Eco-evolutionary shifts in interactions between a globally invasive plant and below-ground putative pathogens coincide with shifts in plant performance

Enemy release may promote plant invasions and trigger rapid evolution in traits related to growth and defence in non-native populations. However, to what extent plants escape enemies, such as root-associated pathogens, is little known as comparisons between native and non-native ranges remain scarce. Also, whether plant–pathogen interactions vary between native and non-native populations under common garden conditions, and if such differences coincide with plant performance, is poorly understood. We identified putative fungal pathogens (hereafter pathogens) in roots and rhizosphere soil of the invader Conyza canadensis. We sampled 17 populations in the native range and 17 in the non-native range spanning wide and comparable environmental gradients across both ranges. We also sampled soil from adjacent plant communities where C. canadensis was absent. Potential evolutionary shifts in how C. canadensis shapes pathogen communities were assessed by growing native and non-native populations in native soil in the glasshouse (round 1). We then grew seedlings from the same populations in their conditioned soil from round 1 and compared growth to plants grown in sterile soil (round 2). Pathogen communities were dominated by generalist taxa and differed between ranges for both C. canadensis and adjacent communities. However, pathogen richness associated with C. canadensis was greater in the non-native range and proportionally more pathogens occurred in the rhizosphere than in roots relative to C. canadensis in the native range. The ratio of pathogen abundance in rhizosphere versus roots correlated positively with C. canadensis shoot biomass in the non-native, but not native, range. In the glasshouse, non-native C. canadensis promoted more and different pathogens in the rhizosphere than native C. canadensis in round 1, yet was less suppressed by soil biota in round 2. Synthesis. Differences in pathogen communities across ranges may have caused evolutionary changes in plant–pathogen associations in C. canadensis. Populations from the non-native range accumulated pathogens in their rhizosphere while appearing better defended, which coincided with greater performance in both the field and glasshouse relative to native populations. Our findings are relevant to shifting defences, fungal multifunctionality, and the overlooked role of generalist pathogen accumulation in exotic plant invasions.