The macroevolutionary singularity of snakes.

Snakes and lizards (Squamata) represent a third of terrestrial vertebrates and exhibit spectacular innovations in locomotion, feeding, and sensory processing. However, the evolutionary drivers of this radiation remain poorly known. We infer potential causes and ultimate consequences of squamate macroevolution by combining individual-based natural history observations (>60,000 animals) with a comprehensive time-calibrated phylogeny that we anchored with genomic data (5400 loci) from 1018 species. Due to shifts in the dynamics of speciation and phenotypic evolution, snakes have transformed the trophic structure of animal communities through the recurrent origin and diversification of specialized predatory strategies. Squamate biodiversity reflects a legacy of singular events that occurred during the early history of snakes and reveals the impact of historical contingency on vertebrate biodiversity.

How do lizard niches conserve, diverge or converge? Further exploration of saurian evolutionary ecology.

BACKGROUND: Environmental conditions on Earth are repeated in non-random patterns that often coincide with species from different regions and time periods having consistent combinations of morphological, physiological and behavioral traits. Observation of repeated trait combinations among species confronting similar environmental conditions suggest that adaptive trait combinations are constrained by functional tradeoffs within or across niche dimensions. In an earlier study, we assembled a high-resolution database of functional traits for 134 lizard species to explore ecological diversification in relation to five fundamental niche dimensions. Here we expand and further examine multivariate relationships in that dataset to assess the relative influence of niche dimensions on the distribution of species in 6-dimensional niche space and how these may deviate from distributions generated from null models. We then analyzed a dataset with lower functional-trait resolution for 1023 lizard species that was compiled from our dataset and a published database, representing most of the extant families and environmental conditions occupied by lizards globally. Ordinations from multivariate analysis were compared with null models to assess how ecological and historical factors have resulted in the conservation, divergence or convergence of lizard niches. RESULTS: Lizard species clustered within a functional niche volume influenced mostly by functional traits associated with diet, activity, and habitat/substrate. Consistent patterns of trait combinations within and among niche dimensions yielded 24 functional groups that occupied a total niche space significantly smaller than plausible spaces projected by null models. Null model tests indicated that several functional groups are strongly constrained by phylogeny, such as nocturnality in the Gekkota and the secondarily acquired sit-and-wait foraging strategy in Iguania. Most of the widely distributed and species-rich families contained multiple functional groups thereby contributing to high incidence of niche convergence. CONCLUSIONS: Comparison of empirical patterns with those generated by null models suggests that ecological filters promote limited sets of trait combinations, especially where similar conditions occur, reflecting both niche convergence and conservatism. Widespread patterns of niche convergence following ancestral niche diversification support the idea that lizard niches are defined by trait-function relationships and interactions with environment that are, to some degree, predictable and independent of phylogeny.

An inventory of online reptile images.

No central online repository exists for the collection of animal images; hence it remains unclear how extensively species have been illustrated in the published literature or online. Here we compiled a list of more than 8000 reptile species (out of 11,341) that have photos in one of six popular online repositories, namely iNaturalist (6,349 species), the Reptile Database (5,144), Flickr (4,386), CalPhotos (3,071), Wikimedia (2,952), and Herpmapper (2,571). These sites have compiled over one million reptile photos, with some species represented by tens of thousands of images. Despite the number of images, many species have only one or a few images. This suggests that a considerable fraction of morphological and geographic variation is under documented or difficult to access. We highlight prominent gaps in amphisbaenians, lizards, and snakes, with geographic hotspots for species without images in Central Africa, Pacific Islands, and the Andes Mountains. We present a list of ~3,000 species without photos in any of the six databases and ask the community to fill the gaps by depositing images on one of these sites (preferably with minimal copyright restrictions).

