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.     

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.     

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.     

History and the global ecology of squamate reptiles

The structure of communities may be largely a result of evolutionary changes that occurred many millions of years ago. We explore the historical ecology of squamates (lizards and snakes), identify historically derived differences among clades, and examine how this history has affected present-day squamate assemblages globally. A dietary shift occurred in the evolutionary history of squamates. Iguanian diets contain large proportions of ants, other hymenopterans, and beetles, whereas these are minor prey in scleroglossan lizards. A preponderance of termites, grasshoppers, spiders, and insect larvae in their diets suggests that scleroglossan lizards harvest higher energy prey or avoid prey containing noxious chemicals. The success of this dietary shift is suggested by dominance of scleroglossans in lizard assemblages throughout the world. One scleroglossan clade, Autarchoglossa, combined an advanced vomeronasal chemosensory system with jaw prehension and increased activity levels. We suggest these traits provided them a competitive advantage during the day in terrestrial habitats. Iguanians and gekkotans shifted to elevated microhabitats historically, and gekkotans shifted activity to nighttime. These historically derived niche differences are apparent in extant lizard assemblages and account for some observed structure. These patterns occur in a variety of habitats at both regional and local levels throughout the world.     

The evolution of a family of short interspersed repeats in primate DNA

Summary Human DNA contains 300 nucleotide interspersed repeated sequences which mostly belong to a single family of sequences called the Alu family. This work examines the evolution of this family of sequences in primates. Bonnet monkey (Macaque radiata) DNA contains a predominant family of 300 nucleotide repeats which has nearly the same restriction map as the human Alu family and which hybridizes to human Alu family repeats under Southern blotting conditions. Prosimian (Galago crassicaudatus pangeniesis) DNA also contains a prominent group of 300 nucleotide long repeated sequences which does not have the same restriction sites as the human Alu family but which does hybridize to the human Alu family under reduced stringency conditions.     

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.     

Short interspersed elements (SINEs) of squamate reptiles (Squam1 and Squam2): structure and phylogenetic significance

Short interspersed elements (SINEs) are important nuclear molecular markers of the evolution of many eukaryotes. However, the SINEs of squamate reptile genomes have been little studied. We first identified two families of SINEs, termed Squam1 and Squam2, in the DNA of meadow lizard Darevskia praticola (Lacertidae) by performing DNA hybridization and PCR. Later, the same families of retrotransposons were found using the same methods in members of another 25 lizard families (from Iguania, Scincomorpha, Gekkota, Varanoidea, and Diploglossa infraorders) and two snake families, but their abundances in these taxa varied greatly. Both SINEs were Squamata-specific and were absent from mammals, birds, crocodiles, turtles, amphibians, and fish. Squam1 possessed some characteristics common to tRNA-related SINEs from fish and mammals, while Squam2 belonged to the tRNA(Ala) group of SINEs and had a more unusual and divergent structure. Squam2-related sequences were found in several unannotated GenBank sequences of squamate reptiles. Squam1 abundance in the Polychrotidae, Agamidae, Leiolepididae, Chamaeleonidae, Scincidae, Lacertidae, Gekkonidae, Varanidae, Helodermatidae, and two snake families were 10(2) -10(4) times higher than those in other taxa (Corytophanidae, Iguanidae, Anguidae, Cordylidae, Gerrhosauridae, Pygopodidae, and Eublepharidae). A less dramatic degree of copy number variation was observed for Squam2 in different taxa. Several Squam1 copies from Lacertidae, Chamaeleonidae, Gekkonidae, Varanidae, and Colubridae were sequenced and found to have evident orthologous features, as well as taxa-specific autapomorphies. Squam1 from Lacertidae and Chamaeleonidae could be divided into several subgroups based on sequence differences. Possible applications of these SINEs as Squamata phylogeny markers are discussed.     

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.     

Reassociation of interspersed moderate DNA repeats

Reassociation kinetics of the fragments of DNA consisting of interspersed repetitive and non-repetitive nucleotide sequences is considered in this paper. Based on the model, suggested by Gavrilov and Mazo (Mol. biol., 11, 101 1977), which takes into account the random DNA shearing, both reassociation kinetics of the total DNA in the region corresponding to interspersed repeat reassociation and that of the isolated preparation of interspersed repetitive sequences are calculated. In both cases influence of the repeat length on the reassociation rate is demonstrated. The estimation of the repetition frequency of rare repeats from pigeon genome is specified using calculations performed.     

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.     

A new family of dispersed repeats from Brassica nigra: characterization and localization

The 459-bp HindIII (pBN-4) and the 1732-bp Eco RI (pBNE8) fragments from the Brassica nigra genome were cloned and shown to be members of a dispersed repeat family. Of the three major diploid Brassica species, the repeat pBN-4 was found to be highly specific for the B. nigra genome. The family also hybridized to Sinapis arvensis showing that B. nigra had a closer relationship with the S. arvensis genome than with B. oleracea or B. campestris. The clone pBNE8 showed homology to a number of tRNA species indicating that this family of repeats may have originated from a tRNA sequence. The species-specific 459-bp repeat pBN-4 was localized on the B. nigra chromosomes using monosomic addition lines. In addition to the localization of pBN-4, the chromosomal distribution of two other species-specific repeats, pBN34 and pBNBH35 (reported earlier), was studied. The dispersed repeats pBN-4 and pBNBH35 were found to be present on all of the chromosomes, whereas the tandem repeat pBN34 was localized on two chromosomes.     

