Ecological and evolutionary implications of spatial heterogeneity during the off-season for a wild plant pathogen

While recent studies have elucidated many of the factors driving parasite dynamics during the growing season, the ecological and evolutionary dynamics during the off-season (i.e. the period between growing seasons) remain largely unexplored. We combined large-scale surveys and detailed experiments to investigate the overwintering success of the specialist plant pathogen Podosphaera plantaginis on its patchily distributed host plant Plantago lanceolata in the Åland Islands. Twelve years of epidemiological data establish the off-season as a crucial stage in pathogen metapopulation dynamics, with c. 40% of the populations going extinct during the off-season. At the end of the growing season, we observed environmentally mediated variation in the production of resting structures, with major consequences for spring infection at spatial scales ranging from single individuals to populations within a metapopulation. Reciprocal transplant experiments further demonstrated that pathogen population of origin and overwintering site jointly shaped infection intensity in spring, with a weak signal of parasite adaptation to the local off-season environment. We conclude that environmentally mediated changes in the distribution and evolution of parasites during the off-season are crucial for our understanding of host–parasite dynamics, with applied implications for combating parasites and diseases in agriculture, wildlife and human disease systems.