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An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars.

ABSTRACT: Herbivore-induced plant volatiles (HIPVs) can mediate tritrophic interactions by attracting natural enemies of insect herbivores such as predators and parasitoids. Whether HIPVs can also mediate tritrophic interactions by influencing the attractiveness of the herbivores themselves remains unknown. We explored this question by studying the role of indole, a common HIPV in the plant kingdom. We found that herbivory-induced indole increases the recruitment of the solitary endoparasitoid Microplitis rufiventris to maize plants that are induced by Spodoptera littoralis caterpillars. Surprisingly, however, indole reduces parasitoid recruitment when the caterpillars themselves are present on the plants. Further experiments revealed that indole exposure renders S. littoralis caterpillars unattractive to M. rufiventris, leading to an overall reduction in attractiveness of plant-herbivore complexes. Furthermore, indole increases S. littoralis resistance and decreases M. rufiventris parasitization success. S. littoralis caterpillars are repelled by indole in the absence of M. rufiventris but specifically stop avoiding the volatile in the presence of the parasitoid. Our study shows how an HIPV can undermine tritrophic interactions by reducing the suitability and attractiveness of caterpillars to parasitoids.

SUBMITTER: Ye M

PROVIDER: S-EPMC5955622 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars.

Ye Meng M Veyrat Nathalie N Xu Hao H Hu Lingfei L Turlings Ted C J TCJ Erb Matthias M

Science advances 20180516 5

Herbivore-induced plant volatiles (HIPVs) can mediate tritrophic interactions by attracting natural enemies of insect herbivores such as predators and parasitoids. Whether HIPVs can also mediate tritrophic interactions by influencing the attractiveness of the herbivores themselves remains unknown. We explored this question by studying the role of indole, a common HIPV in the plant kingdom. We found that herbivory-induced indole increases the recruitment of the solitary endoparasitoid <i>Micropli ...[more]

PMID: 29774237

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Project description:Predatory mites locate herbivorous mites, their prey, by the aid of herbivore-induced plant volatiles (HIPV). These HIPV differ with plant and/or herbivore species, and it is not well understood how predators cope with this variation. We hypothesized that predators are attracted to specific compounds in HIPV, and that they can identify these compounds in odor mixtures not previously experienced. To test this, we assessed the olfactory response of Phytoseiulus persimilis, a predatory mite that preys on the highly polyphagous herbivore Tetranychus urticae. The responses of the predatory mite to a dilution series of each of 30 structurally different compounds were tested. They mites responded to most of these compounds, but usually in an aversive way. Individual HIPV were no more attractive (or less repellent) than out-group compounds, i.e., volatiles not induced in plants fed upon by spider-mites. Only three samples were significantly attractive to the mites: octan-1-ol, not involved in indirect defense, and cis-3-hexen-1-ol and methyl salicylate, which are both induced by herbivory, but not specific for the herbivore that infests the plant. Attraction to individual compounds was low compared to the full HIPV blend from Lima bean. These results indicate that individual HIPV have no a priori meaning to the mites. Hence, there is no reason why they could profit from an ability to identify individual compounds in odor mixtures. Subsequent experiments confirmed that naive predatory mites do not prefer tomato HIPV, which included the attractive compound methyl salicylate, over the odor of an uninfested bean. However, upon associating each of these odors with food over a period of 15 min, both are preferred. The memory to this association wanes within 24 hr. We conclude that P. persimilis possesses a limited ability to identify individual spider mite-induced plant volatiles in odor mixtures. We suggest that predatory mites instead learn to respond to prey-associated mixtures of volatiles and, thus, to odor blends as a whole.

Project description:BackgroundPlants, plant-feeding insects, and insect parasitoids form some of the most complex and species-rich food webs. According to the classic escape-and-radiate (EAR) hypothesis, these hyperdiverse communities result from coevolutionary arms races consisting of successive cycles of enemy escape, radiation, and colonization by new enemy lineages. It has also been suggested that "enemy-free space" provided by novel host plants could promote host shifts by herbivores, and that parasitoids could similarly drive diversification of gall form in insects that induce galls on plants. Because these central coevolutionary hypotheses have never been tested in a phylogenetic framework, we combined phylogenetic information on willow-galling sawflies with data on their host plants, gall types, and enemy communities.ResultsWe found that evolutionary shifts in host plant use and habitat have led to dramatic prunings of parasitoid communities, and that changes in gall phenotype can provide "enemy-free morphospace" for millions of years even in the absence of host plant shifts. Some parasites have nevertheless managed to colonize recently-evolved gall types, and this has apparently led to adaptive speciation in several enemy groups. However, having fewer enemies does not in itself increase speciation probabilities in individual sawfly lineages, partly because the high diversity of the enemy community facilitates compensatory attack by remaining parasite taxa.ConclusionTaken together, our results indicate that niche-dependent parasitism is a major force promoting ecological divergence in herbivorous insects, and that prey divergence can cause speciation in parasite lineages. However, the results also show that the EAR hypothesis is too simplistic for species-rich food webs: instead, diversification seems to be spurred by a continuous stepwise process, in which ecological and phenotypic shifts in prey lineages are followed by a lagged evolutionary response by some of the associated enemies.

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An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars.

Publications

An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars.

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