Abstract
Foundational theories in plant-animal interactions are being updated with input from modern metabolomic approaches that offer more comprehensive phytochemical profiles than were previously available. Here we use a recently-formed plant-insect interaction, the colonization of alfalfa (Medicago sativa) by the Melissa blue butterfly (Lycaeides melissa), to describe the landscape of primary and secondary plant metabolites and the performance of caterpillars as affected by both individual compounds and suites of covarying phytochemicals. We find that survival, development time and adult weight are all affected by a large number of compounds, including biomolecules associated with plant cell function and putative anti-herbivore action. The dimensionality of the plant-insect interface is high, with clusters of covarying compounds in many cases encompassing divergent effects on different aspects of caterpillar performance. The sapogenic glycosides are represented by more than 20 individual compounds with some of the strongest beneficial and detrimental effects on caterpillars, which highlights the value of metabolomic data as opposed to previous approaches that relied on total concentrations within defensive classes. Considering positive and negative effects of both secondary compounds and primary metabolites (possibly associated with nutritional imbalance), theories of the evolution of plant defense based on a simple dichotomy between investment in defense or primary metabolism appear to be overly simplistic. Results are also discussed in light of previous work on local adaptation to alfalfa by the focal herbivore.