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Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade

dc.contributor.authorSchloegel, Lisa M.en_US
dc.contributor.authorToledo, Luís Felipeen_US
dc.contributor.authorLongcore, Joyce E.en_US
dc.contributor.authorGreenspan, Sasha E.en_US
dc.contributor.authorVieira, Conrado Augustoen_US
dc.contributor.authorLee, Mariaen_US
dc.contributor.authorZhao, Serenaen_US
dc.contributor.authorWangen, Catherineen_US
dc.contributor.authorFerreira, Claudia Marisen_US
dc.contributor.authorHipolito, Márcioen_US
dc.contributor.authorDavies, Angela J.en_US
dc.contributor.authorCuomo, Christina A.en_US
dc.contributor.authorDaszak, Peteren_US
dc.contributor.authorJames, Timothy Y.en_US
dc.date.accessioned2012-11-07T17:04:41Z
dc.date.available2014-01-07T14:51:08Zen_US
dc.date.issued2012-11en_US
dc.identifier.citationSchloegel, Lisa M. ; Toledo, Luís Felipe ; Longcore, Joyce E. ; Greenspan, Sasha E. ; Vieira, Conrado Augusto ; Lee, Maria ; Zhao, Serena ; Wangen, Catherine ; Ferreira, Claudia Maris ; Hipolito, Márcio ; Davies, Angela J. ; Cuomo, Christina A. ; Daszak, Peter ; James, Timothy Y. (2012). "Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade." Molecular Ecology 21(21). <http://hdl.handle.net/2027.42/94283>en_US
dc.identifier.issn0962-1083en_US
dc.identifier.issn1365-294Xen_US
dc.identifier.urihttps://hdl.handle.net/2027.42/94283
dc.description.abstractGlobal amphibian declines are linked with the presence of specific, highly virulent genotypes of the emerging fungal disease chytridiomycosis caused by Batrachochytrium dendrobatidis ( Bd ) known as the global panzootic lineage ( Bd ‐GPL). The global trade in amphibians for human consumption is suspected to have facilitated emergence of the disease, but evidence to support this is largely lacking. Here, we investigated the role the Lithobates catesbeianus (North American bullfrog) trade in spreading Bd genotypes by comparing strains associated with L. catesbeianus to a global panel using 36 sequenced loci from multiple chromosomal regions. Most bullfrogs were infected with Bd ‐GPL genotypes, but we also detected novel, highly divergent Bd genotypes ( Bd ‐Brazil) from a live bullfrog in a US market and from native Brazilian anurans in the Atlantic Forest where bullfrogs are widely farmed. Sexual reproduction was also detected for the first time in Bd in the form of a hybrid genotype between the Bd‐ GPL and Bd ‐Brazil lineages in the Atlantic Forest. Despite the demonstration that ribosomal RNA types in Bd fail to undergo concerted evolution (over 20 sequence types may be found in a single strain), the Bd‐ GPL and Bd ‐Brazil lineages form largely separate clusters of related internal transcribed spacer (ITS) RNA sequences. Using ITS sequences, we then demonstrate the presence of Bd ‐Brazil in Japan, primarily on invasive L. catesbeianus . The finding that Bd is capable of sexual reproduction between panzootic and endemic genotypes emphasizes the risk of international wildlife trade as a source of additional Bd epizootics owing to hybridization. See also the Perspective by Mckenzie and Petersonen_US
dc.publisherWiley Periodicals, Inc.en_US
dc.publisherBlackwell Publishing Ltden_US
dc.subject.otherAneuploidyen_US
dc.subject.otherChytriden_US
dc.subject.otherEmerging Infectious Diseaseen_US
dc.subject.otherLoss of Heterozygosityen_US
dc.subject.otherRanacultureen_US
dc.titleNovel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog tradeen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelEcology and Evolutionary Biologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USAen_US
dc.contributor.affiliationotherThe Broad Institute of MIT and Harvard, Cambridge, MA 02142, USAen_US
dc.contributor.affiliationotherBiological Institute, São Paulo, Brazilen_US
dc.contributor.affiliationotherFishery Institute, São Paulo, Brazilen_US
dc.contributor.affiliationotherMuseu de Zoologia, “Prof. Adão José Cardoso”, Instituto de Biologia (IB) Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazilen_US
