Phytochemical variation is one of the most fascinating features of the natural world. It acts as both a mechanism governing trophic interactions and is a product of complex ecological interactions between plants and animals. Recent advances in chemical ecology have taken us to a point where we were able to bring informatics and metabolomic innovations to bear on fundamental questions about the ecology of host plant specialization. Our goal was to uncover the extent to which passion vine (Passiflora) metabolomic and life history traits drive simultaneous dietary specialization by sympatric flea beetle (Coleoptera: Chrysomelidae) and heliconiine caterpillar (Lepidoptera: Nymphalidae) assemblages within the same communities. Is phytochemical diversity as important as quantity of secondary metabolites in predicting host usage? Are hosts utilized by many herbivores less chemically diverse than those with few? What about the influence of plant traits other than chemistry? These questions were tested at three sites spanning a latitudinal gradient from a lowland wet forest in Costa Rica to deciduous forests of the southeastern USA. We used structural equation models to test causal relationships between molecular networks of plant metabolites, secondary chemical concentration, constitutive defenses, habitat specificity and host usage by parallel structured specialist herbivore assemblages.
Results/Conclusions
Chemical diversity drives flea beetle and heliconiine patterns of host usage between Passiflora species, and subgeneric sections. Monophagous beetle and heliconiine species consume Passiflora species with unique molecular networks and high cyanogenic glycoside concentrations. Herbivore species that consumed multiple host species across Passiflora subgenera used hosts with similar molecular networks, were characterized by low chemical diversity and low cyanogenic glycoside concentration. Passiflora subgenera had distinct molecular networks that largely restricted the diet breadth of beetles and caterpillars consuming them. Several Passiflora species possess unique constitutive defenses that limit herbivore richness to those with specialized behavioral adaptations for consuming them, effectively establishing enemy-free-space irrespective of chemistry. Plant habitat specificity and extrafloral nectary size contribute to host usage to a lesser extent than phytochemical quantity and diversity. This is one of the first studies to establish causal relationships between host plant defensive traits, life history and community scale patterns of host usage by distinct specialist insect assemblages across latitudes. These results provide support for the coevolutionary arms race hypothesis and open the door to answering new questions about how competition and natural enemies contribute to structuring these communities.