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      Pathogen invasion history elucidates contemporary host pathogen dynamics

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          Abstract

          Amphibians, the most threatened group of vertebrates, are seen as indicators of the sixth mass extinction on earth. Thousands of species are threatened with extinction and many have been affected by an emerging infectious disease, chytridiomycosis, caused by the fungal pathogen, Batrachochytrium dendrobatidis ( Bd). However, amphibians exhibit different responses to the pathogen, such as survival and population persistence with infection, or mortality of individuals and complete population collapse after pathogen invasion. Multiple factors can affect host pathogen dynamics, yet few studies have provided a temporal view that encompasses both the epizootic phase (i.e. pathogen invasion and host collapse), and the transition to a more stable co-existence (i.e. recovery of infected host populations). In the Sierra Nevada mountains of California, USA, conspecific populations of frogs currently exhibit dramatically different host/ Bd-pathogen dynamics. To provide a temporal context by which present day dynamics may be better understood, we use a Bd qPCR assay to test 1165 amphibian specimens collected between 1900 and 2005. Our historical analyses reveal a pattern of pathogen invasion and eventual spread across the Sierra Nevada over the last century. Although we found a small number of Bd-infections prior to 1970, these showed no sign of spread or increase in infection prevalence over multiple decades. After the late 1970s, when mass die offs were first noted, our data show Bd as much more prevalent and more spatially spread out, suggesting epizootic spread. However, across the ~400km 2 area, we found no evidence of a wave-like pattern, but instead discovered multiple, nearly-simultaneous invasions within regions. We found that Bd invaded and spread in the central Sierra Nevada (Yosemite National Park area) about four decades before it invaded and spread in the southern Sierra Nevada (Sequoia and Kings Canyon National Parks area), and suggest that the temporal pattern of pathogen invasion may help explain divergent contemporary host pathogen dynamics.

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          Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community.

          Pathogens rarely cause extinctions of host species, and there are few examples of a pathogen changing species richness and diversity of an ecological community by causing local extinctions across a wide range of species. We report the link between the rapid appearance of a pathogenic chytrid fungus Batrachochytrium dendrobatidis in an amphibian community at El Copé, Panama, and subsequent mass mortality and loss of amphibian biodiversity across eight families of frogs and salamanders. We describe an outbreak of chytridiomycosis in Panama and argue that this infectious disease has played an important role in amphibian population declines. The high virulence and large number of potential hosts of this emerging infectious disease threaten global amphibian diversity.
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            Batrachochytrium Dendrobatidis gen. et sp. nov., a Chytrid Pathogenic to Amphibians

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              Dynamics of an emerging disease drive large-scale amphibian population extinctions.

              Epidemiological theory generally suggests that pathogens will not cause host extinctions because the pathogen should fade out when the host population is driven below some threshold density. An emerging infectious disease, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is directly linked to the recent extinction or serious decline of hundreds of amphibian species. Despite continued spread of this pathogen into uninfected areas, the dynamics of the host-pathogen interaction remain unknown. We use fine-scale spatiotemporal data to describe (i) the invasion and spread of Bd through three lake basins, each containing multiple populations of the mountain yellow-legged frog, and (ii) the accompanying host-pathogen dynamics. Despite intensive sampling, Bd was not detected on frogs in study basins until just before epidemics began. Following Bd arrival in a basin, the disease spread to neighboring populations at approximately 700 m/yr in a wave-like pattern until all populations were infected. Within a population, infection prevalence rapidly reached 100% and infection intensity on individual frogs increased in parallel. Frog mass mortality began only when infection intensity reached a critical threshold and repeatedly led to extinction of populations. Our results indicate that the high growth rate and virulence of Bd allow the near-simultaneous infection and buildup of high infection intensities in all host individuals; subsequent host population crashes therefore occur before Bd is limited by density-dependent factors. Preventing infection intensities in host populations from reaching this threshold could provide an effective strategy to avoid the extinction of susceptible amphibian species in the wild.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 September 2019
                2019
                : 14
                : 9
                : e0219981
                Affiliations
                [1 ] Department of Biology, San Francisco State University, San Francisco, California, United States of America
                [2 ] Museum of Vertebrate Zoology, University of California Berkeley, Berkeley, California, United States of America
                [3 ] Center for Biological Diversity, Oakland, California, United States of America
                [4 ] EcoLab, Université de Toulouse, Toulouse, France
                [5 ] Department of Ecology Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California, United States of America
                University of South Dakota, UNITED STATES
                Author notes

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

                ‡ These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-9682-1190
                http://orcid.org/0000-0002-3061-2185
                http://orcid.org/0000-0002-3860-9933
                http://orcid.org/0000-0003-0932-1911
                http://orcid.org/0000-0002-7930-8635
                http://orcid.org/0000-0001-8674-5385
                Article
                PONE-D-19-01282
                10.1371/journal.pone.0219981
                6752790
                31536501
                478367ea-c4ca-4a97-b504-0668d653de35
                © 2019 Vredenburg 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
                : 14 January 2019
                : 5 July 2019
                Page count
                Figures: 4, Tables: 4, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1633948
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1557190
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 0728279
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 5R01GM109499
                Award Recipient :
                This work, as part of the People, Pollution, and Pathogens Project (P3 project), was funded partly through the call "Mountains as Sentinels of Change" by the Belmont-Forum (ANR-15-MASC-0001-P3, DFG-SCHM 3059/6-1, NERC-1633948, and NSFC-41661144004). This work was also funded in part by National Science Foundation (Briggs, NSF LTREB DEB-1557190; Vredenburg, Belmont Forum project NSF 1633948; Vredenburg NSF 0728279), the Axa Chair for Functional Mountain Ecology by Axa Research Fund awarded to Schmeller, and the National Institutes of Health (Briggs, NIH 5R01GM109499). 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
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amphibians
                Research and Analysis Methods
                Research Facilities
                Museum Collections
                Biology and Life Sciences
                Zoology
                Animal Diseases
                Epizootics
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amphibians
                Frogs
                Biology and Life Sciences
                Conservation Biology
                Species Extinction
                Ecology and Environmental Sciences
                Conservation Science
                Conservation Biology
                Species Extinction
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Species Extinction
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Biology and Life Sciences
                Population Biology
                Population Dynamics
                Custom metadata
                Data are freely available through AmphibiaWeb's amphibian disease portal: Butler, H. 2017 "Sierra Nevada Retrospective Analysis" AmphibiaWeb: Amphibian Disease Portal https://n2t.net/ark:/21547/Ars2.

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