Phenotypic integration and modularity are ubiquitous features of complex organisms, describing the magnitude and pattern of relationships among biological traits. A key prediction is that these relationships, reflecting genetic, developmental, and functional interactions, shape evolutionary processes by governing evolvability and constraint. Over the last 60 years, a rich literature of research has quantified patterns of integration and modularity across a variety of clades and systems. Only recently has it become possible to contextualize these findings in a phylogenetic framework to understand how trait integration interacts with evolutionary tempo and mode. Here, we review the state of macroevolutionary studies of integration and modularity, synthesizing empirical and theoretical work into a conceptual framework for predicting the effects of integration on evolutionary rate and disparity: a fly in a tube. While magnitude of integration is expected to influence the potential for phenotypic variation to be produced and maintained, thus defining the shape and size of a tube in morphospace, evolutionary rate, or the speed at which a fly moves around the tube, is not necessarily controlled by trait interactions. Finally, we demonstrate this reduced disparity relative to the Brownian expectation for a given rate of evolution with an empirical example: the avian cranium.
SUMMARY Morphological integration and modularity, which describe the relationships among morphological attributes and reflect genetic, developmental, and functional interactions, have been hypothesized to be major influences on trait responses to selection and thus morphological evolution. The mammalian presacral vertebral column shows little variation in vertebral count and therefore specialization for function occurs primarily through modification of vertebral shape. However, vertebral shape has been suggested to be under strong control from developmental canalization, although this has never been explicitly tested. Here, we assess hypotheses of developmental modules in the vertebrae of felids to determine whether developmental interactions are a primary influence on vertebral modularity. Additionally, we analyze the magnitudes of both intravertebral integration and disparity to evaluate if level of integration varies along the vertebral column and, if so, whether integration and disparity are associated. Our results confirm the hypothesis of vertebral developmental modularity, with most presacral vertebrae displaying two modules. Exceptions are concentrated in the boundaries among traditional and functional regions, suggesting that intravertebral modularity may reflect larger‐scale modularity of the felid vertebral column. We further demonstrate that overall integration and disparity are highest in posterior vertebrae, thus providing an empirical example of integration potentially promoting greater morphological responses to selection.
The body masses of cats (Mammalia, Carnivora, Felidae) span a ~300-fold range from the smallest to largest species. Despite this range, felid musculoskeletal anatomy remains remarkably conservative, including the maintenance of a crouched limb posture at unusually large sizes. The forelimbs in felids are important for body support and other aspects of locomotion, as well as climbing and prey capture, with the assistance of the vertebral (and hindlimb) muscles. Here, we examine the scaling of the anterior postcranial musculature across felids to assess scaling patterns between different species spanning the range of felid body sizes. The muscle architecture (lengths and masses of the muscle-tendon unit components) for the forelimb, cervical and thoracic muscles was quantified to analyse how the muscles scale with body mass. Our results demonstrate that physiological cross-sectional areas of the forelimb muscles scale positively with increasing body mass (i.e. becoming relatively larger). Many significantly allometric variables pertain to shoulder support, whereas the rest of the limb muscles become relatively weaker in larger felid species. However, when phylogenetic relationships were corrected for, most of these significant relationships disappeared, leaving no significantly allometric muscle metrics. The majority of cervical and thoracic muscle metrics are not significantly allometric, despite there being many allometric skeletal elements in these regions. When forelimb muscle data were considered in isolation or in combination with those of the vertebral muscles in principal components analyses and MANOVAs, there was no significant discrimination among species by either size or locomotory mode. Our results support the inference that larger felid species have relatively weaker anterior postcranial musculature compared with smaller species, due to an absence of significant positive allometry of forelimb or vertebral muscle architecture. This difference in strength is consistent with behavioural changes in larger felids, such as a reduction of maximal speed and other aspects of locomotor abilities.
Members of the mammalian family Felidae (extant and extinct cats) are grossly phenotypically similar, but display a 300-fold range in body size, from less than 1 kg to more than 300 kg. In addition to differences in body mass, felid species show dietary and locomotory specializations that correlate to skull and limb osteological measurements, such as shape or cross-sectional area. However, ecological correlates to the axial skeleton are yet untested. Here, we build on previous studies of the biomechanical and morphological evolution of the felid appendicular skeleton by conducting a quantitative analysis of morphology and allometry in the presacral vertebral column across extant cats. Our results demonstrate that vertebral columns of arboreal, scansorial and terrestrial felids significantly differ in morphology, specifically in the lumbar region, while no distinction based on dietary specialization was found. Body size significantly influences vertebral morphology, with clear regionalization of allometry along the vertebral column, suggesting that anterior (cervicals and thoracics) and posterior (lumbar) vertebrae may be independently subjected to distinct selection pressures.
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