Differential processing of host plant toxins by insect herbivores as a driver of multi-trophic interactions

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Plant toxins play a major role for insect-plant coevolution as they represent a barrier that herbivorous insects must overcome through adaptations. It is generally assumed that insects develop resistance to certain plant toxins for exploiting plants as a dietary resource. In addition, however, many insects store plant toxins for protection against predators and parasitoids (sequestration). Notably, certain resistance mechanisms are directly related to the sequestration of plant toxins, i.e. predators and parasitoids can also select for resistance mechanisms. We showed that in the milkweed bugs (Heteroptera: Lygaeinae) pre-existing resistance mechanisms and the ability to sequester favored evolutionarily novel associations with certain plants that produce the same plant toxins as the ancestral host family of this group. Accordingly, the acquisition of defense substances and not just the colonization of novel dietary resources can mediate specialized plant-insect interactions. The milkweed bug Spilostethus saxatilis sequesters large amounts of the toxic tubulin inhibitor colchicine from autumn crocus (Colchicum autumnale). This is of special interest since it is already able to sequester cardiac glycosides and has a cardiac glycoside-resistant Na+/K+-ATPase like all milkweed bugs. In addition, S. saxatilis possesses a resistance mechanism to colchicine, which is missing in the closely related S. pandurus. Here, we will examine the basis of colchicine resistance in S. saxatilis and address the evolution of colchicine sequestration and colchicine resistance. We will test hypotheses a) at the molecular level, b) at the functional level, and c) in a phylogenetic and organismic context. Using existing transcriptome and genome data, we will investigate whether S. saxatilis has evolved target site insensitivity to colchicine. For this purpose, we will anaylze the α- and β-tubulin encoding genes of S. saxatilis for amino acid exchanges in the colchicine binding site as well as for gene duplications and compare them with other milkweed bug species. Furthermore, we will study S. saxatilis tubulin in vitro to test if it shows reduced affinity to colchicine. At the same time, we will carry out injection experiments with competitive colchicine antagonists to test if S. saxatilis shows cross-resistance to these substances. Finally, we will conduct comparative studies in a phylogenetic context to understand the evolution of colchicine sequestration, resistance to orally ingested (as observed in S. pandurus) and sequestered colchicine. Our investigations will allow the mechanistic basis and the evolution of a novel sequestration syndrome to be understood comprehensively.