- NSF-PAR ID:
- 10144102
- Date Published:
- Journal Name:
- Journal of Mammalian Evolution
- ISSN:
- 1064-7554
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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 .more » « less
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null (Ed.)Extant mammals are both taxonomically and ecologically diverse, having evolved a remarkable array of locomotor ecologies (e.g., swimming, digging, and flying). Evolution of the therian-type forelimb, with a highly reduced pectoral girdle and ball-and-socket shoulder joint, has been heralded as a key innovation that enabled mammals to co-opt their forelimbs for diverse functions. The acquisition of the mammal forelimb can be traced through their forerunners, the non-mammalian synapsids (NMS), but exactly how this musculoskeletal transformation proceeded and its impact on functional diversification have not be quantitatively tested. To explore the evolution of forelimb functional diversity in synapsids, we measured shoulder joint osteological range of motion (ROM) in a range of extant amniotes (lizards, monotremes, therian mammals), and compared their patterns of joint mobility to exemplars from each of the major grades of NMS: ‘pelycosaurs’, basal therapsids, and non-mammalian cynodonts. Three-dimensional models of the shoulder girdles and humeri were digitally aligned in an anatomical ‘neutral pose’ using a semi-automated approach based on articular surface morphology. ROM was then determined for the shoulder joint using a fully automated method, where the humerus was moved in flexion-extension, adduction-abduction, and pronation-supination until bone-to-bone contact occurred. Relative degree and directionality of mobility were then compared across taxa. We find an increase in total shoulder joint ROM through synapsid evolution, suggesting that more derived NMS could perform a wider range of limb movements. However, we also see more complex trends in directionality of shoulder mobility that may be indicators of forelimb posture. Extant lepidosaurs and monotremes had the greatest ROM in abduction-adduction, whereas therians had more ROM in flexion-extension, likely related to ‘sprawling’ vs. ‘erect’ gaits. Therapsids and cynodonts both had greatest ROM in abduction-adduction, matching previous reconstructions of these taxa as sprawling to semi-erect. However, ‘pelycosaurs’ had the greatest ROM in flexion-extension, despite having abducted forelimbs, suggesting they did not move their forelimbs in same manner as modern sprawling animals. Our results demonstrate the complex nature of forelimb evolution in synapsids and provide novel insights into the functional transformation and diversification of the mammalian forelimb. Funding Sources Funding information: NSF DEB- 1757749 (S.E.P) and NSF DEB-1754502 (K.D.A).more » « less
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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.more » « less
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Abstract The absence of preserved soft tissues in the fossil record is frequently a hindrance for palaeontologists wishing to investigate morphological shifts in key skeletal systems, such as the limbs. Understanding the soft tissue composition of modern species can aid in understanding changes in musculoskeletal features through evolution, including those pertaining to locomotion. Establishing anatomical differences in soft tissues utilising an extant phylogenetic bracket can, in turn, assist in interpreting morphological changes in hard tissues and modelling musculoskeletal movements during evolutionary transitions (e.g. digit reduction in perissodactyls). Perissodactyls (horses, rhinoceroses, tapirs and their relatives) are known to have originated with a four‐toed (tetradactyl) forelimb condition. Equids proceeded to reduce all but their central digit, resulting in monodactyly, whereas tapirs retained the ancestral tetradactyl state. The modern Malayan tapir (
Tapirus indicus ) has been shown to exhibit fully functional tetradactyly in its forelimb, more so than any other tapir, and represents an ideal case‐study for muscular arrangement and architectural comparison with the highly derived monodactylEquus . Here, we present the first quantification of muscular architecture of a tetradactyl perissodactyl (T. indicus ), and compare it to measurements from modern monodactyl caballine horse (Equus ferus caballus ). Each muscle of the tapir forelimb was dissected out from a cadaver and measured for architectural properties: muscle‐tendon unit (MTU) length, MTU mass, muscle mass, pennation angle, and resting fibre length. Comparative parameters [physiological cross‐sectional area (PCSA), muscle volume, and % muscle mass] were then calculated from the raw measurements. In the shoulder region, theinfraspinatus ofT. indicus exhibits dual origination sites on either side of the deflected scapular spine. Within ungulates, this condition has only been previously reported in suids. Differences in relative contribution to limb muscle mass betweenT. indicus andEquus highlight forelimb muscles that affect mobility in the lateral and medial digits (e.g.extensor digitorum lateralis ). These muscles were likely reduced in equids during their evolutionary transition from tetradactyl forest‐dwellers to monodactyl, open‐habitat specialists. Patterns of PCSA across the forelimb were similar betweenT. indicus andEquus , with the notable exceptions of thebiceps brachii andflexor carpi ulnaris , which were much larger inEquus . The differences observed in PCSA between the tapir and horse forelimb muscles highlight muscles that are essential for maintaining stability in the monodactyl limb while moving at high speeds. This quantitative dataset of muscle architecture in a functionally tetradactyl perissodactyl is a pivotal first step towards reconstructing the locomotor capabilities of extinct, four‐toed ancestors of modern perissodactyls, and providing further insights into the equid locomotor transition. -
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.more » « less