Functional diversity of small-mammal postcrania is linked to both substrate preference and body size

Abstract

Selective pressures favor morphologies that are adapted to distinct ecologies, resulting in trait partitioning among ecomorphotypes. However, the effects of these selective pressures vary across taxa, especially because morphology is also influenced by factors such as phylogeny, body size, and functional tradeoffs. In this study, we examine how these factors impact functional diversification in mammals. It has been proposed that trait partitioning among mammalian ecomorphotypes is less pronounced at small body sizes due to biomechanical, energetic, and environmental factors that favor a ‘generalist’ body plan, whereas larger taxa exhibit more substantial functional adaptations. We title this the Divergence Hypothesis (DH) because it predicts greater morphological divergence among ecomorphotypes at larger body sizes. We test DH by using phylogenetic comparative methods to examine the postcranial skeletons of 129 species of taxonomically diverse, small-to-medium-sized (less than 15 kg) mammals, which we categorize as either ‘tree-dwellers’ or ‘ground-dwellers.’ In some analyses, the morphologies of ground-dwellers and tree-dwellers suggest greater between-group differentiation at larger sizes, providing some evidence for DH. However, this trend is not particularly strong nor supported by all analyses. Instead, a more pronounced pattern emerges that is distinct from the predictions of DH: within-group phenotypic disparity increases with body size in both ground-dwellers and tree-dwellers, driven by morphological outliers among ‘medium’-sized mammals. Thus, evolutionary increases in body size are more closely linked to increases in within-locomotor-group disparity than to increases in between-group disparity. We discuss biomechanical and ecological factors that may drive these evolutionary patterns, and we emphasize the significant evolutionary influences of ecology and body size on phenotypic diversity.

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

“…The post-cranial skeleton therefore tends to exhibit a high degree of inter-element covariance (Young and Hallgrímsson, 2005; Goswami et al, 2009), which may frustrate the production of discontinuous morphological variation that is maximally optimized for a given locomotor demand (Niklas, 1997, 1999, 2004; Marshall, 2014). Scaling of limb proportions in response to changes in body size can also affect functional indices, meaning that more diverse locomotor behaviors can be achieved for a given morphology at small body sizes (Jenkins et al, 1974; Janis and Martín-Serra, 2020; Weaver and Grossnickle, 2020; Wimberly et al, 2021), or that allometric patterns dominate shape change independent of locomotor behavior at larger sizes (Martín-Serra et al, 2014). Finally, while locomotor diversity in Carnivora is striking for a mammalian order, it does not span the full breadth of substrate use, locomotor specialization, or morphological diversity encompassed by sequentially higher-level groupings of mammals, such as Laurasiatheria, Boreoeutheria, or Placentalia, where patterns of shape variation associated with substrate use or behavior may be more discontinuous (Chen and Wilson, 2015; Janis and Martín-Serra, 2020; Weaver and Grossnickle, 2020).…”

“…Scaling of limb proportions in response to changes in body size can also affect functional indices, meaning that more diverse locomotor behaviors can be achieved for a given morphology at small body sizes (Jenkins et al, 1974; Janis and Martín-Serra, 2020; Weaver and Grossnickle, 2020; Wimberly et al, 2021), or that allometric patterns may dominate shape change independent of locomotor behavior at larger sizes (Martín-Serra et al, 2014), further clouding ecomorphological relationships in the post-cranial skeleton. Finally, while locomotor diversity in Carnivora is striking for a mammalian order, it does not span the full breadth of substrate use, locomotor specialization, or morphological diversity encompassed by sequentially higher-level groupings of mammals, such as Laurasiatheria, Boreoeutheria, or Placentalia, where patterns of shape variation associated with substrate use or behavior may be more discontinuous (Chen and Wilson, 2015; Janis and Martín-Serra, 2020; Weaver and Grossnickle, 2020). In other words, failure to detect early-burst like patterns at a given level of the phylogenetic hierarchy, such as in mammalian orders, does not preclude the possibility that a burst occurred at a higher level than the one sampled (Foote, 1996; Jablonski, 2017).…”

Incomplete convergence of gliding mammal skeletons*

“…We include scansorial taxa in our “arboreal” category because distinguishing arborealists and scansorialists is often difficult or subjective, especially for species of which little behavioral information is known (Nowak 1999). Further, arboreal and scansorial taxa are both tree‐dwelling and commonly possess very similar skeletal morphologies (e.g., Chen and Wilson 2015; Weaver and Grossnickle 2020). Thus, merging scansorial and arboreal taxa into a single locomotor category should not bias our results.…”

The mammalian forelimb diversity as a morphological gradient of increasing evolutionary versatility

“…Autopodial specialisations are also evident among smaller-sized mammals. For example, body size is positively associated with the tempo of evolution of postcranial morphology (hand and foot bones included) in both ground and tree dwelling animals, where medium-sized animals tend to exhibit higher stationary variances than small-sized species (Weaver and Grossnickle, 2020). Nevertheless, in both cases, functional specializations related to the locomotion likely played a role on driving the morphological evolution of the limb, potentially involved with the accelerated evolution of hand bone morphologies.…”