Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids
Symbiotic relationships benefit organisms in utilization of new niches. In parasitoid wasps, symbiotic viruses and venom that are injected together with wasp eggs into the host caterpillar suppress immune responses of the host and enhance parasitoid survival. We found that the virus also has negative effects on offspring survival when placing these interactions in a community context. The virus and venom drive a chain of interactions that includes the herbivore and its food plant and attracts the hyperparasitoid enemies of the parasitoid. Our results shed new light on the importance of symbionts associated with their host in driving ecological interactions and highlight the intricacy of how…
Plant-phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars
Early Access; International audience; 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 harbor a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behavior. 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…
Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications
Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta‐analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated t…
Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores
Abstract 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 colon…
Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents
Seed coating (‘seed treatment’) is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control …
IPM-recommended insecticides harm beneficial insects through contaminated honeydew
The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insec…
Next-generation biological control
Biological control is widely successful at controlling pests, but effective biocontrol agents are now more difficult to import from countries of origin due to more restrictive international trade laws (the Nagoya Protocol). Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genomic approaches. Although they have been underutilised in the past, application of genetic and genomic techniques is becoming more feasible from both technological and economic perspectives. We review current methods and provide a framework for using them. First, it is necessary to identify which biocontrol trait to select and in what direction. Nex…
Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack
Infochemicals play an important role in structuring intra-and interspecific interactions. Many parasitoid wasp species rely on herbivory or oviposition-induced plant volatiles (HIPVs/OIPVs) to locate their herbivorous hosts, and must cope with variation in the volatile blends due to factors such as plant/host species, herbivore density or attack by several herbivores. However, little is known about how dual herbivory or changes in herbivore density affect multiple parasitoid species, each attacking a different herbivore, in the same system. In a natural system, we investigated the effect of dual attack on the ability of three parasitoid species to differentiate between volatiles induced by …
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…
Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context
In response to insect herbivory, plants emit volatile organic compounds which may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. In nature, plants are often attacked by multiple herbivores, but the majority of studies which have investigated indirect plant defenses to date have focused on the recruitment of different parasitoid species in a single-herbivore context. Here, we report our investigation on the attraction of egg parasitoids of lepidopteran hosts (Trichogramma brassicae and T. evanescens) toward plant volatiles induced by different insect herbivores in olfactometer bioassays. We used a system consisting of a native crucifer, Brassica nigr…
Neonicotinoids in excretion product of phloem-feeding insects kill beneficial insects
Significance The use of insecticides in agriculture is one of the suggested causes of the decline in insect populations. Neonicotinoids are among the most widely used insecticides. However, they have important negative side effects, especially for pollinators and other beneficial insects feeding on floral nectar and pollen. We identified an exposure route: Neonicotinoids reach and kill beneficial insects when they feed on the most abundant carbohydrate source for insects in agroecosystems, honeydew. Honeydew is the excretion product of phloem-feeding hemipteran insects such as aphids, mealybugs, whiteflies, or psyllids. This route of exposure is likely to affect a much wider range of benefi…
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 th…
Data from: 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 o…