Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids

Abstract

Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid's progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid's progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities.

Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity

“…In certain contexts, there may be costs associated with PDV manipulation of host plant defenses. The benefits to parasitoid fitness provided by PDVs could be mitigated in circumstances where hyperparasitoids may more easily locate their parasitoid hosts through changes in herbivore-induced plant volatiles ( 36 ). Nevertheless, these studies reveal that PDVs play far more prominent roles in shaping plant–herbivore interactions across multiple trophic levels than previously understood.…”

Chemical cues linked to risk: Cues from below‐ground natural enemies enhance plant defences and influence herbivore behaviour and performance

“…An intriguing parallel with our system has been reported in recent studies documenting differences in plant defence responses to caterpillars infected with parasitoid wasps and their symbiotic polydnaviruses compared to uninfected caterpillars. While one study identified suppression of plant defences that benefitted the parasitoid, another study reported changes in HIPVs that betrayed parasitoids to their hyperparasitoids (Tan et al, ; Zhu et al, ). These findings provide further evidence that organisms at the third trophic level and their associated symbionts can influence plant responses, which sometimes benefit and are sometimes detrimental for the natural enemies.…”

The microbiome of theMelitaea cinxiabutterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

“…This may result from parasitoid infection modifying host's immune (Tan et al, 2018) or metabolic (Potter and Woods, 2012;Mrinalini et al, 2015) homeostasis that can further influence the intestinal microbial community. Several studies have recently reported an impact of polydnaviruses injected in the caterpillars through the venoms of parasitoid wasps Tan et al, 2018;Zhu et al, 2018). These symbiotic viruses induce changes in the caterpillar-plant interactions as well as in host immunity.…”