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1. Musculoskeletal modeling untangles the origins of mammal forelimb function and posture; 2023 International Congress of Vertebrate Morphology Abstracts

   Brocklehurst, R_J; Pierce, S_E (July 2023, The Anatomical Record)

   The ‘sprawling–parasagittal’ transition was a major postural shift that occurred in the ancestors of mammals, [PSE1] underpinned by musculoskeletal reorganization of the limbs. However, ‘when’ and ‘how’ this important postural shift occurred is unknown. While the anatomical changes characterizing this transition can be traced through the fossil record, how these relate to functional changes, and the acquisition of parasagittal posture, remains poorly understood. Here, we produced three-dimensional musculoskeletal models of the forelimbs of extant (n=3) and fossil (n=8) taxa that phylogenetically and functionally span the sprawling–parasagittal transition. We calculated joint range of motion (ROM) to determine a 3D pose space, using the novel APSE algorithm (Accelerated Pose Searching with Electrostatics). We then estimated muscle moment arms (MMAs) across the entire pose space for all muscles crossing the shoulder and elbow joints. Models of extant species were validated against empirical measures of ROM and MMA derived from ex vivo XROMM (X-ray reconstruction of moving morphology). Among extant species, our parasagittal taxon occupied a distinct region of pose-space, with more retracted and depressed shoulder joint angles. MMA data show increased emphasis on shoulder elevation associated with a parasagittal posture, but greater shoulder depression in sprawlers. Results from the fossil species show complex, non-linear patterns of forelimb transformation, demonstrating that the ‘sprawling-parasagittal’ transition is characterized by homoplasy and postural variation within the mammalian lineage. 

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2. Shoulder joint range of motion in fossil synapsids and the origins of mammalian locomotor diversity

   Brocklehurst, R. J. (July 2020, Journal of Vertebrate Paleontology, Program and Abstracts, 2020)

   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). 

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3. Adaptive landscapes reveal complex evolution of forelimb posture in stem mammals (Synapsida)

   Brocklehurst, Robert; Mercado, Magdalen; Pierce, Stephanie (January 2023, Integrative and comparative biology)

   The ‘sprawling–parasagittal’ transition was a major postural shift during mammal evolution, but ‘when’ and ‘how’ it occurred has been debated for decades. Previous work focused on a few exceptional fossils from discrete points in time, but broader studies of individual limb elements may provide a more comprehensive evolutionary perspective. Here we address when and how parasagittal forelimb posture evolved in the ancestors of mammals, the non-mammalian synapsids (NMS), using functional adaptive landscape analysis of the humerus bone, incorporating data from morphology, function, and phylogeny, to assess forelimb evolution in deep time. The humerus is subjected to different functional stresses in parasagittal vs. sprawling limbs, and so its morphology is expected to reflect postural differences. We measured humerus shape and various functional traits on a large sample of NMS (n = 61), with a diverse array of extant taxa (n = 140) serving as a robust comparative dataset. We recover distinct adaptive landscapes for extant sprawling and parasagittal taxa, highlighting functional specialization of the humerus associated with different postures. The landscapes for NMS had distinct adaptive peaks from extant sprawlers. While there is repeated evolution of humeri representing ‘transitional’ postures in NMS, humeri consistent with parasagittal posture do not appear until the crown group. Our data reveal the complexity of postural evolution within Synapsida, with the ‘sprawling-parasagittal’ transition typified by considerable homoplasy, and postural variation within individual synapsid clades. 

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

   https://doi.org/10.7717/peerj.8556  

   Fahn-Lai, Philip; Biewener, Andrew A.; Pierce, Stephanie E. (January 2020, PeerJ)

   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 . 

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5. Validation of an Echidna Forelimb Musculoskeletal Model Using XROMM and diceCT

   https://doi.org/10.3389/fbioe.2021.751518  

   Regnault, Sophie; Fahn-Lai, Philip; Pierce, Stephanie E. (November 2021, Frontiers in Bioengineering and Biotechnology)

   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. 

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