A new family of interspersed repetitive DNA sequences in the mouse genome

Repetitive DNA sequences near immunoglobulin genes in the mouse genome (Steinmetz et al., 1980a,b) were characterized by restriction mapping and hybridization. Six sequences were determined that turned out to belong to a new family of dispersed repetitive DNA. From the sequences, which are called R1 to R6, a 475 base-pair consensus sequence was derived. The R family is clearly distinct from the mouse B1 family (Krayev et al., 1980). According to saturation hybridization experiments, there are about 100,000 R sequences per haploid genome, and they are probably distributed throughout the genome. The individual R sequences have an average divergence from the consensus sequence of 12.5%, which is largely due to point mutations and, among those, to transitions. Some R sequences are severly truncated. The R sequences extend into A-rich sequences and are flanked by short direct repeats. Also, two large insertions in the R2 sequence are flanked by direct repeats. In the neighbourhood of and within R sequences, stretches of DNA have been identified that are homologous to parts of small nuclear RNA sequences. Mouse satellite DNA-like sequences and members of the B1 family were also found in close proximity to the R sequences. The dispersion of R sequences within the mouse genome may be a consequence of transposition events. The possible role of the R sequences in recombination and/or gene conversion processes is discussed.     

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.     

A new pachyostotic squamate reptile from the Cenomanian of France

Cenomanian beds from western France have yielded a new pythonomorph squamate (Reptilia) that is described here as Carentonosaurus mineaui gen. et sp. nov. This fossil is referred to non-mosasaurid mosasauroid lizards, i.e. to 'aigialosaurs'. It has been found in sediments of marine origin and its anatomy confirms that it was an aquatic lizard. It is characterized by a combination of characters that has not been reported, thus far, for squamates. Moreover, its vertebral column includes non-pachyostotic cervical vertebrae and highly pachyostotic dorsal vertebrae as in several other 'aigialosaurs'. This new taxon is perhaps restricted to the upper Cenomanian. It lived in shallow and rather warm water of the inner shelf. It is worth mentioning that nearly all pachyostotic squamates are concentrated in the Cenomanian and/or lower Turonian deposits of the present European-North African-Middle East portion of the Tethys. A parallel is drawn between the high percentage of pachyostotic squamates and the fact that this period corresponds to both the largest transgression of the Phanerozoic and the warmest period in the whole of the Mesozoic and Caenozoic.     

Proximate developmental mediators of sexual dimorphism in size: case studies from squamate reptiles

Sexual dimorphism in size (sexual size dimorphism; SSD) is nearlyubiquitous, but the relative importance of genetic versus environmentalcontrol of SSD is not known for most species. We investigatedproximate determinants of SSD in several species of squamatereptiles, including three species of Sceloporus lizards andthe diamond-backed rattlesnake (Crotalus atrox). In naturalpopulations of these species, SSD is caused by sexual differencesin age-specific growth. Males and females, however, may oftenshare similar potentials for growth: growth is strongly responsiveto the availability of food, and sexual differences in growthcan be greatly suppressed or completely absent under commonenvironmental conditions in the laboratory. Sexually divergentgrowth is expressed in natural environments because of inherentecological differences between males and females and becauseof potential epigenetic effects of sex-specific growth regulators.In field-active Sceloporus, sexual differences in growth rateare associated with sexual divergence in plasma testosterone.Experiments confirm that testosterone inhibits growth in speciesin which females are larger (for example, S. undulatus and S.virgatus) and stimulates growth in those in which males arelarger (for example, S. jarrovii). Interestingly, however, sexualdivergence in plasma testosterone is not accompanied by divergencein growth in S. jarrovii or in male-larger C. atrox in the laboratory.Furthermore, experimental effects of castration and testosteronereplacement on growth are not evident in captive S. jarrovii,possibly because growth effects of testosterone are supersededby an abundant, high-quality diet. In female-larger S. undulatus,growth may be traded-off against testosterone-induced reproductivecosts of activity. In male-larger species, costs of reproductionin terms of growth are suggested by supplemental feeding ofreproductive female C. atrox in their natural environment andby experimental manipulation of reproductive cost in femaleS. jarrovii. Growth costs of reproduction, however, do not contributesubstantially to the development of SSD in male-larger S. jarrovii.We conclude that the energetic costs of testosterone-induced,male reproductive behavior may contribute substantially to thedevelopment of SSD in some female-larger species. However, despitestrong evidence that reproductive investment exacts a substantialcost in growth, we do not support the reproductive cost hypothesisas a general explanation of SSD in male-larger species.