Functional relationship between myology and ecology in carnivores: do forelimb muscles reflect adaptations to prehension (original) (raw)
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Biological Journal of the Linnean Society
The arboreal environment is complex and irregular and imposes significant constraints on the locomotor ability of vertebrates, resulting in morphological adaptations. Carnivorans are of particular interest because they radiated several times independently into the arboreal milieu, leading to convergence in long bone anatomy. We investigated whether the forelimb muscles show differences in arboreal vs. terrestrial species and tested for convergence in muscle architecture. To do so, we studied the forelimb muscles in 17 species of carnivorans with different locomotor modes (arboreal and terrestrial). Our results showed that the forelimb musculature evolved in a convergent manner in arboreal species, resulting in more forceful and heavier wrist rotators and elbow flexors, even when accounting for phylogeny. This suggests that selective forces imposed by the environment drive the evolution of the muscular system towards a convergent phenotype that provides a functional advantage for locomotion in the complex threedimensional arboreal habitat.
Canadian Journal of Zoology, 2000
Using a new rating scale of forelimb dexterity that separates the contribution of proximal components (shoulder, upper forelimb, and lower forelimb) from distal components (forepaw), we examined the relationship between functional demands and phylogeny and forelimb dexterity in 45 species of fissiped carnivores (Carnivora). Specifically, we examined the effects of body size, phylogenetic relatedness, diet (vertebrate predation), and locomotion (arboreality) on the differential evolution of forelimb dexterity. Regression analyses indicate that, although body size does appear to be positively correlated with the dexterity of the proximal components, the inclusion of phylogenetic information results in a nonsignificant relationship. Phylogenetic relatedness was found to account for a significant amount of interspecific variation in proximal, distal, and total (proximal + distal) dexterity. When phylogenetic effects were incorporated, arboreality was not significantly correlated with any of the dexterity scores, but vertebrate predation was, albeit a negative correlation. The amount of variation in the dexterity of proximal and distal components did, however, differ in magnitude within each significant result. Thus, each component can be differentially affected by specific functional demands. By examining the significant associations with diet and phylogeny and mapping the dexterity scores onto the phylogeny, we also demonstrate that the ancestral degree of forelimb dexterity of both the caniform and feliform lineages was approximately equal to that of the average extant carnivore. Thus, forelimb dexterity has decreased or increased within particular lineages, with reductions or elaborations in some species resulting from the invasion of specific niches not occupied by congeners.
The evolution of skilled forelimb movements in carnivorans
2000
Emancipating the forelimbs from locomotion for use in other activities, such as food manipulation, is a major evolutionary milestone. A variety of selective forces and evolutionary correlates may influence the evolution of various degrees of skill with which the forelimbs are used. Using the order Carnivora as a test group, I assessed the relative influence of six factors: relative brain size, neocortical volume, manus proportions, body size, phylogenetic relatedness, type of locomotion and diet I developed a rating system to describe the dexterity of individual species and compared the scores to the six factors using modem comparative methods. Only phylogeny and diet were significantly correlated with forelimb dexterity. More specifically, forelimb dexterity tends to be higher in caniform than in feliform carnivorans and decreases with increasing specialisation on vertebrate prey. I conclude that food handling and feeding niche breadth have a significant effect upon the evolution of skilled forelimb movements. iv ACKNOWLEDGEMENTS Firstly, I wish to thank Ian Whishaw and Sergio Pellis for offering me the opportunity to be their graduate student at such short notice and for their unwavering support throughout my thesis research. They both provided me the freedom, willingly or not, to 'do my own thing', but were always there when I needed some guidance. I would not have arrived here at all, however, without the inspiration of John Nelson who first introduced me to the behavioural analysis of reaching and grasping and provided me with the intellectual freedom to investigate behavioural phenomena on my own. This project could not have been completed without the assistance of the helpful staff at the following zoological institutions which I relied upon for my behavioural observations: Assiniboine Zoo (Winnipeg, MB), Calgary Zoo (Calgary, AB), Los Angeles County Zoo
Canadian Journal of Zoology, 2001
The relationship between manus proportions and forepaw dexterity in 33 species of carnivores (Carnivora) was examined. Both the analysis of "raw" data and independent contrasts revealed no significant correlation between the metacarpal-phalanx (MCP) ratio and forepaw dexterity. This result was corroborated by a common origins test, which indicated that changes in the MCP ratio were not coincident with changes in forepaw dexterity throughout carnivore evolution. Together, these results suggest that the morphological basis for variations in manipulative behaviour may be quite complex. Other morphological features, such as manus and carpal shape and myology, may play a critical role in forepaw dexterity, but are not manifested as changes in manus proportions. Behavioural observations also suggest that manus proportions may be correlated more closely with locomotion rather than non-locomotory forepaw usage.
