Sceloporus variabilis

Number of Pages: 3Integrative BiologyGeological Science

How important is it to consider lineage diversification heterogeneity in macroevolutionary studies? Lessons from the lizard family Liolaemidae

Macroevolutionary and biogeographical studies commonly apply multiple models to test state-dependent diversification. These models track the association between states of interest along a phylogeny, although many of them do not consider whether different clades might be evolving under different evolutionary drivers. Yet, they are still commonly applied to empirical studies without careful consideration of possible lineage diversification heterogeneity along the phylogenetic tree. A recent biogeographic study has suggested that orogenic uplift of the southern Andes has acted as a species pump, driving diversification of the lizard family Liolaemidae (307 described species), native to temperate southern South America. Here, we argue against the Andean uplift as main driver of evolution in this group. We show that there is a clear pattern of heterogeneous diversification in the Liolaemidae, which biases state- and environment-dependent analyses in, respectively, the GeoSSE and RPANDA programs. We show here that there are two shifts to accelerated speciation rates involving two clades that have both been classified as having Andean distributions. We incorporated the Geographic Hidden-State Speciation and Extinction model (GeoHiSSE) to accommodate unrelated diversification shifts, and also re-analyzed the data in RPANDA program after splitting biologically distinct clades for separate analyses, as well as including a more appropriate set of models. We demonstrate that the ?Andean uplift? hypothesis is not supported when the heterogeneous diversification histories among these lizards is considered. We use the Liolaemidae as an ideal system to demonstrate potential risks of ignoring clade-specific differences in diversification patterns in macroevolutionary studies. We also implemented simulations to show that, in agreement with previous findings, the HiSSE approach can effectively and substantially reduce the level of distribution- dependent models receiving the highest AIC weights in such scenarios. However, we still find a relatively high rate (15%) of distribution-dependent models receiving the highest AIC weights, and provide recommendations related to the set of models included in the analyses that reduce these rates by half. Finally, we demonstrate that trees including clades following different dependent-drivers affect RPANDA analyses by producing different outcomes, ranging from partially correct models to completely misleading results. We provide recommendations for the implementation of both programs.Fil: Olave, Melisa. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Provincia de Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Universidad Nacional de Cuyo. Instituto Argentino de Investigaciones de las Zonas Áridas; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados UnidosFil: Morando, Mariana. Universidad Nacional de la Patagonia "San Juan Bosco"; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; Argentin

Model-based approach to test hard polytomies in the Eulaemus clade of the most diverse South American lizard genus Liolaemus (Liolaemini, Squamata)

Lack of resolution in a phylogenetic tree is usually represented as a polytomy, and often adding more data (loci and taxa) resolves the species tree. These are the ‘soft’ polytomies, but in other cases additional data fail to resolve relationships; these are the ‘hard’ polytomies. This latter case is often interpreted as a simultaneous radiation of lineages in the history of a clade. Although hard polytomies are difficult to address, model-based approaches provide new tools to test these hypotheses. Here, we used a clade of 144 species of the South American lizard clade Eulaemus to estimate phylogenies using a traditional concatenated matrix and three species tree methods: *BEAST, BEST, and minimizing deep coalescences (MDC). The different species tree methods recovered largely discordant results, but all resolved the same polytomy (e.g. very short internodes amongst lineages and low nodal support in Bayesian methods). We simulated data sets under eight explicit evolutionary models (including hard polytomies), tested these against empirical data (a total of 14 loci), and found support for two polytomies as the most plausible hypothesis for diversification of this clade. We discuss the performance of these methods and their limitations under the challenging scenario of hard polytomies.Fil: Olave, Melisa. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados UnidosFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentin

Accuracy and Precision of Species Trees: Effects of Locus, Individual, and Base Pair Sampling on Inference of Species Trees in Lizards of the Liolaemus darwinii Group (Squamata, Liolaemidae)

Molecular phylogenetics has entered a new era in which species trees are estimated from a collection of gene trees using methods that accommodate their heterogeneity and discordance with the species tree. Empirical evaluation of species trees is necessary to assess the performance (i.e., accuracy and precision) of these methods with real data, which consists of gene genealogies likely shaped by different historical and demographic processes. We analyzed 20 loci for 16 species of the South American lizards of the Liolaemus darwinii species group and reconstructed a species tree with *BEAST, then compared the performance of this method under different sampling strategies of loci, individuals, and sequence lengths. We found an increase in the accuracy and precision of species trees with the number of loci, but for any number of loci, accuracy substantially decreased only when using only one individual per species or 25% of the full sequence length (~147 base-pairs). In addition, locus ´informativeness´ was an important factor in the accuracy/precision of species trees when using a few loci, but it became increasingly irrelevant with additional loci. Our empirical results combined with previous simulation studies suggest that there is an optimal range of sampling effort of loci, individuals, and sequence lengths for a given speciation history and information content of the data. Future studies should be directed towards further assessment of other factors that can impact performance of species trees, including gene flow, locus ´informativeness´, tree shape, missing data, and errors in species delimitation.Fil: Camargo Bentaberry, Arley. University Brigham Young; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados Unido

