Batrachochytrium dendrobatidis (Bd) is a globally ubiquitous fungal infection that has emerged to become a primary driver of amphibian biodiversity loss. Despite widespread effort to understand the emergence of this panzootic, the origins of the infection, its patterns of global spread, and principle mode of evolution remain largely unknown. Using comparative population genomics, we discovered three deeply diverged lineages of Bd associated with amphibians. Two of these lineages were found in multiple continents and are associated with known introductions by the amphibian trade. We found that isolates belonging to one clade, the global panzootic lineage (BdGPL) have emerged across at least five continents during the 20th century and are associated with the onset of epizootics in North America, Central America, the Caribbean, Australia, and Europe. The two newly identified divergent lineages, Cape lineage (BdCAPE) and Swiss lineage (BdCH), were found to differ in morphological traits when compared against one another and BdGPL, and we show that BdGPL is hypervirulent. BdGPL uniquely bears the hallmarks of genomic recombination, manifested as extensive intergenomic phylogenetic conflict and patchily distributed heterozygosity. We postulate that contact between previously genetically isolated allopatric populations of Bd may have allowed recombination to occur, resulting in the generation, spread, and invasion of the hypervirulent BdGPL leading to contemporary disease-driven losses in amphibian biodiversity.
Bibliographical noteWe thank Joyce Longcore for supplying isolates of Bd that we sequenced in this project, Beni Schmidt and Ursina Tobler for facilitating the collection of animals from which BdCH was isolated, and Andrew Rambaut and Philippe Lemey for advice on the phylogenetic analysis. The government of Montserrat issued permits for the isolation and export of Bd from L. fallax. Computational analysis was supported by the University of California San Diego's Center for AIDS Research BEAST Core (National Institutes of Health AI 036214). SOLiD sequencing was performed by International Society for Systems Biology and Centre for Integrative Systems Biology, Imperial College. This project was funded by the UK Natural Environmental Research Council Grant NE/E006701/1, the UK Department for Environment, Food and Rural Affairs Grant FC1195, the Biotechnology and Biological Sciences Research Council Grant BB/H008802/1, the European Research Council Grant 260801-BIG_IDEA, and the Biodiversa project RACE: Risk Assessment of Chytridiomycosis to European Amphibian Biodiversity (http://www.bd-maps.eu).