A developmental synapomorphy of squamate reptiles

The reptilian clade Squamata is defined primarily by osteological synapomorphies, few of which are entirely unambiguous. Studies of developing squamate eggs have revealed a uniquely specialized feature not known to occur in any other amniotes. This feature—the yolk cleft/isolated yolk mass complex—lines the ventral hemisphere of the egg. During its formation, extraembryonic mesoderm penetrates the yolk and an exocoelom (the yolk cleft [YC]) forms in association with it, cutting off a thin segment of yolk (the “isolated yolk mass” [IYM]) from the main body of the yolk. The YC–IYM complex has been observed and described in more than 65 squamate species in 12 families. In viviparous species, it contributes to the “omphaloplacenta,” a type of yolk sac placenta unique to squamates. The only squamates known to lack the IYM are a few highly placentotrophic skinks with minuscule eggs, viviparous species in which it clearly has been lost. Given its absence in mammals, chelonians, crocodylians, and birds, the YC–IYM complex warrants recognition as a developmental synapomorphy of the squamate clade. As in extant viviparous lizards and snakes, the YC–IYM complex presumably contributed to the placenta of extinct viviparous squamates.     

Vertebral evolution and the diversification of squamate reptiles

Taxonomic, morphological, and functional diversity are often discordant and independent components of diversity. A fundamental and largely unanswered question in evolutionary biology is why some clades diversify primarily in some of these components and not others. Dramatic variation in trunk vertebral numbers (14 to >300) among squamate reptiles coincides with different body shapes, and snake-like body shapes have evolved numerous times. However, whether increased evolutionary rates or numbers of vertebrae underlie body shape and taxonomic diversification is unknown. Using a supertree of squamates including 1375 species, and corresponding vertebral and body shape data, we show that increased rates of evolution in vertebral numbers have coincided with increased rates and disparity in body shape evolution, but not changes in rates of taxonomic diversification. We also show that the evolution of many vertebrae has not spurred or inhibited body shape or taxonomic diversification, suggesting that increased vertebral number is not a key innovation. Our findings demonstrate that lineage attributes such as the relaxation of constraints on vertebral number can facilitate the evolution of novel body shapes, but that different factors are responsible for body shape and taxonomic diversification.     

Evolutionary diversification of clades of squamate reptiles

We analysed the diversification of squamate reptiles (7488 species) based on a new molecular phylogeny, and compared the results to similar estimates for passerine birds (5712 species). The number of species in each of 36 squamate lineages showed no evidence of phylogenetic conservatism. Compared with a random speciation-extinction process with parameters estimated from the size distribution of clades, the alethinophidian snakes (2600 species) were larger than expected and 13 clades, each having fewer than 20 species, were smaller than expected, indicating rate heterogeneity. From a lineage-through-time plot, we estimated that a provisional rate of lineage extinction (0.66 per Myr) was 94% of the rate of lineage splitting (0.70 per Myr). Diversification in squamate lineages was independent of their stem age, but strongly related to the area of the region within which they occur. Tropical vs. temperate latitude exerted a marginally significant influence on species richness. In comparison with passerine birds, squamates share several clade features, including: (1) independence of species richness and age; (2) lack of phylogenetic signal with respect to clade size; (3) general absence of exceptionally large clades; (4) over-representation of small clades; (5) influence of region size on clade size; and (6) similar rates of speciation and extinction. The evidence for both groups suggests that clade size has achieved long-term equilibrium, suggesting negative feedback of species richness on the rate of diversification.     

Climatic correlates of live-bearing in squamate reptiles

Summary We use a stepwise multiple regression procedure to correlate geographic patterns in the distribution of live-bearing reptilian species with patterns in climatic variables, in both Australia and North America. Previous authors have interpreted reptilian live-bearing as an evolutionary adaptation to cold climates. Our results indicate that environmental temperature and irradiance measures are no more highly correlated with the percent live-bearing species than are measures of precipitation, evaporation and humidity. We conclude that, except in very cold environments in North America, environmental temperatures seem to play little role in the relative success of live-bearing versus egg-laying reptilian reproductive strategies. It appears from previous work that reptilian live-bearing evolves mainly, or exclusively, because of the advantage it confers in enabling successful reproduction in cold climates. The present study suggests that the subsequent radiation of live-bearing reptilian species may be due to entirely different selective forces.     

Egg teeth of squamate reptiles and their phylogenetic significance

Original and published data on the structure of egg teeth in squamate reptiles and the phylogenetic significance of corresponding characters are reviewed, elaborating A.M. Sergeev’s ideas on the subject. Problems are discussed concerning the use of this character in modern phylogenetic constructions and the necessity of new embryological investigations to resolve the issue concerning the formation of an unpaired egg tooth rudiment in all Squamata except the Dibamidae and Gekkota.     

