Below-ground abiotic and biotic heterogeneity shapes above-ground infection outcomes and spatial divergence in a host-parasite interaction.

We investigated the impact of below-ground and above-ground environmental heterogeneity on the ecology and evolution of a natural plant-pathogen interaction. We combined field measurements and a reciprocal inoculation experiment to investigate the potential for natural variation in abiotic and biotic factors to mediate infection outcomes in the association between the fungal pathogen Melampsora lini and its wild flax host, Linum marginale, where pathogen strains and plant lines originated from two ecologically distinct habitat types that occur in close proximity ('bog' and 'hill'). The two habitat types differed strikingly in soil moisture and soil microbiota. Infection outcomes for different host-pathogen combinations were strongly affected by the habitat of origin of the plant lines and pathogen strains, the soil environment and their interactions. Our results suggested that tradeoffs play a key role in explaining the evolutionary divergence in interaction traits among the two habitat types. Overall, we demonstrate that soil heterogeneity, by mediating infection outcomes and evolutionary divergence, can contribute to the maintenance of variation in resistance and pathogenicity within a natural host-pathogen metapopulation.