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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 organismsmay 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.