Extinction debt and functional traits mediate community saturation over large spatiotemporal scales.

Determining if ecological communities are saturated (have a limit to the number of species they can support) has important implications for understanding community assembly, species invasions, and climate change. However, previous studies have generally been limited to short time frames that overlook extinction debt and have not explicitly considered how functional trait diversity may mediate patterns of community saturation. Here, we combine data from biodiversity surveys with functional and phylogenetic data to explore if the colonisation events after the Great American Biotic Interchange (closure of the Panamanian Isthmus) resulted in increases in species richness of communities of the snake family Dipsadidae. We determined the number and the direction of dispersal events between Central and South America by estimating ancestral areas based on a Bayesian time-calibrated phylogenetic analysis. We then evaluated whether variation in community saturation was mediated by the functional similarity of six traits for the resident and colonizing snakes and/or local environmental conditions. We found that colonised communities did not support more species than those that were not colonised. Moreover, we did not find an association between the functional diversity across sites and whether they were colonised by members from the lineages dispersing across the Isthmus or not. Instead, variation in species richness was predicted best by covariates such as time since colonisation and local environment. Taken together, our results suggest that snake communities of the Dipsadidae across the neotropics are saturated. Moreover, our research highlights two important factors to consider in studies of community saturation: extinction debt and the functional differences and similarities in species' ecological roles.

Determinar si las comunidades ecológicas están saturadas (si tienen un límite en el número de especies que pueden albergar) tiene importantes implicaciones para entender el ensamblaje de comunidades, las invasiones de especies y el cambio climático. Sin embargo, los estudios previos en esta área se han limitado generalmente a marcos temporales cortos, ignorando el concepto de deuda de extinción y no considerando explícitamente cómo la diversidad de rasgos funcionales puede mediar en los patrones de saturación de las comunidades. En este trabajo combinamos datos publicados de muestreos de campo con datos funcionales y filogenéticos para explorar si los eventos de colonización después del Gran Intercambio Biótico Americano (ocurrido con el cierre del istmo de Panamá) resultaron en aumentos en la riqueza de especies de las comunidades de la familia de serpientes Dipsadidae. Determinamos el número y la dirección de los eventos de dispersión entre América Central y América del Sur mediante la estimación de áreas ancestrales basada en un análisis filogenético Bayesiano calibrado en el tiempo. Luego evaluamos si la variación en la saturación de las comunidades estaba mediada por la similitud funcional de seis rasgos para las serpientes residentes y colonizadoras y/o por las condiciones ambientales locales. Encontramos que las comunidades colonizadas no contienen más especies que aquellas que no fueron colonizadas. Además, no encontramos ninguna relación entre la diversidad funcional de los sitios considerados y el hecho de que estuvieran colonizados o no por miembros de los linajes que se dispersaron a través del Istmo. En cambio, la variación en la riqueza de especies se predijo mejor por covariantes como el tiempo transcurrido desde la colonización y el clima local. En conjunto, nuestros resultados sugieren que las comunidades de Dipsadidae a lo largo del neotrópico están saturadas. Además, nuestra investigación destaca dos factores importantes a considerar en los estudios de saturación de comunidades: la existencia de una deuda de extinción y las diferencias y similitudes funcionales en los papeles ecológicos de las especies.

A New Diploid Parthenogenetic Whiptail Lizard from Sonora, Mexico, Is the "Missing Link" in the Evolutionary Transition to Polyploidy.

AbstractTransitions between sexual and unisexual reproductive modes have significant consequences for the evolutionary trajectories of species. These transitions have occurred numerous times in vertebrates and are frequently mediated by hybridization events. Triploid unisexual vertebrates are thought to arise through hybridization between individuals of a diploid unisexual lineage and a sexual species, although additional evidence that confirms this mechanism is needed in numerous groups. North American whiptail lizards (Aspidoscelis) are notable for being one of the largest radiations of unisexual vertebrates, and the most diverse group of Aspidoscelis includes numerous triploid lineages that have no known diploid unisexual ancestors. This pattern of "missing" ancestors may result from the short evolutionary life span of unisexual lineages or the selective advantages of polyploidy, or it could suggest that alternative mechanisms of triploid formation are operating in nature. We leverage genomic, morphological, and karyotypic data to describe a new diploid unisexual whiptail and show that it is likely the unisexual progenitor of an extant triploid lineage, A. opatae. We also resolve patterns of polyploidization within the A. sexlineatus species group and test predictions about the phenotypic outcomes of hybridization.

