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      More than Skin Deep: Functional Genomic Basis for Resistance to Amphibian Chytridiomycosis

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          Abstract

          The amphibian-killing chytrid fungus Batrachochytrium dendrobatidis ( Bd) is one of the most generalist pathogens known, capable of infecting hundreds of species globally and causing widespread population declines and extinctions. However, some host species are seemingly unaffected by Bd, tolerating or clearing infections without clinical signs of disease. Variation in host immune responses is commonly evoked for these resistant or tolerant species, yet to date, we have no direct comparison of amphibian species responses to infection at the level of gene expression. In this study, we challenged four Central American frog species that vary in Bd susceptibility, with a sympatric virulent strain of the pathogen. We compared skin and spleen orthologous gene expression using differential expression tests and coexpression gene network analyses. We found that resistant species have reduced skin inflammatory responses and increased expression of genes involved in skin integrity. In contrast, only highly susceptible species exhibited suppression of splenic T-cell genes. We conclude that resistance to chytridiomycosis may be related to a species’ ability to escape the immunosuppressive activity of the fungus. Moreover, our results indicate that within-species differences in splenic proteolytic enzyme gene expression may contribute to intraspecific variation in survival. This first comparison of amphibian functional immunogenomic architecture in response to Bd provides insights into key genetic mechanisms underlying variation in disease outcomes among amphibian species.

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          Most cited references70

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          Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.

          Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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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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              Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs

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                Author and article information

                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                January 2015
                23 December 2014
                23 December 2014
                : 7
                : 1
                : 286-298
                Affiliations
                1Department of Ecology and Evolutionary Biology, Cornell University
                2Department of Biology, University of Maryland, College Park
                3Department of Biological Sciences, Virginia Tech
                4Department of Biology, James Madison University
                5Smithsonian Tropical Research Institute, Balboa, Ancón, Republic of Panamá
                Author notes
                *Corresponding author: E-mail: are35@ 123456cornell.edu .

                Associate editor: Eric Bapteste

                Data deposition: All sequence data submitted to NCBI SRA: SRP029154, SRP046003, SRP045866, SRP045871.

                Article
                evu285
                10.1093/gbe/evu285
                4316636
                25539724
                d40dae3f-d874-4622-abc7-452295419d65
                © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 16 December 2014
                Page count
                Pages: 13
                Categories
                Research Article

                Genetics
                batrachochytrium dendrobatidis,immunogenomics,comparative transcriptomics,immunosuppression,amphibian immunity

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