Serial disparity in the carnivoran backbone unveils a complex adaptive role in metameric evolution

Abstract

Organisms comprise multiple interacting parts, but few quantitative studies have analysed multi-element systems, limiting understanding of phenotypic evolution. We investigate how disparity of vertebral morphology varies along the axial column of mammalian carnivores — a chain of 27 subunits — and the extent to which morphological variation have been structured by evolutionary constraints and locomotory adaptation. We find that lumbars and posterior thoracics exhibit high individual disparity but low serial differentiation. They are pervasively recruited into locomotory functions and exhibit relaxed evolutionary constraint. More anterior vertebrae also show signals of locomotory adaptation, but nevertheless have low individual disparity and constrained patterns of evolution, characterised by low-dimensional shape changes. Our findings demonstrate the importance of the thoracolumbar region as an innovation enabling evolutionary versatility of mammalian locomotion. Moreover, they underscore the complexity of phenotypic macroevolution of multi-element systems and that the strength of ecomorphological signal does not have a predictable influence on macroevolutionary outcomes.

Intravertebral vs. intervertebral integration and modularity in the vertebral column of mammalian carnivorans

“…On the other hand, the integration strength between the centrum and the neural spine of the boundary vertebrae, especially those of the diaphragmatic boundary, is lower than for those located within intervertebral modules (Figure 5–7, Figures S2–S4). This weaker intravertebral integration could be related to their low across‐species disparities and high evolutionary constraints (Figueirido et al, 2021).…”

“…All diaphragmatic vertebrae are joined together regardless of their position, and the remaining vertebrae are established as pre‐ and post‐diaphragmatic in cranial and caudal directions. We did not use the selected vertebrae procedure described by Jones, Benitez, et al (2018) and applied by Martín‐Serra et al (2021) and Figueirido et al (2021) because we were interested in testing the association between intravertebral and intervertebral integration. The procedure of Jones, Benitez, et al (2018) analyzed a phylogenetically wider dataset (52 mammalian species) with variation in count across taxa, but they solely used five thoracolumbar vertebrae for which homology across species was clear.…”

“…This was interpreted by Martín‐Serra et al (2021) as related to the ability to move excessively that characterizes the ‘Diaphragmatic joint complex’ (Filler, 1986; Flower, 1885; Slijper, 1946). This reorganization of vertebral column regions has been linked to different locomotor strategies and, therefore, it probably reflects the action of natural selection towards different locomotory demands (e.g., Jones, Benitez, et al, 2018; Randau & Goswami, 2017b; Martín‐Serra et al, 2021; Figueirido et al, 2021).…”

“…However, recent studies on evolutionary integration and modularity among presacral vertebrae in different mammalian species, including carnivorans, demonstrate that their organization into modules, i.e., sets of tightly integrated vertebrae that are relatively independent of other vertebral sets, does not match the classic morphological regions (e.g., Buchholtz, 2007;Randau & Goswami, 2017a, 2017bJones, Benitez, et al, 2018;Jones et al, 2020;Martín-Serra et al, 2021;Smith and Angielzyk, 2022).…”

Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time

“…This can also manifest theoretical combinations of developmental variables with the potential to answer how much variation in the organization of the tetrapod body-axis has been explored by organic evolution ( figure 2 a ). Different methods have been developed to study and quantify patterns of morphospace occupation [ 37 – 39 ] and phylomorphospaces [ 40 ] allowing to ascertain the evolutionary path of target lineages, including morphological convergence [ 41 ].

Figure 2 Schematic workflow (divided in three interconnected blocks) for testing competing hypotheses on developmental and functional triggers of evolutionary convergence in the tetrapod body-axis.

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