Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids.

Philip Fahn-Lai,Andrew A Biewener,Stephanie E Pierce

doi:10.7717/peerj.8556

Abstract

The evolution of upright limb posture in mammals may have enabled modifications of the forelimb for diverse locomotor ecologies. A rich fossil record of non-mammalian synapsids holds the key to unraveling the transition from “sprawling” to “erect” limb function in the precursors to mammals, but a detailed understanding of muscle functional anatomy is a necessary prerequisite to reconstructing postural evolution in fossils. Here we characterize the gross morphology and internal architecture of muscles crossing the shoulder joint in two morphologically-conservative extant amniotes that form a phylogenetic and morpho-functional bracket for non-mammalian synapsids: the Argentine black and white tegu Salvator merianae and the Virginia opossum Didelphis virginiana. By combining traditional physical dissection of cadavers with nondestructive three-dimensional digital dissection, we find striking similarities in muscle organization and architectural parameters. Despite the wide phylogenetic gap between our study species, distal muscle attachments are notably similar, while differences in proximal muscle attachments are driven by modifications to the skeletal anatomy of the pectoral girdle that are well-documented in transitional synapsid fossils. Further, correlates for force production, physiological cross-sectional area (PCSA), muscle gearing (pennation), and working range (fascicle length) are statistically indistinguishable for an unexpected number of muscles. Functional tradeoffs between force production and working range reveal muscle specializations that may facilitate increased girdle mobility, weight support, and active stabilization of the shoulder in the opossum—a possible signal of postural transformation. Together, these results create a foundation for reconstructing the musculoskeletal anatomy of the non-mammalian synapsid pectoral girdle with greater confidence, as we demonstrate by inferring shoulder muscle PCSAs in the fossil non-mammalian cynodont Massetognathus pascuali.

Highlights

The differences separating therian locomotion from that of other extant quadrupeds are usually understood as a contrast between derived “erect” or “parasagittal” versus plesiomorphic “sprawling” limb posture (Bakker, 1971)
Quantifying and comparing muscle architecture between representatives of these extant amniote groups should furnish a baseline picture of architectural variation across two contrasting morphological and functional paradigms, and help bookend reconstructions of architecture in analogous or intermediate non-mammalian synapsids. 105 In this study, we present an in-depth qualitative and quantitative comparison of shoulder musculature in two amniotes that comprise an extant phylogenetic bracket as well as morpho-functional analogues for extinct non-mammalian synapsids: the Argentine black and white tegu Salvator merianae and the Virginia opossum Didelphis virginiana
By combining non-destructive diffusible iodine-based contrast-enhanced computed 111 tomography(Gignac et al, 2016) with traditional physical dissection in an experimentally112 controlled context, we provide a comprehensive picture of shoulder musculoskeletal anatomy in two 113 morphologically-conservative, comparably-sized amniotes

Summary

Introduction

The differences separating therian locomotion from that of other extant quadrupeds are usually understood as a contrast between derived “erect” or “parasagittal” versus plesiomorphic “sprawling” limb posture (Bakker, 1971). Mammal-like posture is associated with adducted limbs, joints aligned in a single plane, dorsoventral bending of the axial skeleton, and the ability to use asymmetrical gaits On the other hand, sprawling posture features abducted limbs, multiaxial joints, mediolateral axial bending, and mostly symmetrical gaits While kinematic studies of “erect” mammals (Jenkins, 1971b) and “sprawling” non mammals (Nyakatura et al, 2019) have shown enough variation within each locomotor archetype to cast doubt on the usefulness of a rigid postural framework (Gatesy, 1991), it remains the case that mammalian limb use is uniquely diverse among amniotes. The forelimbs, in particular, have been transformed almost beyond recognition in many cases, becoming wings and flippers, or elongated with reduced digits and hooves, and finding use in various non-locomotor behaviors such as prehension, excavation, 54 grooming, and manipulation (Polly, 2007; Vaughan, Ryan & Czaplewski, 2013)

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