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The evolutionary transition from early synapsids to therian mammals involved profound reorganization in locomotor anatomy and function, centered around a shift from “sprawled” to “erect” limb postures. When and how this functional shift was accomplished has remained difficult to decipher from the fossil record alone. Through biomechanical modeling of hindlimb force-generating performance in eight exemplar fossil synapsids, we demonstrate that the erect locomotor regime typifying modern therians did not evolve until just before crown Theria. Modeling also identifies a transient phase of increased performance in therapsids and early cynodonts, before crown mammals. Further, quantifying the global actions of major hip muscle groups indicates a protracted juxtaposition of functional redeployment and conservatism, highlighting the intricate interplay between anatomical reorganization and function across postural transitions. We infer a complex history of synapsid locomotor evolution and suggest that major evolutionary transitions between contrasting locomotor behaviors may follow highly nonlinear trajectories. 

Abstract This paper is the second in a two‐part series that charts the evolution of appendicular musculature along the mammalian stem lineage, drawing upon the exceptional fossil record of extinct synapsids. Here, attention is focused on muscles of the hindlimb. Although the hindlimb skeleton did not undergo as marked a transformation on the line to mammals as did the forelimb skeleton, the anatomy of extant tetrapods indicates that major changes to musculature have nonetheless occurred. To better understand these changes, this study surveyed the osteological evidence for muscular attachments in extinct mammalian and nonmammalian synapsids, two extinct amniote outgroups, and a large selection of extant mammals, saurians, and salamanders. Observations were integrated into an explicit phylogenetic framework, comprising 80 character–state complexes covering all muscles crossing the hip, knee, and ankle joints. These were coded for 33 operational taxonomic units spanning >330 Ma of tetrapod evolution, and ancestral state reconstruction was used to evaluate the sequence of muscular evolution along the stem lineage from Amniota to Theria. The evolutionary history of mammalian hindlimb musculature was complex, nonlinear, and protracted, with several instances of convergence and pulses of anatomical transformation that continued well into the crown group. Numerous traits typically regarded as characteristically “mammalian” have much greater antiquity than previously recognized, and for some traits, most synapsids are probably more reflective of the ancestral amniote condition than are extant saurians. More broadly, this study highlights the utility of the fossil record in interpreting the evolutionary appearance of distinctive anatomies. 

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. 

In evolutionary biomechanics, musculoskeletal computer models of extant and extinct taxa are often used to estimate joint range of motion (ROM) and muscle moment arms (MMAs), two parameters which form the basis of functional inferences. However, relatively few experimental studies have been performed to validate model outputs. Previously, we built a model of the short-beaked echidna ( Tachyglossus aculeatus ) forelimb using a traditional modelling workflow, and in this study we evaluate its behaviour and outputs using experimental data. The echidna is an unusual animal representing an edge-case for model validation: it uses a unique form of sprawling locomotion, and possesses a suite of derived anatomical features, in addition to other features reminiscent of extinct early relatives of mammals. Here we use diffusible iodine-based contrast-enhanced computed tomography (diceCT) alongside digital and traditional dissection to evaluate muscle attachments, modelled muscle paths, and the effects of model alterations on the MMA outputs. We use X-ray Reconstruction of Moving Morphology (XROMM) to compare ex vivo joint ROM to model estimates based on osteological limits predicted via single-axis rotation, and to calculate experimental MMAs from implanted muscles using a novel geometric method. We also add additional levels of model detail, in the form of muscle architecture, to evaluate how muscle torque might alter the inferences made from MMAs alone, as is typical in evolutionary studies. Our study identifies several key findings that can be applied to future models. 1) A light-touch approach to model building can generate reasonably accurate muscle paths, and small alterations in attachment site seem to have minimal effects on model output. 2) Simultaneous movement through multiple degrees of freedom, including rotations and translation at joints, are necessary to ensure full joint ROM is captured; however, single-axis ROM can provide a reasonable approximation of mobility depending on the modelling objectives. 3) Our geometric method of calculating MMAs is consistent with model-predicted MMAs calculated via partial velocity, and is a potentially useful tool for others to create and validate musculoskeletal models. 4) Inclusion of muscle architecture data can change some functional inferences, but in many cases reinforced conclusions based on MMA alone. 

Monotremes are a group of egg-laying mammals, possessing a mosaic of ancestral and derived anatomical features. Despite much interest in monotremes from phylogenetic, morphological, and ecological perspectives, they have been the subject of relatively few biomechanical studies. In this study, we examined shoulder and proximal forelimb muscle anatomy and architecture in the short-beaked echidna, Tachyglossus aculeatus, through contrast-enhanced computed tomography and gross dissection. Muscle architecture is a major determinant of muscle function and can indicate specialized muscle roles, such as the capacity for generating large forces (through large physiological cross-sectional area, PCSA) or working ranges (through long fascicle lengths). We hypothesized that some muscles would exhibit architectural specializations convergent with other fossorial and/or sprawling animals, and that other muscles would reflect the echidna’s unusual anatomy and locomotor style. Instead, we found the shoulder and proximal forelimb muscles in echidna to have little variation in their architecture. The muscles generally had long fascicles and small-to-intermediate PCSAs, consistent with force production over a wide working range. Further, muscles did not show overt differences in architecture that, in therian mammals, have been linked to increased forelimb mobility and the transition from sprawling to parasagittal posture. Our measures of architectural disparity placed the echidna closer to the tegu lizard than other sprawling fossorial mammals (e.g., mole). The low architectural diversity found in the echidna’s shoulder and proximal forelimb muscles is interpreted as a lack of functional specialization into distinct roles. We hope our study will contribute to greater understanding of monotreme anatomy and biomechanical function, and to the reconstruction of musculoskeletal evolution in mammals. 

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 .