Complex patterns of hybridization and introgression across evolutionary timescales in Mexican whiptail lizards (Aspidoscelis).

Identifying patterns of introgression across the tree of life is foundational to understanding general mechanisms that govern the impacts of gene flow on the speciation process. There are few vertebrate groups in which hybridization is associated with as large a diversity of outcomes as in North American whiptail lizards (Aspidoscelis). Of particular interest is that hybridization among divergent whiptail species has repeatedly led to the formation of unisexual (parthenogenetic) lineages. Understanding the hybrid origin of these unisexual lineages requires an accurate understanding of species boundaries among gonochoristic whiptails. Doing so has historically been an extremely challenging problem which, in part, may be a consequence of widespread hybridization and incomplete reproductive isolation among lineages. The lack of a robust phylogenetic framework and uncertainty in species boundaries precludes studies of general patterns and mechanisms of introgression among whiptail species. Here, we use genomic data to reconstruct a robust estimate of evolutionary history in the largest clade of whiptail lizards (A. sexlineatus species group) and use it to identify patterns of introgression. Our results indicate substantial introgressive hybridization and admixture has occurred among multiple lineages of whiptails across diverse evolutionary time scales, and illustrate their impact on phylogenetic inference. Thus, hybridization among whiptail species appears to have been a prominent feature throughout their evolutionary history, which could, in part, explain why parthenogenesis has evolved so many times in whiptails in comparison to other vertebrate groups.

Multilocus phylogeny of alligator lizards (Elgaria, Anguidae): Testing mtDNA introgression as the source of discordant molecular phylogenetic hypotheses.

The increased availability of nuclear DNA sequence data has led to a better appreciation of the role and frequency of introgressive hybridization and subsequent mitochondrial capture in misleading phylogenetic hypotheses based on mtDNA sequence data alone. Relationships among members of the alligator lizard genus Elgaria have been addressed with morphology, allozyme and mtDNA sequence data with discordant results. In this study, we use seven nuclear loci (total of 5.9kb) and ∼3kb of mtDNA to infer the phylogenetic relationships among Elgaria species and test whether the discordance among previous phylogenetic hypotheses is due to introgression and mtDNA capture. While gene tree topologies varied among the different loci, we recovered a well-resolved coalescent-based species tree. Contrary to our expectations, the nDNA-only species tree does not support the sister relationship between E. kingii and E. panamintina inferred from the previous allozyme study. Nevertheless, we found evidence for possible mitochondrial capture in two unexpected situations. The first instance of mtDNA capture involves E. paucicarinata from the Cape Region of Baja California. MtDNA recovered a clade comprising E. paucicarinata and the other two peninsular endemics, while the nDNA-only species tree recovered E. paucicarinata as sister to the continental E. kingii. We hypothesize that this discordance is the result of ancient mitochondrial capture rather than incomplete lineage sorting. Additionally, analyses of nDNA recovered E. panamintina as sister to an E. multicarinata North lineage, whereas the mtDNA gene tree recovers E. panamintina nested within a southern E. multicarinata clade. We hypothesize that this discordance also may be due to mitochondrial capture. Additionally, hybridization between these two lineages may have resulted in geographically limited nuclear introgression. Divergence dating analyses suggest that oviparous Elgaria species diverged within a relatively narrow timeframe from the late Miocene to early Pliocene. We find that accounting for introgressed alleles is important when inferring phylogenetic relationships when using coalescent-based approaches.

Lineage diversification of fringe-toed lizards (Phrynosomatidae: Uma notata complex) in the Colorado Desert: Delimiting species in the presence of gene flow.