Molecular phylogeny of the liolaemus kriegi complex (Iguania, Liolaemini)

We provide a well-supported phylogenetic hypothesis for all recognized lineages of the Liolaemus kriegi complex based on a multilocus dataset. We used 29 individuals from the eight taxa included in this complex for which we sequenced eight gene regions (two mitochondrial and six nuclear). We implemented maximum likelihood and Bayesian inference methods for the mitochondrial, nuclear, and concatenated sequences and employed BEAST to estimate the species tree. The all genes concatenated analyses and the species trees recovered the L. kriegi complex as monophyletic with high support, including three described species (L. kriegi, Liolaemus ceii, and Liolaemus buergeri) and three previously identified candidate species (Liolaemus sp. A, Liolaemus sp. C, and Liolaemus sp. D), with Liolaemus tregenzai as a closely related taxon. Another previously proposed candidate species (L. sp. B) has a labile topological position that varies depending on the type of markers and analytical methods used. In the mitochondrial gene tree, L. sp. B is recovered within the L. kriegi complex whereas in the "all genes concatenated" analyses and in the nuclear species tree analyses, it is recovered outside of this complex as sister to Liolaemus petrophilus (a representative of the L. petrophilus group). Morphologically, L. sp. B is indistinguishable from L. austromendocinus (also included in the L. petrophilus group); thus, we do not consider L. sp. B as part of the L. kriegi complex. We estimated divergence times for the major clades of the complex based on the species tree hypothesis, and all were inferred to have a Pleistocene origin.Fil: Medina, Cintia Débora. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados UnidosFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentin

Early stages of divergence: phylogeography, climate modeling, and morphological differentiation in the South American lizard Liolaemus petrophilus (Squamata: Liolaemidae)

This study examines the phylogeographic structure within the Patagonian lizard Liolaemus petrophilus and tests for patterns of between-clade morphological divergence and sexual dimorphism as well as demographic and niche changes associated with Pleistocene climate changes. We inferred intra-specific relationships, tested hypotheses for historical patterns of  population expansion, and incorporated ecological niche modeling (ENM) with standard  morphological and geometric morphometric analyses to examine between-clade divergence as indirect evidence for adaptation to different niches. The two inferred haploclades diverged during the early Pleistocene with the Southern clade depicting the genetic signature of a recent population increase associated with expanding niche envelope, whereas the Northern clade shows stable populations in a shrinking niche envelope. The combination of molecular evidence for post-isolation demographic change and ENM, suggest that the two haploclades have responded differently to Pleistocene climatic events.Fil: Fontanella, Frank M.. Morehead State University; Estados UnidosFil: Feltrin, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados UnidosFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentin

Phylogenetic insights on evolutionary novelties in lizards and snakes: sex, birth, bodies, niches

Abstract Squamate reptiles (lizards and snakes) are a diverse clade in which there appear to have been multiple origins of many remarkable traits, including (a) parthenogenetic reproduction, (b) viviparity, (c) snake-like, limb-reduced body form, (d ) herbivory, and (e) venom. These repeated transitions make squamates an outstanding/excellent system for addressing many fundamental questions in evolutionary biology. For example, they are the only vertebrate group with true parthenogenesis (with at least 40 separate origins), they have more origins of viviparity than any other group of vertebrates, and they have undergone dramatic changes in body form (lizard-like to snake-like) dozens of times. New molecular phylogenies for squamates have overturned many traditional hypotheses and taxonomies based on morphology and are now revealing exciting new insights into the evolution of many of these traits at both higher and lower taxonomic levels. In this review, we summarize many of these new insights and outline important areas for future research

Phylogenomic evidence for a recent and rapid radiation of lizards in the Patagonian Liolaemus fitzingerii species group

Rapid evolutionary radiations are difficult to resolve because divergence events are nearly synchronous and gene flow among nascent species can be high, resulting in a phylogenetic “bush”. Large datasets composed of sequence loci from across the genome can potentially help resolve some of these difficult phylogenetic problems. A suitable test case is the Liolaemus fitzingerii species group of lizards, which includes twelve species that are broadly distributed in Argentinean Patagonia. The species in the group have had a complex evolutionary history that has led to high morphological variation and unstable taxonomy. We generated a sequence capture dataset for 28 ingroup individuals of 580 nuclear loci, alongside a mitogenomic dataset, to infer phylogenetic relationships among species in this group. Relationships among species were generally weakly supported with the nuclear data, and along with an inferred age of ∼2.6 million years old, indicate either rapid evolution, hybridization, incomplete lineage sorting, non-informative data, or a combination thereof. We inferred a signal of mito-nuclear discordance, indicating potential hybridization between L. melanops and L. martorii, and phylogenetic network analyses provided support for 5 reticulation events among species. Phasing the nuclear loci did not provide additional insight into relationships or suspected patterns of hybridization. Only one clade, composed of L. camarones, L. fitzingerii, and L. xanthoviridis was recovered across all analyses. Genomic datasets provide molecular systematists with new opportunities to resolve difficult phylogenetic problems, yet the lack of phylogenetic resolution in Patagonian Liolaemus is biologically meaningful and indicative of a recent and rapid evolutionary radiation. The phylogenetic relationships of the Liolaemus fitzingerii group may be best modeled as a reticulated network instead of a bifurcating phylogeny.Fil: Grummer, Jared A.. University of Washington; Estados UnidosFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados UnidosFil: Leaché, Adam D.. University of Washington; Estados Unido

