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  1. Abstract Background

    Mammalian skeletons are largely formed before birth. Heterochronic changes in skeletal formation can be investigated by comparing the order of ossification for different elements of the skeleton. Due to the challenge of collecting prenatal specimens in viviparous taxa, opportunistically collected museum specimens provide the best material for studying prenatal skeletal development across many mammalian species. Previous studies have investigated ossification sequence in a range of mammalian species, but little is known about the pattern of bone formation in Carnivora. Carnivorans have diverse ecologies, diets, and biomechanical specializations and are well-suited for investigating questions in evolutionary biology. Currently, developmental data on carnivorans is largely limited to domesticated species. To expand available data on carnivoran skeletal development, we used micro-computed tomography (micro-CT) to non-invasively evaluate the degree of ossification in all prenatal carnivoran specimens housed in the Harvard Museum of Comparative Zoology. By coding the presence or absence of bones in each specimen, we constructed ossification sequences for each species. Parsimov-based genetic inference (PGi) was then used to identify heterochronic shifts between carnivoran lineages and reconstruct the ancestral ossification sequence of Carnivora.

    Results

    We used micro-CT to study prenatal ossification sequence in six carnivora species:Eumetopias jubatus(Steller sea lion,n = 6),Herpestes javanicus(small Indian mongoose,n = 1),Panthera leo(lion,n = 1),Urocyon cinereoargenteus(gray fox,n = 1),Ursus arctos arctos(Eurasian brown bear,n = 1), andViverricula indica(small Indian civet,n = 5). Due to the relatively later stage of collection for the available specimens, few heterochronic shifts were identified. Ossification sequences of feliform species showed complete agreement with the domestic cat. In caniforms, the bear and fox ossification sequences largely matched the dog, but numerous heterochronic shifts were identified in the sea lion.

    Conclusions

    We use museum specimens to generate cranial and postcranial micro-CT data on six species split between the two major carnivoran clades: Caniformia and Feliformia. Our data suggest that the ossification sequence of domestic dogs and cats are likely good models for terrestrial caniforms and feliforms, respectively, but not pinnipeds.

     
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  2. 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. 
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  3. Skeletal muscle mass, architecture and force-generating capacity are well known to scale with body size in animals, both throughout ontogeny and across species. Investigations of limb muscle scaling in terrestrial amniotes typically focus on individual muscles within select clades, but here this question was examined at the level of the whole limb across amniotes generally. In particular, the present study explored how muscle mass, force-generating capacity (measured by physiological cross-sectional area) and internal architecture (fascicle length) scales in the fore- and hindlimbs of extant mammals, non-avian saurians (‘reptiles’) and bipeds (birds and humans). Sixty species spanning almost five orders of magnitude in body mass were investigated, comprising previously published architectural data and new data obtained via dissections of the opossum Didelphis virginiana and the tegu lizard Salvator merianae . Phylogenetic generalized least squares was used to determine allometric scaling slopes (exponents) and intercepts, to assess whether patterns previously reported for individual muscles or functional groups were retained at the level of the whole limb, and to test whether mammals, reptiles and bipeds followed different allometric trajectories. In general, patterns of scaling observed in individual muscles were also observed in the whole limb. Reptiles generally have proportionately lower muscle mass and force-generating capacity compared to mammals, especially at larger body size, and bipeds exhibit strong to extreme positive allometry in the distal hindlimb. Remarkably, when muscle mass was accounted for in analyses of muscle force-generating capacity, reptiles, mammals and bipeds almost ubiquitously followed a single common scaling pattern, implying that differences in whole-limb force-generating capacity are principally driven by differences in muscle mass, not internal architecture. In addition to providing a novel perspective on skeletal muscle allometry in animals, the new dataset assembled was used to generate pan-amniote statistical relationships that can be used to predict muscle mass or force-generating capacity in extinct amniotes, helping to inform future reconstructions of musculoskeletal function in the fossil record. 
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