Population genomic analysis of two independent clonal invasions of the sudden oak death pathogen into one forest

Authors: CAULDRON, N - Oregon State University; DANIELS, HAZEL - Oregon State University; LEBOLDUS, JARED - Oregon State University; Grunwald, Niklaus

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/17/2025
Publication Date: 9/2/2025
Citation: Cauldron, N.C., Daniels, H.A., LeBoldus, J.M., Grünwald, N.J. 2025. Population genomic analysis of two independent clonal invasions of the sudden oak death pathogen into one forest. Phytopathology. 115(10):1382-1391. https://doi.org/10.1094/PHYTO-10-24-0329-FI.
DOI: https://doi.org/10.1094/PHYTO-10-24-0329-FI

Interpretive Summary: After introduction to a region, invasive pathogen populations are expected to be genetically less diverse than in the population of origin (e.g. genetic bottleneck). The genetic diversity can be used to infer the number of introductions. Two distinct genetic groups of the sudden oak death pathogen Phytophthora ramorum recently invaded forests in the Western United States, providing the unique opportunity to study this genetic bottleneck. We characterized populations during early invasion using whole genome sequencing of two separate genetic populations of P. ramorum sampled in the first five years following their detection. Our results indicate that both populations exhibit a genetic bottleneck and are consistent with the hypothesis of one introduction for each genetic group. This work provides novel insights into the invasion biology of plant pathogens in natural ecosystems.

Technical Abstract: Upon introduction, clonal and invasive pathogen populations are expected to go through a genetic bottleneck followed by gradual clonal divergence. Two distinct 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 five years following their detection. We re-sequenced genomes from populations of NA1 (n=135; 2001-2005) and EU1 (n=160; 2015-2019) and obtained 106,070 high-quality SNPs 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 distance than EU1 and more cryptic 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 cryptic diversity in NA1 is strongly driven by loss of heterozygosity polymorphisms, which impacted more than one-third of the sampled NA1 populations. However, loss of heterozygosity was rare in EU1. This work provides novel insights into the invasion biology and dynamics of plant pathogens in natural ecosystems.