Quaternary range and demographic expansion of Liolaemus darwinii (Squamata: Liolaemidae) in the Monte Desert of Central Argentina using Bayesian phylogeography and ecological niche modelling

Until recently, most phylogeographic approaches have been unable to distinguís between demographic and range expansion processes, making it difficult to test for the possibility of range expansion without population growth and vice versa. In this study, we applied a Bayesian phylogeographic approach to reconstruct both demographic and range expansion in the lizard Liolaemus darwinii of the Monte Desert in Central Argentina, during the Late Quaternary. Based on analysis of 14 anonymous nuclear loci and the cytochrome b mitochondrial DNA gene, we detected signals of demographic expansion starting at ~55 ka based on Bayesian Skyline and Skyride Plots. In contrast, Bayesian relaxed models of spatial diffusion suggested that range expansion occurred only between ~95 and 55 ka, and more recently, diffusion rates were very low during demographic expansion. The possibility of population growth without substantial range expansion could account for the shared patterns of demographic expansion during the Last Glacial Maxima (OIS 2 and 4) in fish, small mammals and other lizards of the Monte Desert. We found substantial variation in diffusion rates over time, and very high rates during the range expansion phase, consistent with a rapidly advancing expansion front towards the southeast shown by palaeo-distribution models. Furthermore, the estimated diffusion rates are congruent with observed dispersal rates of lizards in field conditions and therefore provide additional confidence to the temporal scale of inferred phylogeographic patterns. Our study highlights how the integration of phylogeography with palaeo-distribution models can shed light on both demographic and range expansion processes and their potential causes.Fil: Camargo Bentaberry, Arley. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Werneck, Fernanda P.. Brigham Young University. Life Science Museum. Department of Biology & Bean; Estados Unidos. Universidade de Brasılia. Departamento de Zoologia; BrasilFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Sites Jr., Jack W.. Brigham Young University. Life Science Museum. Department of Biology & Bean; Estados UnidosFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentin

Lagartijas de la provincia de Santa Cruz, Argentina: distribución geográfica, diversidad genética y estado de conservación

Este trabajo resume las características geográficas, genéticas y de conservación de los saurios de la provincia de Santa Cruz; se presentan también comentarios acerca del estado del arte de la investigación en la provincia y las perspectivas futuras de los mismos. Utilizando ~ 1500 registros de presencia, se realiza un inventario biológico actualizado y se incluyen mapas de distribución, fotografías de las especies, comentarios genéticos y estatus de conservación para las lagartijas de Santa Cruz. El número de especies de lagartijas distribuidas en esta provincia es de 29 (27 especies y dos subespecies), sin embargo tres de éstas no presentan registros actuales. En base a los patrones genéticos se identifican al menos diez especies candidatas, linajes no descriptos que poseen suficiente diferenciación genética como para representar especies nuevas, cuyo estatus específico tiene que ser evaluado en futuras investigaciones. Este trabajo combina la información tradicionalmente presentada en inventarios biológicos con información genética, de distribución y estatus de conservación. Más allá de la novedosa integración realizada, este trabajo tiene la potencialidad de guiar el desarrollo de estudios detallados, en los que se puedan identificar (entre otras) zonas tanto para conservación como para explotación sustentable, así como también puede acelerar la descripción de nuevos taxa llenando los vacíos en el conocimiento de la taxonomía alfa.In this paper we present a revision of the geographic distribution, genetic characteristics and conservation status of lizards from the Santa Cruz province. We summarize the state-of-the-art knowledge base and future perspectives of herpetological research in this province. We present an updated checklist using ~1500 records of lizards, and include distributional maps, species photographs, comments on genetic variability and the conservation status of all recognized species. Twenty-nine species of lizards (26 species and 3 subspecies) are cited for this territory, although three of them lack of recent references, and from the genetic patterns we identify at least ten candidate species. These are defined as non-described lineages characterized by suffi - cient genetic differentiation to likely represent new species, but intensive taxonomic work is needed in order to confirm their specific status. In combining traditional information presented in checklists with genetic data, distributional patterns, and conservation status, we hope that this novel data integration approach will lead other investigators to develop similar studies. These types of studies represent the first step towards identification of priority conservation areas, as well as identification of those that are more appropriate for intense anthropogenic use; moreover this study will accelerate the description of new taxa, thereby filling gaps in alpha taxonomic knowledge.Fil: Breitman, Maria Florencia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Minoli, Ignacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Medina, Cintia Débora. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Sites Jr., Jack W.. University Brigham Young; Estados UnidosFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; Argentin