Reassociation of specialist herbivores with an invasive plant selects for reduced allocation to soil mutualists

Invasive plants often escape specialist herbivores and can evolve to reallocate resources to growth from defense, but reunion with specialists can reverse this evolutionary trade-off. It remains unclear whether specialist-triggered changes affect soil mutualisms, which can also promote invasion success. Here, we investigate colonization of arbuscular mycorrhizal fungi (AMF) in roots of the invasive Ambrosia artemisiifolia from populations that vary in duration of reassociation with the specialist herbivore Ophraella communa. We then investigated chemically mediated changes in AMF colonization and plant defenses after reassociation with O. communa. Ambrosia artemisiifolia populations with a longer reassociation history had lower AMF colonization rates than populations with shorter or no reassociation history. We detected a genetically based increase in resistance to herbivores but decreased AMF colonization in A. artemisiifolia populations after the reassociation. These changes in antagonisms and mutualisms corresponded with increasing leaf tannins but decreasing fatty acid concentrations in roots and root exudates. These results suggest that reassociation with specialist herbivores may trigger shifts in resource allocation back to herbivore defense and away from plant–AMF mutualisms, providing new insights into links between enemy release and enhanced mutualism, with potential ramifications for the long-term effects of classical biological control programs.