dc.contributor.affiliationotherEcoHealth Alliance, New York, NY 10001, USAen_US
dc.contributor.affiliationotherSchool of Life Sciences, Kingston University, Kingston‐upon‐Thames, Surrey KT1 2EE, UKen_US
dc.contributor.affiliationotherSchool of Biology and Ecology, University of Maine, Orono, ME 04469, USAen_US
dc.identifier.pmid22857789en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/94283/1/mec5710.pdf
dc.identifier.doi10.1111/j.1365-294X.2012.05710.xen_US
dc.identifier.sourceMolecular Ecologyen_US
dc.identifier.citedreferenceMountain JL, Cavalli‐Sforza LL ( 1997 ) Multilocus genotypes, a tree of individuals, and human evolutionary history. American Journal of Human Genetics, 61, 705 – 718.en_US
dc.identifier.citedreferenceGiovanelli JGR, Haddad CFB, Alexandrino J ( 2008 ) Predicting the potential distribution of the alien invasive American bullfrog ( Lithobates catesbeianus ) in Brazil. Biological Invasions, 10, 585 – 590.en_US
dc.identifier.citedreferenceGoka K, Yokoyama J, Une Y et al. ( 2009 ) Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molecular Ecology, 18, 4757 – 4774.en_US
dc.identifier.citedreferenceGuindon S, Gascuel O ( 2003 ) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696 – 704.en_US
dc.identifier.citedreferenceHechinger RF, Lafferty KD ( 2005 ) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B – Biological Sciences, 272, 1059 – 1066.en_US
dc.identifier.citedreferenceHoulahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL ( 2000 ) Quantitative evidence for global amphibian population declines. Nature, 404, 752 – 755.en_US
dc.identifier.citedreferenceJames TY, Litvintseva AP, Vilgalys R et al. ( 2009 ) Rapid expansion of an emerging fungal disease into declining and healthy amphibian populations. PLoS Pathogens, 5, e1000458.en_US
dc.identifier.citedreferenceJombart T ( 2008 ) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403 – 1405.en_US
dc.identifier.citedreferenceJones KE, Patel NG, Levy MA et al. ( 2008 ) Global trends in emerging infectious diseases. Nature, 451, 990 – U994.en_US
dc.identifier.citedreferenceKielgast J, Rodder D, Veith M, Lotters S ( 2010 ) Widespread occurrence of the amphibian chytrid fungus in Kenya. Animal Conservation, 13, 36 – 43.en_US
dc.identifier.citedreferenceKondrashov AS ( 1994 ) The asexual ploidy cycle and the origin of sex. Nature, 370, 213 – 216.en_US
dc.identifier.citedreferenceLever C ( 2003 ) Naturalized Amphibians and Reptiles of the World. Oxford University Press, New York.en_US
dc.identifier.citedreferenceLongcore JE ( 2000 ) Culture technics for amphibian chytrids: recognizing, isolating, and culturing Batrachochytrium dendrobatidis from amphibians, 52 – 54.en_US
dc.identifier.citedreferenceLongcore JR, Longcore JE, Pessier AP, Halteman WA ( 2007 ) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management, 71, 435 – 444.en_US
dc.identifier.citedreferenceLynch M, Walsh B ( 1998 ) Genetics and Analysis of Quantitative Traits. Sinauer Associates Inc., Sunderland, MA.en_US
dc.identifier.citedreferenceMaddison D, Maddison W ( 2000 ) MacClade Version 4: Analysis of Phylogeny and Character Evolution. Version 4.08. Sinauer Associates, Sunderland, MA, USA.en_US
dc.identifier.citedreferenceMazzoni R, Cunningham AA, Daszak P, Apolo A, Perdomo E, Speranza G. ( 2003 ) Emerging pathogen of wild amphibians in frogs ( Rana catesbeiana ) farmed for international trade. Emerging Infectious Diseases, 9, 995 – 998.en_US
dc.identifier.citedreferenceMorehouse EA, James TY, Ganley ARD et al. ( 2003 ) Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Molecular Ecology, 12, 395 – 403.en_US
dc.identifier.citedreferenceMorens DM, Folkers GK, Fauci AS ( 2004 ) The challenge of emerging and re‐emerging infectious diseases. Nature, 430, 242 – 249.en_US
dc.identifier.citedreferenceMorgan JAT, Vredenburg VT, Rachowicz LJ et al. ( 2007 ) Population genetics of the frog‐killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America, 104, 13845 – 13850.en_US
