Generalist herbivores are important consumers of most plant species, yet evolutionary and ecological theory has mainly focused on the importance of interactions between specialized natural enemies and host plants. 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? In addition, Herbivores can influence the geographic distribution of host plants, yet very little is known about the overlap in geographic distribution of plants and their herbivores in tropical forests, which harbor the great majority of both plant and insect species.
Here we present the most detailed accounting to date of the insect herbivore fauna and a tropical tree genus (Protium, Burseraceae) surveying 890 individual plants once a week for 64 weeks in the Allpahuayo-Mishana National Reserve near Iquitos Peru . In Manaus, Brazil (1500 km distant) 260 individuals of the 12 of the same Protium species (Burseraceae) were surveyed for herbivores every week for one year. In total, we observed ca. 5500 feeding events by 394 insect morphospecies from 13 families and 5 orders Herbivore species were DNA barcoded to confirm their identity across both sites and to determine the presence of potential cryptic species. Leaves from 6 individuals of each Protium species were exhaustively characterized for secondary metabolites. Secondary 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. Moreover, the chemical diversity in Protium appears to function with similar effectiveness against herbivore communities in two widely-separated areas, highlighting the importance of high chemical diversity for plants.