title: Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations.
abstract: Amphibians have been affected globally by the disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), and we are just now beginning to understand how immunogenetic variability contributes to disease susceptibility. Lineages of an expressed major histocompatibility complex (MHC) class II locus involved in acquired immunity are associated with chytridiomycosis susceptibility in controlled laboratory challenge assays. Here, we extend these findings to natural populations that vary both in exposure and response to Bd We find that MHC alleles and supertypes associated with Bd survival in the field show a molecular signal of positive selection, while those associated with susceptibility do not, supporting the hypothesis that heritable Bd tolerance is rapidly evolving. We compare MHC supertypes to neutral loci to demonstrate where selection versus demography is shaping MHC variability. One population with Bd tolerance in nature shows a significant signal of directional selection for the same allele (allele Q) that was significantly associated with survival in an earlier laboratory study. Our findings indicate that selective pressure for Bd survival drives rapid immunogenetic adaptation in some natural populations, despite differences in environment and demography. Our field-based analysis of immunogenetic variation confirms that natural amphibian populations have the evolutionary potential to adapt to chytridiomycosis.
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, NY 14853, USA anna.savage@ucf.edu.
authors.forename: Anna E
authors.initials: AE
authors.lastname: Savage
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, NY 14853, USA.
authors.forename: Kelly R
authors.initials: KR
authors.lastname: Zamudio
mesh_terms: D056704:Adaptive Immunity; D000483:Alleles; D000818:Animals; D001130:Arizona / Q000453:epidemiology; D008411:Chytridiomycota / Q000502:physiology*; D004198:Disease Susceptibility / Q000453:epidemiology / Q000276:immunology / Q000382:microbiology / Q000662:veterinary*; D019143:Evolution, Molecular; D008285:Major Histocompatibility Complex; D009181:Mycoses / Q000453:epidemiology / Q000276:immunology* / Q000382:microbiology / Q000401:mortality; D010802:Phylogeny; D015995:Prevalence; D011898:Ranidae; D017422:Sequence Analysis, DNA / Q000662:veterinary
keywords: Batrachochytrium dendrobatidis; adaptation; amphibian; chytridiomycosis; immunogenetics; major histocompatibility complex