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 plant disease and 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 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.

Six sets of primers were used on the extracted P. ramorum DNA to amplify the following ten microsatellite loci known to be variable in the NA1 lineage; Ms18 and Ms64 (Ivors et al. 2006), Ms39a, Ms39b, Ms43b, Ms43b, Ms45 (Prospero et al. 2007) and MsILVO145a, MsILVO145b, MsILVO145c (Vercauteren et al. 2010). PCR reactions were carried out as described by Eyre et al. (2013) and the thermal cycling program for each primer was set by following the varying protocols outlined in Ivors et al. 2006, Prospero et al. 2007, Mascheretti et al. 2008, and Vercauteren et al. 2010. Fragment analysis was performed with a 3730 ABI Sequencer using a LIZ 500 size standard (Applied Biosystems, Foster City, California). Fragment sizes were scored using Peakscanner V1.0 (ABI Biosystems) and were then converted to the appropriate number of microsatellite motif repeats for analysis. Each isolate was assigned a multilocus genotype (MLG) isolate using the Poppr package in R version 3.4.0 (R Core Team, 2017) for genetic analysis of populations with clonal reproduction (Kamvar et al. 2014).