Abstract: Leaf chemistry plays a central role in structuring phyllosphere microbiomes. Plant populations often evolve genetic differences in leaf chemistry across region due to both abiotic and biotic selection pressures, including insect herbivory. Plants in invasive populations may reassociate with native specialist insects, providing an ideal system to examine how herbivory-mediated changes in plant chemistry affect phyllosphere microbiome. Here, we conducted a common garden experiment using Ambrosia artemisiifolia populations differing in leaf chemistry and reassociation history with a specialist beetle—Ophraella communa. We found that plant populations with a longer reassociation history exhibited stronger herbivore resistance and supported phyllosphere communities with higher alpha diversity and more complex composition. These changes were associated with shifts in concentrations of plant metabolites and the expression levels of corresponding biosynthetic genes. The abundance of the fungal pathogens, Golovinomyces, decreased with increasing herbivore resistance, while Pestaliopsis showed the opposite trend. Although reassociation history was linked to population latitude, climatic and soil conditions at the sites of origin also contributed to between-population variation in leaf chemistry and phyllosphere fungal community composition. Our study suggests that genetic differences in leaf chemistry among plant populations can strongly affect herbivore resistance and phyllosphere fungal communities. The observed alignment of reassociation history, chemical traits and phyllosphere fungal communities suggests that herbivore-mediated selection may be a key driver of microbial community evolution in invasive plants.

Key words: Phyllosphere fungal community, species diversity, plant–insect–microbe interactions, invasive plant, secondary chemicals, herbivorous insects, Ambrosia artemisiifolia