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.

Keywords: Musteloidea; allometry; inner ear; locomotion; morphology; phylogeny; semilandmark sliding; three-dimensional geometric morphometrics.

Figure 1

Right bony labyrinth of Lontra canadensis (Lutrinae, Mustelidae): (A) Line drawing of the labyrinth in anterolateral view, illustrating the main anatomical structures referred to in this study, and (B‐D) location of 3D landmarks and sliding semilandmarks, illustrating the dataset used for the musteloid sample in this study (see Table 2 for definition of the landmarks). (B) Anterolateral view. (C) Posterolateral view. (D) Anteromedial view. aam, anterior ampulla; asc, anterior semicircular canal; cc, common crus; co, cochlea; fc, fenestra cochleae (= round window); fv, fenestra vestibuli (= oval window); lam, lateral ampulla; lsc, lateral semicircular canal; pam, posterior ampulla; psc, posterior semicircular canal; vb, vestibule.

Figure 2

3D reconstructions of the right bony labyrinth for each species of the musteloid sample studied, figured in anterior view. Specimen numbers can be found in Table 1. For species represented by two individuals we illustrate only one: Spilogale putorius AMNH 35207; Mephitis mephitis MNHN MO 2005‐655; Ailurus fulgens AMNH 185436; Potos flavus AMNH 239990; Nasua nasua UM 141N; Procyon lotor UM 091N; Taxidea taxus MNHN MO 1895‐417; Gulo gulo MNHN MO 1873‐39; Enhydra lutris AMNH 24186; Lutra lutra UPPal M02.5.005 (see Table 1 caption for institutional abbreviations). Bony labyrinths are not shown to scale. dors, dorsal; lat, lateral

Figure 3

Phylogenetic tree topology used for this study. Branch lengths equal to 1. Respective ecological categories are provided for each species following Nowak (2005) and Helgen et al. (2013; for Bassaricyon pauli). Clades tested in the statistical analyses are numbered in grey (see Tables 5 and 6).

Figure 4

Principal components analyses (PCA) based on the mean 3D Procrustes coordinates for each species, obtained by semilandmark sliding using minimum Procrustes distance (A,B) and minimum bending energy (C,D) criteria. The first three axes of each PCA are displayed: (A,C) PC1 and PC2, (B,D) PC1 and PC3. Bony labyrinth morphospaces of families are outlined by grey polygons. Triangle: Mephitidae; Square: Procyonidae; Star: Ailuridae; Circle: Mustelidae.

Figure 5

Visualizations of shape changes in Musteloidea using 3D warped bony labyrinth surfaces for the first three axes of the PCA (see Fig. 3). Each warped bony labyrinth surface is represented in posterolateral, anterolateral and dorsal views, from top to bottom. (A) Minimum Procrustes distance criterion; (B) minimum bending energy criterion. Arrows indicate the accentuated variation from (A) to (B) for PC2 and PC3. lat, lateral; post, posterior; ventr, ventral.

Figure 6

Phylomorphospace of the mean bony labyrinths for each species of Musteloidea. Individuals are colored by ecological habitus (red, semi‐fossorial; blue, semi‐aquatic; brown, terrestrial; light green, arboreal; dark green, semi‐arboreal). (A,B) Minimum Procrustes distance criterion. (C,D) Minimum bending energy criterion.

Figure 7

Mean shape of non‐aquatic musteloids (A) and aquatic musteloids (B) in anterolateral (top) and posterolateral (bottom) views. Arrows indicate the location of the morphological differences between the mean shapes.