Anatomical diversification of a skeletal novelty in bat feet

Abstract

Neomorphic, membrane‐associated skeletal rods are found in disparate vertebrate lineages, but their evolution is poorly understood. Here we show that one of these elements—the calcar of bats (Chiroptera)—is a skeletal novelty that has anatomically diversified. Comparisons of evolutionary models of calcar length and corresponding disparity‐through‐time analyses indicate that the calcar diversified early in the evolutionary history of Chiroptera, as bats phylogenetically diversified after evolving the capacity for flight. This interspecific variation in calcar length and its relative proportion to tibia and forearm length is of functional relevance to flight‐related behaviors. We also find that the calcar varies in its tissue composition among bats, which might affect its response to mechanical loading. We confirm the presence of a synovial joint at the articulation between the calcar and the calcaneus in some species, which suggests the calcar has a kinematic functional role. Collectively, this functionally relevant variation suggests that adaptive advantages provided by the calcar led to its anatomical diversification. Our results demonstrate that novel skeletal additions can become integrated into vertebrate body plans and subsequently evolve into a variety of forms, potentially impacting clade diversification by expanding the available morphological space into which organisms can evolve.

Variation in cross‐sectional shape and biomechanical properties of the bat humerus under Wolff's law

“…Combining three‐dimensional comparative morphology and functional biomechanics, this study represents a novel approach to investigate the correspondence between the ecological and biological drivers shaping humeral variation, by deconstructing its biomechanical and morphological components. Our results showed a link between phenotypic variation and foraging and behavioral differences between taxa, corresponding with previous studies both in bats (Arbour et al, 2019) and a wide variety of other vertebrates (Arbour et al, 2019; Esquerré, Sherratt, & Keogh, 2017; Maestri et al, 2017; Pimiento, Cantalapiedra, Shimada, Field, & Smaers, 2019; Stanchak, Arbour, & Santana, 2019; Stange, Aguirre‐Fernandez, Salzburger, & Sanchez‐Villagra, 2018). Our findings of differences in shape and biomechanics of the humerus supports the general notion of Wolff's law of bone functional adaptation (Ruff, Holt, & Trinkaus, 2006; Wolff, 1986), contrary to common allometric trajectories found in crocodylians (Meers, 2002).…”

Differing effects of size and lifestyle on bone structure in mammals

“…All subsequent data acquisition was performed with the software Fiji/ImageJ (Schindelin et al, 2012) (2.0). Many studies have quantified bone structure traits for long bones, and we will focus on three parameters for the humerus: CSS, DE, and mean Cg, which can be argued to reflect torsional and bending loads for the former two, as well as compressive loads (terrestrial locomotion) and buoyancy (aquatic locomotion) for the latter (Houssaye and Botton-Divet, 2018; Kilbourne and Hutchinson, 2019; Stanchak et al, 2019; Swartz et al, 1992). CSS –the ratio of maximum and minimum second moment of area (Ruff and Hayes, 1983)– was acquired at midshaft (plug-in Slice Geometry , BoneJ v. 1.4.; Doube et al, 2010).…”

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

“…(2010); Slater and Friscia (2019); Stanchak et al. (2019), while support for diversification on a rugged adaptive landscape has been recovered in some clades (e.g., Benson et al., 2018; Godoy et al., 2019; Mahler et al., 2013; Mongiardino Koch, 2021) but not in others (Law et al., 2019).…”