Convergent evolution leads to identical phenotypic traits in different species or populations. Convergence can be driven by standing variation allowing selection to favour identical alleles in parallel or the same mutations can arise independently. However, the molecular basis of such convergent adaptation remains often poorly resolved. Pesticide resistance in agricultural ecosystems is a hallmark of convergence in phenotypic traits. Here, we analyse the major fungal pathogen Zymoseptoria tritici causing serious losses on wheat and with fungicide resistance emergence across several continents. We sampled three population pairs each from a different continent spanning periods early and late in the application of fungicides. To identify causal loci for resistance, we combined knowledge from molecular genetics work and performed genome-wide association studies (GWAS) on a global set of isolates. We discovered yet unknown factors in azole resistance including a gene encoding membrane associated functions. We found strong support for the “hotspot” model of resistance evolution with convergent changes in a small set of loci but additional loci showed more population-specific allele frequency changes. Genome-wide scans of selection showed that half of all known resistance loci were overlapping a selective sweep region. Hence, the application of fungicides was one of the major selective agents acting on the pathogen over the past decades. Furthermore, loci identified through GWAS showed the highest overlap with selective sweep regions underlining the importance to map phenotypic trait variation in evolving populations. Our population genomic analyses highlighted that both de novo mutations and gene flow contributed to convergent pesticide adaptation.

中文翻译：

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真菌植物病原体跨大陆对农药快速趋同适应的复杂基因组基础

趋同进化导致不同物种或种群中相同的表型特征。趋同可以由常设变异驱动，允许选择平行的相同等位基因，或者相同的突变可以独立出现。然而，这种趋同适应的分子基础通常仍然很难解决。农业生态系统中的农药抗性是表型性状趋同的标志。在这里，我们分析了主要的真菌病原体Zymoseptoria tritici造成小麦严重损失，并且在几个大洲出现了杀菌剂抗药性。我们在杀菌剂应用的早期和晚期从不同的大陆对三个种群进行了采样。为了确定耐药性的致病基因座，我们结合了分子遗传学工作的知识，并对一组全球分离株进行了全基因组关联研究 (GWAS)。我们发现了唑类抗性的未知因素，包括编码膜相关功能的基因。我们发现了对抗性进化的“热点”模型的强烈支持，其中一小部分基因座会发生收敛变化，但额外的基因座显示出更多的群体特异性等位基因频率变化。全基因组选择扫描显示，所有已知抗性基因座中有一半与选择性扫描区域重叠。因此，杀菌剂的应用是过去几十年作用于病原体的主要选择性药剂之一。此外，通过 GWAS 鉴定的基因座与选择性扫描区域的重叠度最高，强调了在进化种群中绘制表型性状变异图的重要性。我们的群体基因组分析强调，从头突变和基因流动都有助于趋同农药适应。