Multi-locus nuclear DNA data were used to delimit species of fringe-toed lizards of the Uma notata complex, which are specialized for living in wind-blown sand habitats in the deserts of southwestern North America, and to infer whether Quaternary glacial cycles or Tertiary geological events were important in shaping the historical biogeography of this group. We analyzed ten nuclear loci collected using Sanger sequencing and genome-wide sequence/single-nucleotide polymorphism (SNP) data collected using restriction-associated DNA (RAD) sequencing. A combination of species discovery methods (concatenated phylogenies, parametric and non-parametric clustering algorithms) and species validation approaches (coalescent-based species tree/isolation-with-migration models) were used to delimit species, infer phylogenetic relationships, and to estimate effective population sizes, migration rates, and speciation times. Uma notata, U. inornata, U. cowlesi, and an undescribed species from Mohawk Dunes, Arizona (U. sp.) were supported as distinct in the concatenated analyses and by clustering algorithms, and all operational taxonomic units were decisively supported as distinct species by ranking hierarchical nested speciation models with Bayes factors based on coalescent-based species tree methods. However, significant unidirectional gene flow (2NM>1) from U. cowlesi and U. notata into U. rufopunctata was detected under the isolation-with-migration model. Therefore, we conservatively delimit four species-level lineages within this complex (U. inornata, U. notata, U. cowlesi, and U. sp.), treating U. rufopunctata as a hybrid population (U. notata×cowlesi). Both concatenated and coalescent-based estimates of speciation times support the hypotheses that speciation within the complex occurred during the late Pleistocene, and that the geological evolution of the Colorado River delta during this period was an important process shaping the observed phylogeographic patterns.

When do species-tree and concatenated estimates disagree? An empirical analysis with higher-level scincid lizard phylogeny.

Simulation studies suggest that coalescent-based species-tree methods are generally more accurate than concatenated analyses. However, these species-tree methods remain impractical for many large datasets. Thus, a critical but unresolved issue is when and why concatenated and coalescent species-tree estimates will differ. We predict such differences for branches in concatenated trees that are short, weakly supported, and have conflicting gene trees. We test these predictions in Scincidae, the largest lizard family, with data from 10 nuclear genes for 17 ingroup taxa and 44 genes for 12 taxa. We support our initial predictions, andsuggest that simply considering uncertainty in concatenated trees may sometimes encompass the differences between these methods. We also found that relaxed-clock concatenated trees can be surprisingly similar to the species-tree estimate. Remarkably, the coalescent species-tree estimates had slightly lower support values when based on many more genes (44 vs. 10) and a small (∼30%) reduction in taxon sampling. Thus, taxon sampling may be more important than gene sampling when applying species-tree methods to deep phylogenetic questions. Finally, our coalescent species-tree estimates tentatively support division of Scincidae into three monophyletic subfamilies, a result otherwise found only in concatenated analyses with extensive species sampling.

Species delimitation using Bayes factors: simulations and application to the Sceloporus scalaris species group (Squamata: Phrynosomatidae).

Current molecular methods of species delimitation are limited by the types of species delimitation models and scenarios that can be tested. Bayes factors allow for more flexibility in testing non-nested species delimitation models and hypotheses of individual assignment to alternative lineages. Here, we examined the efficacy of Bayes factors in delimiting species through simulations and empirical data from the Sceloporus scalaris species group. Marginal-likelihood scores of competing species delimitation models, from which Bayes factor values were compared, were estimated with four different methods: harmonic mean estimation (HME), smoothed harmonic mean estimation (sHME), path-sampling/thermodynamic integration (PS), and stepping-stone (SS) analysis. We also performed model selection using a posterior simulation-based analog of the Akaike information criterion through Markov chain Monte Carlo analysis (AICM). Bayes factor species delimitation results from the empirical data were then compared with results from the reversible-jump MCMC (rjMCMC) coalescent-based species delimitation method Bayesian Phylogenetics and Phylogeography (BP&P). Simulation results show that HME and sHME perform poorly compared with PS and SS marginal-likelihood estimators when identifying the true species delimitation model. Furthermore, Bayes factor delimitation (BFD) of species showed improved performance when species limits are tested by reassigning individuals between species, as opposed to either lumping or splitting lineages. In the empirical data, BFD through PS and SS analyses, as well as the rjMCMC method, each provide support for the recognition of all scalaris group taxa as independent evolutionary lineages. Bayes factor species delimitation and BP&P also support the recognition of three previously undescribed lineages. In both simulated and empirical data sets, harmonic and smoothed harmonic mean marginal-likelihood estimators provided much higher marginal-likelihood estimates than PS and SS estimators. The AICM displayed poor repeatability in both simulated and empirical data sets, and produced inconsistent model rankings across replicate runs with the empirical data. Our results suggest that species delimitation through the use of Bayes factors with marginal-likelihood estimates via PS or SS analyses provide a useful and complementary alternative to existing species delimitation methods.

