A farewell to arms and legs: a review of limb reduction in squamates

Abstract

Elongated snake-like bodies associated with limb reduction have evolved multiple times throughout vertebrate history. Limb-reduced squamates (lizards and snakes) account for the vast majority of these morphological transformations, and thus have great potential for revealing macroevolutionary transitions and modes of body-shape transformation. Here we present a comprehensive review on limb reduction, in which we examine and discuss research on these dramatic morphological transitions. Historically, there have been several approaches to the study of squamate limb reduction: (i) definitions of general anatomical principles of snake-like body shapes, expressed as varying relationships between body parts and morphometric measurements; (ii) framing of limb reduction from an evolutionary perspective using morphological comparisons; (iii) defining developmental mechanisms involved in the ontogeny of limb-reduced forms, and their genetic basis; (iv) reconstructions of the evolutionary history of limb-reduced lineages using phylogenetic comparative methods; (v) studies of functional and biomechanical aspects of limb-reduced body shapes; and (vi) studies of ecological and biogeographical correlates of limb reduction. For each of these approaches, we highlight their importance in advancing our understanding, as well as their weaknesses and limitations. Lastly, we provide suggestions to stimulate further studies, in which we underscore the necessity of widening the scope of analyses, and of bringing together different perspectives in order to understand better these morphological transitions and their evolution. In particular, we emphasise the importance of investigating and comparing the internal morphology of limb-reduced lizards in contrast to external morphology, which will be the first step in gaining a deeper insight into body-shape variation.

Digit and Ungual Morphology Suggest Adaptations for Scansoriality in the Late Carboniferous Eureptile Anthracodromeus longipes

“…Variation in phalangeal counts and digit morphology can arise from adaptive evolution to new ecological niches including aquatic, fossorial, scansorial, and cursorial habits, but also disruptions to limb development (Romer, 1956;Shapiro et al, 2007). In Anthracodromeus, a lack of any common aquatic or fossorial anatomical specializations makes these lifestyles unlikely candidates for explaining the hypophalangy observed in the manus and pes (Gans, 1975;Greer, 1987;Greer, 1991;Fedak and Hall, 2004;Camaiti et al, 2021). We find the most likely explanation for the combination of features found in the manus and pes of Anthracodromeus is that they are adaptations for scansoriality.…”

“…We find the most likely explanation for the combination of features found in the manus and pes of Anthracodromeus is that they are adaptations for scansoriality. Unlike living fossorial lizards (Camaiti et al, 2021), the reduced phalangeal counts of Anthracodromeus contrast the proportional elongation of phalanges in the manus and pes, which accounts for their formidable length. Hypophalangy in Anthracodromeus reduced the number of joints in the affected fingers and toes and consequently likely reduced the flexibility of the elongated digits, which may have provided further stability while clinging to surfaces and climbing over terrain.…”

A database of the morphology, ecology and literature of the world's limb‐reduced skinks

“…Limbless species were coded as character state 1, limb‐reduced ones as 2, and fully limbed species as 3. All models considered treated limb status as an ordered character, as to become limbless a species must necessarily first become limb‐reduced (Bergmann & Morinaga, 2019; Brandley et al, 2008; Camaiti et al, 2021).…”

“…We used these criteria rather than loss of digits because a significant proportion of taxa with four ‘long’ limbs are characterised by digit loss (e.g. Carlia, and outside of lizards, Equus ), while some short‐limbed elongated taxa (e.g., Anepischetosia ) are characterised by no digit losses at all (Camaiti et al, 2021; Greer, 1991). We chose the arbitrary cut‐offs of 15% (for forelimbs) and 20% (for hindlimbs) of SVL as we observed that virtually all species characterised by losses of digital elements and/or increased presacral vertebrae counts fall within those bounds.…”

Phylogenetic history influences convergence for a specialized ecology: comparative skull morphology of African burrowing skinks (Squamata; Scincidae)

“…The family is also morphologically and ecologically diverse, occurring in a range of habitats on every continent apart from Antarctica. Whereas the typical skink has four well-developed limbs, limb reduction and loss are common, with numerous independent events of limb reduction estimated in the group [ 34 , 35 ], including multiple times within some genera [ 36 , 37 ]. Limb reduction is typically correlated with a fossorial lifestyle and accompanied by a suite of other adaptations [ 38 , 39 ].…”