Reassociation of an invasive plant with its specialist herbivore provides a test of the shifting defence hypothesis

1. The shifting defence hypothesis (SDH) predicts that after invasive plants are introduced to new ranges, they will evolve reduced resistance to specialist herbivores and increased resistance to generalist herbivores because they can escape from specialists but are still attacked by generalists in their nonnative ranges. For this to be true, the subsequent introduction of native specialist herbivores should reverse the above evolutionary processes, but evidence collected so far is scarce. 2. Here, we address this research gap by comparing resistance to specialist and generalist herbivores and resistance-related traits in the invasive plant Ambrosia artemisiifolia from five populations with about a decade history of infestation by the accidentally introduced native specialist leaf beetle Ophraella communa (infested populations), and three populations without such infestation history (uninfested populations). 3. In common garden experiments, the specialist O. communa performed better on uninfested populations than on infested populations, whereas two generalist insects, Spodoptera litura and Helicoverpa armigera, performed better on infested populations. Chemical analyses showed that plants from infested populations had lower concentrations of chlorogenic acid, an antigeneralist secondary compound that can attract O. communa. Furthermore, across mother plants from all populations studied, chlorogenic acid content was negatively correlated with larval growth of S. litura and positively correlated with that of O. communa. Finally, quantitative defence traits did not differ between infested and uninfested populations. 4. Although our results are most consistent with rapid evolution caused by enemy reassociation, we cannot exclude the possibility that observed differences in resistance result from multiple introductions or selections from other environmental factors. 5. Synthesis. These results suggest that reassociation with a specialist herbivore from the native range may result in a rapid evolution of increased resistance to specialist herbivores and reduced resistance to generalist herbivores in the introduced range, which is likely to be mediated by the reduced production of secondary chemicals that can deter generalists while attracting the introduced specialist. This study supports the shifting defence hypothesis (SDH) from a new viewpoint, emphasizing the importance of incorporating the impacts of both specialist and generalist herbivores when evaluating the long-term control effects of classical biological control programmes.