Phenotypic integration in the carnivoran backbone and the evolution of functional differentiation in metameric structures

Abstract

Explaining the origin and evolution of a vertebral column with anatomically distinct regions that characterizes the tetrapod body plan provides understanding of how metameric structures become repeated and how they acquire the ability to perform different functions. However, despite many decades of inquiry, the advantages and costs of vertebral column regionalization in anatomically distinct blocks, their functional specialization, and how they channel new evolutionary outcomes are poorly understood. Here, we investigate morphological integration (and how this integration is structured [modularity]) between all the presacral vertebrae of mammalian carnivorans to provide a better understanding of how regionalization in metameric structures evolves. Our results demonstrate that the subunits of the presacral column are highly integrated. However, underlying to this general pattern, three sets of vertebrae are recognized as presacral modules—the cervical module, the anterodorsal module, and the posterodorsal module—as well as one weakly integrated vertebra (diaphragmatic) that forms a transition between both dorsal modules. We hypothesize that the strength of integration organizing the axial system into modules may be associated with motion capability. The highly integrated anterior dorsal module coincides with a region with motion constraints to avoid compromising ventilation, whereas for the posterior dorsal region motion constraints avoid exceeding extension of the posterior back. On the other hand, the weakly integrated diaphragmatic vertebra belongs to the “Diaphragmatic joint complex”—a key region of the mammalian column of exceedingly permissive motion. Our results also demonstrate that these modules do not match with the traditional morphological regions, and we propose natural selection as the main factor shaping this pattern to stabilize some regions and to allow coordinate movements in others.

Phenotypic regionalization of the vertebral column in the thorny skateAmblyraja radiata: Stability and variation

“…Data on transitional vertebrae in mammals include few vertebrae and the number of vertebrae involved display very little inter‐individual variation. Indeed, four transitional vertebrae are reported between the cervical and thoracic modules in Felidae (Randau & Goswami, 2017), two are observed between the thoracic and lumbar regions in the domestic cat Felis catus (Macpherson & Ye, 1998), while antero‐dorsal and postero‐dorsal modules (including thoracolumbar vertebrae 1–10 and 12–20, respectively) are separated by one vertebra in Carnivora (Martín‐Serra et al, 2021), and one and two transitional vertebrae are mentioned, respectively, between the thoracic and lumbar, and lumbar and caudal regions in the Florida manatee Trichechus manatus (Buchholtz et al, 2007). In teleosts, however, the number of transitional vertebrae between the abdominal and the caudal regions depends on the species and shows inter‐individual variation.…”

“…Increasing knowledge about the morphological disparity of vertebrae and vertebral columns can thus significantly contribute to our understanding of evolutionary trends among vertebrates (Arratia et al, 2001;Buchholtz, 2007;Johanson et al, 2013;Jones et al, 2020;Martín-Serra et al, 2021;Oulion et al, 2011;Sallan, 2012).…”

“…However, more recent studies on axial regionalization highlighted the relationships between morphological traits of vertebral regions and anteroposterior gene expression patterns during development (Krumlauf, 1994; Burke et al, 1995; Wellik, 2007; Oulion et al, 2011; Head & Polly, 2015; Johanson et al, 2019). The regionalization of the vertebral column also correlates with life history traits as well as with functional adaptations; accordingly, it is shaped by the mode of life of a species (Buchholtz, 1998; Randau et al, 2016; Jones et al, 2020; Martín‐Serra et al, 2021).…”

“…Vertebrae are among the main vertebrate evolutionary novelties and have been conserved for more than 400 million years (Janvier, 1996). Increasing knowledge about the morphological disparity of vertebrae and vertebral columns can thus significantly contribute to our understanding of evolutionary trends among vertebrates (Arratia et al, 2001; Buchholtz, 2007; Johanson et al, 2013; Jones et al, 2020; Martín‐Serra et al, 2021; Oulion et al, 2011; Sallan, 2012). The vertebral column is the main skeletal support of the anteroposterior body axis of vertebrates and provides anatomical cohesion between the cranium and appendages.…”

A Shrewd Inspection of Vertebral Regionalization in Large Shrews (Soricidae: Crocidurinae)

“…We therefore assume that there is some developmental and phylogenetic signature in the gross morphology of mammalian vertebrae (e.g., Asher et al. 2011 ; Jones 2015 ; Kivell 2016 ; Martín-Serra et al. 2021 ; Figueirido et al.…”