Emergence and diversification of a highly invasive chestnut pathogen lineage across south-eastern Europe

Abstract Invasive microbial species constitute a major threat to biodiversity, agricultural production and human health. Invasions are often dominated by one or a small number of genotypes, yet the underlying factors driving invasions are poorly understood. A prime example for a successful global invasion is the recent outbreak of the chestnut blight fungus Cryphonectria parasitica. Native to East Asia, the pathogen colonized North America and Europe during the first half of the 20th century. After decimation of the American chestnut, the pathogen threatens European chestnut trees. To unravel the mechanisms underpinning the most recent invasion of south-eastern Europe over the past decades, we sequenced genomes of 188 predominantly European strains. Genotypes outside of the invasion zone showed high levels of diversity with evidence for frequent and ongoing recombination. The invasive lineage emerged from the highly diverse European genotype pool rather than a secondary introduction from Asia. The expansion across south-eastern Europe was mostly clonal and shows distinct signs of mutation accumulation. The lineage is also dominated by a single mating type suggesting a fitness advantage to switch to asexual reproduction. However, we show experimentally that the lineage retained the ability to undergo mating consistent with the low degree of recombination detected among strains within the lineage and possibly closely related strains. Our findings show how an intermediary, highly diverse bridgehead population gave rise to an invasive, largely clonally expanding pathogen.