Rapid Global Expansion of the Fungal Disease Chytridiomycosis into Declining and Healthy Amphibian Populations

Abstract

The fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis, is enigmatic because it occurs globally in both declining and apparently healthy (non-declining) amphibian populations. This distribution has fueled debate concerning whether, in sites where it has recently been found, the pathogen was introduced or is endemic. In this study, we addressed the molecular population genetics of a global collection of fungal strains from both declining and healthy amphibian populations using DNA sequence variation from 17 nuclear loci and a large fragment from the mitochondrial genome. We found a low rate of DNA polymorphism, with only two sequence alleles detected at each locus, but a high diversity of diploid genotypes. Half of the loci displayed an excess of heterozygous genotypes, consistent with a primarily clonal mode of reproduction. Despite the absence of obvious sex, genotypic diversity was high (44 unique genotypes out of 59 strains). We provide evidence that the observed genotypic variation can be generated by loss of heterozygosity through mitotic recombination. One strain isolated from a bullfrog possessed as much allelic diversity as the entire global sample, suggesting the current epidemic can be traced back to the outbreak of a single clonal lineage. These data are consistent with the current chytridiomycosis epidemic resulting from a novel pathogen undergoing a rapid and recent range expansion. The widespread occurrence of the same lineage in both healthy and declining populations suggests that the outcome of the disease is contingent on environmental factors and host resistance. Amphibian species are facing a current global extinction crisis of unprecedented magnitude. The major factors causing their decline are the emerging disease chytridiomycosis and habitat destruction. Chytridiomycosis is caused by the aquatic fungus Batrachochytrium dendrobatidis and has been linked to species extinctions and population declines in montane regions including Australia, Panama, North America, and Spain. Currently, it is debated whether the recent emergence of the pathogen is largely the result of environmental factors triggering an outbreak of an endemic pathogen or if the epidemic has been caused by widespread introduction of the pathogen into naïve host populations (“pathogen pollution”). We studied the population genetics of chytridiomycosis using DNA sequences from a global panel of strains. These data showed evidence of a strong genetic bottleneck in the history of the pathogen, and the epidemic appears traceable to the widespread dispersal of a single genotype. Populations were not structured by host-origin, and the same lineage was detected in populations of both resistant and highly sensitive species. The data suggest that the chytridiomycosis epidemic is caused by the emergence of a novel pathogen but that disease outcome is contingent on host resistance and environmental factors.