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1. The fossil record of appendicular muscle evolution in Synapsida on the line to mammals: Part II —Hindlimb

   https://doi.org/10.1002/ar.25310  

   Bishop, Peter J; Pierce, Stephanie E (September 2023, The Anatomical Record)

   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. 

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2. 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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3. 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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4. Antiquity of forelimb ecomorphological diversity in the mammalian stem lineage (Synapsida)

   https://doi.org/10.1073/pnas.1802543116  

   Lungmus, Jacqueline K.; Angielczyk, Kenneth D. (April 2019, Proceedings of the National Academy of Sciences)

   Mammals and their closest fossil relatives are unique among tetrapods in expressing a high degree of pectoral girdle and forelimb functional diversity associated with fully pelagic, cursorial, subterranean, volant, and other lifestyles. However, the earliest members of the mammalian stem lineage, the “pelycosaur”-grade synapsids, present a far more limited range of morphologies and inferred functions. The more crownward nonmammaliaform therapsids display novel forelimb morphologies that have been linked to expanded functional diversity, suggesting that the roots of this quintessentially mammalian phenotype can be traced to the pelycosaur–therapsid transition in the Permian period. We quantified morphological disparity of the humerus in pelycosaur-grade synapsids and therapsids using geometric morphometrics. We found that disparity begins to increase concurrently with the emergence of Therapsida, and that it continues to rise until the Permo-Triassic mass extinction. Further, therapsid exploration of new regions of morphospace is correlated with the evolution of novel ecomorphologies, some of which are characterized by changes to overall limb morphology. This evolutionary pattern confirms that nonmammaliaform therapsid forelimbs underwent ecomorphological diversification throughout the Permian, with functional elaboration initially being more strongly expressed in the proximal end of the humerus than the distal end. The role of the forelimbs in the functional diversification of therapsids foreshadows the deployment of forelimb morphofunctional diversity in the evolutionary radiation of mammals. 

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5. Phylogeny, function and ecology in the deep evolutionary history of the mammalian forelimb

   https://doi.org/10.1098/rspb.2021.0494  

   Lungmus, Jacqueline K.; Angielczyk, Kenneth D. (April 2021, Proceedings of the Royal Society B: Biological Sciences)

   Mammals are the only living members of the larger clade Synapsida, which has a fossil record spanning 320 Ma. Despite the fact that much of the ecological diversity of mammals has been considered in the light of limb morphology, the ecological comparability of mammals to their fossil forerunners has not been critically assessed. Because of the wide use of limb morphology in testing ecomorphological hypothesis about extinct tetrapods, we sought: (i) to estimate when in synapsid history, modern mammals become analogues for predicting fossil ecologies; (ii) to document examples of ecomorphological convergence; and (iii) to compare the functional solutions of distinct synapsid radiations. We quantitatively compared the forelimb shapes of the multiple fossil synapsid radiations to a broad sample of extant Mammalia representing a variety of divergent locomotor ecologies. Our results indicate that each synapsid radiation explored different areas of morphospace and arrived at functional solutions that reflected their distinctive ancestral morphologies. This work counters the narrative of non-mammalian synapsid forelimb evolution as a linear progression towards more mammalian morphologies. Instead, a disparate array of early-evolving shapes subsequently contracted towards more mammal-like forms. 

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