Bony labyrinth shape variation in extant Carnivora: a case study of Musteloidea

Abstract

The bony labyrinth provides a proxy for the morphology of the inner ear, a primary cognitive organ involved in hearing, body perception in space, and balance in vertebrates. Bony labyrinth shape variations often are attributed to phylogenetic and ecological factors. Here we use three-dimensional (3D) geometric morphometrics to examine the phylogenetic and ecological patterns of variation in the bony labyrinth morphology of the most species-rich and ecologically diversified traditionally recognized superfamily of Carnivora, the Musteloidea (e.g. weasels, otters, badgers, red panda, skunks, raccoons, coatis). We scanned the basicrania of specimens belonging to 31 species using high-resolution X-ray computed micro-tomography (μCT) to virtually reconstruct 3D models of the bony labyrinths. Labyrinth morphology is captured by a set of six fixed landmarks on the vestibular and cochlear systems, and 120 sliding semilandmarks, slid at the center of the semicircular canals and the cochlea. We found that the morphology of this sensory structure is not significantly influenced by bony labyrinth size, in comparisons across all musteloids or in any of the individual traditionally recognized families (Mephitidae, Procyonidae, Mustelidae). PCA (principal components analysis) of shape data revealed that bony labyrinth morphology is clearly distinguishable between musteloid families, and permutation tests of the Kmult statistic confirmed that the bony labyrinth shows a phylogenetic signal in musteloids and in most mustelids. Both the vestibular and cochlear regions display morphological differences among the musteloids sampled, associated with the size and curvature of the semicircular canals, angles between canals, presence or absence of a secondary common crus, degree of lateral compression of the vestibule, orientation of the cochlea relative to the semicircular canals, proportions of the cochlea, and degree of curvature of its turns. We detected a significant ecological signal in the bony labyrinth shape of musteloids, differentiating semi-aquatic taxa from non-aquatic ones (the taxa assigned to terrestrial, arboreal, semi-arboreal, and semi-fossorial categories), and a significant signal for mustelids, differentiating the bony labyrinths of terrestrial, semi-arboreal, arboreal, semi-fossorial and semi-aquatic species from each other. Otters and minks are distinguished from non-aquatic musteloids by an oval rather than circular anterior canal, sinuous rather than straight lateral canal, and acute rather than straight angle between the posterior and lateral semicircular canals - each of these morphological characters has been related previously to animal sensitivity for detecting head motion in space.

Comparative analysis of vestibular ecomorphology in birds

“…) and musteloid carnivorans (Grohé et al. ). Qualitative inferences of form–function relationships were also made for these groups.…”

“…As an illustration of the pitfalls of interpreting phylogenetic comparative results, note that Grohé et al. () reported evidence for differentiation of labyrinth morphologies among musteloid carnivorans with different ecologies (e.g. aquatic, terrestrial, fossorial) when using non‐phylogenetic statistical tests.…”

Bony labyrinth morphology in early neopterygian fishes (Actinopterygii: Neopterygii)

“…Beyond this systematic application, new data on inner ears have potential to shed light on additional aspects of early neopterygian biology. Semicircular canal morphology has been shown to correlate with functional and ecological specialisation in a great variety of tetrapod groups (e.g., charadriiform birds: Smith and Clarke, ; hominids: Spoor et al, ; mustelid nannaks: Grohé et al ; rodents: Pfaff et al, ; snakes: Yi and Norell, ). Few data exist to test this hypothesis in fishes, although Gauldie and Radtke () found evidence that the labyrinth morphology of the walking catfish Clarius fuscus , which is able to spend time on land, is more similar to those of terrestrial vertebrates than other fishes, suggesting that its inner ear shows adaptations toward a swaying (i.e., walking‐like) rather than undulatory (i.e., swimming‐like) gait.…”

Semicircular Canal Size and Locomotion in Colobine Monkeys: A Cautionary Tale

“…2 ) were constructed via manual segmentation in Avizo version 8 (Visualization Sciences Group, Burlington, Mass., USA). Although other parameters of vestibular morphology have been investigated [Pfaff et al, 2015;Grohé et al, 2016], the present study focuses on the radius of curvature (R) as a measure of canal size [Schmelzle et al, 2007]. R is derived from internal height and width measurements: height is measured from the protrusion of the ampulla at the lowest point of the canal to its maximum possible extent on the canal opposite, width was then determined as the maximum length line intersecting the height line at 90° ( fig.…”