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

Abstract

BackgroundMorphological diversity of limb bone lengths, diameters, and proportions in mammals is known to vary strongly with locomotor habit. It remains less well known how different locomotor habits are correlated with cross-sectional traits of the limb skeleton, such as cross-sectional area (CSA), second moments of area (SMA), and section modulus (MOD) and whether these traits have evolved adaptively. CSA and SMA represent the bone’s resistance to axial compression and bending, respectively, whereas MOD represents bone structural strength related to shape. Sampling 28 species of mustelids, a carnivoran lineage with diverse locomotor habits, we tested for differences in humeral, radial, and ulnar cross-sectional traits among specialists for climbing, digging, and swimming, in addition to generalists. Given that the limbs of digging specialists function in the dense substance of soil, and that swimming specialists need to counteract buoyancy, we predicted that these mustelids with these specializations should have the greatest values of cross-sectional traits.ResultsWe analyzed cross-sectional traits (calculated via μCT scanning and rendered dimensionless) in 5% increments along a bone’s length and found significant differences among locomotor habits, though differences in ulnar cross-sectional traits were fewer than those for the humerus and radius. Swimming specialists had the greatest values of cross-sectional traits, followed by digging specialists. Climbing specialists had the lowest values of cross-sectional traits. However, phylogenetic affinity underlies these results. Fitting models of trait evolution to CSA and SMA revealed that a multi-rate Brownian motion model and a multi-optima Ornstein-Uhlenbeck model are the best-fitting models of evolution for these traits. However, inspection of α-values uncovered that many of the OU models did not differ from a Brownian motion model.ConclusionsWithin Mustelidae, differences in limb function and locomotor habit influence cross-sectional traits in ways that produce patterns that may diverge from adaptive patterns exhibited by external traits (e.g., bone lengths) of the mammalian limb skeleton. These results suggest that not all the traits of a single organ evolve under a single evolutionary process and that models of trait evolution should be fit to a range of traits for a better understanding of the evolution of the mammalian locomotor system.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1349-8) contains supplementary material, which is available to authorized users.

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

“…Research performed on primates' long bone CSP indicated sturdier bones for arboreal species when compared to terrestrial ones (Kimura, 1991(Kimura, , 1995 and more robust femurs in non-anthropoid primates that tend to leap compared to those that avoid leaping (Demes & Jungers, 1993). Kilbourne and Hutchinson (2019) found less robust forelimb long bones in scansorial mustelids when compared to generalized, natatorial, and fossorial mustelids. In Sciuromorpha, we expected differences in CSP among all three lifestyle categories, with decreasing mean values from aerial to arboreal and finally fossorial species.…”

“…Here, we aimed to gain insight into the evolution of adaptations of the cross‐sectional properties (CSP) of the sciuromorph femur. For this purpose, we quantified them in 5% increments along the length of the bone following the approach of Doube et al (, ) and Kilbourne and Hutchinson (). The three CSP analyzed here are proxies of different uni‐ or multidimensional forces the bones experience (Ruff & Runestad, ; Schaffler, Burr, Jungers, & Ruff, ).…”

“…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).…”

“…Here, we aimed to gain insight into the evolution of adaptations of the cross-sectional properties (CSP) of the sciuromorph femur. For this purpose, we quantified them in 5% increments along the length of the bone following the approach of Doube et al (2009Doube et al ( , 2018 and Kilbourne and Hutchinson (2019).…”

Trabecular bone architecture in the stylopod epiphyses of mustelids (Mammalia, Carnivora)

“…Mustelidae are a carnivoran lineage exhibiting a diversity of locomotor habits. Specifically among mustelids, three main locomotor specializations can be defined [7,8]: badgers are fossorial, featuring specialized digging skills; martens are scansorial, as they are preponderantly found climbing; otters are natatorial, being skilful swimmers. In addition to these three specializations, weasels exhibit a more generalized locomotor habit.…”