An inventory of online reptile images

No central online repository exists for the collection of animal images; hence it remains unclear how extensively species have been illustrated in the published literature or online. Here we compiled a list of more than 8000 reptile species (out of 11,341) that have photos in one of six popular online repositories, namely iNaturalist (6,349 species), the Reptile Database (5,144), Flickr (4,386), CalPhotos (3,071), Wikimedia (2,952), and Herpmapper (2,571). These sites have compiled over one million reptile photos, with some species represented by tens of thousands of images. Despite the number of images, many species have only one or a few images. This suggests that a considerable fraction of morphological and geographic variation is under documented or difficult to access. We highlight prominent gaps in amphisbaenians, lizards, and snakes, with geographic hotspots for species without images in Central Africa, Pacific Islands, and the Andes Mountains. We present a list of ~3,000 species without photos in any of the six databases and ask the community to fill the gaps by depositing images on one of these sites (preferably with minimal copyright restrictions).

Population genetic structure and species delimitation of a widespread, Neotropical dwarf gecko.

Amazonia harbors the greatest biological diversity on Earth. One trend that spans Amazonian taxa is that most taxonomic groups either exhibit broad geographic ranges or small restricted ranges. This is likely because many traits that determine a species range size, such as dispersal ability or body size, are autocorrelated. As such, it is rare to find groups that exhibit both large and small ranges. Once identified, however, these groups provide a powerful system for isolating specific traits that influence species distributions. One group of terrestrial vertebrates, gecko lizards, tends to exhibit small geographic ranges. Despite one exception, this applies to the Neotropical dwarf geckos of the genus Gonatodes. This exception, Gonatodes humeralis, has a geographic distribution almost 1,000,000 km2 larger than the combined ranges of its 30 congeners. As the smallest member of its genus and a gecko lizard more generally, G. humeralis is an unlikely candidate to be a wide-ranged Amazonian taxon. To test whether or not G. humeralis is one or more species, we generated molecular genetic data using restriction-site associated sequencing (RADseq) and traditional Sanger methods for samples from across its range and conducted a phylogeographic study. We conclude that G. humeralis is, in fact, a single species across its contiguous range in South America. Thus, Gonatodes is a unique clade among Neotropical taxa, containing both wide-ranged and range-restricted taxa, which provides empiricists with a powerful model system to correlate complex species traits and distributions. Additionally, we provide evidence to support species-level divergence of the allopatric population from Trinidad and we resurrect the name Gonatodes ferrugineus from synonymy for this population.

Thermal physiology of Amazonian lizards (Reptilia: Squamata).

We summarize thermal-biology data of 69 species of Amazonian lizards, including mode of thermoregulation and field-active body temperatures (Tb). We also provide new data on preferred temperatures (Tpref), voluntary and thermal-tolerance ranges, and thermal-performance curves (TPC's) for 27 species from nine sites in the Brazilian Amazonia. We tested for phylogenetic signal and pairwise correlations among thermal traits. We found that species generally categorized as thermoregulators have the highest mean values for all thermal traits, and broader ranges for Tb, critical thermal maximum (CTmax) and optimal (Topt) temperatures. Species generally categorized as thermoconformers have large ranges for Tpref, critical thermal minimum (CTmin), and minimum voluntary (VTmin) temperatures for performance. Despite these differences, our results show that all thermal characteristics overlap between both groups and suggest that Amazonian lizards do not fit into discrete thermoregulatory categories. The traits are all correlated, with the exceptions of (1) Topt, which does not correlate with CTmax, and (2) CTmin, and correlates only with Topt. Weak phylogenetic signals for Tb, Tpref and VTmin indicate that these characters may be shaped by local environmental conditions and influenced by phylogeny. We found that open-habitat species perform well under present environmental conditions, without experiencing detectable thermal stress from high environmental temperatures induced in lab experiments. For forest-dwelling lizards, we expect warming trends in Amazonia to induce thermal stress, as temperatures surpass the thermal tolerances for these species.

Toward a Periodic Table of Niches, or Exploring the Lizard Niche Hypervolume.

