Environmental and genetic drivers of disease aggregation within wild plant populations
Disease can be highly aggregated within wild plant populations. However, little is known about the relative contributions of environmental and genetic factors to small-scale spatial variation in disease. Specifically, to what extent does epidemiology reflect spatial structure in host and pathogen genotypes, soil environment, or microclimate? We addressed this question with field and lab experiments using the model herbaceous perennial host, Plantago lanceolata, and its powdery mildew pathogen, Podosphaera plantaginis, in the Åland archipelago of Finland. Five discrete host populations (600-6000 m2 in area, 5-20 km apart) were intensively surveyed for disease weekly during summer. At 15 sites within each population, we deployed temperature/humidity dataloggers and groups of five greenhouse-reared sentinel plants in commercial potting soil. The sentinel plants were from five highly susceptible maternal lines, allopatric to the focal populations. After 20 days in the field, sentinel plants were screened for infection and mildew strains were collected from sentinels and wild plants. Seeds from the sentinel lines and from five infected and five uninfected wild plants per population were planted under controlled conditions in the greenhouse. We then performed an inoculation experiment exposing these plants to mildew strains collected from the sentinel and wild plants.
Prevalence of powdery mildew infection in wild and sentinel plants differed significantly among populations and among sites within populations. Spatial heterogeneity in microclimate explained some of this epidemiological variation. Near hot-spots of disease in wild plants, sentinels also tended to be infected. However, sentinel plants also frequently became infected at sites far from infected wild plants, suggesting that mildew was able to disperse to those cold-spots but failed to infect wild plants due to unsuitable host condition or genetic mismatch. The lab inoculation experiment revealed that average susceptibility of wild plant lines to sympatric mildew strains varied among populations, and was significantly lower than that of sentinel plant lines exposed to those same strains. Mildew strains also varied in their average infectivity on sympatric host lines. Thus, spatial variation in host-pathogen genotypes likely contributes to disease aggregation within populations. Ongoing analysis of spatial structure of pathogen genotypes will shed additional light on this process. Overall, this study reveals key abiotic and biotic mechanisms which drive disease aggregation at small spatial scales.