Coordinating tiny limbs and long bodies: Geometric mechanics of lizard terrestrial swimming

Heterochronic shifts in the ossification sequences of surface- and subsurface-dwelling skinks are correlated with the degree of limb reduction

AimThe relationship between changes in body form (limb reduction and body elongation) and geographical range size was investigated across 68 species ofLerista, a species‐rich clade of Australian scincid lizards that exhibits extensive interspecific variability in both body form and range size.LocationLeristaoccurs across the entire Australian mainland, with diversity concentrated in arid and semi‐arid regions.MethodsGeographical range size was estimated directly fromc. 14,000 museum specimens using bioclimatic modelling inMaxEnt. Body form was quantified using principal components analysis of morphometric variables. Comparative analyses testing for a correlation between these two variables used a full Bayesian approach that accounts for uncertainties in trait optimization as well as in tree topology and branch lengths.ResultsA serpentine body form (elongated with reduced limbs) was significantly associated with smaller geographical range size, in both phylogenetically corrected and uncorrected analyses – but only if species from single localities (whose ranges could not be modelled using the above methods) were excluded.Main conclusionsThese results suggest a general predictive relationship between body form and geographical range size in lizards: elongate, limb‐reduced lizards tend to exhibit more restricted geographical ranges that may reflect reduced dispersal ability and may also predispose them to greater vulnerability of extinction.

Embryonic development in Anadia bogotensis and body plan evolution in Gymnophthalmoidea(Squamata). Gymnophthalmoidea lizards inhabit in Central and South America fromlowlands to highland Andes. This clade presents species with different body plans; lacertiformspecies exhibit short and robust bodies and well-developed limbs whereas serpentiform specieshave elongate bodies and limb reduction. Between these two extreme body plans, we foundintermediate forms such as Anadia bogotensis, with a less elongated body and limbs fully developedbut not very robust. We describe the embryonic development of Anadia bogotensis,and compare it with serpentiform species of Gymnophthalmidae, and lacertiform species ofTeiidae and Alopoglossidae. We found differences in the development time in somites andlimbs. With respect to lacertiform species, there is an accelerated development of somites inserpentiform gymnophthalmids, which is involved in body elongation. Besides, hypomorphosisis the heterochronic perturbation involved in limb reduction. Therefore, there are differences inthe development time of different structures, which are related to the evolution of body plansin Gymnophthalmoidea.

One of the most striking morphological transformations in vertebrate evolution is the transition from a lizardlike body form to an elongate, limbless (snakelike) body form. Despite its dramatic nature, this transition has occurred repeatedly among closely related species (especially in squamate reptiles), making it an excellent system for studying macroevolutionary transformations in body plan. In this paper, we examine the evolution of body form in the lizard family Anguidae, a clade in which multiple independent losses of limbs have occurred. We combine a molecular phylogeny for 27 species, our morphometric data, and phylogenetic comparative methods to provide the first statistical phylogenetic tests of several long-standing hypotheses for the evolution of snakelike body form. Our results confirm the hypothesized relationships between body elongation and limb reduction and between limb reduction and digit reduction. However, we find no support for the hypothesized sequence going from body elongation to limb reduction to digit loss, and we show that a burrowing lifestyle is not a necessary correlate of limb loss. We also show that similar degrees of overall body elongation are achieved in two different ways in anguids, that these different modes of elongation are associated with different habitat preferences, and that this dichotomy in body plan and ecology is widespread in limb-reduced squamates. Finally, a recent developmental study has proposed that the transition from lizardlike to snakelike body form involves changes in the expression domains of midbody Hox genes, changes that would link elongation and limb loss and might cause sudden transformations in body form. Our results reject this developmental model and suggest that this transition involves gradual changes occurring over relatively long time scales.

The variation in limb reduction in vertebrates has generally been observed as characterizing higher-level taxa. Such structural changes are thus considered to reflect macroevolutionary processes. A statistical analysis of metric variables of some species of the African catfish family, Clariidae, suggests that fin reduction occurs at the microevolutionary level as well. In at least three species of that family intraspecific variation in the presence/absence of the pelvic fins was observed, and one species also showed similar variation for the pectoral fins. Discriminant function analysis confirmed that the variation is intraspecific, and even occurs within the same population. Sexual dimorphism could be excluded. This variation can be observed in the most anguilliform species of the clariid family, suggesting a link with body elongation (as is the case in tetrapods that show limb reduction). Pelvic fin loss appears to precede pectoral fin reduction during evolution. From the morphology it could be ascertained that the loss of the pelvic fins is coupled to the loss of the pelvic girdle, contrary to the case for the pectoral fins and girdle. Differences in functionality may explain this. Breeding results support the occurrence of intraspecific variation, as an F1 offspring showed a difference compared with the parents. For at least one species, the benefit from body elongation and limb reduction can be related to its highly specialized life style, as it lives subterraneanly in muddy soil of the Central African rainforest. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 75, 2002, 367‐377. ADDITIONAL KEYWORDS: catfish ‐ Clariidae ‐ intraspecific variation ‐ limblessness ‐ microevolution.

