Plant viruses can change hosts in ways that increase vector contacts, virion acquisition, and subsequent vector dispersal to susceptible hosts. Based on this, researchers have proposed that virus-induced phenotypes are the product of adaptations to “manipulate” hosts in ways that increase transmission. Theoretical models of virus spread in crops support this proposition; “manipulative” viruses spread faster and to a greater extent. However, both empirical and theoretical studies on manipulation are disproportionately focused on a few persistently transmitted pathogens and rarely consider the broader ecological implications of virus infections. To address these knowledge gaps, we documented the effects of different stages of infection by an economically devastating, semi-persistently transmitted crinivirus, Cucurbit yellow stunting disorder virus [CYSDV] on Cucumis melo (muskmelon) phenotypes, behavior and performance of whitefly vectors (Bemisia tabaci) and non-vector aphid competitors (Aphis gossypii). Whiteflies were strongly attracted to CYSDV-infected hosts in a symptomatic stage of disease, but not in an asymptomatic stage, and fed more easily on infected plants regardless of symptoms. In contrast, aphids tended to avoid infected hosts, fed for shorter periods of time, and produced fewer offspring on infected hosts. Metabolomics revealed that host manipulations by CYSDV do not rely on virus-induced shifts in leaf primary metabolites or volatiles but may involve changes to phloem architecture and other compounds not measured here. Our study demonstrates a sophisticated host manipulation by CYSDV, whereby infection discourages colonization by a non-vector competitor while inducing a suite of progressively more transmission-conducive changes that encourage virion acquisition by the vector.

植物病毒可以通过增加载体接触、病毒粒子获取以及随后载体向易感宿主的传播的方式改变宿主。基于此，研究人员提出病毒诱导的表型是适应以增加传播的方式“操纵”宿主的产物。病毒在作物中传播的理论模型支持这一主张；“操纵性”病毒传播得更快、范围更广。然而，关于操纵的实证研究和理论研究都过分关注少数持续传播的病原体，很少考虑病毒感染的更广泛的生态影响。为了解决这些知识空白，我们记录了一种经济破坏性、半持久性传播的 crinivirus 感染不同阶段的影响，葫芦黄发育迟缓病毒[CYSDV] 对甜瓜（甜瓜）表型、粉虱载体（烟粉虱）和非载体蚜虫竞争者（棉蚜）的表型、行为和性能）。在有症状的疾病阶段，粉虱被 CYSDV 感染的宿主强烈吸引，但在无症状阶段则不然，并且无论症状如何，都更容易以受感染的植物为食。相比之下，蚜虫倾向于避开受感染的宿主，喂食时间较短，并在受感染的宿主上产生较少的后代。代谢组学表明，CYSDV 对宿主的操作不依赖于病毒诱导的叶片初级代谢物或挥发物的变化，但可能涉及韧皮部结构和此处未测量的其他化合物的变化。我们的研究证明了 CYSDV 对宿主的复杂操纵，感染阻止了非载体竞争者的定植，同时诱导了一套逐渐更有利于传播的变化，鼓励载体获取病毒粒子。