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      Amphibian infection tolerance to chytridiomycosis

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          Abstract

          Animal defences against infection involve two distinct but complementary mechanisms: tolerance and resistance. Tolerance measures the animal's ability to limit detrimental effects from a given infection, whereas resistance is the ability to limit the intensity of that infection. Tolerance is a valuable defence for highly prevalent, persistent or endemic infections where mitigation strategies based on traditional resistance mechanisms are less effective or evolutionarily stable. Selective breeding of amphibians for enhanced tolerance to Batrachochytrium spp . has been suggested as a strategy for mitigating the impacts of the fungal disease, chytridiomycosis. Here, we define infection tolerance and resistance in the context of chytridiomycosis, present evidence for variation in tolerance to chytridiomycosis, and explore epidemiological, ecological and evolutionary implications of tolerance to chytridiomycosis. We found that exposure risk and environmental moderation of infection burdens are major confounders of resistance and tolerance, chytridiomycosis is primarily characterized by variation in constitutive rather than adaptive resistance, tolerance is epidemiologically important in driving pathogen spread and maintenance, heterogeneity of tolerance leads to ecological trade-offs, and natural selection for resistance and tolerance is likely to be dilute. Improving our understanding of infection tolerance broadens our capacity for mitigating the ongoing impacts of emerging infectious diseases such as chytridiomycosis.

          This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.

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          Most cited references120

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          A Contribution to the Mathematical Theory of Epidemics

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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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              Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity

              Anthropogenic trade and development have broken down dispersal barriers, facilitating the spread of diseases that threaten Earth’s biodiversity. We present a global, quantitative assessment of the amphibian chytridiomycosis panzootic, one of the most impactful examples of disease spread, and demonstrate its role in the decline of at least 501 amphibian species over the past half-century, including 90 presumed extinctions. The effects of chytridiomycosis have been greatest in large-bodied, range-restricted anurans in wet climates in the Americas and Australia. Declines peaked in the 1980s, and only 12% of declined species show signs of recovery, whereas 39% are experiencing ongoing decline. There is risk of further chytridiomycosis outbreaks in new areas. The chytridiomycosis panzootic represents the greatest recorded loss of biodiversity attributable to a disease.
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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: Formal analysisRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                July 31, 2023
                June 12, 2023
                June 12, 2023
                : 378
                : 1882 , Theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’ compiled and edited by Vania Regina Assis, Jacques Robert and Stefanny Christie Monteiro Titon
                : 20220133
                Affiliations
                Centre for Planetary Health and Food Security, and School of Environment and Science, Griffith University, , Gold Coast Campus, Parklands Drive, Southport, Queensland 4222, Australia
                Author notes

                One contribution of 14 to a theme issue ‘ Amphibian immunity: stress, disease and ecoimmunology’.

                Author information
                http://orcid.org/0000-0002-2553-7598
                https://orcid.org/0000-0003-0687-4852
                https://orcid.org/0000-0002-3493-0412
                Article
                rstb20220133
                10.1098/rstb.2022.0133
                10258672
                37305912
                3e73e069-9edf-42ac-9fa1-2c7e7352b99f
                © 2023 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : August 26, 2022
                : October 28, 2022
                Funding
                Funded by: Australian Research Council, http://dx.doi.org/10.13039/501100000923;
                Award ID: DE200100490
                Award ID: DP180101415
                Funded by: Griffith University, http://dx.doi.org/10.13039/501100001791;
                Award ID: Griffith University International Postgraduate Res
                Award ID: Griffith University Postgraduate Research Scholars
                Categories
                1001
                199
                70
                60
                Articles
                Review Articles
                Custom metadata
                July 31, 2023

                Philosophy of science
                disease,frogs,host,defence,pathogen,animal
                Philosophy of science
                disease, frogs, host, defence, pathogen, animal

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