Adaptation of pathogens to their local plant host, Silphium integrifolium, along a precipitation gradient

Empirical evidence of the influence of climate on plant-pathogen coevolution is limited but crucial to understand, as anthropogenic pressures including fragmentation and climate change threaten biodiversity. In this study, we tested patterns of plant-pathogen coevolution using Silphium integrifolium Michx., a native tallgrass prairie species that is undergoing domestication, and its foliar pathogens. We collected seeds from four native prairie remnants from each of three regions along an east-west precipitation gradient in central North America and used these to create three common gardens in each region. In common gardens and remnant prairie populations, we measured symptoms of foliar disease (leaf rust and leaf blotch, both caused by fungal pathogens, and Silphium clear vein (SCV), which we have evidence is associated with a virus). While we did not observe greater disease in the East common garden, we did find that on average the East populations had greater resistance to disease than West populations, consistent with an evolutionary legacy of more rapid coevolution with high precipitation. We also found strong interactions between source region and region of planting for all diseases. The Silphium rust, caused by the specialist pathogen Puccinia silphii, was better able to infect plant populations from the same region. These patterns are consistent with local adaptation of specialist pathogens to their local hosts as expected from Red Queen dynamics. For the generalist fungal pathogen driving leaf blotch, we did not observe evidence of local adaptation. However, we observed a positive correlation in the average level of leaf blotch symptoms observed in individual populations in common gardens with the levels of disease in the S. integrifolium individuals in the prairie remnants of origin, consistent with S. integrifolium genetics determining symptoms in the field. Our results are consistent with pathogen ecology being a major driver of coevolutionary dynamics along productivity gradients. As S. integrifolium is being domesticated for oilseed production, our results identify distinct targets for resistance alleles in breeding efforts and can guide pathogen management strategies.