Generalist herbivores are important consumers of most plant species, yet evolutionary and ecological theory has focused on the importance of interactions between plants and their specialist natural enemies. For example, the arsenal of plant secondary metabolites has been hypothesized to result from an evolutionary arms race between plant species and specialized natural enemies. Consequently, the vast majority of studies on the evolution of plant chemical defenses have typically included one plant, a few metabolites, and a small set of handpicked herbivores. However, plant species are bombarded by dozens of different herbivore species from disparate phylogenetic lineages that span a wide range of dietary breadths and have distinctive physiological constraints that interact differently with particular metabolites. How do plant defense chemicals evolve under such multiple and contrasting selective pressures imposed by entire herbivore communities? Here we present the most detailed accounting to date of the insect herbivore fauna and phytochemistry of a tropical tree genus to understand the interaction between insects and plant chemical defenses. We censused 860 individual saplings of 32 Protium species (Burseraceae) once a week for 64 weeks in the Allpahuayo-Mishana National Reserve near Iquitos Peru and observed ca. 4500 feeding events by 210 insect morphospecies from 13 families and 5 orders. Leaves from 6 individuals of each species were exhaustively characterized for secondary metabolites.
Host-specialist herbivores were extremely rare; on average insect herbivores consumed 9 different Protium species. We found ca. 600 different chemicals (on average 71 compounds per species). Chemical diversity and investment significantly correlated with herbivore feeding records; Protium species with a higher diversity and abundance of natural products had a lower diversity and abundance of herbivores. We adapted a set of Statistical Learning tools to assess the effect that different metabolites had on each herbivore species. Almost all herbivore species were repelled by at least one plant metabolite, however; no single compound repelled more than 8 herbivore species. Moreover, metabolites with a strong negative effect on herbivore attack were more conserved across the Protium phylogeny and showed a stronger phylogenetic signal than other metabolites. In combination, these results confirm the role that insect herbivores have had on the diversification of Protium’s rich chemical arsenal. Furthermore, these findings suggest that plant chemical diversity is likely the cumulative result of a multitude of plant-herbivore interactions rather than the outcome of a chemical defense escalation driven by a small set of specialized herbivores.