Topographically distinct adaptive landscapes for teeth, skeletons, and size explain the adaptive radiation of Carnivora (Mammalia)

Abstract

Models of adaptive radiation were originally developed to explain the early, rapid appearance of distinct modes of life within diversifying clades. Phylogenetic tests of this hypothesis have yielded limited support for temporally declining rates of phenotypic evolution across diverse clades, but the concept of an adaptive landscape that links form to fitness, while also crucial to these models, has received more limited attention. Using methods that assess the temporal accumulation of morphological variation and estimate the topography of the underlying adaptive landscape, I found evidence of an early partitioning of mandibulo-dental morphological variation in Carnivora (Mammalia) that occurs on an adaptive landscape with multiple peaks, consistent with classic ideas about adaptive radiation. Although strong support for this mode of adaptive radiation is present in traits related to diet, its signal is not present in body mass data or for traits related to locomotor behavior and substrate use. These findings suggest that adaptive radiations may occur along some axes of ecomorphological variation without leaving a signal in others and that their dynamics are more complex than simple univariate tests might suggest.

Uncovering the mosaic evolution of the carnivoran skeletal system

“…Lastly, we found that the clade-specific shift model (mvOUM phyloEM ; AICcW > 0.99) best described the overall skeletal phenome (electronic supplementary material, table S2), a pattern that is consistent with previous investigations of whole-body proxies such as body size and body shape [28,38,39]. The mammalian body plan is comprised of cranial, axial and appendicular components; therefore, its multidimensionality transcends one-to-one mapping relationships between morphology and ecological function.…”

Turbulent adaptive landscape shaped size evolution in modern ocean giants

“…We performed disparity through time analyses 51 using the dtt function in the R package geiger 52 , with 10,000 simulated datasets used to generate a null, constant-rates distribution. The centre of gravity was computed as the weighted sum of the product of standardised average subclade disparity and relative node age, with significance determined as the proportion of simulated centres of gravity that were lower than the empirical value 53 .…”

Uncovering the mosaic evolution of the carnivoran skeletal system

“…The ability of individual skeletal components to adapt to specific ecological factors independently from each other may have contributed to the clade's hierarchical [62,63] evolution. As previously hypothesized [26,36], the restriction of carnassial shear to the P4/m1 pair may have been the key innovation that facilitated the initial carnivoran diversification early in the clade's evolutionary history. Subsequent evolution led to the continual partitioning between clades, resulting in the origination of extant carnivoran families as discrete phylogenetic clusters that occupy different adaptive zones [64] with distinct morphologies including body size and shape [37,65] and various components of the skeleton ( [6]; Fig.…”

“…For example, the anterior region exhibits low disparity due to phylogenetic constraints or ecological conservatism, whereas the posterior region exhibits higher disparity that may be due to adaptations to various locomotor ecologies [12,31]. In contrast to these anatomically-localized studies, researchers examining proxies of the overall body plan report that the evolution of traits like body mass, skeletal size, and body shape often follow a Brownian motion model or clade-based shift model rather than being associated with ecological regimes [23,32,33].…”

“…Anterior (i.e., more cranial) vertebrae exhibits low disparity due to phylogenetic constraints or ecological conservatism, whereas posterior (i.e., more caudal) vertebrae exhibits higher disparity that may be due to adaptations to various locomotor ecologies [13,37]. In contrast to these morphologically-localized studies, analyses of the evolution of whole-body traits like body mass, skeletal size, and body shape often follow a Brownian motion model or clade-based shift model rather than being associated with ecological regimes [28,38,39]. Compared to skeletal system-specific findings, simultaneous investigation of skulls, limbs, vertebrae, and overall body plan are rarely conducted, likely because of the enormous amount of data that would need to be collected and the complexity of the multivariate analyses required.…”