Selective regimes and functional anatomy in the mustelid forelimb: Diversification toward specializations for climbing, digging, and swimming

Abstract

Anatomical traits associated with locomotion often exhibit specializations for ecological niche, suggesting that locomotor specializations may constitute selective regimes acting on limb skeletal traits. To test this, I sampled 42 species of Mustelidae, encompassing climbing, digging, and swimming specialists, and determined whether trait variation reflects locomotor specialization by performing a principal components analysis on 14 forelimb traits. In addition to Brownian motion models, three Ornstein–Uhlenbeck models of selective regimes were applied to PC scores describing trait variation among mustelids: one without a priori defined phenotypic optima, one with optima based upon locomotor habit, and one with a single phenotypic optimum. PC1, which explained 43.8% of trait variance, represented a trade‐off in long bone gracility and deltoid ridge length vs. long robustness and olecranon process length and distinguished between climbing specialists and remaining mustelids. PC2, which explained 17.4% of trait variance, primarily distinguished the sea otter from other mustelids. Best fitting trait diversification models are selective regimes differentiating between scansorial and nonscansorial mustelids (PC1) and selective regimes distinguishing the sea otter and steppe polecat from remaining mustelids (PC2). Phylogenetic half‐life values relative to branch lengths suggest that, in spite of a strong rate of adaptation, there is still the influence of past trait values. However, simulations of likelihood ratios suggest that the best fitting models are not fully adequate to explain morphological diversification within extant mustelids.

Morphological diversification of biomechanical traits: mustelid locomotor specializations and the macroevolution of long bone cross-sectional morphology

“…The low values of cross-sectional traits of the forelimb skeleton in scansorial mustelids correspond to the greater gracility of their forelimb skeleton [27, 53] and the relatively elongate and lightweight limbs of scansorial mammals in general [51, 52]. The gracile and elongate forelimb skeleton of martens, though not as extreme as in other scansorial carnivorans [64], likely confers advantages in bridging discontinuities in supports (e.g., tree branches) while climbing [13].…”

“…An exception to the general trend among otters is the small-clawed otter ( Amblonyx cinereus ), which lies comfortably in the range of scansorial mustelids. Notably, this species possesses rather gracile long bones more comparable to scansorial mustelids [27, 53] than to other otters, with its humerus further lacking the strong anterior bowing characteristic of other otters ([9]; pers. obs.).…”

“…Specializations in mammalian limb morphology are well documented and have been the subject of study for more than a century [21, 33, 66, 75, 91], with these studies primarily focusing on bone lengths, diameters, and the in-levers of muscles [9, 10, 12, 23, 27, 28, 39, 40, 53, 69, 78, 84, 87, 88, 97]. Notably, differing locomotor habits within mammals are associated with distinct limb morphologies.…”

“…For instance, the functioning of fossorial limbs in soil should be associated with higher values of CSA, SMA, and MOD due to the high density of soil (1.83–2.58 g/cm 3 ; [85]). Notably, limbs specialized for digging have longer in-levers for stronger joint extension and often long bones with more robust external dimensions [22, 23, 53, 78, 84]. Similarly, the limbs of natatorial taxa are also associated with a greater robustness and more prominent in-levers [9, 78], and greater values of bone cross-sectional traits could also be beneficial to mitigating larger mechanical loads due to functioning in water, which also has a high density.…”

The evolution of femoral cross‐sectional properties in sciuromorph rodents: Influence of body mass and locomotor ecology

“…Furthermore, different substrate textures (e.g., branches vs. dirt) appear to also impact the properties of bones (Polk et al, 2000). Morphological correlates to these differing functional demands, which are posed during the locomotion in a specific habitat, therefore often have been identified in several tetrapod lineages (Botton-Divet, Cornette, Fabre, Herrel, & Houssaye, 2016;Burr et al, 1989;Doube et al, 2018;Kilbourne, 2017;Kilbourne & Hutchinson, 2019;Kimura, 1991Kimura, , 1995Polk et al, 2000;Polly, 2007).…”