Repatterning of mammalian backbone regionalization in cetaceans

Abstract

Cetacean reinvasion of the aquatic realm is an iconic ecological transition that led to drastic modifications of the mammalian body plan, especially in the axial skeleton. Relative to the vertebral column of other mammals that is subdivided into numerous anatomical regions, regional boundaries of the cetacean backbone appear obscured. Whether the traditional mammalian regions are present in cetaceans but hard to detect due to anatomical homogenization or if regions have been entirely repatterned remains unresolved. Here we combine a segmented linear regression approach with spectral clustering to quantitatively investigate the number, position, and homology of vertebral regions across 62 species from all major cetacean clades. We propose the Nested Regions hypothesis under which the cetacean backbone is composed of six homologous modules subdivided into six to nine post-cervical regions, with the degree of regionalization dependent on vertebral count and ecology. Compared to terrestrial mammals, the cetacean backbone is less regionalized in the precaudal segment but more regionalized in the caudal segment, indicating repatterning of the vertebral column associated with the transition from limb-powered to axial-driven locomotion.

Fig. 1. Mammalian (a) and cetacean (b-e) backbone regionalization hypotheses.

a Vertebral regions in terrestrial mammals. Presacral regions as identified by Jones et al. and caudal regions as identified in New World Monkeys. Proxi.: proximal, Transi.: transitional. Modified from artwork by April Neander. b Subdivision between precaudal (cervical, thoracic, and lumbar in c) and caudal (caudal and fluke in c) segments. c. Traditional mammalian anatomical regions transposed onto the cetacean backbone following Rommel. Thoracic vertebrae bear ribs and caudal vertebrae bear chevrons. Fluke vertebrae are dorso-ventrally flattened. d Cetacean-specific regionalization pattern from Buchholtz^,. The general cetacean backbone is divided into neck, chest, torso, tail stock, and fluke regions, with the torso further subdivided into anterior, mid, and posterior in more derived oceanic dolphins. e Nested Regions hypothesis based on segmented linear regression and clustering analyses in this study. Vertebrae are colour-coded according to the six modules homologous across cetaceans, with the posterior lumbar module being present only in some oceanic dolphins and porpoises. Each module is composed of one to four morphological regions depending on the species, which are represented by different colour shades. For all panels, the grey bar under anterior vertebrae indicates rib-bearing vertebrae. See also Supplementary Fig. 1.

Fig. 2. Vertebral morphospace (a, b) and regionalization map (c).

Common morphospace of all vertebrae from all specimens derived through a principal coordinates analysis (a: PCOs 1 and 2, b: PCOs 2 and 3), with vertebrae colour-coded by the six modules recovered by spectral clusting analysis (anterior thoracic, thoraco-lumbar, posterior lumbar, caudal, peduncle, and fluke). Grey curves represent the average path from the first to the last vertebra of the backbone for specimens with (dashed line) and without (solid line) a posterior lumbar module. c. Vertebral maps showing regions obtained from segmented linear regressions grouped by homologous modules from spectral clustering analysis. Different modules are represented by different colours while regions are represented by different shades. Phylogeny adapted from ref. . See Supplementary Fig. 4 for common morphospace variable loadings, Supplementary Fig. 5 for position of anterior thoracic module boundary relative to anatomical landmarks and terrestrial mammals, and Supplementary Fig. 6 for variation in vertebral centrum shape across modules. Source data are provided as a Source Data file.

Fig. 3. Cetacean phylogenetic tree with mapped region score (left) and vertebral disparity (right).

Region score represents the level of regionalization (weighted average number of regions) of the backbone taking into consideration the fact that multiple models with different numbers of regions might fit the data well. Disparity corresponds to the average Euclidean distance between successive vertebrae along the backbone based on PCO scores from axes 1 to 3 of the common morphospace (see Fig. 2a, b). Oceanic dolphins and porpoises have the highest region scores but the lowest morphological disparity while river dolphins and beaked whales have high vertebral disparity but the lowest regionalization scores. Phylogeny adapted from ref. . See Supplementary Data 3 for detailed region score and disparity values per species. Source data are provided as a Source Data file.

Fig. 4. Effect of vertebral count on regionalization and disparity.

The average number of regions is higher in the caudal segment of the backbone compared to the precaudal segment (b) despite similar number of vertebrae in each segment (a). In b, dot size is proportional to the number of vertebrae in the whole backbone. Phylogenetically-corrected linear regressions indicating significant increase in regionalization level (c) and significant decrease in disparity (d) with increasing vertebral count in each segment. Dots and regression lines are colour-coded by segment (whole backbone: blue, precaudal: sand, caudal: teal). See Supplementary Table 1 for detailed results of the linear regressions. Source data are provided as a Source Data file.

Fig. 5. Correlations between vertebral morphology, habitat, and swimming speed.

a, b Based on phylogenetically-corrected ANOVAs, habitat has a significant effect on region score (P = 0.009) and disparity (P < 0.001). Riverine species, which have lower vertebral counts, tend to have lower regionalization levels (a) but higher morphological disparity between successive vertebrae (b). Species (black dots) were divided in four habitat categories: rivers and bays (n = 7), coasts (n = 11), mixed (n = 8), and offshore (n = 36). For each habitat category, median (center line), first and third quartiles (box limits), and 1.5x interquartile range (whiskers). c. Phylogenetically-corrected linear regressions between region score and swimming speed show that species with higher vertebral regionalization levels can achieve higher speeds during burst swimming (blue line and dots), with porpoises and oceanic dolphins (circles) achieving higher speeds than other families (triangles). In contrast, there is no significant relationship between regionalization and sustained swimming speed (green line and dots). P-values and R² of the phylogenetically-corrected linear regressions are presented for each type of swimming speed. See also Supplementary Tables 2 and 3 for detailed results. Source data are provided as a Source Data file.