Table_2_Parasitoid Causes Cascading Effects on Plant-Induced Defenses Mediated Through the Gut Bacteria of Host Caterpillars.docx

Koinobiont endoparasitoid wasps whose larvae develop inside a host insect alter several important facets of host physiology, potentially causing cascading effects across multiple trophic levels. For instance, the hijacking of the host immune responses may have effects on how insects interact with host plants and microbial associates. However, the parasitoid regulation of insect–plant–microbiome interactions is still understudied. In this study, we used the fall armyworm (FAW), Spodoptera frugiperda, and the braconid parasitoid Cotesia marginiventris to evaluate impacts of parasitism on the gut microbiome of FAW larvae, and respective maize plant defense responses. The level of reactive oxygen species and the microbial community in larval gut underwent significant changes in response to parasitism, leading to a significant reduction of Enterococcus, while elevating the relative abundance of Pseudomonas. FAW with parasitism had lower glucose oxidase (GOX) activity in salivary glands and triggered lower defense responses in maize plants. These changes corresponded to effects on plants, as Pseudomonas inoculated larvae had lower activity of salivary GOX and triggered lower defense responses in maize plants. Our results demonstrated that parasitism had cascading effects on microbial associates across trophic levels and also highlighted that insect gut bacteria may contribute to complex interrelationships among parasitoids, herbivores, and plants.

共生性内寄生蜂幼虫在宿主昆虫体内发育，会改变宿主生理的多个重要方面，可能引发跨多个营养级的级联效应。例如，劫持宿主免疫反应可能影响昆虫与宿主植物以及微生物伙伴的相互作用。然而，寄生蜂对昆虫-植物-微生物组相互作用的调节仍属研究不足。在本研究中，我们利用舞毒蛾（FAW），即 Spodoptera frugiperda，以及茧蜂科寄生蜂 Cotesia marginiventris，评估了寄生对舞毒蛾幼虫肠道微生物组和相应玉米植物防御反应的影响。幼虫肠道中的活性氧水平和微生物群落对寄生反应产生了显著变化，导致肠球菌显著减少，而假单胞菌的相对丰度增加。受寄生影响的舞毒蛾唾液腺中葡萄糖氧化酶（GOX）活性降低，并引发了玉米植物较低的防御反应。这些变化与植物效应相对应，因为接种了假单胞菌的幼虫具有较低的唾液GOX活性，并引发了玉米植物较低的防御反应。我们的研究结果证明了寄生对微生物伙伴在营养级上的级联效应，并突显了昆虫肠道细菌可能对寄生蜂、食草动物和植物之间的复杂相互关系做出贡献。