The ecological and evolutionary trajectory of oak powdery mildew in Europe

Oak powdery mildew in Europe is an example of disease in a wild perennial plant which has displayed dramatic changes over the course of a century; from typical invasion dynamics after pathogen introduction into a new area, characterized by severe damage, to a new equilibrium with moderate damage. Several non-mutually exclusive hypotheses could account for this, including pathogen evolution towards lower virulence, a reciprocal increase in oak population resistance, and both environmental biotic (phyllosphere microbes) and abiotic (climate) factors. We show that understanding the pathosystem requires the accounting of both seasonality (i.e. succession of epidemic and inter-epidemic phases linked to availability of susceptible leaves) and the occurrence of a pathogen complex with several cryptic fungal species differing in their life history traits. Observational data suggests that the severity of annual epidemics is linked to inter-annual pathogen transmission, including winter survival and the infection success of the primary inoculum in spring. Climate-driven phenological synchrony between host and pathogen in spring thus appears to be a critical factor. Several cryptic Erysiphe species are associated with the disease and co-occur at multiple spatial scales from individual leaves to continent. A semi-discrete model combining a SIR model in the epidemic phase and a discrete-time model between years, based on a within season (intra-epidemic)-between season (inter-epidemic) transmission trade-off, adequately describes seasonality and the coexistence of pathogen species. We discuss the refinement of this model, through the introduction of age classes in the host population in particular, and other modelling approaches for the evolution of pathogen virulence and host resistance in a context of changing environment.