Small- to medium-sized mammals show greater morphological disparity in cervical than lumbar vertebrae across different terrestrial modes of locomotion

Abstract

During mammalian terrestrial locomotion, body flexibility facilitated by the vertebral column is expected to be correlated with observed modes of locomotion, known as gait (e.g., sprawl, trot, hop, bound, gallop). In small- to medium-sized mammals (average weight up to 5 kg), the relationship between locomotive mode and vertebral morphology is largely unexplored. Here we studied the vertebral column from 46 small- to medium-sized mammals. Nine vertebrae across cervical, thoracic, and lumbar regions were chosen to represent the whole vertebral column. Vertebra shape was analysed using three-dimensional geometric morphometrics with the phylogenetic comparative method. We also applied the multi-block method, which can consider all vertebrae as a single structure for analysis. We calculated morphological disparity, phylogenetic signal, and evaluated the effects of allometry and gait on vertebral shape. We also investigated the pattern of integration in the column. We found the cervical vertebrae show the highest degree of morphological disparity, and the first thoracic vertebra shows the highest phylogenetic signal. A significant effect of gait type on vertebrae shape was found, with the lumbar vertebrae having the strongest correlation; but this effect was not significant after taking phylogeny into account. On the other hand, allometry has a significant effect on all vertebrae regardless of the contribution from phylogeny. The regions showed differing degrees of integration, with cervical vertebrae most strongly correlated. With these results, we have revealed novel information that cannot be captured from study of a single vertebra alone: although the lumbar vertebrae are the most correlated with gait, the cervical vertebrae are more morphologically diverse and drive the diversity among species when considering whole column shape.

Keywords: allometry; axial skeleton; gait; geometric morphometrics; regularised consensus principal component analysis.

FIGURE 1

Phylogenetic tree of the 46 species studied herein, with detail about their average body weight. Time scale for branch lengths is in millions of years. Pruned in vertlife.org, from Upham et al. (2019a, 2019b). The three clades of mammals are represented by symbols: Monotremata (triangle), Marsupialia (square), and Placental (circle). Fast‐gaits are represented by colours: sprawl (black), trot (pink), bound (blue), hop (green), and gallop (orange). The same symbols and colours scheme are used throughout.

FIGURE 2

A hare's (Lepus europaeus) vertebral column as a representative showing the vertebrae studied herein. (a) Nine vertebrae considered in this study are highlighted. The landmarking scheme on the (b) atlas, (c) axis, and (d) lumbar at one‐third position (L1/3), in cranial, left lateral, and caudal views (left to right). The description of each landmark is provided in Appendix 2: Table A2.

FIGURE 3

Phylomorphospace represented by the first three global components (GCs) from a regularised consensus principal components analysis (RCPCA). (A) GC1 and GC2, (B) GC1 and GC3. Symbols identify evolutionary clade, and colours identify different gaits. Sizes of the symbol reflect average size of the species: Monotremata (triangle), Marsupialia (square), and Placental (circle). Fast‐gaits are represented by colours: sprawl (black), trot (pink), bound (blue), hop (green), and gallop (orange). The symbols with dotted outline adjacent to the silhouettes show representative species for reference: Notomys mitchellii (NM), Bettongia lesueur (BL), Lepus europaeus (LE), Vombatus ursinus (VU), Setonix brachyurus (SB), Mustela putorius (MP), Canis latrans (CL), and Tachyglossus aculeatus (TA), Viverricula indica (VI), Isoodon macrourus (IM), and Dasyurus viverrinus (DV). Note that all nodes are in the predicted position as inferred from the time‐calibrated phylogeny, and are used for illustration purposes only. The silhouettes are sourced from phylopic.org and are under the public domain, except: SB by T. Michael Keesey (photo by Sean Mack) (https://creativecommons.org/licenses/by‐sa/3.0/); and DV by Gabriela Palomo‐Munoz (https://creativecommons.org/licenses/by‐nc/3.0/).

FIGURE 4

Shape variation of the nine vertebrae depicted by four species selected to represent the minima and maxima of global components (GC)1 and GC2 of the consensus space: Notomys mitchellii, Viverricula indica, Tachyglossus aculeatus, and Isoodon macrourus, respectively. A wireframe of each vertebra is shown in cranio‐left‐lateral view, with a representative vertebra from Lepus europaeus for reference. Images not to scale.

FIGURE 5

Procrustes ANOVA of each vertebra and the whole column for the factors (a) size (allometry), and (b) gait. The coefficient of determination (R ²) values from ordinary least squares (OLS) and phylogenetic generalised least squares (PGLS) models are plotted. The grey highlighted areas are significant R ² values from the regression.

FIGURE 6

Morphological disparity (Procrustes variance) and phylogenetic signal (K _mult) for each vertebra.

FIGURE 7

A heatmap of standardised Mantel's correlation coefficients between each pair of vertebrae or between each vertebra and the whole column. The correlations were calculated from the phylomorphospace containing (a) only placentals, (b) only marsupials, and (c) all taxa. Darker shades indicate a higher degree of similarity in the morphospace occupation of species given by the respective pair of vertebrae.

FIGURE 8

Shape variation of the nine vertebrae depicted by two species selected to represent the negative and positive ends of global component (GC) 3 of the consensus space: Dasyurus viverrinus and Setonix brachyurus, respectively. A wireframe of each vertebra is shown in cranio‐left‐lateral view, with a representative vertebra from Lepus europaeus for reference. Images not to scale.

FIGURE 9

Phylomorphospace of each vertebra from principal component analysis. The numbers correspond to the species list in Appendix 1: Table A1. The three clades of mammals are represented by symbols: Monotremata (triangle), Marsupialia (square), and Placental (circle). Fast‐gaits are represented by colours: sprawl (black), trot (pink), bound (blue), hop (green), and gallop (orange). Note that all nodes are in the predicted position as inferred from the time‐calibrated phylogeny, and are used for illustration purposes only.

FIGURE 10

Shape variation of the nine vertebrae predicted at the minima and maxima of principal component (PC) 1, PC2, and PC3 of each vertebra morphospace. A wireframe of each vertebra is shown in cranio‐left‐lateral view, with a representative vertebra from Lepus europaeus for reference. Images not to scale.