Yin Xiaoshen, Martinez Alexander S, Perkins Abigail, Sparks Morgan M, Harder Avril M, Willoughby Janna R, Sepúlveda Maria S, Christie Mark R
Department of Biological Sciences Purdue University West Lafayette IN USA.
Department of Anatomy, Cell Biology & Physiology Indiana University School of Medicine Indianapolis IN USA.
Evol Appl. 2020 Dec 14;14(3):847-859. doi: 10.1111/eva.13166. eCollection 2021 Mar.
The resistance of pest species to chemical controls has vast ecological, economic, and societal costs. In most cases, resistance is only detected after spreading throughout an entire population. Detecting resistance in its incipient stages, by comparison, provides time to implement preventative strategies. Incipient resistance can be detected by coupling standard toxicology assays with large-scale gene expression experiments. We apply this approach to a system where an invasive parasite, sea lamprey (), has been treated with the highly effective pesticide 3-trifluoromethyl-4-nitrophenol (TFM) for 60 years. Toxicological experiments revealed that lamprey from treated populations did not have higher survival to TFM exposure than lamprey from untreated populations, demonstrating that full-fledged resistance has not yet evolved. In contrast, we find hundreds of genes differentially expressed in response to TFM in the population with the longest history of exposure, many of which relate to TFM's primary mode of action, the uncoupling of oxidative phosphorylation, and subsequent depletion of ATP. Three genes critical to oxidative phosphorylation, and , were nearly fixed for alternative alleles in comparisons of SNPs between treated and untreated populations ( > 5 from the mean). encodes subunit b of ATP synthase and an additional subunit, , was canalized for high expression in treated populations, but remained plastic in response to TFM treatment in individuals from the untreated population. These combined genomic and transcriptomic results demonstrate that an adaptive, genetic response to TFM is likely driving incipient resistance in a damaging pest species.
害虫物种对化学防治产生的抗性会带来巨大的生态、经济和社会成本。在大多数情况下，抗性只有在整个种群中传播后才会被发现。相比之下，在抗性初期阶段进行检测，可以争取时间实施预防策略。通过将标准毒理学检测与大规模基因表达实验相结合，能够检测出初期抗性。我们将这种方法应用于一个系统，在该系统中，一种入侵性寄生虫海七鳃鳗（）已经用高效杀虫剂3-三氟甲基-4-硝基苯酚（TFM）处理了60年。毒理学实验表明，经过处理的种群中的七鳃鳗在接触TFM时的存活率并不比未处理种群中的七鳃鳗高，这表明完全抗性尚未演化出来。相比之下，我们发现，在接触时间最长的种群中，有数百个基因因TFM而发生差异表达，其中许多基因与TFM的主要作用模式、氧化磷酸化的解偶联以及随后的ATP耗竭有关。在比较处理种群和未处理种群的单核苷酸多态性时，对氧化磷酸化至关重要的三个基因和，其替代等位基因几乎固定下来（与平均值相差>5）。编码ATP合酶的亚基b，另一个亚基在处理种群中被定向为高表达，但在未处理种群的个体中，其表达对TFM处理仍具有可塑性。这些基因组和转录组的综合结果表明，对TFM的适应性遗传反应可能正在推动一种有害害虫物种产生初期抗性。
