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

Smith, Donal; O'Brien, C; Hall, Jeanette; Sergeant, Chris; Brookes, Lola M.; Harrison, Xavier A.; Garner, Trenton W. J.; Jehle, Robert

Abstract

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 characterise 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.

• Journal Article Type: Article
• Acceptance Date: Feb 7, 2022
• Online Publication Date: Feb 28, 2022
• Publication Date: Feb 15, 2022
• Deposit Date: Feb 8, 2022
• Publicly Available Date: Feb 24, 2022
• Journal: Journal of Evolutionary Biology
• Print ISSN: 1010-061X
• Electronic ISSN: 1420-9101
• Publisher: Wiley
• Volume: 35
• Issue: 4
• Pages: 589-598
• DOI: https://doi.org/10.1111/jeb.13987
• Keywords: Ecology, Evolution, Behavior and Systematics
• Publisher URL: https://doi.org/10.1111/jeb.13987
• Related Public URLs: http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1420-9101/
• Additional Information: Funders : University of Salford Pathway to Excellence PhD studentship;Natural Environment Research Council (NERC);Highland Biological Recording Group; Projects : Quantifying host species contributions to pathogen transmission in a multihost community: the case of chytrid fungus in amphibian communities;Understanding links between microbial communities and emerging fungal pathogens in complex ecosystem; Grant Number: NE/N009967/1; Grant Number: NE/S000992/1