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

Abstract

The sprawling-parasagittal postural shift was a major transition during synapsid evolution and is considered key to mammalian ecological diversity. Despite a good fossil record, debate remains over when the shift to parasagittal posture occurred, primarily due to limited comparative biomechanical data on extant species. Here, we built forelimb musculoskeletal models of three extant taxa that bracket the sprawling-parasagittal transition: a tegu lizard, an echidna, and an opossum. We measured shoulder joint range of motion (ROM) about all three degrees of rotational freedom and characterized shoulder muscle moment arms (MMAs) across the entire pose space. Our results show that both the opossum and the tegu had high shoulder joint ROM, and both were substantially higher than the echidna. However, the opossum occupied a distinct region of pose space characterized by high humeral retraction angles. There are clear interspecific differences in MMAs related to posture, with the sprawling tegu and echidna emphasizing humeral depression, and the parasagittal opossum emphasizing humeral elevation. There are also notable differences between our sprawling taxa, with the echidna possessing much greater moment arms for humeral pronation than the tegu. We demonstrate clear functional variation between locomotor grades and use these data to hypothesize major shifts in forelimb function and posture along the mammalian stem.

Convergent evolution of quadrupedality in ornithischian dinosaurs was achieved through disparate forelimb muscle mechanics

“…The relative joint axis orientations and rotational centres (figure 1 c,d ) followed the approach of previous studies of tetrapod forelimbs (e.g. [17,30,34], see also electronic supplementary material, §S1), in which each joint was modelled with three rotational axes passing through fixed centres. For the glenohumeral joint, the axis parented to the scapulocoracoid and oriented to the long axis of the glenoid is referred to as abduction–adduction, the axis parented to the humerus and oriented to its long axis is referred to as mediolateral long axis rotation, and the axis that passes through the humeral head perpendicular to both the abduction–adduction and mediolateral long axis rotation axes is referred to as protraction–retraction (figure 1 c,d ).…”

“…Models were initially constructed in a standardized reference pose from which 0° at all joint angles was defined, based on previous studies (e.g. [17,30]) (figure 1 c ). These were subsequently placed into a standardized range of functional poses that fell within the likely range of possible weight-bearing poses for the quadrupedal taxa, and from which muscle moment arms were extracted (see also electronic supplementary material, §S1).…”

“…Extant quadrupedal animals show adaptations in the arrangements of their forelimb muscles associated with different modes of locomotion (e.g. [13–17]), suggesting that basic measures of muscle function can also guide interpretation of hypotheses regarding overall limb mechanics in extinct taxa. In bipedal archosaurs, quantitative studies of muscle leverage in fossil and extant taxa have provided insights into convergent musculoskeletal evolution in archosaur hind limbs [18,19], and shifts in the mechanisms of bipedal gait along the archosaurian lineage to birds [20].…”

“…Herein, we apply multi-body dynamics analysis (e.g. [15,17–20,25–33]) to a sample of ornithischian forelimbs representing the wide array of bauplans present throughout the clade (figure 1 a,e ) to quantitatively investigate, for the first time to our knowledge, how basic forelimb muscle mechanics and function changed across the ornithischian tree, and the extent to which the clades that evolved quadrupedal posture also exhibited mechanical convergence in their solutions to quadrupedal locomotion.…”

From sprawling to parasagittal locomotion in Therapsida: A preliminary study of historically collected museum specimens

“…Fore-and hindlimb. In all tetrapods, the connection between the extremities and the trunk varies between the anterior and the posterior girdles (e.g., Brocklehurst et al 2022). Preuschoft (2022) has proposed to explain why one girdle is mobile and the other rigid by an experiment: If two persons carry a ladder and press one ladder rung firmly against their hips, they have to adjust their stride length and frequency and walk in lock-step, otherwise they would interfere with each other.…”