Estimating divergence dates and evaluating dating methods using phylogenomic and mitochondrial data in squamate reptiles.

Recently, phylogenetics has expanded to routinely include estimation of clade ages in addition to their relationships. Various dating methods have been used, but their relative performance remains understudied. Here, we generate and assemble an extensive phylogenomic data set for squamate reptiles (lizards and snakes) and evaluate two widely used dating methods, penalized likelihood in r8s (r8s-PL) and Bayesian estimation with uncorrelated relaxed rates among lineages (BEAST). We obtained sequence data from 25 nuclear loci (∼500-1,000 bp per gene; 19,020bp total) for 64 squamate species and nine outgroup taxa, estimated the phylogeny, and estimated divergence dates using 14 fossil calibrations. We then evaluated how well each method approximated these dates using random subsets of the nuclear loci (2, 5, 10, 15, and 20; replicated 10 times each), and using ∼1 kb of the mitochondrial ND2 gene. We find that estimates from r8s-PL based on 2, 5, or 10 loci can differ considerably from those based on 25 loci (mean absolute value of differences between 2-locus and 25-locus estimates were 9.0 Myr). Estimates from BEAST are somewhat more consistent given limited sampling of loci (mean absolute value of differences between 2 and 25-locus estimates were 5.0 Myr). Most strikingly, age estimates using r8s-PL for ND2 were ∼68-82 Myr older (mean=73.1) than those using 25 nuclear loci with r8s-PL. These results show that dates from r8s-PL with a limited number of loci (and especially mitochondrial data) can differ considerably from estimates derived from a large number of nuclear loci, whereas estimates from BEAST derived from fewer nuclear loci or mitochondrial data alone can be surprisingly similar to those from many nuclear loci. However, estimates from BEAST using relatively few loci and mitochondrial data could still show substantial deviations from the full data set (>50 Myr), suggesting the benefits of sampling many nuclear loci. Finally, we found that confidence intervals on ages from BEAST were not significantly different when sampling 2 vs. 25 loci, suggesting that adding loci decreased errors but did not increase confidence in those estimates.

Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species.

Squamate reptiles (lizards and snakes) are one of the most diverse groups of terrestrial vertebrates. Recent molecular analyses have suggested a very different squamate phylogeny relative to morphological hypotheses, but many aspects remain uncertain from molecular data. Here, we analyse higher-level squamate phylogeny with a molecular dataset of unprecedented size, including 161 squamate species for up to 44 nuclear genes each (33 717 base pairs), using both concatenated and species-tree methods for the first time. Our results strongly resolve most squamate relationships and reveal some surprising results. In contrast to most other recent studies, we find that dibamids and gekkotans are together the sister group to all other squamates. Remarkably, we find that the distinctive scolecophidians (blind snakes) are paraphyletic with respect to other snakes, suggesting that snakes were primitively burrowers and subsequently re-invaded surface habitats. Finally, we find that some clades remain poorly supported, despite our extensive data. Our analyses show that weakly supported clades are associated with relatively short branches for which individual genes often show conflicting relationships. These latter results have important implications for all studies that attempt to resolve phylogenies with large-scale phylogenomic datasets.

Intercontinental dispersal by a microendemic burrowing reptile (Dibamidae).

