Data from: Symbiotic polydnavirus and venom reveal parasitoid to its 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 multi-trophic 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 towards 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 hyperparsitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multi-trophic 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.

共生关系可为生物提供助力其开拓新生态位的关键创新。例如，在产卵行为（oviposition）中，部分幼虫发育于其他昆虫体内的寄生蜂（parasitoid wasps）物种会向宿主体内注入多分DNA病毒（polydnavirus）。这类共生病毒会破坏宿主的免疫应答，使寄生蜂的后代得以存活。本研究表明，共生多分DNA病毒还会为寄生蜂后代带来负面影响——其引发的多营养级交互链会将寄生蜂幼虫暴露于天敌面前。这些天敌为重寄生蜂（hyperparasitoids），它们会将寄生蜂后代作为自身后代的宿主。我们发现，寄生蜂产卵时注入的病毒与毒液（而非寄生蜂后代本身）会影响重寄生蜂对被寄生毛虫取食诱导的植物挥发物的趋性。我们在毛虫唾液腺中检测到了病毒相关基因的表达活性。此外，该病毒会影响源自唾液的诱导子（elicitor）的活性——这类诱导子可触发植物对毛虫取食的应答反应。毛虫唾液的变化对于诱导植物挥发物的产生至关重要，而这类挥发物正是重寄生蜂定位被寄生毛虫的线索。我们的研究结果证实，共生生物可能是多营养级生态交互的关键驱动因素。鉴于生态群落中跨营养级的共生微生物分布广泛，我们推测这一现象在自然界中普遍存在。在研究自然与人工管理生态系统的组织形式，以及理解隶属于这些群落的单个生物的适应性时，应更为突出地纳入共生生物的作用，以完善相关认知。