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      Defense of Milkweed Bugs (Heteroptera: Lygaeinae) against Predatory Lacewing Larvae Depends on Structural Differences of Sequestered Cardenolides

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          Abstract

          Predators and parasitoids regulate insect populations and select defense mechanisms such as the sequestration of plant toxins. Sequestration is common among herbivorous insects, yet how the structural variation of plant toxins affects defenses against predators remains largely unknown. The palearctic milkweed bug Lygaeus equestris (Heteroptera: Lygaeinae) was recently shown to sequester cardenolides from Adonis vernalis (Ranunculaceae), while its relative Horvathiolus superbus also obtains cardenolides but from Digitalis purpurea (Plantaginaceae). Remarkably, toxin sequestration protects both species against insectivorous birds, but only H. superbus gains protection against predatory lacewing larvae. Here, we used a full factorial design to test whether this difference was mediated by the differences in plant chemistry or by the insect species. We raised both species of milkweed bugs on seeds from both species of host plants and carried out predation assays using the larvae of the lacewing Chrysoperla carnea. In addition, we analyzed the toxins sequestered by the bugs via liquid chromatography (HPLC). We found that both insect species gained protection by sequestering cardenolides from D. purpurea but not from A. vernalis. Since the total amount of toxins stored was not different between the plant species in H. superbus and even lower in L. equestris from D. purpurea compared to A. vernalis, the effect is most likely mediated by structural differences of the sequestered toxins. Our findings indicate that predator–prey interactions are highly context-specific and that the host plant choice can affect the levels of protection to various predator types based on structural differences within the same class of chemical compounds.

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            Sequestration of defensive substances from plants by Lepidoptera.

            A number of aposematic butterfly and diurnal moth species sequester unpalatable or toxic substances from their host plants rather than manufacturing their own defensive substances. Despite a great diversity in their life histories, there are some general features in the selective utilization of plant secondary metabolites to achieve effective protection from predators. This review illustrates the biochemical, physiological, and ecological characteristics of phytochemical-based defense systems that can shed light on the evolution of the widely developed sequestering lifestyles among the Lepidoptera.
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              Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions.

              Cardenolides are remarkable steroidal toxins that have become model systems, critical in the development of theories for chemical ecology and coevolution. Because cardenolides inhibit the ubiquitous and essential animal enzyme Na⁺/K⁺-ATPase, most insects that feed on cardenolide-containing plants are highly specialized. With a huge diversity of chemical forms, these secondary metabolites are sporadically distributed across 12 botanical families, but dominate the Apocynaceae where they are found in > 30 genera. Studies over the past decade have demonstrated patterns in the distribution of cardenolides among plant organs, including all tissue types, and across broad geographic gradients within and across species. Cardenolide production has a genetic basis and is subject to natural selection by herbivores. In addition, there is strong evidence for phenotypic plasticity, with the biotic and abiotic environment predictably impacting cardenolide production. Mounting evidence indicates a high degree of specificity in herbivore-induced cardenolides in Asclepias. While herbivores of cardenolide-containing plants often sequester the toxins, are aposematic, and possess several physiological adaptations (including target site insensitivity), there is strong evidence that these specialists are nonetheless negatively impacted by cardenolides. While reviewing both the mechanisms and evolutionary ecology of cardenolide-mediated interactions, we advance novel hypotheses and suggest directions for future work. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.
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                Author and article information

                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                31 July 2020
                August 2020
                : 11
                : 8
                : 485
                Affiliations
                [1 ]Institute of Phytomedicine, University of Hohenheim, 70599 Stuttgart, Germany; prayan.pokharel@ 123456uni-hohenheim.de
                [2 ]Institute for Insect Biotechnology, Justus Liebig University Giessen, 35392 Giessen, Germany; marlon.sippel@ 123456student.uva.nl (M.S.); andreas.vilcinskas@ 123456agrar.uni-giessen.de (A.V.)
                Author notes
                [* ]Correspondence: Georg.Petschenka@ 123456uni-hohenheim.de ; Tel.: +49-711-459-22400
                Author information
                https://orcid.org/0000-0001-8879-8544
                https://orcid.org/0000-0001-7294-9993
                https://orcid.org/0000-0001-8276-4968
                Article
                insects-11-00485
                10.3390/insects11080485
                7469174
                32752003
                a74cdbd2-02e8-47db-ba31-bf249c8cd387
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 June 2020
                : 28 July 2020
                Categories
                Article

                predatory–prey interactions,multi-trophic interactions,cardiac glycosides,cardenolides,lygaeinae,plant toxins,milkweed bugs

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