Evolutionary rates and shape variation along the anuran vertebral column with attention to phylogeny, body size, and ecology

Abstract

The vertebral column is critical to a vertebrate species' flexibility and skeletal support, making vertebrae a clear target for selection.Anurans (frogs and toads) have a unique, truncated vertebral column that appears constrained to provide axial rigidity for efficient jumping. However, no study has examined how presacral vertebrae shape varies among anuran species at the macroevolutionary scale nor how intrinsic (developmental and phylogenetic) and extrinsic (ecological) factors may have influenced vertebrae shape evolution. We used microCT scans and phylogenetic comparative methods to examine the vertebrae of hundreds of anuran species that vary in body size as well as adult and larval ecology. We found variation in shape and evolutionary rates among anuran vertebrae, dispelling any notion that trunk vertebrae evolve uniformly. We discovered the highest evolutionary rates in the cervical vertebrae and in the more caudal trunk vertebrae. We found little evidence for selection pressures related to adult or larval ecology affecting vertebrae evolution, but we did find body size was highly associated with vertebrae shape and microhabitat (mainly burrowing) affected those allometric relationships. Our results provide an interesting comparison to vertebrae evolution in other clades and a jumping-off point for studies of anuran vertebrae evolution and development.

Scaling patterns of body plans differ among squirrel ecotypes

“…However, extrinsic and intrinsic factors often constrain bodies towards certain sizes; therefore, in instances when evolutionary change in body size is limited, new adaptations can arise through evolutionary changes in the shape or proportions of traits ( Zelditch et al, 2017 ). Unsurprisingly, a plethora of work has found that ecological factors affect the evolution of the shape and proportions of the skull ( Janis, 1990 ; Olsen, 2017 ; Law et al, 2018 ; Arbour, Curtis & Santana, 2019 ; Grossnickle et al, 2020 ; Paluh, Stanley & Blackburn, 2020 ), limbs ( Van Valkenburgh, 1985 ; Higham et al, 2015 ; Citadini et al, 2018 ; Baeckens, Goeyers & Van Damme, 2020 ) and vertebrae ( Buchholtz, 1998 ; Randau et al., 2016 ; Jones et al, 2018 ; Gillet, Frédérich & Parmentier, 2019 ; Luger et al, 2019 ; Adler et al, 2022 ). The evolution of diverse overall body shapes can also facilitate morphological, functional, and ecological innovations that can lead to increased diversification and niche specialization ( Wiens, Brandley & Reeder, 2006 ; Collar et al, 2016 ; Law, 2019 ; Friedman, Price & Wainwright, 2021 ; Morinaga & Bergmann, 2020 ).…”

Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity

“…Both functional and developmental factors predict that distal elements should show greater variation of form than more proximal elements. Developmental mechanisms predict this pattern due to the timing and spatial structure of morphogenesis, which has been suggested to influence the macroevolutionary outcome of adult morphologies, including that of the skull ( Bardua et al, 2021 ; Fabre et al, 2020 ), the vertebrae ( Adler et al, 2022 ), and the limbs ( Holder, 1983 ; Stepanova and Womack, 2020 ). Each limb initiates as a bud that extends from the body wall and where skeletal elements are generally specified in a proximal to distal sequence that matches their evolutionary appearance during tetrapod origins: development begins with the stylopod, followed by the zeugopod, and terminating in the autopod at the distal end ( Figure 2A ; Schneider and Shubin, 2013 ; Shubin et al, 1997 ; Stopper and Wagner, 2005 ).…”

Scaling patterns of body plans differ among squirrel ecotypes

“…However, extrinsic and intrinsic factors often constrain bodies towards certain sizes; therefore, in instances when evolutionary change in body size is limited, new adaptations can arise through evolutionary changes in the shape or proportions of traits (Zelditch et al 2017). Unsurprisingly, a plethora of work has found that ecological factors affect the evolution of the shape and proportions of the skull (Janis 1990; Olsen 2017; Law et al 2018; Arbour et al 2019; Grossnickle 2020; Paluh et al 2020), limbs (Van Valkenburgh 1985; Higham et al 2015; Citadini et al 2018; Baeckens et al 2020) and vertebrae (Buchholtz 1998; Randau et al 2016; Jones et al 2018; Gillet et al 2019; Luger et al 2019; Adler et al 2022). The evolution of diverse overall body shapes can also facilitate morphological, functional, and ecological innovations that can lead to increased diversification and niche specialization (Wiens et al 2006; Collar et al 2016; Law 2019; Friedman et al 2020; Morinaga and Bergmann 2020).…”