Insect herbivory reshapes a native leaf microbiome

Insect herbivory is pervasive in natural plant communities, but its impact on microbial plant colonizers has not been well-studied outside of laboratory or agricultural systems. Here we report that insect herbivory on a native herbaceous plant amplifies within-host abundance of most leaf microbiome (phyllosphere) taxa, most dramatically so for the phytopathogen Pseudomonas syringae. This insect-associated amplification of absolute bacterial abundance was reflected in community-wide compositional shifts towards lower ecological diversity. Such community-level analyses using relative abundances mask the extent and direction of underlying abundance changes, as these are non-identifiable in the presence of variation in bacterial load. In parallel, using 12 genetically diverse field isolates of the dominant bacterial genus Pseudomonas, we found that anti-herbivore plant defenses amplify the growth of only a subset of P. syringae strains, and such strain-level variation in within-host fitness are masked at coarser taxonomic levels. In the field, herbivore damage was inversely correlated with plant reproductive success and was highly clustered across plant patches, which predicts extensive co-clustering with the P. syringae population across plants. Together, these results establish that herbivores can alter the phylogenetic and spatial structure of plant microbiomes by generating variation in within-host bacterial fitness. Plant disease surveillance and control efforts may also benefit from considering how herbivorous insects shape the population dynamics and epidemiology of phytopathogens.