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      High Levels of Diversity Uncovered in a Widespread Nominal Taxon: Continental Phylogeography of the Neotropical Tree Frog Dendropsophus minutus

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      1 , 2 , * ,   3 , 4 , 5 , 1 , 6 , 7 , 3 ,   8 , 9 , 10 , 11 , 12 , 13 , 10 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 18 , 1 , 22
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          Abstract

          Species distributed across vast continental areas and across major biomes provide unique model systems for studies of biotic diversification, yet also constitute daunting financial, logistic and political challenges for data collection across such regions. The tree frog Dendropsophus minutus (Anura: Hylidae) is a nominal species, continentally distributed in South America, that may represent a complex of multiple species, each with a more limited distribution. To understand the spatial pattern of molecular diversity throughout the range of this species complex, we obtained DNA sequence data from two mitochondrial genes, cytochrome oxidase I (COI) and the 16S rhibosomal gene (16S) for 407 samples of D. minutus and closely related species distributed across eleven countries, effectively comprising the entire range of the group. We performed phylogenetic and spatially explicit phylogeographic analyses to assess the genetic structure of lineages and infer ancestral areas. We found 43 statistically supported, deep mitochondrial lineages, several of which may represent currently unrecognized distinct species. One major clade, containing 25 divergent lineages, includes samples from the type locality of D. minutus. We defined that clade as the D. minutus complex. The remaining lineages together with the D. minutus complex constitute the D. minutus species group. Historical analyses support an Amazonian origin for the D. minutus species group with a subsequent dispersal to eastern Brazil where the D. minutus complex originated. According to our dataset, a total of eight mtDNA lineages have ranges >100,000 km 2. One of them occupies an area of almost one million km 2 encompassing multiple biomes. Our results, at a spatial scale and resolution unprecedented for a Neotropical vertebrate, confirm that widespread amphibian species occur in lowland South America, yet at the same time a large proportion of cryptic diversity still remains to be discovered.

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          Cryptic species as a window on diversity and conservation.

          The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
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            The integrative future of taxonomy

            Background Taxonomy is the biological discipline that identifies, describes, classifies and names extant and extinct species and other taxa. Nowadays, species taxonomy is confronted with the challenge to fully incorporate new theory, methods and data from disciplines that study the origin, limits and evolution of species. Results Integrative taxonomy has been proposed as a framework to bring together these conceptual and methodological developments. Here we review perspectives for an integrative taxonomy that directly bear on what species are, how they can be discovered, and how much diversity is on Earth. Conclusions We conclude that taxonomy needs to be pluralistic to improve species discovery and description, and to develop novel protocols to produce the much-needed inventory of life in a reasonable time. To cope with the large number of candidate species revealed by molecular studies of eukaryotes, we propose a classification scheme for those units that will facilitate the subsequent assembly of data sets for the formal description of new species under the Linnaean system, and will ultimately integrate the activities of taxonomists and molecular biologists.
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              Isolation by resistance.

