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

Subject Area Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Animal Physiology and Biochemistry
Evolution, Anthropology
Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems
Term from 2016 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 325915028
 
Final Report Year 2024

Final Report Abstract

Reciprocal adaptations between herbivorous insects and their host plants are considered an important evolutionary driving force of biodiversity. Plants possess numerous toxins to which insects have adapted in various ways. However, to fully understand the evolution of plant-insect interactions, it is not enough to only consider their interactions. Antagonists such as predators and parasitoids also have a significant influence. Remarkably, many insects use plants not only as food but also store their toxins to defend against predators (sequestration). However, our understanding of the mechanisms of sequestration is very limited, and little is known about how sequestered plant toxins influence the evolutionary interactions between plants and insects. In this project, these relationships were studied using butterflies (Nymphalidae: Danaini) and seed bugs (Lygaeidae: Lygaeinae) as a model. The larvae of the monarch butterfly were compared with those of the related butterfly Euploea core, which also tolerates toxic cardenolides but does not sequester them. Using cuttingedge technology, cardenolides were visualized in caterpillar tissues for the first time. It was found that both caterpillar species employ different strategies in dealing with these toxins, with quantitative differences already emerging in the gut lumen. Through in vitro experiments, we found that the guts of monarch caterpillars, as well as those of other caterpillars, are permeable to cardenolides. This suggests that mechanisms other than previously assumed (such as degradation or excretion) explain the differences between sequestering and non-sequestering species. Like many insects that feed on latex-bearing plants, monarch caterpillars sever latex canals (sabotage) to remove the sticky and toxic latex before feeding. Contrary to textbook opinion, however, we were able to show that monarch caterpillars do not avoid the latex but actively drink it to sequester toxins. In seed bugs, we found that their association with toxic plants is mediated by the availability of toxins for sequestration rather than the exploitation of new food sources. Our studies further suggest that some seed bugs are so highly adapted to plant toxins that they even benefit physiologically, developing faster and living longer. In species that have lost their association with cardenolide-containing plants during evolution, there does not appear to be a loss of resistance-conferring mutations in the Na+/K+-ATPase (the target site of cardenolides) but rather a reduced expression of highly adapted Na+/K+-ATPases. However, the ability to sequester has been lost in several species. We also showed that the seed bug Spilostethus saxatilis sequesters the alkaloid colchicine from autumn crocus and likely possesses a target site resistance in its tubulin.

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