Insect herbivory reshapes a native leaf microbiome

Insect herbivory is pervasive in plant communities, but its impact on microbial plant colonizers is not well-studied in natural systems. By calibrating sequencing-based bacterial detection to absolute bacterial load, we find that the within-host abundance of most leaf microbiome (phyllosphere) taxa colonizing a native forb is amplified within leaves affected by insect herbivory. Herbivore-associated bacterial amplification reflects community-wide compositional shifts towards lower ecological diversity, but the extent and direction of such compositional shifts can be interpreted only by quantifying absolute abundance. Experimentally eliciting anti-herbivore defences reshaped within-host fitness ranks among Pseudomonas spp. field isolates and amplified a subset of putatively phytopathogenic P. syringae in a manner causally consistent with observed field-scale patterns. Herbivore damage was inversely correlated with plant reproductive success and was highly clustered across plants, which predicts tight co-clustering with putative phytopathogens across hosts. Insect herbivory may thus drive the epidemiology of plant-infecting bacteria as well as the structure of a native plant microbiome by generating variation in within-host bacterial fitness at multiple phylogenetic and spatial scales. This study emphasizes that ‘non-focal’ biotic interactions between hosts and other organisms in their ecological settings can be crucial drivers of the population and community dynamics of host-associated microbiomes. Quantifying bacterial load in plant leaves, the authors show that insect herbivory can cause compositional shifts in bacterial community structure, primarily by enhancing the growth of putative phytopathogens. Across a native host population, insect–bacteria co-infection load is highly clustered and associated with lower plant fitness.