Widespread niche convergence suggests that species can be organized according to functional trait combinations to create a framework analogous to a periodic table. We compiled ecological data for lizards to examine patterns of global and regional niche diversification, and we used multivariate statistical approaches to develop the beginnings for a periodic table of niches. Data (50+ variables) for five major niche dimensions (habitat, diet, life history, metabolism, defense) were compiled for 134 species of lizards representing 24 of the 38 extant families. Principal coordinates analyses were performed on niche dimensional data sets, and species scores for the first three axes were used as input for a principal components analysis to ordinate species in continuous niche space and for a regression tree analysis to separate species into discrete niche categories. Three-dimensional models facilitate exploration of species positions in relation to major gradients within the niche hypervolume. The first gradient loads on body size, foraging mode, and clutch size. The second was influenced by metabolism and terrestrial versus arboreal microhabitat. The third was influenced by activity time, life history, and diet. Natural dichotomies are activity time, foraging mode, parity mode, and habitat. Regression tree analysis identified 103 cases of extreme niche conservatism within clades and 100 convergences between clades. Extending this approach to other taxa should lead to a wider understanding of niche evolution.

Life-History Patterns of Lizards of the World.

Identification of mechanisms that promote variation in life-history traits is critical to understand the evolution of divergent reproductive strategies. Here we compiled a large life-history data set (674 lizard populations, representing 297 species from 263 sites globally) to test a number of hypotheses regarding the evolution of life-history traits in lizards. We found significant phylogenetic signal in most life-history traits, although phylogenetic signal was not particularly high. Climatic variables influenced the evolution of many traits, with clutch frequency being positively related to precipitation and clutches of tropical lizards being smaller than those of temperate species. This result supports the hypothesis that in tropical and less seasonal climates, many lizards tend to reproduce repeatedly throughout the season, producing smaller clutches during each reproductive episode. Our analysis also supported the hypothesis that viviparity has evolved in lizards as a response to cooler climates. Finally, we also found that variation in trait values explained by clade membership is unevenly distributed among lizard clades, with basal clades and a few younger clades showing the most variation. Our global analyses are largely consistent with life-history theory and previous results based on smaller and scattered data sets, suggesting that these patterns are remarkably consistent across geographic and taxonomic scales.

Molecular systematics and historical biogeography of tree boas (Corallus spp.).

Inferring the evolutionary and biogeographic history of taxa occurring in a particular region is one way to determine the processes by which the biodiversity of that region originated. Tree boas of the genus Corallus are an ancient clade and occur throughout Central and South America and the Lesser Antilles, making it an excellent group for investigating Neotropical biogeography. Using sequenced portions of two mitochondrial and three nuclear loci for individuals of all recognized species of Corallus, we infer phylogenetic relationships, present the first molecular analysis of the phylogenetic placement of the enigmatic C. cropanii, develop a time-calibrated phylogeny, and explore the biogeographic history of the genus. We found that Corallus diversified within mainland South America, via over-water dispersals to the Lesser Antilles and Central America, and via the traditionally recognized Panamanian land bridge. Divergence time estimates reject the South American Caribbean-Track as a general biogeographic model for Corallus and implicate a role for events during the Oligocene and Miocene in diversification such as marine incursions and the uplift of the Andes. Our findings also suggest that recognition of the island endemic species, C. grenadensis and C. cookii, is questionable as they are nested within the widely distributed species, C. hortulanus. Our results highlight the importance of using widespread taxa when forming and testing biogeographic hypotheses in complex regions and further illustrate the difficulty of forming broadly applicable hypotheses regarding patterns of diversification in the Neotropical region.

Understanding the formation of ancient intertropical disjunct distributions using Asian and Neotropical hinged-teeth snakes (Sibynophis and Scaphiodontophis: Serpentes: Colubridae).