The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora)
Canadian Journal of Zoology, 1999
We tested the validity of previously described relationships between forelimb structure and behaviour in mammals by measuring the forelimbs of 22 species of North American carnivores. Nine ratios were calculated from these measurements and made independent of the effects of allometry and phylogeny through the use of log-transformed regressions and independent contrasts analysis. The ratios were then directly compared with two behavioural traits: arboreal locomotion and vertebrate predation. Only five of the nine ratios exhibited a significant relationship with arboreal locomotion and three with vertebrate predation. It was concluded that the brachial index, relative size of the olecranon process, and total forelimb robusticity may be reliable predictors of arboreal locomotion, and that the brachial index, relative size of the olecranon process, and radial robusticity may be accurate predictors of vertebrate predation. The data also suggest that the morphology of the lower forelimb m...
BMC Evolutionary Biology, 2014
Background: The shape of the appendicular bones in mammals usually reflects adaptations towards different locomotor abilities. However, other aspects such as body size and phylogeny also play an important role in shaping bone design. We used 3D landmark-based geometric morphometrics to analyse the shape of the hind limb bones (i.e., femur, tibia, and pelvic girdle bones) of living and extinct terrestrial carnivorans (Mammalia, Carnivora) to quantitatively investigate the influence of body size, phylogeny, and locomotor behaviour in shaping the morphology of these bones. We also investigated the main patterns of morphological variation within a phylogenetic context. Results: Size and phylogeny strongly influence the shape of the hind limb bones. In contrast, adaptations towards different modes of locomotion seem to have little influence. Principal Components Analysis and the study of phylomorphospaces suggest that the main source of variation in bone shape is a gradient of slenderness-robustness. Conclusion: The shape of the hind limb bones is strongly influenced by body size and phylogeny, but not to a similar degree by locomotor behaviour. The slender-robust "morphological bipolarity" found in bone shape variability is probably related to a trade-off between maintaining energetic efficiency and withstanding resistance to stresses. The balance involved in this trade-off impedes the evolution of high phenotypic variability. In fact, both morphological extremes (slender/robust) are adaptive in different selective contexts and lead to a convergence in shape among taxa with extremely different ecologies but with similar biomechanical demands. Strikingly, this "one-to-many mapping" pattern of evolution between morphology and ecology in hind limb bones is in complete contrast to the "many-to-one mapping" pattern found in the evolution of carnivoran skull shape. The results suggest that there are more constraints in the evolution of the shape of the appendicular skeleton than in that of skull shape because of the strong biomechanical constraints imposed by terrestrial locomotion.
Brain, Behavior and Evolution, 1999
To test the hypothesis that brain size and forelimb dexterity are positively correlated, the relative brain size of 41 species of fissiped (terrestrial) carnivores (Order: Carnivora) was examined with respect to their forelimb use during feeding. With the use of a newly derived dexterity index, the forelimb dexterity executed by each of the species was calculated as a single, continuous variable which was then regressed against the residuals of brain size. To account for confounding effects of phylogenetic inertia, the analysis was performed with independent contrasts analysis using a speciational model of evolutionary change (i.e. equal branch lengths). The results suggest that relative brain size and isocortex size are not correlated with the dexterity of the proximal or distal segments or a combination of the two (total forelimb dexterity). The presence of species with widely different brain sizes and similar dexterities, and vice versa, suggests that an increase in the amount of...
