Abstract
The pathogenic chytrid fungus Batrachochytrium dendrobatidis (Bd) can cause precipitous population declines in its amphibian hosts. Responses of individuals to infection vary greatly with the capacity of their immune system to respond to the pathogen. We used a combination of comparative and experimental approaches to identify major histocompatibility complex class II (MHC-II) alleles encoding molecules that foster the survival of Bd-infected amphibians. We found that Bd-resistant amphibians across four continents share common amino acids in three binding pockets of the MHC-II antigen-binding groove. Moreover, strong signals of selection acting on these specific sites were evident among all species co-existing with the pathogen. In the laboratory, we experimentally inoculated Australian tree frogs with Bd to test how each binding pocket conformation influences disease resistance. Only the conformation of MHC-II pocket 9 of surviving subjects matched those of Bd-resistant species. This MHC-II conformation thus may determine amphibian resistance to Bd, although other MHC-II binding pockets also may contribute to resistance. Rescuing amphibian biodiversity will depend on our understanding of amphibian immune defence mechanisms against Bd. The identification of adaptive genetic markers for Bd resistance represents an important step forward towards that goal.
Highlights
The emerging infectious skin disease chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis [1,2], is a primary driver of global amphibian population declines and species extinctions [3,4]
We have shown that chytridiomycosis appears to select for specific properties of the major histocompatibility complex (MHC) class II molecule P9-binding pocket
While our comparative study points to specific P4 and P6 pocket conformations that correlate with Batrachochytrium dendrobatidis (Bd) resistance worldwide, these conformations did not improve survival of infected L. v. alpina, nor are they abundant in Korean Bufo and Bombina populations
Summary
The emerging infectious skin disease chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis (denoted Bd) [1,2], is a primary driver of global amphibian population declines and species extinctions [3,4]. For each MHC-II binding pocket, the proportion of b1 sequences containing all the amino acids most frequent in resistant amphibians was compared with that characteristic of susceptible species. Alpina that we had infected with Bd This selection included the only six individuals that survived the experiment and 94 individuals randomly chosen and encompassing all the clutches collected from the three populations (8–10 individuals per clutch; electronic supplementary material, table S4). Parameters included in the initial model were site of origin, clutch, maximum Bd infection load, mass at the start of the experiment, change in mass over the course of the experiment, MHC heterozygosity, allelic divergence (measured as p-distance) and pocket residue composition (table 1). We tested whether specific biochemical properties were driving substitutions at the peptide-binding sites using the property-informed model of evolution (PRIME) method [42], which includes the Holm–Bonferroni procedure to control for familywise false positives within sites
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