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Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion

The putatively positive association between host genetic diversity and the ability to defend against pathogens has long attracted the attention of evolutionary biologists. Chytridiomycosis, a disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), has emerged in recent decades as a...

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Autores principales: Smith, Donal, O'Brien, David, Hall, Jeanette, Sergeant, Chris, Brookes, Lola M., Harrison, Xavier A., Garner, Trenton W. J., Jehle, Robert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306973/
https://www.ncbi.nlm.nih.gov/pubmed/35167143
http://dx.doi.org/10.1111/jeb.13987
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author Smith, Donal
O'Brien, David
Hall, Jeanette
Sergeant, Chris
Brookes, Lola M.
Harrison, Xavier A.
Garner, Trenton W. J.
Jehle, Robert
author_facet Smith, Donal
O'Brien, David
Hall, Jeanette
Sergeant, Chris
Brookes, Lola M.
Harrison, Xavier A.
Garner, Trenton W. J.
Jehle, Robert
author_sort Smith, Donal
collection PubMed
description The putatively positive association between host genetic diversity and the ability to defend against pathogens has long attracted the attention of evolutionary biologists. Chytridiomycosis, a disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), has emerged in recent decades as a cause of dramatic declines and extinctions across the amphibian clade. Bd susceptibility can vary widely across populations of the same species, but the relationship between standing genetic diversity and susceptibility has remained notably underexplored so far. Here, we focus on a putatively Bd‐naive system of two mainland and two island populations of the common toad (Bufo bufo) at the edge of the species’ range and use controlled infection experiments and dd‐RAD sequencing of >10 000 SNPs across 95 individuals to characterize the role of host population identity, genetic variation and individual body mass in mediating host response to the pathogen. We found strong genetic differentiation between populations and marked variation in their susceptibility to Bd. This variation was not, however, governed by isolation‐mediated genetic erosion, and individual heterozygosity was even found to be negatively correlated with survival. Individual survival during infection experiments was strongly positively related to body mass, which itself was unrelated to population of origin or heterozygosity. Our findings underscore the general importance of context‐dependency when assessing the role of host genetic variation for the ability of defence against pathogens.
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spelling pubmed-93069732022-07-28 Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion Smith, Donal O'Brien, David Hall, Jeanette Sergeant, Chris Brookes, Lola M. Harrison, Xavier A. Garner, Trenton W. J. Jehle, Robert J Evol Biol Issue The putatively positive association between host genetic diversity and the ability to defend against pathogens has long attracted the attention of evolutionary biologists. Chytridiomycosis, a disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), has emerged in recent decades as a cause of dramatic declines and extinctions across the amphibian clade. Bd susceptibility can vary widely across populations of the same species, but the relationship between standing genetic diversity and susceptibility has remained notably underexplored so far. Here, we focus on a putatively Bd‐naive system of two mainland and two island populations of the common toad (Bufo bufo) at the edge of the species’ range and use controlled infection experiments and dd‐RAD sequencing of >10 000 SNPs across 95 individuals to characterize the role of host population identity, genetic variation and individual body mass in mediating host response to the pathogen. We found strong genetic differentiation between populations and marked variation in their susceptibility to Bd. This variation was not, however, governed by isolation‐mediated genetic erosion, and individual heterozygosity was even found to be negatively correlated with survival. Individual survival during infection experiments was strongly positively related to body mass, which itself was unrelated to population of origin or heterozygosity. Our findings underscore the general importance of context‐dependency when assessing the role of host genetic variation for the ability of defence against pathogens. John Wiley and Sons Inc. 2022-02-28 2022-04 /pmc/articles/PMC9306973/ /pubmed/35167143 http://dx.doi.org/10.1111/jeb.13987 Text en © 2022 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Issue
Smith, Donal
O'Brien, David
Hall, Jeanette
Sergeant, Chris
Brookes, Lola M.
Harrison, Xavier A.
Garner, Trenton W. J.
Jehle, Robert
Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion
title Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion
title_full Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion
title_fullStr Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion
title_full_unstemmed Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion
title_short Challenging a host–pathogen paradigm: Susceptibility to chytridiomycosis is decoupled from genetic erosion
title_sort challenging a host–pathogen paradigm: susceptibility to chytridiomycosis is decoupled from genetic erosion
topic Issue
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306973/
https://www.ncbi.nlm.nih.gov/pubmed/35167143
http://dx.doi.org/10.1111/jeb.13987
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