Numerous taxa show ancient intertropical disjunct distributions. Many can be explained by well-known processes of historical vicariance, such as the breakup of Gondwanaland. Others, such as Asian-Neotropical divergences are not as well understood. To clarify the phylogenetic position and understand biogeographic and temporal origins of the geographically disjunct and morphologically unique genera of hinged-teeth snakes, Scaphiodontophis (n=1) and Sibynophis (n=9; Colubridae), we inferred a time-calibrated phylogeny with additional 107 taxa representing the superfamily Colubroidea using four genes (c-mos, cyt-b, ND2, RAG-1; 3085 bp). We used this tree to estimate ancestral areas for the group. The results show that Scaphiodontophis is sister to Sibynophis, both originated in the late Eocene/Oligocene in Asia and likely dispersed through Beringia to the New World, but unlike other snake groups left no extant species in temperate North America. Current recognition of Scaphiodontophiinae renders Colubrinae paraphyletic, and we resurrect the previously named subfamily Sibynophiinae to encompass both genera and use the tribes Sibynophiini (Sibynophis) and Scaphiodontophiini (Scaphiodontophis) to highlight the geographically distinct areas occupied by these taxa. These results suggest that intercontinental dispersal with extinction in intermediate areas can explain puzzling patterns of ancient intertropical disjunct distributions.

Helminths of Cnemidophorus ruthveni (Squamata: Teiidae) from Bonaire, Netherlands Antilles, with description of a new species of Alaeuris (Nematoda: Pharyngodonidae).

Alaeuris rinconensis n. sp. (Oxyuroidea, Pharyngodonidae) from the large intestine of the Bonaire whiptail lizard, Cnemidophorus ruthveni, is described and illustrated. Alaeuris rinconensis n. sp. represents the 13th Neotropical species assigned to the genus. It is most similar to Alaeuris iguanae in that only these 2 Neotropical species have postbulbar excretory pores; in A. iguanae, a tail filament is absent; in A. rinconensis, a tail filament is present. Two additional helminth species were found, i.e., the cestode Oochoristica iguanae and a nematode, Ozolaimus megatyphlon. Cnemidoporus ruthveni represents a new host record for the latter 2 species.

A new genus of miniaturized and pug-nosed gecko from South America (Sphaerodactylidae: Gekkota).

Sphaerodactyl geckos comprise five genera distributed across Central and South America and the Caribbean. We estimated phylogenetic relationships among sphaerodactyl genera using both separate and combined analyses of seven nuclear genes. Relationships among genera were incongruent at different loci and phylogenies were characterized by short, in some cases zero length, internal branches and poor phylogenetic support at most nodes. We recovered a polyphyletic Coleodactylus, with Coleodactylus amazonicus being deeply divergent from the remaining Coleodactylus species sampled. The C. amazonicus lineage possessed unique codon deletions in the genes PTPN12 and RBMX while the remaining Coleodactylus species had unique codon deletions in RAG1. Topology tests could not reject a monophyletic Coleodactylus, but we show that short internal branch lengths decreased the accuracy of topology tests because there were not enough data along short branches to support one phylogenetic hypothesis over another. Morphological data corroborated results of the molecular phylogeny, with Coleodactylus exhibiting substantial morphological heterogeneity. We identified a suite of unique craniofacial features that differentiate C. amazonicus not only from other Coleodactylus species, but also from all other geckos. We describe this novel sphaerodactyl lineage as a new genus, Chatogekko gen. nov. We present a detailed osteology of Chatogekko, characterizing osteological correlates of miniaturization that provide a framework for future studies in sphaerodactyl systematics and biology.

The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees.

