Microbial symbionts of parasitoids

Parasitoids depend on other insects for the development of their offspring. Their eggs are laid in or on a host insect that is consumed during juvenile development. Parasitoids harbor a diversity of microbial symbionts including viruses, bacteria, and fungi. In contrast to symbionts of herbivorous and hematophagous insects, parasitoid symbionts do not provide nutrients. Instead, they are involved in parasitoid reproduction, suppression of host immune responses, and manipulation of the behavior of herbivorous hosts. Moreover, recent research has shown that parasitoid symbionts such as polydnaviruses may also influence plant-mediated interactions among members of plant-associated communities at different trophic levels, such as herbivores, parasitoids, and hyperparasitoids. This implies that these symbionts have a much more extended phenotype than previously thought. This review focuses on the effects of parasitoid symbionts on direct and indirect species interactions and the consequences for community ecology

Hyperparasitoids exploit herbivore-induced plant volatiles during host location to assess host quality and non-host identity

Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing hyperparasitoids to find their preferred hosts in heterogeneous environments

Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests

Insect hyperparasitoids are fourth trophic level organisms that commonly occur in terrestrial food webs, yet they are relatively understudied. These top-carnivores can disrupt biological pest control by suppressing the populations of their parasitoid hosts, leading to pest outbreaks, especially in confined environments such as greenhouses where augmentative biological control is used. There is no effective eco-friendly strategy that can be used to control hyperparasitoids. Recent advances in the chemical ecology of hyperparasitoid foraging behavior have opened opportunities for manipulating these top-carnivores in such a way that biological pest control becomes more efficient. We propose various infochemical-based strategies to manage hyperparasitoids. We suggest that a push-pull strategy could be a promising approach to ‘push’ hyperparasitoids away from their parasitoid hosts and ‘pull’ them into traps. Additionally, we discuss how infochemicals can be used to develop innovative tools improving biological pest control (i) to restrict accessibility of resources (e.g. sugars and alternative hosts) to primary parasitoid only or (ii) to monitor hyperparasitoid presence in the crop for early detection. We also identify important missing information in order to control hyperparasitoids and outline what research is needed to reach this goal. Testing the efficacy of synthetic infochemicals in confined environments is a crucial step towards the implementation of chemical ecology-based approaches targeting hyperparasitoids. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry

Genotypic variation in genome-wide transcription profiles induced by insect feeding: Brassica oleracea – Pieris rapae interactions

<p>Abstract</p> <p>Background</p> <p>Transcriptional profiling after herbivore attack reveals, at the molecular level, how plants respond to this type of biotic stress. Comparing herbivore-induced transcriptional responses of plants with different phenotypes provides insight into plant defense mechanisms. Here, we compare the global gene expression patterns induced by <it>Pieris rapae </it>caterpillar attack in two white cabbage (<it>Brassica oleracea </it>var. <it>capitata</it>) cultivars. The two cultivars are shown to differ in their level of direct defense against caterpillar feeding. Because <it>Brassica </it>full genome microarrays are not yet available, 70-mer oligonucleotide microarrays based on the <it>Arabidopsis thaliana </it>genome were used for this non-model plant.</p> <p>Results</p> <p>The transcriptional responses of the two cultivars differed in timing as characterized by changes in their expression pattern after 24, 48 and 72 hours of caterpillar feeding. In addition, they also differed qualitatively. Surprisingly, of all genes induced at any time point, only one third was induced in both cultivars. Analyses of transcriptional responses after jasmonate treatment revealed that the difference in timing did not hold for the response to this phytohormone. Additionally, comparisons between <it>Pieris rapae</it>- and jasmonate-induced transcriptional responses showed that <it>Pieris rapae </it>induced more jasmonate-independent than jasmonate-dependent genes.</p> <p>Conclusion</p> <p>The present study clearly shows that global transcriptional responses in two cultivars of the same plant species in response to insect feeding can differ dramatically. Several of these differences involve genes that are known to have an impact on <it>Pieris rapae </it>performance and probably underlie different mechanisms of direct defense, present in the cultivars.</p

