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 multispecies interactions are reflected in adaptations of individual species such as the host-finding behavior of hyperparasitoids.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.
|Tijdschrift||Proceedings of the National Academy of Sciences of the United States of America|
|Nummer van het tijdschrift||20|
|Status||Gepubliceerd - 2018|
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Data from: Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids
Zhu, F. (Maker), Cusumano, A. (Maker), Bloem, J. (Maker), Weldegergis, B. T. (Maker), Villela, A. (Maker), Fatouros, N. E. (Maker), van Loon, J. J. A. (Maker), Dicke, M. (Maker), Harvey, J. A. (Maker), Vogel, H. (Maker) & Poelman, E. H. (Maker), Dryad, 02 mei 2018