The superfamily Colubroidea (> 2500 species) includes the majority of snake species and is one of the most conspicuous and well-known radiations of terrestrial vertebrates. However, many aspects of the phylogeny of the group remain contentious, and dozens of genera have yet to be included in molecular phylogenetic analyses. We present a new, large-scale, likelihood-based phylogeny for the colubroids, including 761 species sampled for up to five genes: cytochrome b (93% of 761 species sampled), ND4 (69%), ND2 (28%), c-mos (54%), and RAG-1 (13%), totaling up to 5814bp per species. We also compare likelihood bootstrapping and a recently proposed ultra-fast measure of branch support (Shimodaira-Hasegawa-like [SHL] approximate likelihood ratio), and find that the SHL test shows strong support for several clades that were weakly-supported by bootstrapping in this or previous analyses (e.g., Dipsadinae, Lamprophiidae). We find that SHL values are positively related to branch lengths, but show stronger support for shorter branches than bootstrapping. Despite extensive missing data for many taxa (mean=67% per species), neither bootstrap nor SHL support values for terminal species are related to their incompleteness, and that most highly incomplete taxa are placed in the expected families from previous taxonomy, typically with very strong support. The phylogeny indicates that the Neotropical colubrine genus Scaphiodontophis represents an unexpectedly ancient lineage within Colubridae. We present a revised higher-level classification of Colubroidea, which includes a new subfamily for Scaphiodontophis (Scaphiodontophiinae). Our study provides the most comprehensive phylogeny of Colubroidea to date, and suggests that SHL values may provide a useful complement to bootstrapping for estimating support on likelihood-based trees.

Why tropical forest lizards are vulnerable to climate warming.

Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.

Niche expansion and the niche variation hypothesis: does the degree of individual variation increase in depauperate assemblages?

The niche expansion and niche variation hypotheses predict that release from interspecific competition will promote niche expansion in depauperate assemblages. Niche expansion can occur by different mechanisms, including an increase in within-individual, among-individual, or bimodal variation (sexual dimorphism). Here we explore whether populations with larger niche breadth have a higher degree of diet variation. We also test whether populations from depauperate lizard assemblages differ in dietary resource use with respect to variation within and/or among individuals and sexual dimorphism. We found support for the niche expansion and niche variation hypotheses. Populations in assemblages with low phylogenetic diversity had a higher degree of individual variation, suggesting a tendency for niche expansion. We also found evidence suggesting that the mechanism causing niche expansion is an increase in variation among individuals rather than an increase in within-individual variation or an increase in bimodal variation due to sexual dimorphism.

Tertiary climate change and the diversification of the Amazonian gecko genus Gonatodes (Sphaerodactylidae, Squamata).

The genus Gonatodes is a monophyletic group of small-bodied, diurnal geckos distributed across northern South America, Central America, and the Caribbean. We used fragments of three nuclear genes (RAG2, ACM4, and c-mos) and one mitochondrial gene (16S) to estimate phylogenetic relationships among Amazonian species of Gonatodes. We used Penalized Likelihood to estimate timing of diversification in the genus. Most cladogenesis occurred in the Oligocene and early Miocene and coincided with a burst of diversification in other South American animal groups including mollusks, birds, and mammals. The Oligocene and early Miocene were periods dominated by dramatic climate change and Andean orogeny and we suggest that these factors drove the burst of cladogenesis in Gonatodes geckos as well as other taxa. A common pattern in Amazonian taxa is a biogeographic split between the eastern and western Amazon basin. We observed two clades with this spatial distribution, although large differences in timing of divergence between the east-west taxon pairs indicate that these divergences were not the result of a common vicariant event.

New species of Rhabdias (Nematoda: Rhabdiasidae) and other helminths from Norops capito (Sauria: Polychrotidae) from Nicaragua.

Rhabdias nicaraguensis n. sp. (Rhabditida: Rhabditidae) from the lungs of Norops capito (Sauria: Polychrotidae) is described and illustrated. Rhabdias nicaraguensis n. sp. represents the 54th species assigned to the genus and the 12th from the Neotropical realm. Of the 12 Neotropical Rhabdias species, nicaraguensis is most similar to tobagoensis and vellardi. These 3 species have equatorial placement of the vulva, inflated cuticle, and 6 small circumoral lips. Rhabdias nicaraguensis is easily separated from R. tobagoensis by the shape of the buccal cavity and from R. vellardi by body size and shape of the tail. Rhabdias nicaraguensis differs from both species by host preference, the amount of inflated cuticle covering the body, and the phasmids situated posterior to the midpoint of the tail.

