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

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.

SUBMITTER: Pokharel P

PROVIDER: S-EPMC7469174 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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

Pokharel Prayan P Sippel Marlon M Vilcinskas Andreas A Petschenka Georg G

Insects 20200731 8

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</ ...[more]

PMID: 32752003

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Project description:Sequestration, that is, the accumulation of plant toxins into body tissues for defense, was predicted to incur physiological costs and may require resistance traits different from those of non-sequestering insects. Alternatively, sequestering species could experience a cost in the absence of toxins due to selection on physiological homeostasis under permanent exposure of sequestered toxins in body tissues. Milkweed bugs (Heteroptera: Lygaeinae) sequester high amounts of plant-derived cardenolides. Although being potent inhibitors of the ubiquitous animal enzyme Na+/K+-ATPase, milkweed bugs can tolerate cardenolides by means of resistant Na+/K+-ATPases. Both adaptations, resistance and sequestration, are ancestral traits of the Lygaeinae. Using four milkweed bug species (Heteroptera: Lygaeidae: Lygaeinae) and the related European firebug (Heteroptera: Pyrrhocoridae: Pyrrhocoris apterus) showing different combinations of the traits "cardenolide resistance" and "cardenolide sequestration," we tested how the two traits affect larval growth upon exposure to dietary cardenolides in an artificial diet system. While cardenolides impaired the growth of P. apterus nymphs neither possessing a resistant Na+/K+-ATPase nor sequestering cardenolides, growth was not affected in the non-sequestering milkweed bug Arocatus longiceps, which possesses a resistant Na+/K+-ATPase. Remarkably, cardenolides increased growth in the sequestering dietary specialists Caenocoris nerii and Oncopeltus fasciatus but not in the sequestering dietary generalist Spilostethus pandurus, which all possess a resistant Na+/K+-ATPase. We furthermore assessed the effect of dietary cardenolides on additional life history parameters, including developmental speed, longevity of adults, and reproductive success in O. fasciatus. Unexpectedly, nymphs under cardenolide exposure developed substantially faster and lived longer as adults. However, fecundity of adults was reduced when maintained on cardenolide-containing diet for their entire lifetime but not when adults were transferred to non-toxic sunflower seeds. We speculate that the resistant Na+/K+-ATPase of milkweed bugs is selected for working optimally in a "toxic environment," that is, when sequestered cardenolides are stored in the body.

Project description:BACKGROUND: The predatory mirids of the genus Macrolophus are key natural enemies of various economically important agricultural pests. Both M. caliginosus and M. pygmaeus are commercially available for the augmentative biological control of arthropod pests in European greenhouses. The latter species is known to be infected with Wolbachia -inducing cytoplasmic incompatibility in its host- but the presence of other endosymbionts has not been demonstrated. In the present study, the microbial diversity was examined in various populations of M. caliginosus and M. pygmaeus by 16S rRNA sequencing and denaturing gradient gel electrophoresis. RESULTS: Besides Wolbachia, a co-infection of 2 Rickettsia species was detected in all M. pygmaeus populations. Based on a concatenated alignment of the 16S rRNA gene, the gltA gene and the coxA gene, the first is phylogenetically related to Rickettsia bellii, whereas the other is closely related to Rickettsia limoniae. All M. caliginosus populations were infected with the same Wolbachia and limoniae-like Rickettsia strain as M. pygmaeus, but did not harbour the bellii-like Rickettsia strain. Interestingly, individuals with a single infection were not found. A PCR assay on the ovaries of M. pygmaeus and M. caliginosus indicated that all endosymbionts are vertically transmitted. The presence of Wolbachia and Rickettsia in oocytes was confirmed by a fluorescence in situ hybridisation. A bio-assay comparing an infected and an uninfected M. pygmaeus population suggested that the endosymbionts had minor effects on nymphal development of their insect host and did not influence its fecundity. CONCLUSION: Two species of the palaearctic mirid genus Macrolophus are infected with multiple endosymbionts, including Wolbachia and Rickettsia. Independent of the origin, all tested populations of both M. pygmaeus and M. caliginosus were infected with three and two endosymbionts, respectively. There was no indication that infection with endosymbiotic bacteria had a fitness cost in terms of development and fecundity of the predators.

Dataset Information

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

Publications

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

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