Pectoral girdle and forelimb musculoskeletal function in the echidna (Tachyglossus aculeatus): insights into mammalian locomotor evolution

Abstract

Although evolutionary transformation of the pectoral girdle and forelimb appears to have had a profound impact on mammalian locomotor and ecological diversity, both the sequence of anatomical changes and the functional implications remain unclear. Monotremes can provide insight into an important stage of this evolutionary transformation, due to their phylogenetic position as the sister-group to therian mammals and their mosaic of plesiomorphic and derived features. Here we build a musculoskeletal computer model of the echidna pectoral girdle and forelimb to estimate joint ranges of motion (ROM) and muscle moment arms (MMA)—two fundamental descriptors of biomechanical function. We find that the echidna's skeletal morphology restricts scapulocoracoid mobility and glenohumeral flexion–extension compared with therians. Estimated shoulder ROMs and MMAs for muscles crossing the shoulder indicate that morphology of the echidna pectoral girdle and forelimb is optimized for humeral adduction and internal rotation, consistent with limited in vivo data. Further, more muscles act to produce humeral long-axis rotation in the echidna compared to therians, as a consequence of differences in muscle geometry. Our musculoskeletal model allows correlation of anatomy and function, and can guide hypotheses regarding function in extinct taxa and the morphological and locomotor transformation leading to therian mammals.

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

“…Finally, the morphologically-specialized (Jenkins, 1971a) extant monotremes invite comparison as similarly-sized phylogenetic intermediates between tegus and opossums. While a musculoskeletal model for the short-beaked echidna Tachyglossus aculeatus already exists (Regnault & Pierce, 2018), our ability to interpret this animal's joint mobility and muscle moment arms will improve once its muscle architecture is described as well.…”

“…Hence, two equal-sized muscles with identical attachments but differing architectural properties might have very different functional characteristics, complicating the interpretation of muscles reconstructed on the basis of skeletal anatomy alone (Bates & Schachner, 2012;Bates & Falkingham, 2018). Finding a way to reconstruct muscle architecture would greatly strengthen reconstructions of posture and locomotion in fossil synapsids, as it would provide a means to estimate input parameters for computational musculoskeletal models and test competing postural/locomotor hypotheses (Hutchinson, 2004;Nagano et al, 2005;Charles et al, 2016;Regnault & Pierce, 2018;Bates & Falkingham, 2018).…”

Decoupling Functional and Morphological Convergence, the Study Case of Fossorial Mammalia

“…For talpids, chrysochlorids and proscalopids we replicated the modeling approach presented in Piras et al (2015) simulating the action of the main muscles involved in digging for each functional group. For notoryctids and tachyglossids, we utilized detailed anatomical descriptions of both myology and osteology in order to identify the main muscle groups involved in the digging kinematics (Jenkins, 1970;Warburton, 2003Warburton, , 2006Archer et al, 2010;Beck et al, 2016;Regnault and Pierce, 2018). Due to the comparative nature of this study, we applied the same resultant force to all the models.…”

“…For notoryctids we selected the areas corresponding to insertion of m. triceps, m. pectoralis and areas of the medial epicondyle corresponding to the attachment of muscles aimed at wrist and digit flexion (Warburton, 2006;Beck et al, 2016). For tachyglossids we selected the areas where m. latissimus dorsi and m. teres major insert (Regnault and Pierce, 2018). Orientation of muscles has been based on anatomical descriptions available (Jenkins, 1970;Puttick andJarvis, 1977, Gasc et al, 1986;Gambaryan et al, 2002;Warburton, 2006; see Figures 1C,D).…”

Peer Review #3 of "Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids (v0.1)"

“…Hence, two equal-sized muscles with identical attachments but differing architectural properties might have very different functional characteristics, complicating the interpretation of muscles reconstructed on the basis of skeletal anatomy alone (Bates & Schachner, 2012;Bates & Falkingham, 2018). Finding a way to reconstruct muscle architecture would greatly strengthen reconstructions of posture and locomotion in fossil synapsids, as it would provide a means to estimate input parameters for computational musculoskeletal models and test competing postural/locomotor hypotheses (Hutchinson, 2004;Nagano et al, 2005;Charles et al, 2016;Regnault & Pierce, 2018;Bates & Falkingham, 2018). Unlike attachments, muscle architecture cannot be rigorously inferred using the extant phylogenetic bracket, since internal fiber organization has no known skeletal correlates.…”