Data from: Landscape genomics of Colorado potato beetle provides evidence of polygenic adaptation to insecticides

The ability of insect pests to rapidly and repeatedly adapt to insecticides has long challenged entomologists and evolutionary biologists. Since Crow’s seminal paper on insecticide resistance in 1957, new data and insights continue to emerge that are relevant to the old questions about how insecticide resistance evolves: such as whether it is predominantly mono- or polygenic, and evolving from standing vs. <i>de novo</i> genetic variation. Many studies support the monogenic hypothesis, and current management recommendations assume single- or two-locus models. But inferences could be improved by integrating data from a broader sample of pest populations and genomes. Here we generate evidence relevant to these questions by applying a landscape genomics framework to the study of insecticide resistance in a major agricultural pest, Colorado potato beetle, <i>Leptinotarsa decemlineata</i> (Say). Genome-environment association tests using genomic variation from 16 populations spanning gradients of landscape variables associated with insecticide exposure over time revealed 42 strong candidate insecticide resistance genes, with potentially overlapping roles in multiple resistance mechanisms. Measurements of resistance to a widely-used insecticide, imidacloprid, among 47 <i>L. decemlineata</i> populations revealed heterogeneity at a small (2 km) scale and no spatial signature of origin or spread throughout the landscape. Analysis of nucleotide diversity suggested candidate resistance loci have undergone varying degrees of selective sweeps, often maintaining similar levels of nucleotide diversity to neutral loci. This study suggests that many genes are involved in insecticide resistance in <i>L. decemlineata</i> and that resistance likely evolves from both <i>de novo</i> and standing genetic variation.

害虫快速且反复演化出对杀虫剂的适应性的现象，长期以来始终困扰着昆虫学家与进化生物学家。自1957年克劳（Crow）发表关于杀虫剂抗性的开创性论文以来，围绕杀虫剂抗性演化的一系列经典问题——例如抗性主要为单基因还是多基因调控、其演化源自现存遗传变异还是新发（de novo）遗传变异——相关的新数据与新认知持续涌现。诸多研究支持单基因假说，当前的害虫抗性治理方案也多基于单基因或双基因座模型。但若能纳入更广范围的害虫种群与基因组数据开展整合分析，相关推论的可靠性可得到进一步提升。本研究以重大农业害虫科罗拉多马铃薯甲虫（*Leptinotarsa decemlineata* (Say)）为研究对象，运用景观基因组学（landscape genomics）框架开展杀虫剂抗性相关研究，为解答上述问题提供实证依据。研究团队对覆盖随时间推移与杀虫剂暴露相关的景观变量梯度的16个种群的基因组变异进行全基因组-环境关联分析（genome-environment association tests），共鉴定出42个强效杀虫剂抗性候选基因，这些基因可能在多种抗性机制中存在功能重叠。对47个*L. decemlineata*种群开展的广谱杀虫剂吡虫啉（imidacloprid）抗性检测结果显示，其抗性在2公里的小尺度下即存在异质性，且未在整个研究景观中呈现出抗性起源或扩散的空间特征。核苷酸多样性（nucleotide diversity）分析结果表明，候选抗性基因座经历了不同程度的选择性清除（selective sweeps），且其核苷酸多样性水平通常与中性基因座相当。本研究表明，*L. decemlineata*的杀虫剂抗性涉及众多基因，且抗性的演化可能同时源自新发遗传变异与现存遗传变异。