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.

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.

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.

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.

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.

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.

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).

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.

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.

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.

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.

New species of Allopharynx (Digenea: Plagiorchiidae) and other helminths in Uranoscodon superciliosus (Squamata: Tropiduridae) from Amazonian Brazil.

Allopharynx daileyi n. sp. (Digenea: Plagiorchiidae) from the small intestine of the tropidurid lizard Uranoscodon superciliosus from Amazonian Brazil is described and illustrated. Of the 11 currently recognized species of Allopharynx, we consider Allopharynx megorchis Simha, 1961 a synonym of Allopharynx mehrai (Gogate, 1935) Price 1938 and Allopharynx puertoricensis Acholonu, 1976 a synonym of Allopharynx riopedrensis Garcia-Diaz; thus, A. daileyi becomes the 10th species assigned to the genus. The trematode species Mesocoelium monas and 2 species of Nematoda, Africana chabaudi and Cosmocerca vrcibradici, were also present.

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).

Lingual and biting responses to selected lipids by the lizard Podarcis lilfordi.

Many lizards can identify food using chemical cues, but very little is known about the chemical constituents used for this purpose. We experimentally investigated responses to several lipid stimuli by the omnivorous lacertid lizard Podarcis lilfordi, which had been shown previously to be capable of identifying prey using only chemical cues and to respond to pork fat by tongue-flicking and biting. In 60-s trials in which stimuli were presented on cotton swabs, the lizards responded very strongly to pure pork fat and to oleic acid, but not to cholesterol or glycerol. Latency to bite swabs, the number of individuals that bit swabs, and the tongue-flick attack score, TFAS(R), which combines effects of tongue-flicks and bites, showed stronger responses to fat than to cholesterol, glycerol, and distilled water but did not differ significantly from responses to oleic acid. Several lines of evidence show that oleic acid elicited strong chemosensory and feeding responses. For individuals that did not bite, the number of tongue-flicks was significantly greater for oleic acid than for distilled water or glycerol, and nearly so for cholesterol. Latency to bite was significantly shorter for oleic acid than for distilled water, and TFAS(R) was significantly greater for oleic acid than for distilled water and glycerol. In combination with pilot data indicating no strong response to the waxy, saturated palmitic acid, these findings suggest that oleic acid in particular and probably other unsaturated fatty acids found in animal fat contribute strongly to the food-related responses to lipids.

Sexual selection versus alternative causes of sexual dimorphism in teiid lizards.

The presence and extent of sexual dimorphisms in body form (size and shape) of adult macroteiid lizards were investigated. Males were significantly larger than females in the temperate species, Cnemidophorus tigris, and in the tropical species, Ameiva ameiva and C. ocellifer. Young adult C. tigris males grew faster than young adult females within and between reproductive seasons. Adult males of all species had larger heads than adult females of the same body size; this difference increased with body size. Moreover, male C. tigris were heavier than females of the same snout-vent length. The causes and consequences of the sexual dimorphisms were also examined. The possible causes of body size are especially numerous, and distinguishing the relative influences of the various causal selection factors on body size is problematical. Nevertheless, observational field data were used to tentatively conclude that intrasexual selection was the cause of larger body size of C. tigris males relative to females because (1) larger males won in male aggressive interactions, (2) the winning males gained access to more females by repelling competitors and by female acceptance, (3) larger males consequently had higher reproductive success, and (4) other hypothetical causes of larger male size were unsupported.

Specializations of the chorioallantoic placenta in the Brazilian scincid lizard, Mabuya heathi: a new placental morphotype for reptiles.

New World skinks of the genus Mabuya exhibit a unique form of viviparity that involves ovulation of tiny (1 mm) eggs and provision of virtually all of the nutrients for embryonic development by placental means. Studies of the Brazilian species M. heathi reveal that the chorioallantoic placenta is unlike those reported in any other squamate genus and exhibits striking specializations for maternal-fetal nutrient transfer. The uterine lining is intimately apposed to the chorioallantois, with no trace of an intervening shell membrane or of epithelial erosion; thus, the placenta is epitheliochorial. The uterus exhibits multicellular glands that secrete organic material into the uterine lumen. Opposite the openings of these glands, the chorion develops areolae, invaginated pits that are lined by absorptive, columnar epithelium. A single, mesometrial placentome develops, formed by radially oriented uterine folds that project into a deep invagination of the chorion. Uterine epithelium of the placentome appears to be syncytial and secretory and overlies a rich vascular supply. The apposed chorionic epithelium is absorptive in morphology and contains giant binucleated cells that bear microvilli. Several specializations of the placental membranes of M. heathi are found among eutherian mammals, signifying evolutionary convergence that extends to histological and cytological levels. The chorioallantoic placenta of M. heathi and its relatives warrants recognition as a new morphotype for reptiles, defined here as the "Type IV" placenta. This is the first new type of chorioallantoic placenta to be defined formally for reptiles in over half a century.

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.