Pathogenic fungi constitute a growing threat to both plant and animal species on a global scale. Despite a clonal mode of reproduction dominating the population genetic structure of many fungi, putatively asexual species are known to adapt rapidly when confronted by efforts to control their growth and transmission. However, the mechanisms by which adaptive diversity is generated across a clonal background are often poorly understood. We sequenced a global panel of the emergent amphibian pathogen, Batrachochytrium dendrobatidis (Bd), to high depth and characterized rapidly changing features of its genome that we believe hold the key to the worldwide success of this organism. Our analyses show three processes that contribute to the generation of de novo diversity. Firstly, we show that the majority of wild isolates manifest chromosomal copy number variation that changes over short timescales. Secondly, we show that cryptic recombination occurs within all lineages of Bd, leading to large regions of the genome being in linkage equilibrium, and is preferentially associated with classes of genes of known importance for virulence in other pathosystems. Finally, we show that these classes of genes are under directional selection, and that this has predominantly targeted the Global Panzootic Lineage (BdGPL). Our analyses show that Bd manifests an unusually dynamic genome that may have been shaped by its association with the amphibian host. The rates of variation that we document likely explain the high levels of phenotypic variability that have been reported for Bd, and suggests that the dynamic genome of this pathogen has contributed to its success across multiple biomes and host-species.
Pathogenic fungi constitute a growing threat to both plant and animal species on a global scale. However, many features of the fungal genome that enable them to successfully adapt to infect diverse hosts and ecological niches remain cryptic, especially for newly evolved emerging lineages. In this paper, we report three novel features of genome diversity linked to pathogenicity in the emerging amphibian pathogen, Batrachochytrium dendrobatidis (Bd). Firstly, we identified widespread chromosome copy number variation (CCNV) across our lineages, with individual isolates harboring between 2 to 5 copies of each chromosome and rapid rates of CCNV occurring in culture. In addition, by using in vitro divergence of replicate lines of Bd, we showed that changes in ploidy can occur within as few as 40 generations. Secondly, we identified uneven rates of recombination across the genomes and lineages, revealing hot spots in known classes of virulence factors. Finally we identified significant evidence of diversifying selection across the secretome of Bd, and showed that selection also targets putative virulence factors. These findings add to our knowledge of genome-dynamicity and modes of evolution manifested by eukaryote microbial pathogens, and may explain the varied phenotypic responses observed in Bd.