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

Authors: KOZANITAS, MELINA - UNIVERSITY OF CALIFORNIA BERKELEY; KNAUS, BRIAN; TABIMA, JAVIER - OREGON STATE UNIVERSITY; Grunwald, Niklaus - Nik; GARBELOTTO, MATTEO - UNIVERSITY OF CALIFORNIA BERKELEY

Submitted to: Ecography
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/11/2023
Publication Date: 1/31/2024
Citation: Kozanitas, M., Knaus, B.J., Tabima, J.F., Grünwald, N.J., Garbelotto, M. 2024. 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. Ecography. 2024:e07012. https://doi.org/10.1111/ecog.07012.
DOI: https://doi.org/10.1111/ecog.07012

Interpretive Summary: Research on plant pathogens infecting multiple hosts is limited. We studied the pathogen causing Sudden Oak Death (SOD), a disease found in California and Southern Oregon caused by the non-native and invasive pathogen Phytophthora ramorum, resulting in extensive mortality of four oak (Quercus) species and of tanoak (Notholithocarpus densiflorus). Here, we studied the genetic diversity of the pathogen populations in bay laurel, oaks and tanoak. We found that generally bay laurel is the source population for infections of both tanoak and oak, and that tanoak infections contribute minimally to oak infection. We also found that different sites supported a dominance of different pathogen genotypes, and that some pathogen genotypes were widespread, while others were limited to a subset of the study plots. This work provides novel insight into the ecology and evolution of SOD epidemics in forest ecosystems.

Technical Abstract: Multi-host human and animal pathosystems have been extensively studied, but research on multi-host plant diseases is still wanting. Differences in epidemiological roles among hosts have been shown to modify not only the course of animal and human diseases, but also the structure and composition of host populations, and even the evolutionary trajectories of the pathogens themselves. Although most aspects and consequences related to the presence of multiple hosts can be applied to plant pathosystems, plants are sessile, and hence a landscape-scale component needs to be integrated in the study of multi-host plant diseases. This study uses a population genetics approach to clarify the role that temporal environmental variability, spatially distinct locations and different hosts may have in the epidemiology of a plant disease and in the evolution of its causative pathogen. The disease model chosen for the study is Sudden Oak Death (SOD), a disease caused in California and Southern Oregon (USA) by the non-native and invasive pathogen Phytophthora ramorum, resulting in the extensive mortality of four oak (Quercus) species and of tanoak (Notholithocarpus densiflorus). Oaks are dead end hosts for the pathogen, while tanoaks are transmissive hosts. Although the disease can infect over a hundred plant hosts, California bay laurel (Umbellularia californica) has been shown to be the most competent host and its frequency and density have been shown to be correlated with intensity of mortality in both oaks and tanoaks. Disease on bay laurel only affects the leaves, is very mild and never lethal. Here, we employ a population genetics approach to identify the relationship among P. ramorum populations in bay laurel, oaks and tanoak to clarify the contribution that each host may have on the epidemiology of SOD and on the microevolution of its causal agent. Additionally, we use population genetics data to explore differences in population structure across sites and years. We conclude that generally bay laurel is the source population 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 the presence of bay laurel, which sustain the largest populations of the pathogen, and with wet years. We also show that, in spite of bay laurel being a common source of inoculum, oaks and tanoaks are sinks that select and maintain host-specific pathogen genotypes that are not maintained in bay populations and that are different from one another, possibly due to differences in selection pressure in each host species. Finally, we conclude that different sites supported a dominance of different pathogen genotypes, and that some pathogen genotypes were widespread, while others were limited to a subset of the study plots. Sites with higher bay densities, some under the presence of tanoaks, have been dubbed hotspots of disease transmission and were the ones sustaining a higher genotypic diversity of the pathogen. This work provides novel insight into the ecology and evolutionary trajectories of SOD epidemics in natural ecosystems.