Population Genomic Analysis of Two Independent Clonal Invasions of the Sudden Oak Death Pathogen into One Forest

Upon introduction, clonal pathogen populations are expected to go through a genetic bottleneck followed by gradual clonal divergence. Two distinct and purely clonal lineages of the sudden oak death pathogen Phytophthora ramorum recently emerged in forests in the Western United States, providing the unique opportunity to study a naturally replicated invasion into the same ecosystem. We characterized population genomic patterns during early invasion using whole-genome sequencing of two P. ramorum clonal lineages sampled in the first 5 years following their detection. We re-sequenced genomes from populations of two dominant clonal lineages, NA1 (n = 134; 2001 to 2005) and EU1 (n = 160; 2015 to 2019), and obtained 106,070 high-quality single-nucleotide polymorphisms in genic regions. Our results are consistent with the hypothesis of one introduction for each lineage. The NA1 population had a wider distribution of pairwise genetic distances than EU1 and higher genetic diversity, though neither NA1 nor EU1 populations clustered clearly by year. There was significant correlation between genetic distance and geographic distance for NA1 (P = 0.042), but not for EU1 (P = 0.402). The genetic diversity in NA1 is strongly driven by loss of heterozygous positions, which impacted more than one-third of the sampled NA1 population. However, loss of heterozygosity was rare in EU1. This work provides novel insights into the invasion biology and dynamics of clonal plant pathogens in natural ecosystems.