Ecological release in lizard assemblages of neotropical savannas.

We compare lizard assemblages of Cerrado and Amazonian savannas to test the ecological release hypothesis, which predicts that niche dimensions and abundance should be greater in species inhabiting isolated habitat patches with low species richness (Amazonian savannas and isolated Cerrado patches) when compared with nonisolated areas in central Cerrado with greater species richness. We calculated microhabitat and diet niche breadths with data from 14 isolated Cerrado patches and Amazon savanna areas and six central Cerrado populations. Morphological data were compared using average Euclidean distances, and lizard abundance was estimated using the number of lizards captured in pitfall traps over an extended time period. We found no evidence of ecological release with respect to microhabitat use, suggesting that historical factors are better microhabitat predictors than ecological factors. However, data from individual stomachs indicate that ecological release occurs in these areas for one species (Tropidurus) but not others (Ameiva ameiva, Anolis, Cnemidophorus, and Micrablepharus), suggesting that evolutionary lineages respond differently to environmental pressures, with tropidurids being more affected by ecological factors than polychrotids, teiids, and gymnophthalmids. We found no evidence that ecological release occurs in these areas using morphological data. Based on abundance data, our results indicate that the ecological release (density compensation) hypothesis is not supported: lizard species are not more abundant in isolated areas than in nonisolated areas. The ecology of species is highly conservative, varying little from assemblage to assemblage. Nevertheless, increases in niche breadth for some species indicate that ecological release occurs as well.

New species of Oswaldocruzia (Nematoda: Molineidae) in Ameiva festiva (Squamata: Teiidae) from Nicaragua.

Oswaldocruzia nicaraguensis n. sp. (Strongylida: Molineidae) from the intestines of Ameiva festiva (Sauria: Teiidae) is described and illustrated. Oswaldocruzia nicaraguensis represents the 78th species assigned to the genus and is most similar to the Caribbean species of the genus by possessing spicules in which each of the 3 divisions terminates in numerous fine points. Of the 8 species assigned to this group, O. nicaraguensis is most similar to Oswaldocruzia moraveci; of the 8 species, only O. moraveci and O. nicaraguensis possess a type II bursa and lack cervical alae. It is separated from O. moraveci by the position of the tips of ribs 5-6; close together in O. nicaraguensis, well separated in O. moraveci.

Deep history impacts present-day ecology and biodiversity.

Lizards and snakes putatively arose between the early Jurassic and late Triassic; they diversified worldwide and now occupy many different ecological niches, making them ideal for testing theories on the origin of ecological traits. We propose and test the "deep history hypothesis," which claims that differences in ecological traits among species arose early in evolutionary history of major clades, and that present-day assemblages are structured largely because of ancient, preexisting differences. We combine phylogenetic data with ecological data collected over nearly 40 years to reconstruct the evolution of dietary shifts in squamate reptiles. Data on diets of 184 lizard species in 12 families from 4 continents reveal significant dietary shifts at 6 major divergence points, reducing variation by 79.8%. The most striking dietary divergence (27.6%) occurred in the late Triassic, when Iguania and Scleroglossa split. These two clades occupy different regions of dietary niche space. Acquisition of chemical prey discrimination, jaw prehension, and wide foraging provided scleroglossans access to sedentary and hidden prey that are unavailable to iguanians. This cladogenic event may have profoundly influenced subsequent evolutionary history and diversification. We suggest the hypothesis that ancient events in squamate cladogenesis, rather than present-day competition, caused dietary shifts in major clades such that some lizard clades gained access to new resources, which in turn led to much of the biodiversity observed today.