Cohen Zachary P, François Olivier, Schoville Sean D
Department of Entomology, University of Wisconsin-Madison, Madison, WI, USA.
Insect Control and Cotton Disease Research Unit, USDA, Agricultural Research Service, College Station, TX, USA.
Integr Comp Biol. 2022 Dec 30;62(6):1827-1837. doi: 10.1093/icb/icac137.
Despite extensive research on agricultural pests, our knowledge about their evolutionary history is often limited. A mechanistic understanding of the demographic changes and modes of adaptation remains an important goal, as it improves our understanding of organismal responses to environmental change and our ability to sustainably manage pest populations. Emerging genomic datasets now allow for characterization of demographic and adaptive processes, but face limits when they are drawn from contemporary samples, especially in the context of strong demographic change, repeated selection, or adaptation involving modest shifts in allele frequency at many loci. Temporal sampling, however, can improve our ability to reconstruct evolutionary events. Here, we leverage museum samples to examine whether population genomic diversity and structure has changed over time, and to identify genomic regions that appear to be under selection. We focus on the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say 1824; Coleoptera: Chrysomelidae), which is widely regarded as a super-pest due to its rapid, and repeated, evolution to insecticides. By combining whole genome resequencing data from 78 museum samples with modern sampling, we demonstrate that CPB expanded rapidly in the 19th century, leading to a reduction in diversity and limited genetic structure from the Midwest to Northeast United States. Temporal genome scans provide extensive evidence for selection acting in resistant field populations in Wisconsin and New York, including numerous known insecticide resistance genes. We also validate these results by showing that known selective sweeps in modern populations are identified by our genome scan. Perhaps most importantly, temporal analysis indicates selection on standing genetic variation, as we find evidence for parallel evolution in the two geographical regions. Parallel evolution involves a range of phenotypic traits not previously identified as under selection in CPB, such as reproductive and morphological functional pathways that might be important for adaptation to agricultural habitats.
尽管对农业害虫进行了广泛研究，但我们对它们进化历史的了解往往有限。对种群动态变化和适应模式的机制性理解仍然是一个重要目标，因为这能增进我们对生物体对环境变化的反应的理解以及我们可持续管理害虫种群的能力。新兴的基因组数据集现在能够对种群动态和适应过程进行特征描述，但当它们来自当代样本时会面临局限性，特别是在种群动态强烈变化、反复选择或涉及许多位点等位基因频率适度变化的适应情况下。然而，时间序列采样可以提高我们重建进化事件的能力。在这里，我们利用博物馆样本研究种群基因组多样性和结构是否随时间发生了变化，并识别出似乎受到选择的基因组区域。我们聚焦于科罗拉多马铃薯甲虫（CPB），即十星瓢萤叶甲（Leptinotarsa decemlineata (Say 1824; 鞘翅目：叶甲科），由于其对杀虫剂迅速且反复的进化，它被广泛视为一种超级害虫。通过将来自78个博物馆样本的全基因组重测序数据与现代采样相结合，我们证明CPB在19世纪迅速扩张，导致从美国中西部到东北部的多样性降低和遗传结构有限。时间序列基因组扫描为在威斯康星州和纽约的抗性田间种群中起作用的选择提供了大量证据，包括众多已知的抗杀虫剂基因。我们还通过表明我们的基因组扫描能识别出现代种群中已知的选择性清除来验证这些结果。也许最重要的是，时间序列分析表明对现存遗传变异的选择，因为我们在两个地理区域发现了平行进化的证据。平行进化涉及一系列以前未被确定为在CPB中受到选择的表型特征，例如可能对适应农业栖息地很重要的生殖和形态功能途径。