dc.identifier.citedreferencePosada D ( 2008 ) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253 – 1256.en_US
dc.identifier.citedreferencePounds JA, Bustamante MR, Coloma LA et al. ( 2006 ) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 439, 161 – 167.en_US
dc.identifier.citedreferenceRachowicz LJ, Hero JM, Alford RA et al. ( 2005 ) The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology, 19, 1441 – 1448.en_US
dc.identifier.citedreferenceRaymond M, Rousset F ( 1995 ) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248 – 249.en_US
dc.identifier.citedreferenceRetallick RWR, Miera V, Richards KL, Field KJ, Collins JP ( 2006 ) A non‐lethal technique for detecting the chytrid fungus Batrachochytrium dendrobatidis on tadpoles. Diseases of Aquatic Organisms, 72, 77 – 85.en_US
dc.identifier.citedreferenceRosenblum EB, Novembre J ( 2007 ) Ascertainment bias in spatially structured populations: a case study in the eastern fence lizard. Journal of Heredity, 98, 331 – 336.en_US
dc.identifier.citedreferenceSchloegel LM, Hero JM, Berger L, Speare R, McDonald K, Daszak P. ( 2006 ) The decline of the sharp‐snouted day frog ( Taudactylus acutirostris ): the first documented case of extinction by infection in a free‐ranging wildlife species? EcoHealth, 3, 35 – 40.en_US
dc.identifier.citedreferenceSchloegel LM, Picco AM, Kilpatrick AM, Davies AJ, Hyatt AD, Daszak P. ( 2009 ) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs ( Rana catesbeiana ). Biological Conservation, 142, 1420 – 1426.en_US
dc.identifier.citedreferenceSchloegel LM, Daszak P, Cunningham AA, Speare R, Hill B ( 2010a ) Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Diseases of Aquatic Organisms, 92, 101 – 108.en_US
dc.identifier.citedreferenceSchloegel LM, Ferreira CM, James TY et al. ( 2010b ) The North American Bullfrog ( Rana catesbeiana ) as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Animal Conservation, 13, 53 – 61.en_US
dc.identifier.citedreferenceSchloss PD, Westcott SL, Ryabin T et al. ( 2009 ) Introducing mothur: open‐source, platform‐independent, community‐supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537 – 7541.en_US
dc.identifier.citedreferenceSkerratt LF, Berger L, Speare R et al. ( 2007 ) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4, 125 – 134.en_US
dc.identifier.citedreferenceSmith KF, Behrens M, Schloegel LM, Marano N, Burgiel S, Daszak P. ( 2009 ) Reducing the risks of the wildlife trade. Science, 324, 594 – 595.en_US
dc.identifier.citedreferenceSoto‐Azat C, Clarke BT, Poynton JC, Cunningham AA ( 2010 ) Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Diversity and Distributions, 16, 126 – 131.en_US
dc.identifier.citedreferenceSparrow FK ( 1960 ) Aquatic Phycomycetes, 2nd edn. University of Michigan Press, Ann Arbor, MI.en_US
dc.identifier.citedreferenceSwofford DL ( 2002 ) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MA.en_US
dc.identifier.citedreferenceVelo‐Anton G, Rodriguez D, Savage AE, Parra‐Olea G, Lips KR, Zamudio KR. ( 2012 ) Amphibian‐killing fungus loses genetic diversity as it spreads across the New World. Biological Conservation, 146, 213 – 218.en_US
dc.identifier.citedreferenceWalker DH, Barbour AG, Oliver JH et al. ( 1996 ) Emerging bacterial zoonotic and vector‐borne diseases – ecological and epidemiological factors. JAMA – Journal of the American Medical Association, 275, 463 – 469.en_US
dc.identifier.citedreferenceWalker SF, Bosch J, James TY et al. ( 2008 ) Introduced pathogens threaten species recovery programs. Current Biology, 18, R853 – R854.en_US
dc.identifier.citedreferenceWarnecke L, Turner JM, Bollinger TK et al. ( 2012 ) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white‐nose syndrome. Proceedings of the National Academy of Sciences of the United States of America, 109, 6999 – 7003.en_US
