Cetaceans, the clade comprising whales, dolphins, and porpoises, represents one of the most emblematic group of living mammals. Besides their status of “ambassadors of the seas”, it is quite remarkable that about 53 million years ago their terrestrial ancestors started a major ecological transition back into the aquatic realm, later giving rise to the most diverse group of extant fully aquatic mammals. This land-to-water transition involved a transition from a limb-based mode of locomotion on land to an axial-powered locomotion relying on oscillations of the body and underlying backbone. This was accompanied by deep modifications of their body plan such as the reduction of hindlimbs, the acquisition of pectoral, dorsal, and caudal fins, and migration of the nares on top of their skull, leading to a fish-like body shape.
The land-to-water transition also had drastic impacts on the vertebral column as the cetacean backbone seems more homogenous in shape compared to the vertebral column of terrestrial mammals which is composed of several well-defined regions (cervical, pectoral, anterior and posterior thoracic, lumbar, sacral, caudal) (see this Science paper from my co-authors), notably due to the loss of a well-defined sacral region. In addition to this apparent “de-regionalization” of the backbone, the vertebral counts of cetaceans vary broadly across species – ranging from 42 to 97 vertebrae – compared to terrestrial species, making the transposition of traditional mammalian vertebral regions to the cetacean backbone challenging. Because of this, the pattern of regionalization (or lack thereof) of the cetacean backbone has been a long-standing issue limiting our ability to compare their vertebral features with those of terrestrial mammals.
Fig.1. Vertebral regions in terrestrial mammals as identified by previous studies and in cetaceans based on our segmented linear regression and spectral clustering approach. The cetacean backbone is made of up to six homologous post-cervical modules (represented by different colors), with each module composed of one to four regions (represented by different color shades) depending on the species. Mouse model modified from artwork by April Isch Neander.
To tackle this question, we took advantage of the morphological dataset of cetacean backbone I built during my PhD (which I conducted at the University of Liège in Belgium) by visiting the collections of numerous museums of natural history in Europe, South Africa and USA. The final dataset for this study comprises measurements on more than 7,500 vertebrae of 62 extant species (about two-thirds of the extant diversity of cetaceans). Because the number of vertebrae varies a lot across species, we could not rely on traditional covariance methods to identify vertebral regions. Instead we used a segmented linear approach which has been used in snakes and terrestrial mammals before. For each specimen individually, the method models regions as gradients and identifies region boundaries as changes in these gradients without requiring a priori information on the final number of regions or the position of their boundaries. However, because of the large size of our dataset, the code would take weeks (or simply crash!) to run a on a computer cluster. We therefore collaborated with Noah Greifer from the Harvard’s Institute for Quantitative Social Science (IQSS) to re-write and streamline the code which now runs in a few minutes on a laptop and is publicly available as the MorphoRegions R-package on CRAN. Because we found some variability in the number of regions across species, we then input the morphological data of all our specimens in a single spectral clustering analyses to homologize regions across species.
Contrary to the common belief – and to our expectations – the cetacean backbone is still highly regionalized as we found between six and nine post-cervical regions. Thanks to the spectral clustering, we could group these regions into six different modules homologous across cetaceans: anterior thoracic, thoraco-lumbar, posterior lumbar (only present in some dolphins and porpoises), caudal, peduncle, and fluke. These modules and regions do not match the regions found in terrestrial mammals, indicating that the cetacean backbone has been repatterned during the land-to-water transition. For instance, we did not find a distinct sacral region but we found numerous regions in the tail, which are most likely associated to their axial-powered aquatic locomotion. Each of the modules can be attributed to either the precaudal segment of the backbone (i.e., all the vertebrae anterior to the tail) or the caudal segment (vertebrae in the tail). We therefore named our regionalization model the “Nested Regions” hypothesis as the backbone can be divided into a precaudal and caudal segment, each of which divided into several modules, which can be further divided into regions.
Fig.2. Offshore dolphins and porpoises living in the open ocean tend to have more vertebrae and higher regionalization levels and can reach higher swimming speeds compared to riverine species living in shallow waters.
Due to the variation in the number of regions across species, we then investigated the impact of the number of vertebrae on the regionalization level. In addition, since the backbone is central to cetacean locomotion, we also examined the link between regionalization and ecology by gathering data from the literature on the habitat of each species (i.e., if species live closer or further away from the shores) and their swimming speeds. We found that offshore dolphins and porpoises with numerous vertebrae tend to have more regions and can reach higher swimming speeds than riverine species which have fewer vertebrae. This suggests that increased vertebral counts allows for the differentiation into more numerous regions which could allow to better restrict swimming movements to specific parts of the backbone and improve hydrodynamics in comparison to riverine species which are slower but require increased maneuverability in more shallow and complex environments.
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Cover image: Common dolphin off the coast of Australia. ©Amandine Gillet.