Convergent Evolution of Claw Shape in a Transcontinental Lizard Radiation

Abstract

Species occupying similar selective environments often share similar phenotypes as the result of natural selection. Recent discoveries, however, have led to the understanding that phenotypes may also converge for other reasons than recurring selection. We argue that the vertebrate claw system constitute a promising but understudied model system for testing the adaptive nature of phenotypic, functional, and genetic convergence. In this study, we combine basic morphometrics and advanced techniques in form analysis to examine claw shape divergence in a transcontinental lizard radiation (Lacertidae). We find substantial interspecific variation in claw morphology and phylogenetic comparative statistics reveal a strong correlation with structural habitat use: ground-dwelling species living in open areas are equipped with long, thick, weakly curved, slender-bodied claws, whereas climbing species carry high, short, strongly curved, full-bodied claws. Species occupying densely vegetated habitats tend to carry intermediately shaped claws. Evolutionary models suggest that claw shape evolves towards multiple adaptive peaks, with structural habitat use pulling species towards a specific selective optimum. Contrary to findings in several other vertebrate taxa, our analyses indicate that environmental pressures, not phylogenetic relatedness, drive convergent evolution of similarly shaped claws in lacertids. Overall, our study suggests that lacertids independently evolved similarly shaped claws as an adaptation to similar structural environments in order to cope with the specific locomotory challenges posed by the habitat. Future biomechanical studies that link form and function in combination with genomic and development research will prove valuable in better understanding the adaptive significance of claw shape divergence.

Functional morphology of vertebrate claws investigated using functionally based categories and multiple morphological metrics

“…Conversely, claw morphology in a variety of birds was considered to be independent of phylogeny and size by Glen and Bennett (2007) and it was recently found to be independent of both specifically in birds of prey, being linked more to biomechanics and relative prey size (Tsang et al, 2019). Another study found only a weak phylogenetic signal in lacertid claw morphology which did not interfere with attempts to link morphology with habitat use (Baeckens et al, 2019). Regardless of these findings and despite the incorporation of claw specimens from a wide variety of bird, mammal, and reptile species, covering a diverse range of phylogenetic, behavioral and size groups, the outcome of the LDA may be phylogenetically biased.…”

“…In one study, the use of geometric morphometric methods showed promise for separating aquatic/terrestrial, arboreal, and predatory birds (McIntosh, 2017) whereas another study found that these methods were unable to significantly separate birds into predatory, ground‐dwelling, and generalist groups (Hedrick et al, 2019). There have been few investigations into the functional morphology of reptile claws, most of which deal with narrow taxonomic groups (Baeckens et al, 2019; D'Amore et al, 2018; M. J. Tulli et al, 2009; Yuan et al, 2020; Yuan et al, 2019; Zani, 2000). This may be due to the relative dearth of information on reptile claw function in the natural history literature, especially compared to that which exists for birds and mammals.…”

Development, structure, and protein composition of reptilian claws and hypotheses of their evolution

“…Ecological information concerning claws is not included in this review. This information can be found elsewhere (Baeckens et al, 2019; Zani, 2000). The review also presents some information on the patterns of immunolabeling detected in developing and adult claws, integrated from the molecular and proteomic data derived from the analyses of extracted claw proteins in some representative species of lizards, tuatara, turtles, and alligator.…”

“…The almost ubiquitous presence of variously shaped claws in amniotes indicates the fundamental importance of these horny structures for life on land. Claws were likely initial adaptations for moving efficiently on a muddy or more solid surface, and became useful for grasping, clinging, manipulating objects, fighting, and tearing (Zani, 2000; Homberger et al, 2009; Moyer, Zheng, & Schweitzer, 2016; Baeckens, Goeyers, & Van Damme, 2019; Figure 1e). The fossil record shows that claws were present in early amniotes of the Permian‐Carboniferous, both synapsids and sauropsids, and even in pre‐amniotes, such as Diadectes (Maddin & Reisz, 2007; Moyer et al, 2016).…”

Size, microhabitat, and loss of larval feeding drive cranial diversification in frogs

“…A daptations to habitats are responsible for some of the most striking examples of phenotypic evolution, driving profound shifts in morphology [1][2][3][4][5][6] , in shape diversity ('disparity') 7 and in rate of shape evolution 1,[8][9][10][11] . Adaptations to similar habitats also result in phenotypic convergence when responses to selection produce similar shifts in phenotypic optima across diverse clades 2,[12][13][14][15] , as in the body forms of pelagic fishes, ichthyosaurs and whales.…”