Data from: Fungal adaptation to contemporary fungicide applications: the case of Botrytis cinerea populations from Champagne vineyards (France)

In addition to being one of the most acute problems impeding chemical control of fungal diseases, the evolution of fungicide resistance is an emblematic case of local adaptation to spatially heterogeneous and temporally variable selection pressures. Here we dissected the adaptation of Botrytis cinerea (the causal agent of grey mould) populations on grapes to several fungicides. We carried out a 2-year survey (four collection dates) on three treated/untreated pairs of plots from vineyards in Champagne (France) and monitored the frequency of four resistant phenotypes that are unambiguously associated with four distinct genotypes. For two loci under selection by currently used fungicides (MDR1 and MDR2), the frequencies of resistant mutations at vintage were greater in treated plots compared to untreated plots, showing that the effect of selection is detectable even at the plot scale. This effect was not detectable for two other loci under selection by previously used fungicides (BenR1 and ImiR1). We also found that treatment with currently used fungicides reduced B. cinerea effective population size, leading to a significant decrease in genic diversity and allelic richness in treated vs. untreated plots. We further highlight that even under ample drift and migration, fungal populations can present an efficient response to selection. Finally, for the four studied loci, the costs of fungicide resistance were estimated by modelling the decrease in the frequency of resistant mutations in the absence of treatment. We discuss the importance of these estimates for defining strategies for limiting or counteracting the local adaptation of pests to fungicides.

除了是阻碍真菌病害化学防控的最棘手问题之一外，杀菌剂抗药性的演化亦是生物种群对空间异质性与时间波动性选择压力产生局部适应的典型范例。本研究解析了葡萄灰霉病病原菌灰葡萄孢（Botrytis cinerea）种群对多种杀菌剂的适应过程。我们于法国香槟产区的葡萄园，针对三组杀菌剂处理与未处理的成对样地开展了为期两年的调查，共设置四个采样时间点，并监测了四种明确对应不同基因型的抗药表型频率。针对当前生产中使用的杀菌剂所靶向的两个抗性位点（MDR1与MDR2），在当季采收时，处理样地内的抗性突变频率显著高于未处理样地，这表明即便在样地尺度下，选择压的效应也可被检测到。而针对此前生产中使用的杀菌剂所靶向的另外两个抗性位点（BenR1与ImiR1），则未观测到该选择效应。我们还发现，施用当前主流杀菌剂会降低灰葡萄孢的有效种群大小（effective population size），使得处理样地的基因多样性（genic diversity）与等位基因丰富度（allelic richness）相较未处理样地出现显著下降。本研究进一步证实，即便存在较强的遗传漂变与基因流，真菌种群仍可对选择压力产生高效的适应性响应。最后，我们通过模拟无杀菌剂处理条件下抗性突变频率的衰减，估算了本次研究涉及的4个抗性位点对应的杀菌剂抗药性适合度代价。本文还探讨了上述估算结果在制定限制或逆转有害生物对杀菌剂产生局部适应的防控策略中的重要价值。