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      Phylogeographic Insights into a Peripheral Refugium: The Importance of Cumulative Effect of Glaciation on the Genetic Structure of Two Endemic Plants

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          Abstract

          Quaternary glaciations and mostly last glacial maximum have shaped the contemporary distribution of many species in the Alps. However, in the Maritime and Ligurian Alps a more complex picture is suggested by the presence of many Tertiary paleoendemisms and by the divergence time between lineages in one endemic species predating the Late Pleistocene glaciation. The low number of endemic species studied limits the understanding of the processes that took place within this region. We used species distribution models and phylogeographical methods to infer glacial refugia and to reconstruct the phylogeographical pattern of Silene cordifolia All. and Viola argenteria Moraldo & Forneris. The predicted suitable area for last glacial maximum roughly fitted current known distribution. Our results suggest that separation of the major clades predates the last glacial maximum and the following repeated glacial and interglacial periods probably drove differentiations. The complex phylogeographical pattern observed in the study species suggests that both populations and genotypes extinction was minimal during the last glacial maximum, probably due to the low impact of glaciations and to topographic complexity in this area. This study underlines the importance of cumulative effect of previous glacial cycles in shaping the genetic structure of plant species in Maritime and Ligurian Alps, as expected for a Mediterranean mountain region more than for an Alpine region.

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          Most cited references18

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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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            Measuring and testing genetic differentiation with ordered versus unordered alleles.

            Estimates and variances of diversity and differentiation measures in subdivided populations are proposed that can be applied to haplotypes (ordered alleles such as DNA sequences, which may contain a record of their own histories). Hence, two measures of differentiation can be compared for a single data set: one (GST) that makes use only of the allelic frequencies and the other (NST) for which similarities between the haplotypes are taken into account in addition. Tests are proposed to compare NST and GST with zero and with each other. The difference between NST and GST can be caused by several factors, including sampling artefacts, unequal effect of mutation rates and phylogeographic structure. The method presented is applied to a published data set where a nuclear DNA sequence had been determined from individuals of a grasshopper distributed in 24 regions of Europe. Additional insights into the genetic subdivision of these populations are obtained by progressively combining related haplotypes and reanalyzing the data each time.
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              Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations.

              Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (G(ST)) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on G(ST). Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (approximately 0.10). G(ST) at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas G(ST) at paternally and biparentally inherited markers also covary positively but more loosely and G(ST) at maternally inherited markers are largely independent of values based on nuclear markers. A model-based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen-to-seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (N(ST) or R(ST)) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.
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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, CA USA )
                1932-6203
                21 November 2016
                2016
                : 11
                : 11
                : e0166983
                Affiliations
                [1 ]DISTAV, Università degli studi di Genova, Genova, Italy
                [2 ]Dipartimento di Biologia, Università degli studi di Bari, Bari, Italy
                [3 ]Dipartimento di Bioscienze, Università degli studi di Milano, Milano, Italy
                Universita degli Studi di Milano-Bicocca, ITALY
                Author notes

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

                • Conceptualization: GC FG GZ LM.

                • Formal analysis: GC FG.

                • Funding acquisition: GC LM.

                • Investigation: FG GZ.

                • Project administration: GC LM.

                • Writing – original draft: GC FG LM.

                Author information
                http://orcid.org/0000-0002-3334-8551
                Article
                PONE-D-16-29168
                10.1371/journal.pone.0166983
                5117763
                27870888
                5eb9609b-37bb-409c-89a0-a283fbdaae6c
                © 2016 Casazza et al

                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.

                History
                : 21 July 2016
                : 7 November 2016
                Page count
                Figures: 5, Tables: 4, Pages: 18
                Funding
                Funded by: Interreg Alcotra
                Award ID: 192
                Award Recipient :
                Interreg Alcotra programme 2007-2013, project n. 192 BIODIVAM.
                Categories
                Research Article
                Biology and Life Sciences
                Biogeography
                Phylogeography
                Ecology and Environmental Sciences
                Biogeography
                Phylogeography
                Earth Sciences
                Geography
                Biogeography
                Phylogeography
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Phylogeography
                Biology and Life Sciences
                Genetics
                Population Genetics
                Phylogeography
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Phylogeography
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Haplotypes
                Biology and Life Sciences
                Genetics
                Population Genetics
                Haplotypes
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Haplotypes
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Biology and Life Sciences
                Genetics
                Population Genetics
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Biology and Life Sciences
                Paleontology
                Paleogenetics
                Earth Sciences
                Paleontology
                Paleogenetics
                Earth Sciences
                Atmospheric Science
                Climatology
                Paleoclimatology
                Biology and Life Sciences
                Paleontology
                Paleoclimatology
                Earth Sciences
                Paleontology
                Paleoclimatology
                Biology and Life Sciences
                Paleontology
                Paleobiology
                Paleobotany
                Earth Sciences
                Paleontology
                Paleobiology
                Paleobotany
                Biology and Life Sciences
                Paleontology
                Paleobotany
                Earth Sciences
                Paleontology
                Paleobotany
                Earth Sciences
                Geology
                Geologic Time
                Cenozoic Era
                Quaternary Period
                Pleistocene Epoch
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Sequencing Techniques
                Sequence Analysis
                Sequence Alignment
                Research and Analysis Methods
                Molecular Biology Techniques
                Sequencing Techniques
                Sequence Analysis
                Sequence Alignment
                Custom metadata
                DNA sequences are available at GenBank data base. Accession numbers are reported in S3 Table. Climatic data are available from WorldClim website ( http://www.worldclim.org). Data from a third party are available upon request directly to the proprietary. In particular, occurrence data from the SILENE and FLORE databases are available upon request from Conservatoire Botanique National Méditerranéen de Porquerolles ( http://www.cbnmed.fr/pres/index.php). The global lithological map dataset (GLiM) is available upon request via email from Dr. Nils Moosdorf (Institute for Biogeochemistry and Marine Chemistry, Universität Hamburg, Germany; http://www.zmt-bremen.de).

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