Genetic variation in leaf chemistry among populations differing in herbivory affects phyllosphere fungal communities

Abstract Leaf chemistry is known to affect phyllosphere microbiomes. Plant populations often evolve genetic differences in leaf chemistry across regions, driven by both abiotic and biotic factors, including insect herbivory. Plants in invasive populations may reassociate with native specialist insects, providing an ideal system to examine chemical-mediated plant-herbivore-phyllosphere microbiome interactions. Here, we conducted a common garden experiment using Ambrosia artemisiifolia populations differing in leaf chemistry and reassociation history with a specialist beetle to investigate how these variables correlate with phyllosphere microbial community diversity and composition. Plants from populations with a longer reassociation history had higher herbivore resistance and more complex phyllosphere communities with higher alpha diversity. These changes were correlated with shifts in concentrations of plant metabolites and expression levels of their underlying biosynthetic genes. The abundance of one of the fungal pathogens, Golovinomyces, decreased with the observed increase in resistance to the herbivore, however, another one, Pestaliopsis, showed the opposite pattern. While 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 between plant populations can strongly affect herbivore resistance as well as phyllosphere fungal community diversity and composition. Because the variations in invasive plant leaf chemistry aligned with the time since the invasive plant populations were reassociated with the herbivore, it is conceivable that selection imposed by the herbivore may have contributed to the variation in herbivore resistance and phylloshpere communities.