Ecomorphology of Carnivora challenges convergent evolution
Organisms Diversity & Evolution, 2015
Convergent evolution is often reported in the mammalian order Carnivora. Their adaptations to particularly demanding feeding habits such as hypercarnivory and durophagy (consumption of tough food) appear to favour morphological similarities between distantly related species, especially in the skull. However, phylogenetic effect in phenotypic data might obscure such a pattern. We first validated the hypotheses that extant hypercarnivorous and durophagous large carnivorans converge in mandibular shape and form (=size and shape). Hypercarnivores generally exhibit smaller volumes of the multidimensional shape and form space than their sister taxa, but this pattern is significantly different from random expectation only when hunting behaviour categorisations are taken into account. Durophages share areas of the morphospace, but this seems to be due to factors of contingency. Carnivorans that hunt in pack exhibit incomplete convergence while even stronger similarities occur in the mandible shape of solitary hunters due to the high functional demands in killing the prey. We identified a stronger phylogenetic signal in mandibular shape than in size. The quantification of evolutionary rates of changes suggests that mandible shape of solitary hunters evolved slowly when compared to the other carnivorans. These results consistently indicate that the need for strong bite force and robust mandible override sheer phylogenetic effect in solitary hunters.
Locomotor correlates of the scapholunar of living and extinct carnivorans
Journal of Morphology, 2019
The relationship of carpal morphology to ecology and habitat is under studied in carnivorans and more generally in mammals. Here, we use 3D-scanning techniques to assess the usefulness of a carpal bone, the scapholunar, in carnivorans to reflect ecology and habitat, and to reconstruct the ecology of five extinct carnivorans from two fossil sites: Rancho La Brea and Natural Trap Cave. We 3D-scanned scapholunars and measured articular surface areas and angles between articular facets using GeoMagic and Rhino 3D-software. We analyzed the difference in these metrics using multivariate analysis of variance and discriminant function analysis. Results show that the scapholunar reflects ecological signal, with clear groupings of cursorial carnivorans and grappling/climbing carnivorans; however, phylogenetic signal was also present in the results with hyaenids, canids, and large felids in distinct morphospaces. Extinct species Miracinonyx trumani (American cheetah) and Smilodon fatalis (sabertooth cat) showed surprising results with M. trumani grouping with pantherines instead of Acinonyx or Puma, suggesting it runs but still retains the ability to grapple prey. S. fatalis groups with pantherines, but also shows some unique adaptations, suggesting it had a different range of wrist motion than living cats. Overall, the scapholunar is a good indicator of ecology and functional morphology and can be another tool to use in modern and fossil carnivorans to reconstruct extinct ecologies
bioRxiv (Cold Spring Harbor Laboratory), 2022
The scaling pattern of the forelimb in Carnivora was determined using a sample of 30 variables measured on the scapula, humerus, radius, ulna, and third metacarpal, of 429 specimens belonging to 137 species of Carnivora. Standardized major axis regressions on body mass were calculated for all variables, using both traditional regression methods and phylogenetically independent contrasts (PIC). In agreement with previous studies on the scaling of the appendicular skeleton, conformity to either the geometric similarity hypothesis or the elastic similarity hypothesis was low. The scaling pattern of several phyletic lines and locomotor types within Carnivora was also determined, and significant deviations from the scaling pattern of the order were found in some of these subsamples. Furthermore, significant evidence for differential scaling was found for several variables, both in the whole sample and in various phylogenetic and locomotor subsamples. Contrary to previous studies, significant differences were found between the allometric exponents obtained with traditional and PIC regression methods, emphasizing the need to take into account phylogenetic relatedness in scaling studies. In light of these and previous results, we conclude that similarity hypotheses are too simplistic to describe scaling patterns in the carnivoran appendicular skeleton, and thus we propose that scaling hypotheses should be built from similarities in the scaling patterns of phylogenetically narrow samples of species with similar locomotor requirements. The present work is a first step in the study of those samples.