One of the most striking morphological transformations in vertebrate evolution is the transition from a lizardlike body form to an elongate, limbless (snakelike) body form. Despite its dramatic nature, this transition has occurred repeatedly among closely related species (especially in squamate reptiles), making it an excellent system for studying macroevolutionary transformations in body plan. In this paper, we examine the evolution of body form in the lizard family Anguidae, a clade in which multiple independent losses of limbs have occurred. We combine a molecular phylogeny for 27 species, our morphometric data, and phylogenetic comparative methods to provide the first statistical phylogenetic tests of several long-standing hypotheses for the evolution of snakelike body form. Our results confirm the hypothesized relationships between body elongation and limb reduction and between limb reduction and digit reduction. However, we find no support for the hypothesized sequence going from body elongation to limb reduction to digit loss, and we show that a burrowing lifestyle is not a necessary correlate of limb loss. We also show that similar degrees of overall body elongation are achieved in two different ways in anguids, that these different modes of elongation are associated with different habitat preferences, and that this dichotomy in body plan and ecology is widespread in limb-reduced squamates. Finally, a recent developmental study has proposed that the transition from lizardlike to snakelike body form involves changes in the expression domains of midbody Hox genes, changes that would link elongation and limb loss and might cause sudden transformations in body form. Our results reject this developmental model and suggest that this transition involves gradual changes occurring over relatively long time scales. Corresponding Editor: T. Garland Jr.

Squamates classified as 'subarenaceous' possess the ability to move long distances within dry sand; body elongation among sand and soil burrowers has been hypothesized to enhance subsurface performance. Using X-ray imaging, we performed the first kinematic investigation of the subsurface locomotion of the long, slender shovel-nosed snake (Chionactis occipitalis) and compared its biomechanics with those of the shorter, limbed sandfish lizard (Scincus scincus). The sandfish was previously shown to maximize swimming speed and minimize the mechanical cost of transport during burial. Our measurements revealed that the snake also swims through sand by propagating traveling waves down the body, head to tail. Unlike the sandfish, the snake nearly followed its own tracks, thus swimming in an approximate tube of self-fluidized granular media. We measured deviations from tube movement by introducing a parameter, the local slip angle, βs, which measures the angle between the direction of movement of each segment and body orientation. The average βs was smaller for the snake than for the sandfish; granular resistive force theory (RFT) revealed that the curvature utilized by each animal optimized its performance. The snake benefits from its slender body shape (and increased vertebral number), which allows propagation of a higher number of optimal curvature body undulations. The snake's low skin friction also increases performance. The agreement between experiment and RFT combined with the relatively simple properties of the granular 'frictional fluid' make subarenaceous swimming an attractive system to study functional morphology and bauplan evolution.

Opening the black box: phylogenetics and morphological evolution of the Malagasy fossorial lizards of the subfamily “Scincinae”

Morphology is among the most important traits influencing the interaction of individual animals with their environments. Fossoriality reflects this functional association between morphology and the use of subterranean habitats and their associated environmental characteristics. Lizards in the families Gymnophthalmidae and Alopoglossidae are model organisms to examine the interplay between morphology and fossoriality because great morphological diversity exists among species, including varying degrees of body elongation and limb reduction, and they have a wide geographical distribution in the Neotropical region. We analysed the morphology of 101 microteiid species and created an index to evaluate their degree of fossoriality. From this index, we traced the evolution of fossoriality in these lizards and assessed its primary environmental correlates. We found that fossoriality evolved independently in several lineages, mainly associated with high temperature and low precipitation, characteristic of more arid and sandy environments.

Squamates are found in a wide range of habitats and show a corresponding diversity of morphologies that can often be correlated with locomotor mode. The evolution of a snake-like body form, frequently associated with fossoriality, from a typical lacertiform morphology involves changes in the morphology of vertebrae, girdles, and limbs; the changes are mainly manifested by the reduction or loss of limbs and body elongation. In this study, we describe the axial and appendicular skeletons of six closely related gymnophthalmid species. Three of them show a lizard-like morphology, with a four-digit forelimb and a five-digit hindlimb, and the other three show a snake-like morphology associated with a burrowing habit, with reduced limbs and a longer body in comparison to the former three species. We show that vertebral morphology is similar among the six species, with the differences being accounted for by an increase in the number of vertebrae and by the structural reduction of girdles and limbs in the snake-like species. Skeletal morphology provides valuable information on locomotion type, physiology, diet, and other biological features. The burrowing morphology usually involves accentuated reduction of girdle and limb elements, reflecting an undulating type of locomotion in which the limbs play little or no role in propelling the body; in contrast, well-developed limbs and girdles indicate a greater reliance on the limbs for body propulsion. Limb reduction is frequent among vertebrates, but many different phenotypes are found in species exhibiting some kind of reduction, indicating that different mechanisms and evolutionary pressures may be involved in generating the diverse morphologies.