Functional and ecological correlates of ecologically-based dimorphisms in squamate reptiles

Sexual dimorphism in phenotypic traits associated with the useof resources is a widespread phenomenon throughout the animalkingdom. While ecological dimorphisms are often initially generatedby sexual selection operating on an animal's size, natural selectionis believed to maintain, or even amplify, these dimorphismsin certain ecological settings. The trophic apparatus of snakeshas proven to be a model system for testing the adaptive natureof ecological dimorphisms because head size is rarely undersexual selection and it limits the maximum ingestible size ofprey in these gape-limited predators. Significantly less attentionhas been paid to the evolution of ecological dimorphisms inlizards, however, which may be due to the fact that lizards’feeding apparatus can be under both sexual and natural selectionsimultaneously, making it difficult to formulate clear-cut hypothesesto distinguish between the influences of natural and sexualselection. In order to tease apart the respective influencesof natural selection and sexual selection on the feeding apparatusof squamates, we take an integrative approach to formulate twohypotheses for snakes and lizards, respectively: (1) For gape-limitedsnakes, we predict that natural selection will act to generatedifferences in maximum gape, which will translate into differencesin maximum ingestible prey size between the sexes. (2) For lizardswhich mechanically reduce their prey, we predict that the degreeof dimorphism in head size should be positively correlated tothe degree of dimorphism in bite force which, in turn, shouldbe correlated to dimorphism in aspects of size or hardness ofprey. Finally, we predict that functional differences in thefeeding apparatus of these animals will also be linked withdifferences in sex-based feeding behavior and with selectionof prey.     

Tikiguania and the antiquity of squamate reptiles (lizards and snakes)

Tikiguania estesi is widely accepted to be the earliest member of Squamata, the reptile group that includes lizards and snakes. It is based on a lower jaw from the Late Triassic of India, described as a primitive lizard related to agamids and chamaeleons. However, Tikiguania is almost indistinguishable from living agamids; a combined phylogenetic analysis of morphological and molecular data places it with draconines, a prominent component of the modern Asian herpetofauna. It is unlikely that living agamids have retained the Tikiguania morphotype unchanged for over 216 Myr; it is much more conceivable that Tikiguania is a Quaternary or Late Tertiary agamid that was preserved in sediments derived from the Triassic beds that have a broad superficial exposure. This removes the only fossil evidence for lizards in the Triassic. Studies that have employed Tikiguana for evolutionary, biogeographical and molecular dating inferences need to be reassessed.     

Rampant horizontal transfer of SPIN transposons in squamate reptiles

Transposable elements (TEs) are highly abundant in the genome and capable of mobility, two properties that make them particularly prone to transfer horizontally between organisms. Although the impact of horizontal transfer (HT) of TEs is well recognized in prokaryotes, the frequency of this phenomenon and its contribution to genome evolution in eukaryotes remain poorly appreciated. Here, we provide evidence that a DNA transposon called SPIN has colonized the genome of 17 species of reptiles representing nearly every major lineage of squamates, including 14 families of lizards, snakes, and amphisbaenians. Slot blot analyses indicate that SPIN has amplified to high copy numbers in most of these species, ranging from 2,000-28,000 copies per haploid genome. In contrast, we could not detect the presence of SPIN in any of the turtles (seven species from seven families) and crocodiles (four species) examined. Genetic distances between SPIN sequences from species belonging to different squamate families are consistently very low (average = 0.1), considering the deep evolutionary divergence of the families investigated (most are >100 My diverged). Furthermore, these distances fall below interfamilial distances calculated for two genes known to have evolved under strong functional constraint in vertebrates (RAG1, average = 0.24 and C-mos, average = 0.27). These data, combined with phylogenetic analyses, indicate that the widespread distribution of SPIN among squamates is the result of at least 13 independent events of HTs. Molecular dating and paleobiogeographical data suggest that these transfers took place during the last 50 My on at least three different continents (North America, South America and, Africa). Together, these results triple the number of known SPIN transfer events among tetrapods, provide evidence for a previously hypothesized transoceanic movement of SPIN transposons during the Cenozoic, and further underscore the role of HT in the evolution of vertebrate genomes.     

