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

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.How to cite this article Fahn-Lai P, Biewener AA, Pierce SE. 2020. Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids. PeerJ 8:e8556

How to build a dinosaur: Musculoskeletal modeling and simulation of locomotor biomechanics in extinct animals

“…Thus, we argue that the best data-driven method to muscle architecture estimation is a “total evidence” one. To this end, further research on extant species (archosaur and non-archosaur) will help refine general principles relating muscular anatomy to function, such as how muscle attachment size and morphology correlate to architecture (Martin et al 2019; Fahn-Lai et al 2020) or how long muscle fibers need to be to be able to effectively execute movement over a range of postures (Sellers et al 2013).…”

“…It was noted earlier how both m musc and ℓ o are crucial for better modeling muscle function, and therefore the more accurate determination of their values in extinct taxa represents a key challenge for future work. For instance, the study of how m musc relates to actual attachment area, type of osteological correlate, and muscle identity may reveal relationships that can be used to produce more anatomically grounded estimates in extinct taxa (Martin et al 2019; Fahn-Lai et al 2020). Similarly, the accurate estimation of ℓ o poses another key challenge.…”

Evolutionary biomechanics: hard tissues and soft evidence?

“…Changes in functional morphology have underpinned some of the most significant evolutionary transitions in the history of life. Colonization of the land by the earliest tetrapods [1], mammalian origins and diversification [2][3][4][5], the evolution of locomotion in dinosaurs and birds [6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23], and functional and ecological shifts in human ancestors [24][25][26][27][28][29][30][31] represent extensively studied examples. The last two decades has seen widespread adoption of sophisticated mathematical-computational approaches to study functional morphology in extinct animals and the biomechanics of evolutionary transitions documented in the fossil record.…”

Musculoskeletal modelling of sprawling and parasagittal forelimbs provides insight into synapsid postural transition

“…the mm. latissimus dorsi and pectoralis, origin and insertion points were placed manually based on 3D muscle geometry [13,16].…”

“…proximally on the humerus, and the humerus itself is much more gracile [13,26]; this brings the muscle insertion sites closer to the axes of rotation, reducing MMAs but increasing the arc of the limb.…”