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.

Highlights

  • Scansorial/climbing mammals are characterized by limb skeletons with relatively elongate and gracile elements both proximally and distally, including elongate digits, whereas cursorial/running mammals are characterized by limb skeletons with gracile elements and elongate distal limb elements

  • For the humerus, radius, and ulna, long bone cross-sectional traits significantly differed among mustelid locomotor habits

  • Cross-sectional morphology and biomechanical advantage Our results demonstrate that the cross-sectional morphology of long bones can differ among specialized locomotor habits in Mustelidae, a functionally diverse and speciose lineage within Carnivora

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Summary

Introduction

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]. Fossorial/ digging mammals are characterized by more robust and relatively shorter long bones (for shorter muscle out-levers) and longer muscle in-levers (e.g., olecranon process), some of which exhibit large tuberosities (e.g., the deltoid ridge/tuberosity). Morphological 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. 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

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