Determinate growth is predominant and likely ancestral in squamate reptiles

Body growth is typically thought to be indeterminate in ectothermic vertebrates. Indeed, until recently, this growth pattern was considered to be ubiquitous in ectotherms. Our recent observations of a complete growth plate cartilage (GPC) resorption, a reliable indicator of arrested skeletal growth, in many species of lizards clearly reject the ubiquity of indeterminate growth in reptiles and raise the question about the ancestral state of the growth pattern. Using X-ray micro-computed tomography (µCT), here we examined GPCs of long bones in three basally branching clades of squamate reptiles, namely in Gekkota, Scincoidea and Lacertoidea. A complete loss of GPC, indicating skeletal growth arrest, was the predominant finding. Using a dataset of 164 species representing all major clades of lizards and the tuataras, we traced the evolution of determinate growth on the phylogenetic tree of Lepidosauria. The reconstruction of character states suggests that determinate growth is ancestral for the squamate reptiles (Squamata) and remains common in the majority of lizard lineages, while extended (potentially indeterminate) adult growth evolved several times within squamates. Although traditionally associated with endotherms, determinate growth is coupled with ectothermy in this lineage. These findings combined with existing literature suggest that determinate growth predominates in both extant and extinct amniotes.     

Buccal swabbing as a source of DNA from squamate reptiles

Buccal swabbing was compared with other tissues as a source of DNA for microsatellite genotyping from two squamate reptiles. For both species, the lizard Lacerta agilis and the snake Coronella austriaca, buccal swabbing proved more reliable than tissues including tail tips, toe clips and ventral scale clips.     

Evolution of placentation among squamate reptiles: recent research and future directions

Squamate reptiles are uniquely suited to study of evolution of reproductive mode and pattern of embryonic nutrition. Viviparous species have evolved from oviparous ancestors on numerous occasions, patterns of nutritional provision to embryos range widely from lecithotrophy, at one end of a continuum, to placentotrophy at the other, and structure and function of the maternal-embryonic relationship is highly constrained resulting in parallel evolutionary trajectories among taxa. Embryos of oviparous species primarily receive nourishment from yolk, but also mobilize a significant quantity of calcium from the eggshell. Most viviparous species also are predominantly lecithotrophic, yet all viviparous species are placentotrophic to some degree. Similarities in embryonic development and nutritional pattern between oviparous species and most viviparous species suggest that the pattern of nutrition of oviparous squamates is an exaptation for the evolution of viviparity and that placentotrophy and viviparity evolve concomitantly. The few species of squamates that rely substantially on placentotrophy have structural modifications of the interface between the embryo and mother that are interpreted as adaptations to enhance nutritional exchange. Recent studies have extended understanding of the diversity of embryonic nutrition and placental structure and have resulted in hypotheses for transitions in the evolution of placentotrophy, yet data are available for few species. Indirect tests of these hypotheses, by comparison of structural-functional relationships among clades in which viviparity has evolved, awaits further study of the reproductive biology of squamates.     

Broad-scale patterns of body size in squamate reptiles of Europe and North America

Aim  To document geographical interspecific patterns of body size of European and North American squamate reptile assemblages and explore the relationship between body size patterns and environmental gradients.
Location  North America and western Europe.
Methods  We processed distribution maps for native species of squamate reptiles to document interspecific spatial variation of body size at a grain size of 110 × 110 km. We also examined seven environmental variables linked to four hypotheses possibly influencing body size gradients. We used simple and multiple regression, evaluated using information theory, to identify the set of models best supported by the data.
Results  Europe is characterized by clear latitudinal trends in body size, whereas geographical variation in body size in North America is complex. There is a consistent association of mean body size with measures of ambient energy in both regions, although lizards increase in size northwards whereas snakes show the opposite pattern. Our best models accounted for almost 60% of the variation in body size of lizards and snakes within Europe, but the proportions of variance explained in North America were less than 20%.
Main conclusions  Although body size influences the energy balance of thermoregulating ectotherms, inconsistent biogeographical patterns and contrasting associations with energy in lizards and snakes suggest that no single mechanism can explain variation of reptile body size in the northern temperate zone.     

Early origin of viviparity and multiple reversions to oviparity in squamate reptiles

Viviparity has putatively evolved 115 times in squamates (lizards and snakes), out of only ~ 140 origins in vertebrates, and is apparently related to colder climates and other factors such as body size. Viviparity apparently evolves from oviparity via egg‐retention, and such taxa may thus still have the machinery to produce thick‐shelled eggs. Parity mode is also associated with variable diversification rates in some groups. We reconstruct ancestral parity modes accounting for state‐dependent diversification in a large‐scale phylogenetic analysis, and find strong support for an early origin of viviparity at the base of Squamata, and a complex pattern of subsequent transitions. Viviparous lineages have higher rates of speciation and extinction, and greater species turnover through time. Viviparity is associated with lower environmental and body temperatures in lizards and amphisbaenians, but not female mass. These results suggest that parity mode is a labile trait that shifts frequently in response to ecological conditions.