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      Delimiting species of Protaphorura (Collembola: Onychiuridae): integrative evidence based on morphology, DNA sequences and geography

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          Abstract

          Species delimitation remains a significant challenge when the diagnostic morphological characters are limited. Integrative taxonomy was applied to the genus Protaphorura (Collembola: Onychiuridae), which is one of most difficult soil animals to distinguish taxonomically. Three delimitation approaches (morphology, molecular markers and geography) were applied providing rigorous species validation criteria with an acceptably low error rate. Multiple molecular approaches, including distance- and evolutionary model-based methods, were used to determine species boundaries based on 144 standard barcode sequences. Twenty-two molecular putative species were consistently recovered across molecular and geographical analyses. Geographic criteria were was proved to be an efficient delimitation method for onychiurids. Further morphological examination, based on the combination of the number of pseudocelli, parapseudocelli and ventral mesothoracic chaetae, confirmed 18 taxa of 22 molecular units, with six of them described as new species. These characters were found to be of high taxonomical value. This study highlights the potential benefits of integrative taxonomy, particularly simultaneous use of molecular/geographical tools, as a powerful way of ascertaining the true diversity of the Onychiuridae. Our study also highlights that discovering new morphological characters remains central to achieving a full understanding of collembolan taxonomy.

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          Bayesian species delimitation using multilocus sequence data.

          In the absence of recent admixture between species, bipartitions of individuals in gene trees that are shared across loci can potentially be used to infer the presence of two or more species. This approach to species delimitation via molecular sequence data has been constrained by the fact that genealogies for individual loci are often poorly resolved and that ancestral lineage sorting, hybridization, and other population genetic processes can lead to discordant gene trees. Here we use a Bayesian modeling approach to generate the posterior probabilities of species assignments taking account of uncertainties due to unknown gene trees and the ancestral coalescent process. For tractability, we rely on a user-specified guide tree to avoid integrating over all possible species delimitations. The statistical performance of the method is examined using simulations, and the method is illustrated by analyzing sequence data from rotifers, fence lizards, and human populations.
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            DNA barcodes distinguish species of tropical Lepidoptera.

            Although central to much biological research, the identification of species is often difficult. The use of DNA barcodes, short DNA sequences from a standardized region of the genome, has recently been proposed as a tool to facilitate species identification and discovery. However, the effectiveness of DNA barcoding for identifying specimens in species-rich tropical biotas is unknown. Here we show that cytochrome c oxidase I DNA barcodes effectively discriminate among species in three Lepidoptera families from Area de Conservación Guanacaste in northwestern Costa Rica. We found that 97.9% of the 521 species recognized by prior taxonomic work possess distinctive cytochrome c oxidase I barcodes and that the few instances of interspecific sequence overlap involve very similar species. We also found two or more barcode clusters within each of 13 supposedly single species. Covariation between these clusters and morphological and/or ecological traits indicates overlooked species complexes. If these results are general, DNA barcoding will significantly aid species identification and discovery in tropical settings.
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              How to fail at species delimitation.

              Species delimitation is the act of identifying species-level biological diversity. In recent years, the field has witnessed a dramatic increase in the number of methods available for delimiting species. However, most recent investigations only utilize a handful (i.e. 2-3) of the available methods, often for unstated reasons. Because the parameter space that is potentially relevant to species delimitation far exceeds the parameterization of any existing method, a given method necessarily makes a number of simplifying assumptions, any one of which could be violated in a particular system. We suggest that researchers should apply a wide range of species delimitation analyses to their data and place their trust in delimitations that are congruent across methods. Incongruence across the results from different methods is evidence of either a difference in the power to detect cryptic lineages across one or more of the approaches used to delimit species and could indicate that assumptions of one or more of the methods have been violated. In either case, the inferences drawn from species delimitation studies should be conservative, for in most contexts it is better to fail to delimit species than it is to falsely delimit entities that do not represent actual evolutionary lineages. © 2013 John Wiley & Sons Ltd.
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                Author and article information

                Contributors
                xtmtd.zf@gmail.com
                wudonghui@iga.ac.cn
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                15 August 2017
                15 August 2017
                2017
                : 7
                : 8261
                Affiliations
                [1 ]ISNI 0000000119573309, GRID grid.9227.e, Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, , Chinese Academy of Sciences, ; Changchun, 130102 China
                [2 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Department of Entomology, College of Plant Protection, , Nanjing Agricultural University, ; Nanjing, 210095 China
                [3 ]ISNI 0000 0000 9888 756X, GRID grid.464353.3, Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, , Jilin Agricultural University, ; Changchun, 130118 China
                [4 ]ISNI 0000000119573309, GRID grid.9227.e, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, , Chinese Academy of Sciences, ; Beijing, 100101 China
                [5 ]ISNI 0000 0004 1936 8024, GRID grid.8391.3, Centre for Geography, Environment and Society, , University of Exeter, ; Penryn, Cornwall, TR10 9FE UK
                [6 ]ISNI 0000 0004 1789 9163, GRID grid.27446.33, Key laboratory for vegetation ecology, ministry of education, , Northeast Normal University, ; Changchun, 130117 China
                [7 ]ISNI 0000 0004 1789 9163, GRID grid.27446.33, Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, , Northeast Normal University, ; Changchun, 130117 China
                Article
                8381
                10.1038/s41598-017-08381-4
                5557941
                28811535
                cb987b16-c7ce-498f-ab4d-34fdbe672805
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 5 December 2016
                : 12 July 2017
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