Intercontinental dispersal via land bridge connections has been important in the biogeographic history of many Holarctic plant and animal groups. Likewise, some groups appear to have accomplished trans-oceanic dispersal via rafting. Dibamid lizards are a clade of poorly known fossorial, essentially limbless species traditionally split into two geographically disjunct genera: Dibamus comprises approximately 20 Southeast Asian species, many of which have very limited geographical distributions, and the monotypic genus Anelytropsis occupies a small area of northeastern Mexico. Although no formal phylogeny of the group exists, a sister-taxon relationship between the two genera has been assumed based on biogeographic considerations. We used DNA sequence data from one mitochondrial and six nuclear protein-coding genes to construct a phylogeny of Dibamidae and to estimate divergence times within the group. Surprisingly, sampled Dibamus species form two deeply divergent, morphologically conserved and geographically concordant clades, one of which is the sister taxon of Anelytropsis papillosus. Our analyses indicate Palaearctic to Nearctic Beringian dispersal in the Late Palaeocene to Eocene. Alternatively, a trans-Pacific rafting scenario would extend the upper limit on dispersal to the Late Cretaceous. Either scenario constitutes a remarkable long-distance dispersal in what would seem an unlikely candidate.

Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation.

Iguanian lizards form a diverse clade whose members have been the focus of many comparative studies of ecology, behavior, and evolution. Despite the importance of phylogeny to such studies, interrelationships among many iguanian clades remain uncertain. Within the Old World clade Acrodonta, Agamidae is sometimes found to be paraphyletic with respect to Chamaeleonidae, and recent molecular studies have produced conflicting results for many major clades. Within the largely New World clade Pleurodonta, relationships among the 12 currently recognized major subclades (mostly ranked as families) have been largely unresolved or poorly supported in previous studies. To clarify iguanian evolutionary history, we first infer phylogenies using concatenated maximum-likelihood (ML) and Bayesian analyses of DNA sequence data from 29 nuclear protein-coding genes for 47 iguanian and 29 outgroup taxa. We then estimate a relaxed-clock Bayesian chronogram for iguanians using BEAST. All three methods produce identical topologies. Within Acrodonta, we find strong support for monophyly of Agamidae with respect to Chamaeleonidae, and for almost all relationships within agamids. Within Pleurodonta, we find strong Bayesian support for almost all relationships, and strong ML support for some interfamilial relationships and for monophyly of almost all families (excepting Polychrotidae). Our phylogenetic results suggest a non-traditional biogeographic scenario in which pleurodonts originated in the Northern Hemisphere and subsequently spread southward into South America. The pleurodont portion of the tree is characterized by several very short, deep branches, raising the possibility of deep coalescences that may confound concatenated analyses. We therefore also use 27 of these genes to implement a coalescent-based species-tree approach for pleurodonts. Although this analysis strongly supports monophyly of the pleurodont families, interfamilial relationships are generally different from those in the concatenated tree, and support is uniformly poor. However, a species-tree analysis using only the seven most variable loci yields higher support and more congruence with the concatenated tree. This suggests that low support in the 27-gene species-tree analysis may be an artifact of the many loci that are uninformative for very short branches. This may be a general problem for the application of species-tree methods to rapid radiations, even with phylogenomic data sets. Finally, we correct the non-monophyly of Polychrotidae by recognizing the pleurodont genus Anolis (sensu lato) as a separate family (Dactyloidae), and we correct the non-monophyly of the agamid genus Physignathus by resurrection of the genus Istiurus for the former Physignathus lesueurii.

Combining phylogenomics and fossils in higher-level squamate reptile phylogeny: molecular data change the placement of fossil taxa.

Molecular data offer great potential to resolve the phylogeny of living taxa but can molecular data improve our understanding of relationships of fossil taxa? Simulations suggest that this is possible, but few empirical examples have demonstrated the ability of molecular data to change the placement of fossil taxa. We offer such an example here. We analyze the placement of snakes among squamate reptiles, combining published morphological data (363 characters) and new DNA sequence data (15,794 characters, 22 nuclear loci) for 45 living and 19 fossil taxa. We find several intriguing results. First, some fossil taxa undergo major changes in their phylogenetic position when molecular data are added. Second, most fossil taxa are placed with strong support in the expected clades by the combined data Bayesian analyses, despite each having >98% missing cells and despite recent suggestions that extensive missing data are problematic for Bayesian phylogenetics. Third, morphological data can change the placement of living taxa in combined analyses, even when there is an overwhelming majority of molecular characters. Finally, we find strong but apparently misleading signal in the morphological data, seemingly associated with a burrowing lifestyle in snakes, amphisbaenians, and dibamids. Overall, our results suggest promise for an integrated and comprehensive Tree of Life by combining molecular and morphological data for living and fossil taxa.

