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      Cryptic diversity of a widespread global pathogen reveals expanded threats to amphibian conservation

      research-article
      a , b , c , d , d , e , f , g , h , i , j , k , l , m , n , o , c , p , q , r , s , t , u , v , w , x , y , z , c , aa , bb , q , cc , dd , a , b , 1
      Proceedings of the National Academy of Sciences of the United States of America
      National Academy of Sciences
      Batrachochytrium dendrobatidis, amphibian, conservation, genetic monitoring

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Significance

          Batrachochytrium dendrobatidis [ Bd] is one of the most devastating wildlife pathogens ever documented. Most surveys for Bd report only the presence/absence of the pathogen. However, Bd has distinct genetic lineages that vary in geographic extent and virulence, thus reporting Bd presence alone is not particularly informative. Our study uses a custom method for genotyping degraded Bd DNA samples, such as those nondestructively collected from live animal or museum specimen skin swabs, and presents the discovery of a divergent lineage of BdBdASIA3. This study advances our understanding of the evolutionary origins of Bd, highlights areas of the world where Bd lineages are coming into contact, and opens the door to affordable, rapid genetic monitoring of this pathogen.

          Abstract

          Biodiversity loss is one major outcome of human-mediated ecosystem disturbance. One way that humans have triggered wildlife declines is by transporting disease-causing agents to remote areas of the world. Amphibians have been hit particularly hard by disease due in part to a globally distributed pathogenic chytrid fungus ( Batrachochytrium dendrobatidis [ Bd]). Prior research has revealed important insights into the biology and distribution of Bd; however, there are still many outstanding questions in this system. Although we know that there are multiple divergent lineages of Bd that differ in pathogenicity, we know little about how these lineages are distributed around the world and where lineages may be coming into contact. Here, we implement a custom genotyping method for a global set of Bd samples. This method is optimized to amplify and sequence degraded DNA from noninvasive skin swab samples. We describe a divergent lineage of Bd, which we call BdASIA3, that appears to be widespread in Southeast Asia. This lineage co-occurs with the global panzootic lineage ( BdGPL) in multiple localities. Additionally, we shed light on the global distribution of BdGPL and highlight the expanded range of another lineage, BdCAPE. Finally, we argue that more monitoring needs to take place where Bd lineages are coming into contact and where we know little about Bd lineage diversity. Monitoring need not use expensive or difficult field techniques but can use archived swab samples to further explore the history—and predict the future impacts—of this devastating pathogen.

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          Most cited references28

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          Emerging Infectious Diseases of Wildlife-- Threats to Biodiversity and Human Health

          P. Daszak (2000)
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            Colloquium paper: are we in the midst of the sixth mass extinction? A view from the world of amphibians.

            Many scientists argue that we are either entering or in the midst of the sixth great mass extinction. Intense human pressure, both direct and indirect, is having profound effects on natural environments. The amphibians--frogs, salamanders, and caecilians--may be the only major group currently at risk globally. A detailed worldwide assessment and subsequent updates show that one-third or more of the 6,300 species are threatened with extinction. This trend is likely to accelerate because most amphibians occur in the tropics and have small geographic ranges that make them susceptible to extinction. The increasing pressure from habitat destruction and climate change is likely to have major impacts on narrowly adapted and distributed species. We show that salamanders on tropical mountains are particularly at risk. A new and significant threat to amphibians is a virulent, emerging infectious disease, chytridiomycosis, which appears to be globally distributed, and its effects may be exacerbated by global warming. This disease, which is caused by a fungal pathogen and implicated in serious declines and extinctions of >200 species of amphibians, poses the greatest threat to biodiversity of any known disease. Our data for frogs in the Sierra Nevada of California show that the fungus is having a devastating impact on native species, already weakened by the effects of pollution and introduced predators. A general message from amphibians is that we may have little time to stave off a potential mass extinction.
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              Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs

