Insecticides promote viral outbreaks by altering herbivore competition

While the management of biological invasions is often characterized by a series of single-species decisions, invasive species exist within larger food webs. These biotic interactions can alter the impact of control/eradication programs and may cause suppression efforts to inadvertently facilitate invasion spread and impact. We document the rapid replacement of the invasive Bemisia MEAM1 cryptic species by the cryptic MED species throughout China, and demonstrate that MED is more tolerant of insecticides and a better vector of tomato yellow leaf curl virus ('TYLCV') than MEAM1. While MEAM1 usually excludes MED under natural conditions, insecticide application reverses the MEAM1-MED competitive hierarchy and allows MED to exclude MEAM1. The insecticide-mediated success of MED has led to TYLCV outbreaks throughout China. Our work strongly supports the hypothesis that insecticide use in China reverses the MEAM1-MED competitive hierarchy and allows MED to displace MEAM1 in managed landscapes. By promoting the dominance of a Bemisia species that is a competent viral vector, insecticides thus increase the spread and impact of TYLCV in heterogeneous agroecosystems.

尽管生物入侵防控通常基于一系列针对单一物种的管控决策，但入侵物种实际生存于更为复杂的食物网之中。这些生物相互作用可改变防控或根除项目的实施效果，甚至可能使物种压制措施在无意间加剧入侵物种的扩散与危害程度。我们记录了烟粉虱属（Bemisia）隐存种MED在全国范围内快速取代入侵性隐存种MEAM1的过程，并证实相较于MEAM1，MED对杀虫剂的耐受性更强，且是更高效的番茄黄化曲叶病毒（tomato yellow leaf curl virus, TYLCV）媒介昆虫。尽管自然条件下MEAM1通常会排挤MED，但杀虫剂的使用会逆转二者的竞争等级，使MED得以取代MEAM1。这种由杀虫剂介导的MED种群优势，已引发全国范围内的番茄黄化曲叶病毒暴发。本研究有力支持了如下假说：在中国境内使用杀虫剂会逆转MEAM1与MED的竞争等级，使MED在人为管理的农田景观中取代MEAM1。因此，杀虫剂通过提升一种具备高效病毒传播能力的烟粉虱属物种的种群优势，加剧了番茄黄化曲叶病毒在异质性农业生态系统中的扩散与危害。