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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The fossil record of appendicular muscle evolution in Synapsida on the line to mammals: Part I—Forelimb
Abstract This paper is the first 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 forelimb. Understanding forelimb muscular anatomy in extinct synapsids, and how this changed on the line to mammals, can provide important perspective for interpreting skeletal and functional evolution in this lineage, and how the diversity of forelimb functions in extant mammals arose. 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 73 character–state complexes covering all muscles crossing the shoulder, elbow, and wrist 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. In addition to producing a comprehensive documentation of osteological evidence for muscle attachments in extinct synapsids, this work has clarified homology hypotheses across disparate taxa and helped resolve competing hypotheses of muscular anatomy in extinct species. The evolutionary history of mammalian forelimb musculature was a complex and nonlinear narrative, punctuated by multiple instances of convergence and concentrated phases of anatomical transformation. More broadly, this study highlights the great insight that a fossil‐based perspective can provide for understanding the assembly of novel body plans.
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- Award ID(s):
- 2122115
- PAR ID:
- 10464487
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- The Anatomical Record
- Volume:
- 307
- Issue:
- 5
- ISSN:
- 1932-8486
- Format(s):
- Medium: X Size: p. 1764-1825
- Size(s):
- p. 1764-1825
- 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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