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 impacted 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 defenses reshaped within-host fitness ranks among Pseudomonas spp. field isolates and amplified a subset of putative P. syringae phytopathogens 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.Introduction 1 For many organisms, attack by multiple enemies is inevitable and often occurs sequentially during the 2 lifetime of individual hosts. Prior attack can alter host phenotypes and change how future attacks unfold, 3 often generating cascading effects at larger spatial and temporal scales 1-4 . Given the large effects of 4 co-infection on host health and the population dynamics of their parasites, explicitly studying co-infection 5 is becoming increasingly common 4-6 . But rarely has this perspective been extended to studies of diverse 6 host-associated microbial communities ('microbiomes'). Instead, microbiome studies tend to focus on 7 effects of host genotype or abiotic variation on microbiome diversity patterns 7-11 . This has left a major 8 gap in our understanding of how host colonization from non-microbial enemies impacts the population 9 biology of microbiome-associated taxa.
10For plants, there is tremendous interest in understanding the structure and function of the 11 microbiome both for applied purposes, such as engineering growth promotion and disease resistance 12,13 , 12 and as model systems for host-microbial symbioses more generally. Insect herbivory represents a pervasive 13 threat to plants in both native and agricultural settings 14 . Herbivory alters plant phenotypes through 14 tissue damage and induction of plant defenses, which can change susceptibility of plants to attack by 15 insects 15 as well as microbes 16,17 . Thus, factors that influence the impact of herbivores on hosts will ...