Understanding insect foraging in complex habitats by comparing trophic levels: insights from specialist host-parasitoid-hyperparasitoid systems

Insects typically forage in complex habitats in which their resources are surrounded by non-resources. For herbivores, pollinators, parasitoids, and higher level predators research has focused on how specific trophic levels filter and integrate information from cues in their habitat to locate resources. However, these insights frequently build specific theory per trophic level and seldom across trophic levels. Here, we synthesize advances in understanding of insect foraging behavior in complex habitats by comparing trophic levels in specialist host-parasitoid-hyperparasitoid systems. We argue that resources may become less apparent to foraging insects when they are member of higher trophic levels and hypothesize that higher trophic level organisms require a larger number of steps in their foraging decisions. We identify important knowledge gaps of information integration strategies by insects that belong to higher trophic levels

Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores

Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant-associated and herbivore-associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third-trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third-trophic level symbionts act in combination with venom to affect plant-mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions

Plant-phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars

There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant-insect interactions are restricted to a few cases belonging to parasitoid-associated bracoviruses. Insect parasitoids harbour a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behaviour. Yet, the function of these symbionts in plant-based trophic webs remains largely overlooked. Here, we provide the first evidence of a parasitoid-associated symbiont belonging to the group of ichnoviruses which affects the strength of plant-insect interactions. A comparative proteomic analysis shows that, upon parasitoid injection of calyx fluid containing ichnovirus particles, the composition of salivary glands of caterpillars changes both qualitatively (presence of two viral-encoded proteins) and quantitatively (abundance of several caterpillar-resident enzymes, including elicitors such as glucose oxidase). In turn, plant phenotypic changes triggered by the altered composition of caterpillar oral secretions affect the performance of herbivores. Ichnovirus manipulation of plant responses to herbivory leads to benefits for their parasitoid partners in terms of reduced developmental time within the parasitized caterpillar. Interestingly, plant-mediated ichnovirus-induced effects also enhance the performances of unparasitized herbivores which in natural conditions may feed alongside parasitized ones. We discuss these findings in the context of ecological costs imposed to the plant by the viral symbiont of the parasitoid. Our results provide intriguing novel findings about the role played by carnivore-associated symbionts on plant-insect-parasitoid systems and underline the importance of placing mutualistic associations in an ecological perspective

Adapted dandelions increase seed dispersal potential when they are attacked by root herbivores

Plants allow their offspring to escape unfavourable local conditions through seed dispersal. Whether plants use this strategy to escape herbivores is not well understood. Here, we explore how different Taraxacum officinale populations modify seed dispersal in response to root herbivore attack by Melolontha melolontha in the field. Root herbivore attack increases seed dispersal potential through a reduction in seed weight in populations that have evolved under high root herbivore pressure, but not in populations that have evolved under low pressure. This increase in dispersal potential is associated with reduced germination, suggesting that adapted plants trade dispersal for establishment. Analysis of vegetative growth parameters suggests that increased dispersal is not the result of stress flowering. These results suggest that root herbivory selects for genotypes that increase their dispersal ability in response to herbivore attack

Metabolomic Plasticity in GM and Non-GM Potato Leaves in Response to Aphid Herbivory and Virus Infection

An important aspect of ecological safety of genetically modified (GM) plants is the evaluation of unintended effects on plant–insect interactions. These interactions are to a large extent influenced by the chemical composition of plants. This study uses NMR-based metabolomics to establish a baseline of chemical variation to which differences between a GM potato line and its parent cultivar are compared. The effects of leaf age, virus infection, and aphid herbivory on plant metabolomes were studied. The metabolome of the GM line differed from its parent only in young leaves of noninfected plants. This effect was small when compared to the baseline. Consistently, aphid performance on excised leaves was influenced by leaf age, while no difference in performance was found between GM and non-GM plants. The metabolomic baseline approach is concluded to be a useful tool in ecological safety assessment