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      Lizards on Ice: Evidence for Multiple Refugia in Liolaemus pictus (Liolaemidae) during the Last Glacial Maximum in the Southern Andean Beech Forests

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          Abstract

          Historical climate changes and orogenesis are two important factors that have shaped intraspecific biodiversity patterns worldwide. Although southern South America has experienced such complex events, there is a paucity of studies examining the effects on intraspecific diversification in this part of the world. Liolaemus pictus is the southernmost distributed lizard in the Chilean temperate forest, whose genetic structure has likely been influenced by Pleistocene glaciations. We conducted a phylogeographic study of L. pictus in Chile and Argentina based on one mitochondrial and two nuclear genes recovering two strongly divergent groups, Northern and Southern clades. The first group is distributed from the northernmost limit of the species to the Araucanía region while the second group is distributed throughout the Andes and the Chiloé archipelago in Southern Chile. Our results suggest that L. pictus originated 751 Kya, with divergence between the two clades occurring in the late Pleistocene. Demographic reconstructions for the Northern and Southern clades indicate a decrease in effective population sizes likely associated with Pleistocene glaciations. Surprisingly, patterns of genetic variation, clades age and historical gene flow in populations distributed within the limits of the Last Glacial Maximum (LGM) are not explained by recent colonization. We propose an “intra-Andean multiple refuge” hypothesis, along with the classical refuge hypothesis previously proposed for the biota of the Chilean Coastal range and Eastern Andean Cordillera. Our hypothesis is supported by niche modelling analysis suggesting the persistence of fragments of suitable habitat for the species within the limits of the LGM ice shield. This type of refuge hypothesis is proposed for the first time for an ectothermic species.

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          Most cited references 21

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          Arlequin (version 3.0): An integrated software package for population genetics data analysis

          Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multi-locus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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            DnaSP, DNA polymorphism analyses by the coalescent and other methods.

            DnaSP is a software package for the analysis of DNA polymorphism data. Present version introduces several new modules and features which, among other options allow: (1) handling big data sets (approximately 5 Mb per sequence); (2) conducting a large number of coalescent-based tests by Monte Carlo computer simulations; (3) extensive analyses of the genetic differentiation and gene flow among populations; (4) analysing the evolutionary pattern of preferred and unpreferred codons; (5) generating graphical outputs for an easy visualization of results. The software package, including complete documentation and examples, is freely available to academic users from: http://www.ub.es/dnasp
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              Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution.

              A mismatch distribution is a tabulation of the number of pairwise differences among all DNA sequences in a sample. In a population that has been stationary for a long time these distributions from nonrecombinant DNA sequences become ragged and erratic, whereas a population that has been growing generates mismatch distributions that are smooth and have a peak. The position of the peak reflects the time of the population growth. The signature of an ancient population expansion is apparent even in the low-resolution mtDNA typings described by Merriwether et al. (1991). The smoothness of the mismatch distribution, an indicator of population expansion, is hardly affected by population structure, whereas mean sequence divergence increases in a pooled sample from highly isolated subpopulations.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                27 November 2012
                : 7
                : 11
                Affiliations
                [1 ]Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile
                [2 ]Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile
                [3 ]Centro de Estudios Avanzados en Zonas Áridas, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile
                [4 ]Department of Biology and Bean Life Science Museum, Brigham Young University, Provo, Utah, United States of America
                [5 ]Centro de Investigaciones de Ecosistemas de la Patagonia CIEP, Coihaique, Chile
                Fordham University, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: IVE PFV. Performed the experiments: IVE CMM. Analyzed the data: IVE CMM FMF NG. Contributed reagents/materials/analysis tools: PFV JWS. Wrote the paper: IVE PFV GD.

                Article
                PONE-D-12-13577
                10.1371/journal.pone.0048358
                3507886
                23209552

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 17
                Funding
                This work was financed by FONDECYT 1120872, DIUC Semilla 2009 016-SP UdeC, DIUC Semilla 205.113.067-1SP UdeC, and NSF-OISE 0530267. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Niche Construction
                Behavioral Ecology
                Spatial and Landscape Ecology
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Population Genetics
                Haplotypes
                Neutral Theory
                Genetics
                Animal Genetics
                Genomics
                Comparative Genomics
                Zoology
                Animal Behavior
                Herpetology

                Uncategorized

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