Employing an integrative approach to investigate the evolution of morphology can yield novel perspectives not attainable from a single field of study. Studies of limb loss and body elongation in squamates (snakes and lizards) present a good example in which integrating studies of systematics and ecology with genetics and development can provide considerable new insight. In this comment we address several misunderstandings of the developmental genetic literature presented in a paper by Wiens and Slingluff (2001) to counter their criticism of previous work in these disciplines and to clarify the apparently contradictory data from different fields of study. Specifically, we comment on (1) the developmental mechanisms underlying axial regionalization, body elongation, and limb loss; (2) the utility of presacral vertebral counts versus more specific partitioning of the primary body axis; (3) the independent, modular nature of limbs and limb girdles and their utility in diagnosing genetic changes in development; and (4) the causal bases of hind limb reduction in ophidian and nonophidian squamates.

Employing an integrative approach to investigate the evolution of morphology can yield novel perspectives not attainable from a single field of study. Studies of limb loss and body elongation in squamates (snakes and lizards) present a good example in which integrating studies of systematics and ecology with genetics and development can provide considerable new insight. In this comment we address several misunderstandings of the developmental genetic literature presented in a paper by Wiens and Slingluff (2001) to counter their criticism of previous work in these disciplines and to clarify the apparently contradictory data from different fields of study. Specifically, we comment on (1) the developmental mechanisms underlying axial regionalization, body elongation, and limb loss; (2) the utility of presacral vertebral counts versus more specific partitioning of the primary body axis; (3) the independent, modular nature of limbs and limb girdles and their utility in diagnosing genetic changes in development; and (4) the causal bases of hind limb reduction in ophidian and nonophidian squamates.

Convergence is the evolution of similar phenotypes often due to similar selective pressures or constraints limiting evolutionary options. Snake-like morphologies, characterized by elongated bodies and reduced limbs, have evolved repeatedly among vertebrates, including numerous times in squamate reptiles (lizards and snakes). It has been suggested that elongation facilitates locomotion through substrates while limb reduction typically occurs in clade-specific patterns, but this has not been tested. We compared the fit of a series of habitat- and clade-specific models for the evolution of digits, phalanges. and trunk vertebrae in lizards. We found that species inhabiting fossorial and cluttered habitats differed in numbers of vertebrae, digits, and phalanges from species in other habitats. A model with habitat-specific rates fit best for vertebral evolution, with sand swimmers, litter dwellers, and burrowers having higher rates of vertebral evolution than non-fossorial taxa. However, we found digits and phalanges evolved in a clade-specific manner, with higher rates of limb evolution in certain clades. This suggests that limb reduction in snake-like lizards is dictated by clade-specific constraints. In contrast, fossoriality appears to relax functional constraints on vertebral number, facilitating body form diversification. These results suggest that the relaxation of constraints may be an additional mechanism for convergent evolution.

Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships

The affinities of three problematic groups of elongate, burrowing reptiles (amphisbaenians, dibamids and snakes) are reassessed through a phylogenetic analysis of all the major groups of squamates, including the important fossil taxaSineoamphisbaena, mosasauroids andPachyrhachis; 230 phylogenetically informative osteological characters were evaluated in 22 taxa. Snakes (includingPachyrhachis) are anguimorphs, being related firstly to large marine mosasauroids, and secondly to monitor lizards (varanids). Scincids and cordylids are not related to lacertiforms as previously thought, but to anguimorphs. Amphisbaenians and dibamids are closely related, andSineoamphisbaenais the sister group to this clade. The amphisbaenian–dibamid–Sineoamphisbaenaclade, in turn, is related to gekkotans and xantusiids. When the fossil taxa are ignored, snakes, amphisbaenians and dibamids form an apparently well-corroborated clade nested within anguimorphs. However, nearly all of the characters supporting this arrangement are correlated with head-first burrowing (miniaturization, cranial consolidation, body elongation, limb reduction), and invariably co-occur in other tetrapods with similar habits. These characters are potentially very misleading because of their sheer number and because they largely represent reductions or losses. It takes very drastic downweighting of these linked characters to alter tree topology: if fossils are excluded from the analysis, a (probably spurious) clade consisting of elongate, fossorial taxa almost always results. These results underscore the importance of including all relevant taxa in phylogenetic analyses. Inferring squamate phylogeny depends critically on the inclusion of certain (fossil) taxa with combinations of character states that demonstrate convergent evolution of the elongate, fossorial ecomorph in amphisbaenians and dibamids, and in snakes. In the all-taxon analysis, the position of snakes within anguimorphs is more strongly-corroborated than the association of amphisbaenians and dibamids with gekkotans. When the critical fossil taxa are deleted, snakes «attract» the amphisbaenian–dibamid clade on the basis of a suite of correlated characters. While snakes remain anchored in anguimorphs, the amphisbaenian–dibamid clade moves away from gekkotans to join them. Regardless of the varying positions of the three elongate burrowing taxa, the interrelationships between the remaining limbed squamates («lizards») are constant; thus, the heterodox affinities of scincids, cordylids, and xantusiids identified in this analysis appear to be robust. Finally, the position ofPachyrhachisas a basal snake rather than (as recently suggested) a derived snake is supported on both phylogenetic and evolutionary grounds.