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      Xenopus fraseri: Mr. Fraser, where did your frog come from?

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          Abstract

          A comprehensive, accurate, and revisable alpha taxonomy is crucial for biodiversity studies, but is challenging when data from reference specimens are difficult to collect or observe. However, recent technological advances can overcome some of these challenges. To illustrate this, we used modern approaches to tackle a centuries-old taxonomic enigma presented by Fraser’s Clawed Frog, Xenopus fraseri, including whether X. fraseri is different from other species, and if so, where it is situated geographically and phylogenetically. To facilitate these inferences, we used high-resolution techniques to examine morphological variation, and we generated and analyzed complete mitochondrial genome sequences from all Xenopus species, including >150-year-old type specimens. Our results demonstrate that X. fraseri is indeed distinct from other species, firmly place this species within a phylogenetic context, and identify its minimal geographic distribution in northern Ghana and northern Cameroon. These data also permit novel phylogenetic resolution into this intensively studied and biomedically important group. Xenopus fraseri was formerly thought to be a rainforest endemic placed alongside species in the amieti species group; in fact this species occurs in arid habitat on the borderlands of the Sahel, and is the smallest member of the muelleri species group. This study illustrates that the taxonomic enigma of Fraser’s frog was a combined consequence of sparse collection records, interspecies conservation and intraspecific polymorphism in external anatomy, and type specimens with unusual morphology.

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          Most cited references18

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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 genome of the Western clawed frog Xenopus tropicalis.

            The western clawed frog Xenopus tropicalis is an important model for vertebrate development that combines experimental advantages of the African clawed frog Xenopus laevis with more tractable genetics. Here we present a draft genome sequence assembly of X. tropicalis. This genome encodes more than 20,000 protein-coding genes, including orthologs of at least 1700 human disease genes. Over 1 million expressed sequence tags validated the annotation. More than one-third of the genome consists of transposable elements, with unusually prevalent DNA transposons. Like that of other tetrapods, the genome of X. tropicalis contains gene deserts enriched for conserved noncoding elements. The genome exhibits substantial shared synteny with human and chicken over major parts of large chromosomes, broken by lineage-specific chromosome fusions and fissions, mainly in the mammalian lineage.
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              Phylogeographic breaks without geographic barriers to gene flow.

              The spatial distribution of genetic markers can be useful both in estimating patterns of gene flow and in reconstructing biogeographic history, particularly when gene genealogies can be estimated. Genealogies based on nonrecombining genetic units such as mitochondrial and chloroplast DNA often consist of geographically separated clades that come into contact in narrow regions. Such phylogeographic breaks are usually assumed to be the result of long-term barriers to gene flow. Here I show that deep phylogeographic breaks can form within a continuously distributed species even when there are no barriers to gene flow. The likelihood of observing phylogeographic breaks increases as the average individual dispersal distance and population size decrease. Those molecular markers that are most likely to show evidence of real geographic barriers are also most likely to show phylogeographic breaks that formed without any barrier to gene flow. These results might provide an explanation as to why some species, such as the greenish warblers (Phylloscopus trochiloides), have phylogeographic breaks in mitochondrial or chloroplast DNA that do not coincide with sudden changes in other traits.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: ConceptualizationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 September 2019
                2019
                : 14
                : 9
                : e0220892
                Affiliations
                [1 ] Department of Biology, McMaster University, Hamilton, ON, Canada
                [2 ] Max Planck Institute for Evolutionary Anthropology, Deutscher Platz, Leipzig, Germany
                [3 ] Florida Museum of Natural History, University of Florida, Gainesville, FL, United States of America
                [4 ] Department of Zoology, Beaty Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada
                [5 ] Forestry Research Institute of Ghana, Kumasi, Ghana
                [6 ] Institute of Vertebrate Biology of the Czech Academy of Sciences, Czech Republic
                [7 ] Department of Zoology, National Museum, Prague, Czech Republic
                [8 ] Department of Life Sciences, The Natural History Museum, London, United Kingdom
                [9 ] Department of Biological Sciences, University of Texas at El Paso, El Paso, United States of America
                [10 ] School of Biological Sciences, University of Bristol, Bristol, United Kingdom
                Leibniz-Institute of Freshwater Ecology and Inland Fisheries, GERMANY
                Author notes

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

                Author information
                http://orcid.org/0000-0002-9512-8845
                Article
                PONE-D-19-18904
                10.1371/journal.pone.0220892
                6738922
                31509539
                1831ed75-9601-450c-95a6-5565ffffcc40
                © 2019 Evans 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
                : 4 July 2019
                : 23 July 2019
                Page count
                Figures: 2, Tables: 0, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100002790, Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada;
                Award ID: RGPIN-2017-05770
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB1202609
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100010952, Museum of Comparative Zoology, Harvard University;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100006363, National Geographic Society;
                Award ID: 8556-08
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB-1145459
                Award Recipient :
                Funded by: Czech Science Foundation
                Award ID: 15-13415Y
                Award Recipient :
                Funded by: Czech Academy of Sciences
                Award ID: 68081766
                Award Recipient :
                Funded by: Ministry of Culture of the Czech Republic
                Award ID: DKRVO 2019–2023/6.VII.a
                Award Recipient :
                Financial support for components of this work came from NSERC RGPIN-2017-05770 (BJE), NSF DEB1202609 (DCB), the Museum of Comparative Zoology, and the Max Planck Institute for Evolutionary Anthropology. EG acknowledges support from a National Geographic Research and Exploration Grant (no. 8556-08) and the US National Science Foundation (DEB-1145459). VG was supported by the Czech Science Foundation (GACR, project number 15-13415Y), Institute of Vertebrate Biology, Czech Academy of Sciences (RVO: 68081766), and Ministry of Culture of the Czech Republic (DKRVO 2019–2023/6.VII.a, National Museum, 00023272).
                Categories
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                Biology and Life Sciences
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                Research and Analysis Methods
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                Custom metadata
                All new sequence data in this study are available on GenBank, (accessions MN259067–MN259098 for all new mitochondrial genomes except the partial sequence of CAS 146198, MN251070–MN251092 for all new Sanger sequences). An alignment of complete mitochondrial genome sequences and the Sanger sequence, including the partial sequence of CAS 146198, is provided in S1 Supplemental File. CT scans are available on MorphoSource ( www.morphosource.org, doi: 10.17602/M2/M67528, 10.17602/M2/M48858, 10.17602/M2/M49944, 10.17602/M2/M69818, 10.17602/M2/M69819, 10.17602/M2/M85216, 10.17602/M2/M85215).

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