Collaborative Research: Insect herbivore feeding guilds and compartmentalized plant defense

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Plants are the basic energy source in nearly all food chains and are responsible for feeding the world. Yet over the eons, tremendous insect pressure on plants has led to the evolution of a remarkable diversity of tactics to defend against being consumed. Plants defend with toxins, spines, and sticky sap. Despite demonstrations of how plant traits can reduce herbivory, in most wild plant systems scientists lack an understanding of the mechanisms of plant defensive responses. Do plants make specific toxins targeted at root feeders versus leaf feeders, all the while not poisoning beneficial visitors such as pollinators? Deciphering the mechanisms of plant defense not only advances scientific knowledge of ecology and evolution but may have important societal benefits. Because wild plants have been engaged in a long-term evolutionary battle with insect pests, studying the mechanisms of defense may enhance crop pest management. This project focuses on milkweeds, which are the only host for the declining monarch butterfly. Basic knowledge of the interaction between monarchs and milkweed will be gained, which could help sustain the monarch's threatened migration. This project blends the latest advances in genomic manipulation, toxicology and chemistry in a way that will train scientists to meld natural history and important ecological problems. The investigators will expand their communication to the public through schools, presentations, and a blog.Little is known about how plant defenses are aimed at different attackers, whether there are trade-offs associated with multiple arms races, and whether tissue-specific phenotypic plasticity is a means to manage interactions with several pests. This work uses milkweeds as a model natural system with well-characterized defense chemistry to test the specificity and interdependence of interactions with diverse insect attackers that include leaf-feeding monarch butterflies, root-feeding beetles, and seed-feeding bugs. From the plant's perspective, trade-offs will be evaluated between multiple defenses and their non-target impacts on pollinating bumblebees as costs associated with constitutive or induced defenses. From the herbivores' perspective, assays of plant toxin expression will be coupled to impacts on insect target site enzymatic function, behavior, and whole-organism performance. Beyond guild-specific plant defense and trade-off hypotheses, classic explanations for diversity in plant defense will also be tested: the non-exclusive hypotheses that (i) naturally occurring toxin mixtures are differentially expressed in plant parts and (ii) mixtures are more effective than equal doses of single compounds. This view on specialization and interaction addresses the dynamic match in offense-defense traits that may generate diversity within plants and insects through distinct arms races occurring from roots to fruits. Feeding trials will be used to address how single cardenolides and natural mixtures impact physiological function, insect behavior, sequestration, and fitness. By extracting the Na/K-ATPase (the target of cardenolides) from the different insects, the specific action of toxins will also be assessed in vitro.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.