Climatic variability, spatial heterogeneity and the presence of multiple hosts drive the population structure of the pathogen Phytophthora ramorum and the epidemiology of Sudden Oak Death

We implement a population genetics approach to clarify the role that temporal and environmental variability, spatially distinct locations and different hosts may have in the epidemiology of a plant disease and in the microevolution of its causative pathogen. In California and southern Oregon (USA), the introduction of the invasive pathogen Phytophthora ramorum, causal agent of the widespread disease Sudden Oak Death (SOD), has resulted in extensive mortality of various oaks Quercus sp. and of tanoak Notholithocarpus densiflorus. Although the disease can infect over a hundred hosts, California bay laurel Umbellularia californica is the most competent transmissive host but is not lethally affected by the disease. Using population genetics data, we identify the relationship among P. ramorum populations in bay laurels, oaks and tanoaks to clarify the contribution of each host on the epidemiology of SOD and on the microevolution of its causal agent and to explore differences in population structure across sites and years. We conclude that bay laurel is the primary source for infections of both tanoak and oak, and that tanoak contributes minimally to oak infection but can infect bay laurel, creating a secondary pathogen amplification process. Overall, pathogen diversity is associated with rainfall and presence of bay laurels, which sustain the largest populations of the pathogen. Additionally, we clarify that while bay laurels are a common source of inoculum, oaks and tanoaks act as sinks that maintain host-specific pathogen genotypes not observed in bay laurel populations. Finally, we conclude that different sites support a dominance of different pathogen genotypes. Some genotypes were widespread, while others were limited to a subset of the plots. Sites with higher bay laurel densities sustained a higher genotypic diversity of the pathogen. This work provides novel insight into the ecology and evolutionary trajectories of SOD epidemics in natural ecosystems.