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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                8 October 2019
                23 September 2019
                23 September 2019
                : 116
                : 41
                : 20382-20387
                Affiliations
                [1] aDepartment of Environmental Science, Policy, and Management, University of California , Berkeley, CA 94720;
                [2] bMuseum of Vertebrate Zoology, University of California , Berkeley, CA 94720;
                [3] cDepartment of Biology, San Francisco State University , San Francisco, CA 94132;
                [4] dDepartment of Pathology, Bacteriology and Avian Diseases, Ghent University , 9820 Merelbeke, Belgium;
                [5] eDepartment of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution , Washington DC 20560;
                [6] fDepartment of Herpetology, California Academy of Sciences , San Francisco, CA 94118;
                [7] gFlorida Museum of Natural History, University of Florida , Gainesville, FL 32601;
                [8] hDepartment of Biology, University of Massachusetts Boston , Boston, MA 02125;
                [9] iMuseo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientificas (CSIC) , 28006 Madrid, Spain;
                [10] jResearch Unit of Biodiversity, CSIC–Universidad de Oviedo–Gobierno del Principado de Asturias , E-33600 Mieres, Spain;
                [11] kDepartment of Ecology, Evolution, and Marine Biology, University of California , Santa Barbara, CA 93106;
                [12] lUniversity of Kansas Biodiversity Institute, University of Kansas , Lawrence, KS 66045;
                [13] mDepartment of Ecology and Evolution, University of Kansas , Lawrence, KS 66045;
                [14] nDepartment of Biological Sciences, Florida International University , Miami, FL 33199;
                [15] oSchool of Environment and Sciences, Griffith University , Gold Coast, QLD 4215, Australia;
                [16] pDepartment of Evolution and Ecology, University of California , Davis, CA 95616;
                [17] qSchool of Life Sciences, University of Nevada , Las Vegas, NV 89154;
                [18] rDepartment of Oceanography, University of Hawai‘i at Manoa , Honolulu, HI 96822;
                [19] sInstitute of Parasitology, Czech Academy of Sciences , 370 05 Ceske Budejovice, Czech Republic;
                [20] tSierra Nevada Aquatic Research Laboratory, University of California , Mammoth Lakes, CA 93546;
                [21] uDepartment of Biodiversity Conservation, El Colegio de la Frontera Sur , San Cristobal de las Casas, Chiapas 29290, México;
                [22] vDepartment of Ecology and Evolution, University of Arizona , Tucson, AZ 85721;
                [23] wDepartment of Biological Sciences, University of Pittsburgh , Pittsburgh, PA 15260;
                [24] xEnvironmental Sciences Graduate Program, Oregon State University , Corvallis, OR 97331;
                [25] yUnidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional , Irapuato, Guanajuato CP36824, México;
                [26] zReptile, Amphibian and Fish Conservation , 6525 ED Nijmegen, The Netherlands;
                [27] aaVietnam National Museum of Nature, Vietnam Academy of Science and Technology , Hanoi, Vietnam;
                [28] bbDepartment of Biology, University of Nevada , Reno, NV 89557;
                [29] ccOne Health Research Group, The University of Melbourne , Werribee, VIC 3030, Australia;
                [30] ddCollege of Forestry, Southwest Forestry University , Kunming 650224, Yunnan, China
                Author notes
                1To whom correspondence may be addressed. Email: rosenblum@ 123456berkeley.edu .

                Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved August 21, 2019 (received for review May 15, 2019)

                Author contributions: A.Q.B. and E.B.R. designed research; A.Q.B., V.T.V., A. Martel, F.P., R.C.B., D.C.B., M.C.B., J.B., C.J.B., R.M.B., A.C., M.F.L., R.F.-V., S.L.G., J.R.J., A.J.J., M.J., R.A.K., A. Muñoz, D.M.P., C.L.R.-Z., H.R., S.M.R., T.S., H.S., N.T.T., J.V., A.W.W., Z.Y., and E.B.R. performed research; V.T.V., A. Martel, F.P., R.C.B., D.C.B., M.C.B., J.B., C.J.B., R.M.B., A.C., M.F.L., R.F.-V., S.L.G., J.R.J., A.J.J., M.J., R.A.K., A. Muñoz, D.M.P., C.L.R.-Z., H.R., S.M.R., T.S., H.S., N.T.T., J.V., A.W.W., and Z.Y. contributed samples; A.Q.B. and E.B.R. analyzed data; and A.Q.B. and E.B.R. wrote the paper.

                Author information
                http://orcid.org/0000-0002-5366-0673
                http://orcid.org/0000-0002-9682-1190
                http://orcid.org/0000-0001-7609-5649
                http://orcid.org/0000-0002-1810-9886
                http://orcid.org/0000-0001-8719-2962
                http://orcid.org/0000-0002-0225-0332
                Article
                201908289
                10.1073/pnas.1908289116
                6789904
                31548391
                39581d52-f543-422a-8316-26a43a5764bd
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 6
                Funding
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: IOS 1354241
                Award Recipient : Allison Q Byrne Award Recipient : Cheryl J. Briggs Award Recipient : Roland A. Knapp Award Recipient : Corinne L Richards-Zawacki Award Recipient : Jamie Voyles Award Recipient : Erica Bree Rosenblum
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB 1557190
                Award Recipient : Allison Q Byrne Award Recipient : Cheryl J. Briggs Award Recipient : Roland A. Knapp Award Recipient : Corinne L Richards-Zawacki Award Recipient : Jamie Voyles Award Recipient : Erica Bree Rosenblum
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB 1551488
                Award Recipient : Allison Q Byrne Award Recipient : Cheryl J. Briggs Award Recipient : Roland A. Knapp Award Recipient : Corinne L Richards-Zawacki Award Recipient : Jamie Voyles Award Recipient : Erica Bree Rosenblum
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: GRFP
                Award Recipient : Allison Q Byrne Award Recipient : Cheryl J. Briggs Award Recipient : Roland A. Knapp Award Recipient : Corinne L Richards-Zawacki Award Recipient : Jamie Voyles Award Recipient : Erica Bree Rosenblum
                Categories
                Biological Sciences
                Applied Biological Sciences
                From the Cover

                batrachochytrium dendrobatidis,amphibian,conservation,genetic monitoring

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