dc.identifier.citedreferenceWeldon C, du Preez LH, Hyatt AD, Muller R, Speare R ( 2004 ) Origin of the amphibian chytrid fungus. Emerging Infectious Diseases, 10, 2100 – 2105.en_US
dc.identifier.citedreferenceWhite TJ, Bruns T, Lee S, Taylor JW ( 1990 ) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications (eds Innis MA, Gelfand DH, Sninsky JJ and White TJ ), pp. 315 – 322. Academic Press, Inc., New York.en_US
dc.identifier.citedreferenceAnderson EC, Thompson EA ( 2002 ) A model‐based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217 – 1229.en_US
dc.identifier.citedreferenceAnnis SL, Dastoor FP, Ziel H, Daszak P, Longcore JE ( 2004 ) A DNA‐based assay identifies Batrachochytrium dendrobatidis in amphibians. Journal of Wildlife Diseases, 40, 420 – 428.en_US
dc.identifier.citedreferenceArchie EA, Luikart G, Ezenwa VO ( 2008 ) Infecting epidemiology with genetics: a new frontier in disease ecology. Trends in Ecology and Evolution, 24, 21 – 30.en_US
dc.identifier.citedreferenceBalloux F, Lehmann L, de Meeus T ( 2003 ) The population genetics of clonal and partially clonal diploids. Genetics, 164, 1635 – 1644.en_US
dc.identifier.citedreferenceBennett RJ, Johnson AD ( 2005 ) Mating in Candida albicans and the search for a sexual cycle. Annual Review of Microbiology, 59, 233 – 255.en_US
dc.identifier.citedreferenceBlaustein AR, Wake DB ( 1990 ) Declining amphibian populations: a global phenomenon? Trends in Ecology & Evolution, 7, 203 – 204.en_US
dc.identifier.citedreferenceBoyle DG, Hyatt AD, Daszak P et al. ( 2003 ) Cryo‐archiving of Batrachochytrium dendrobatidis and other chytridiomycetes. Diseases of Aquatic Organisms, 56, 59 – 64.en_US
dc.identifier.citedreferenceBriggs CJ, Knapp RA, Vredenburg VT ( 2010 ) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America, 107, 9695 – 9700.en_US
dc.identifier.citedreferenceCheng TL, Rovito SM, Wake DB, Vredenburg VT ( 2011 ) Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America, 108, 9502 – 9507.en_US
dc.identifier.citedreferenceColwell RK ( 1997 ) EstimateS: statistical estimation of species richness and complementarity from samples. Available at: http://viceroy.eeb.uconn.edu/EstimateS%02 (accessed on 26 November 2011).en_US
dc.identifier.citedreferenceCrawford AJ, Lips KR, Bermingham E ( 2010 ) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences of the United States of America, 107, 13777 – 13782.en_US
dc.identifier.citedreferenceDaszak P, Cunningham AA, Hyatt AD ( 2000 ) Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science, 287, 443 – 449.en_US
dc.identifier.citedreferenceDray S, Dufour AB ( 2007 ) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1 – 20.en_US
dc.identifier.citedreferenceFarrer RA, Weinert LA, Bielby J et al. ( 2011 ) Multiple emergences of genetically diverse amphibian‐infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences of the United States of America, 108, 18732 – 18736.en_US
dc.identifier.citedreferenceFelsenstein J ( 1989 ) PHYLIP – phylogeny inference package (version 3.2). Cladistics, 5, 164 – 166.en_US
dc.identifier.citedreferenceFisher MC, Walker SF, Garner TWJ ( 2009 ) The global emergence of Batrachochytrium dendrobatidis in space, time, and host. Annual Review of Microbiology, 63, 291 – 310.en_US
dc.identifier.citedreferenceFisher MC, Henk DA, Briggs CJ et al. ( 2012 ) Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186 – 194.en_US
dc.identifier.citedreferenceFlores Nava A ( 2005 ) Cultured aquatic species information programme. Rana catesbeiana. FAO Fisheries and Aquaculture Department, Rome.en_US
dc.identifier.citedreferenceGanley ARD, Kobayashi T ( 2007 ) Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole‐genome shotgun sequence data. Genome Research, 17, 184 – 191.en_US
dc.identifier.citedreferenceGarner TWJ, Perkins MW, Govindarajulu P et al. ( 2006 ) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters, 2, 455 – 459.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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