              Brad McRae (2006)
              Despite growing interest in the effects of landscape heterogeneity on genetic structuring, few tools are available to incorporate data on landscape composition into population genetic studies. Analyses of isolation by distance have typically either assumed spatial homogeneity for convenience or applied theoretically unjustified distance metrics to compensate for heterogeneity. Here I propose the isolation-by-resistance (IBR) model as an alternative for predicting equilibrium genetic structuring in complex landscapes. The model predicts a positive relationship between genetic differentiation and the resistance distance, a distance metric that exploits precise relationships between random walk times and effective resistances in electronic networks. As a predictor of genetic differentiation, the resistance distance is both more theoretically justified and more robust to spatial heterogeneity than Euclidean or least cost path-based distance measures. Moreover, the metric can be applied with a wide range of data inputs, including coarse-scale range maps, simple maps of habitat and nonhabitat within a species' range, or complex spatial datasets with habitats and barriers of differing qualities. The IBR model thus provides a flexible and efficient tool to account for habitat heterogeneity in studies of isolation by distance, improve understanding of how landscape characteristics affect genetic structuring, and predict genetic and evolutionary consequences of landscape change.
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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
                2014
                10 September 2014
                : 9
                : 9
                : e103958
                Affiliations
                [1 ]Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Braunschweig, Germany
                [2 ]Pós-graduação em Sistemática e Evolução, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova, Natal, RN, Brasil
                [3 ]Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
                [4 ]Smithsonian Tropical Research Institute, Panamá, Republic of Panama
                [5 ]Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, São Paulo, Brasil
                [6 ]Trier University, Biogeography Department, Trier, Germany
                [7 ]CNRS-Guyane - USR3456, Immeuble Le Relais - 2, Cayenne, French Guiana
                [8 ]Departamento de Zoologia, Instituto de Biociências, UNESP, Rio Claro, São Paulo, Brasil; Instituto de Investigación Biológica del Paraguay, Asunción, Paraguay
                [9 ]Museo Nacional de Ciencias Naturales, Madrid, Spain
                [10 ]Museum of Zoology, Senckenberg Natural History Collections Dresden, Dresden, Germany
                [11 ]Peruvian Center for Biodiversity and Conservation (PCRC), Nanay, Iquitos, Peru
                [12 ]Zoologische Staatssammlung München, München, Germany
                [13 ]Universidad Tecnológica Indoamérica, Centro de Investigación de la Biodiversidad y el Cambio Climático (BioCamp), Cotocollao, Quito, Ecuador
                [14 ]Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main, Germany
                [15 ]Amphibian Evolution Lab, Department of Biology, Vrije Universiteit Brussel, Brussels, Belgium
                [16 ]German Herpetological Society (DGHT), Mannheim, Germany
                [17 ]Universidade Tecnológica Federal do Paraná, Francisco Beltrão, PR, Brasil
                [18 ]Departamento de Zoologia, Instituto de Biociências, UNESP, Rio Claro, São Paulo, Brasil
                [19 ]Department of Zoology, National Museum, Prague, Czech Republic
                [20 ]Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
                [21 ]Fundación La Salle de Ciencias Naturales, Museo de Historia Natural La Salle, Caracas, Venezuela
                [22 ]Hessisches Landesmuseum Darmstadt, Department of Zoology, Darmstadt, Germany
                [23 ]Laboratorio de Ecología y Genética de Poblaciones, Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela
                [24 ]Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Rodovia Ilhéus-Itabuna, Bahia, Brasil
                [25 ]Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, São Paulo, Brasil
                [26 ]Department of Biology, East Carolina University, Greenville, North Carolina, United States of America
                Australian Museum, Australia
                Author notes

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

                Conceived and designed the experiments: MG MV JK. Performed the experiments: MG AJC VGDO SL AF LSB FB IR RE GGU FG JMG MH MJ PJRK AK RL ML JM JPP FJMR AS JCS MS MTR ET CFBH MV JK. Analyzed the data: MG AJC AR SL MV JK. Contributed reagents/materials/analysis tools: MG AJC VGDO SL AF LSB FB IR RE GGU FG JMG MH MJ PJRK AK RL ML JM JPP FJMR AS JCS MS MTR ET CFBH MV JK. Wrote the paper: MG AJC VGDO MV JK.

                Article
                PONE-D-14-02034
                10.1371/journal.pone.0103958
                4160190
                25208078
                b48b3a2f-6910-4c7d-9224-6ef6affb364e
                Copyright @ 2014

                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
                : 28 January 2014
                : 4 July 2014
                Page count
                Pages: 12
                Funding
                AR was supported by a Post-Doctoral fellowship of the Alexander von Humboldt foundation. CFBH acknowledges support by FAPESP (proc. 2008/50928-1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq. FB thanks Programa Nacional de Incentivo a Investigadores (PRONII, Paraguay) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) for financial support. JM was financially supported by the Ministry of Culture of the Czech Republic (DKRVO 2012 and DKRVO 2013/14; 00023272). MG was supported by a PhD fellowship of the KAAD. MTR acknowledges support by FAPESP (#s 03/10335-8, 10/51071-7, and 11/50146-6), CNPq, and NSF (DEB 1035184 and 1120487). MV acknowledges support by the Deutsche Forschungsgemeinschaft (grant VE247/7-1). PJRK was mainly supported by the Belgian Directorate-General of Development Cooperation, the King Léopold III Fund for Nature Exploration and Conservation, and the Percy Sladen Memorial Fund, with additional support by the non-profit organization “les Amis de l'Institut Royal des Sciences Naturelles”. RE and MH were supported by a research grant from the German Research Foundation (DFG ER 589/2*1). VGDO acknowledges support by Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP (#2012/12500-5). Laboratory work in Colombia was financed by grant #156-09 from Ecopetrol. Funding was provided by the Universidad Tecnológica Indoamérica through the project “Patrones de diversidad de los anfibios andinos del Ecuador”. JPP is grateful to CNPq and FAPERJ for financial support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biogeography
                Evolutionary Biology
                Evolutionary Systematics
                Molecular Systematics
                Phylogenetics
                Taxonomy
                Animal Taxonomy
                Zoology
                Reptile Biology

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