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Plant–insect interactions are common and important in basic and applied biology. Trait and genetic variation can affect the outcome and evolution of these interactions, but the relative contributions of plant and insect genetic variation and how these interact remain unclear and are rarely subject to assessment in the same experimental context. Here, we address this knowledge gap using a recent host-range expansion onto alfalfa by the Melissa blue butterfly. Common garden rearing experiments and genomic data show that caterpillar performance depends on plant and insect genetic variation, with insect genetics contributing to performance earlier in development and plant genetics later. Our models of performance based on caterpillar genetics retained predictive power when applied to a second common garden. Much of the plant genetic effect could be explained by heritable variation in plant phytochemicals, especially saponins, peptides, and phosphatidyl cholines, providing a possible mechanistic understanding of variation in the species interaction. We find evidence of polygenic, mostly additive effects within and between species, with consistent effects of plant genotype on growth and development across multiple butterfly species. Our results inform theories of plant–insect coevolution and the evolution of diet breadth in herbivorous insects and other host-specific parasites. 

Abstract Maternally transmitted microbes are ubiquitous. In insects, maternal microbes can play a role in mediating the insect immune response. Less is known about how ecological factors, such as resource use, interact with maternal microbes to affect immunity.In the context of a recent colonization of a novel host plant by the Melissa blue butterflyLycaeides melissa, we investigated the interaction between host plant use and vertically transmitted, extracellular egg‐associated microbes in determining the strength of the insect immune response.We reared larvae on two different host plant species: a native hostAstragalus canadensisand a novel hostMedicago sativa. Egg‐associated microbes were removed through a series of antimicrobial egg washes prior to hatching. Immune response was measured through three assays: standing phenoloxidase (PO), total PO and melanization.We detected strong effects of microbial removal. Egg washing resulted in larvae with an increased immune response as measured by total PO—contrary to reports from other taxa. The effect of washing was especially strong for larvae consuming the native host plant.This result may explain why consumption of the egg casing is not a universal behaviour in insects, due to negative effects on larval immunity. Read the freePlain Language Summaryfor this article on the Journal blog.