Macro Evolutionary Trends in Tortoise Beetle Host Use and Shield Defenses

Beetle diversity exceeds that of any other animal or plant group. Their inordinate success is related to two factors: herbivory and dietary specialization. Plant chemistry and predation are thought to be major factors responsible for the repeated evolution of dietary specialization. However, their relative importance, and the degree to which they interact to favor specialization, are unknown. This project will test a model of diet evolution, the 'nasty' host plant hypothesis (NHPH), which states that an herbivore's diet becomes restricted to fewer plants as it increases its dependence on dietary sources of chemistry that confer protection from predators. Tortoise beetles (Coleoptera: Chrysomelidae) are a widespread, hyper-diverse group of leaf-eating insects that feed upon hosts in over 10 mono- and dicotyledonous plant families. The most remarkable aspect of their biology and the project's study system - the larval shield - is a mobile appendage that can deflect attacking enemies. Shields are not only barriers, but because they are laced with host-derived, noxious metabolites, they also function as chemical defenses. Shields can be removed, chemically neutralized, augmented with test compounds, and then can be reattached without harming the larvae. The PIs will combine these micro-manipulation techniques with bioassays, and a resolved beetle phylogeny, to test the predictions of NHPH. The project's three aims are: (1) to experimentally test if, as NHPH predicts, the defenses of specialized species are more effective against major predators than are those of their congeneric, oligophagous relatives; (2) to determine if specialists make more efficient use of the host's chemistry for defense than do congeners feeding on the same plant, and; (3) to determine if selection by predators has been intense enough to produce patterns of escalation, due to the inclusion of novel, uniquely host-derived compounds that serve to increase the effectiveness of shield defenses. Chemical screening of shields and host plants will determine shield composition and compound origin (host-derived or de novo synthesis). In field bioassays using a suite of natural predators, the PIs will compare the efficacy of shields and of compounds found in them. The PIs will map shield chemical characters onto the beetle phylogeny, infer ancestor-descendent relationships, and test NHPH's central tenet that predation should produce a sequential host-shift pattern that yields increasingly effective shields - a process that would ultimately result in the colonization of fewer, but more chemically noxious hosts. Identification of the factors guiding host shifts across the tortoise beetles radiation is critical to understanding the evolution of plant-insect associations. This project will yield greater empirical insight into the origin of herbivore dietary specialization as a net response to selection by both an herbivore's predators and by its host's chemistry. In the limit, the PIs want to know how the evolution of dietary specialization has enhanced the rates of beetle speciation that produced much of Earth's biodiversity.