524523 and DEB-1754459 to S.E.P., and the National Institutes of Health grant R21OD022988-03 to K.E.S.

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Correspondence to Mark A. Wright or Stephanie E. Pierce.

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KES is a member of the Editorial Board of the JME but was not involved in the evaluation of this manuscript.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 59 KB) All data analyzed in this study are provided in Online Resource 1.

10914_2022_9608_MOESM2_ESM.pdf

Supplementary file2 (PDF 275 KB) A detailed description outlining our muscle homologies and justification for comparison as well as summary tables detailing the statistical results for each analysis are provided in Online Resource 2.

10914_2022_9608_MOESM3_ESM.pdf

Supplementary file3 (PDF 84 KB) The R script used for all analyses in this study is provided directly in Online Resource 3.

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Wright, M.A., Sears, K.E. & Pierce, S.E. Comparison of Hindlimb Muscle Architecture Properties in Small-Bodied, Generalist Mammals Suggests Similarity in Soft Tissue Anatomy. J Mammal Evol 29, 477–491 (2022). https://doi.org/10.1007/s10914-022-09608-6

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  • DOI: https://doi.org/10.1007/s10914-022-09608-6

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