Phylogenetic relationships of phrynosomatid lizards based on nuclear and mitochondrial data, and a revised phylogeny for Sceloporus.

Phrynosomatid lizards are among the most common and diverse groups of reptiles in western North America, Mexico, and Central America. Phrynosomatidae includes 136 species in 10 genera. Phrynosomatids are used as model systems in many research programs in evolution and ecology, and much of this research has been undertaken in a comparative phylogenetic framework. However, relationships among many phrynosomatid genera are poorly supported and in conflict between recent studies. Further, previous studies based on mitochondrial DNA sequences suggested that the most species-rich genus (Sceloporus) is possibly paraphyletic with respect to as many as four other genera (Petrosaurus, Sator, Urosaurus, and Uta). Here, we collect new sequence data from five nuclear genes and combine them with published data from one additional nuclear gene and five mitochondrial gene regions. We compare trees from nuclear and mitochondrial data from 37 phrynosomatid taxa, including a "species tree" (from BEST) for the nuclear data. We also present a phylogeny for 122 phrynosomatid species based on maximum likelihood analysis of the combined data, which provides a strongly-supported hypothesis for relationships among most phrynosomatid genera and includes most phrynosomatid species. Our results strongly support the monophyly of Sceloporus (including Sator) and many of the relationships within it. We present a new classification for phrynosomatid lizards and the genus Sceloporus, and offer a new tree with branch lengths for use in comparative studies.

Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead?

Using phylogeny-based methods to identify evolutionary transitions has become an integral part of evolutionary biology. Here, we demonstrate the potential for these methods to give statistically well-supported but misleading inferences about character evolution. We also show how inferences of character evolution can be informed using GIS-based methods to reconstruct ancestral environmental regimes. We reconstruct a phylogeny for marsupial frogs (Hemiphractidae) using nuclear and mitochondrial DNA sequences and estimate patterns of life-history evolution across the resulting tree. We find that Gastrotheca species with complex life cycles (i.e., egg, tadpole, and adult stages) are phylogenetically nested among species and genera with direct development (i.e., egg and adult stages only). Assuming a single rate for gains and losses in likelihood reconstructions, there is strong statistical support for the hypothesis that the tadpole stage was lost early in the phylogeny but reappeared within Gastrotheca. Assuming different rates of gain and loss, the model with significantly higher statistical support, the tadpole stage seems to have been lost multiple times but never regained. Given that both hypotheses cannot be correct, at least one reconstruction model must be giving well-supported but misleading results. Several lines of evidence (including GIS-based reconstructions of the ancestral climatic regime) suggest that the former hypothesis is correct, and that the tadpole stage has evolved from direct development within Gastrotheca, the only known case of such a reversal in frogs.

A phylogenetic perspective on elevational species richness patterns in Middle American treefrogs: why so few species in lowland tropical rainforests?

Differences in species richness at different elevations are widespread and important for conservation, but the causes of these patterns remain poorly understood. Here, we use a phylogenetic perspective to address the evolutionary and biogeographic processes that underlie elevational diversity patterns within a region. We focus on a diverse but well-studied fauna of tropical amphibians, the hylid frogs of Middle America. Middle American treefrogs show a "hump-shaped" pattern of species richness (common in many organisms and regions), with the highest regional diversity at intermediate elevations. We reconstructed phylogenetic relationships among 138 species by combining new and published sequence data from 10 genes and then used this phylogeny to infer evolutionary rates and patterns. The high species richness of intermediate elevations seems to result from two factors. First, a tendency for montane clades to have higher rates of diversification. Second, the early colonization of montane regions, leaving less time for speciation to build up species richness in lowland regions (including tropical rainforests) that have been colonized more recently. This "time-for-speciation" effect may explain many diversity patterns and has important implications for conservation. The results also imply that local-scale environmental factors alone may be insufficient to explain the high species richness of lowland tropical rainforests, and that diversification rates are lower in earth's most species-rich biome.

Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles.

Why does a trait evolve repeatedly within a clade? When examining the evolution of a trait, evolutionary biologists typically focus on the selective advantages it may confer and the genetic and developmental mechanisms that allow it to vary. Although these factors may be necessary to explain why a trait evolves in a particular instance, they may not be sufficient to explain phylogenetic patterns of repeated evolution or conservatism. Instead, other factors may also be important, such as biogeography and competitive interactions. In squamate reptiles (lizards and snakes) a dramatic transition in body form has occurred repeatedly, from a fully limbed, lizardlike body form to a limb-reduced, elongate, snakelike body form. We analyze this trait in a phylogenetic and biogeographic context to address why this transition occurred so frequently. We included 261 species for which morphometric data and molecular phylogenetic information were available. Among the included species, snakelike body form has evolved about 25 times. Most lineages of snakelike squamates belong to one of two "ecomorphs," either short-tailed burrowers or long-tailed surface dwellers. The repeated origins of snakelike squamates appear to be associated with the in situ evolution of these two ecomorphs on different continental regions (including multiple origins of the burrowing morph within most continents), with very little dispersal of most limb-reduced lineages between continental regions. Overall, the number of repeated origins of snakelike morphology seems to depend on large-scale biogeographic patterns and community ecology, in addition to more traditional explanations (e.g., selection, development).

Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity.

Why are there more species in the tropics than in temperate regions? In recent years, this long-standing question has been addressed primarily by seeking environmental correlates of diversity. But to understand the ultimate causes of diversity patterns, we must also examine the evolutionary and biogeographic processes that directly change species numbers (i.e., speciation, extinction, and dispersal). With this perspective, we dissect the latitudinal diversity gradient in hylid frogs. We reconstruct a phylogeny for 124 hylid species, estimate divergence times and diversification rates for major clades, reconstruct biogeographic changes, and use ecological niche modeling to identify climatic variables that potentially limit dispersal. We find that hylids originated in tropical South America and spread to temperate regions only recently (leaving limited time for speciation). There is a strong relationship between the species richness of each region and when that region was colonized but not between the latitudinal positions of clades and their rates of diversification. Temperature seasonality seemingly limits dispersal of many tropical clades into temperate regions and shows significant phylogenetic conservatism. Overall, our study illustrates how two general principles (niche conservatism and the time-for-speciation effect) may help explain the latitudinal diversity gradient as well as many other diversity patterns across taxa and regions.

Integrated analyses resolve conflicts over squamate reptile phylogeny and reveal unexpected placements for fossil taxa.

Squamate reptiles (lizards and snakes) are a pivotal group whose relationships have become increasingly controversial. Squamates include >9000 species, making them the second largest group of terrestrial vertebrates. They are important medicinally and as model systems for ecological and evolutionary research. However, studies of squamate biology are hindered by uncertainty over their relationships, and some consider squamate phylogeny unresolved, given recent conflicts between molecular and morphological results. To resolve these conflicts, we expand existing morphological and molecular datasets for squamates (691 morphological characters and 46 genes, for 161 living and 49 fossil taxa, including a new set of 81 morphological characters and adding two genes from published studies) and perform integrated analyses. Our results resolve higher-level relationships as indicated by molecular analyses, and reveal hidden morphological support for the molecular hypothesis (but not vice-versa). Furthermore, we find that integrating molecular, morphological, and paleontological data leads to surprising placements for two major fossil clades (Mosasauria and Polyglyphanodontia). These results further demonstrate the importance of combining fossil and molecular information, and the potential problems of estimating the placement of fossil taxa from morphological data alone. Thus, our results caution against estimating fossil relationships without considering relevant molecular data, and against placing fossils into molecular trees (e.g. for dating analyses) without considering the possible impact of molecular data on their placement.

Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae).

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.