Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia, and the Pacific Islands

Emerging plant pathogens have been increasing exponentially over the last century. To address this issue, it is critical to determine whether these pathogens are native to ecosystems or have been recently introduced. Understanding the ecological and evolutionary processes fostering emergence can help to manage their spread and predict epidemics/epiphytotics. Using restriction site-associated DNA sequencing data, we studied genetic relationships, pathways of spread, and evolutionary history of Phellinus noxius, an emerging root-rotting fungus of unknown origin, in eastern Asia, Australia, and the Pacific Islands. We analyzed patterns of genetic variation using Bayesian inference, maximum likelihood phylogeny, populations splits and mixtures measuring correlations in allele frequencies and genetic drift, and finally applied coalescent based theory using Approximate Bayesian computation (ABC) with supervised machine learning. Population structure analyses revealed five genetic groups with signatures of complex recent and ancient migration histories. The most probable scenario of ancient pathogen spread is movement from an unsampled population to Malaysia and the Pacific Islands, with subsequent spread to Taiwan and Australia. Furthermore, ABC analyses indicate P. noxius spread occurred thousands of generations ago, contradicting previous assumptions that this pathogen was recently introduced to multiple geographic regions. Our results suggest that recent emergence of P. noxiusin eastern Asia, Australia, and the Pacific Islands is likely driven by anthropogenic and natural disturbances, such as deforestation, land-use change, severe weather events, and/or introduction of exotic plants. This study provides a novel example of applying genome-wide allele frequency data to unravel dynamics of pathogen emergence under changing ecosystem conditions.

Methods
The dataset contains three input files obtained from raw RADseq reads with Stacks v.2 to generate results in our paper. It also contains configuration files of five DIYABC analyses performed with DIYABC Random Forest v.1.

近百年来，新兴植物病原物的发生量呈指数级增长态势。针对这一现状，明确此类病原物究竟是本土生态系统固有类群，还是新近入侵的外来物种，是开展防控工作的关键前提。解析推动其暴发的生态与演化机制，可为管控其扩散范围、预测植物流行病（epiphytotics）发生提供科学依据。本研究借助限制性酶切位点相关DNA测序（restriction site-associated DNA sequencing）数据，针对东亚、澳大利亚及太平洋岛屿地区一种起源不明的新兴根腐真菌——恶疫木层孔菌（Phellinus noxius），开展了其遗传关系、扩散路径与演化历史的相关研究。研究团队采用贝叶斯推断、最大似然系统发育分析、种群分化与混合分析（用于衡量等位基因频率相关性与遗传漂变），最终结合近似贝叶斯计算（Approximate Bayesian computation, ABC）与监督机器学习方法，搭建了基于溯祖理论的分析框架。种群结构分析结果显示，该真菌可划分为5个遗传类群，其演化历史兼具复杂的近代与古代迁移特征。最具可能性的古代病原物扩散场景为：从未经采样的种群传播至马来西亚与太平洋岛屿，随后进一步扩散至中国台湾地区与澳大利亚。此外，ABC分析结果表明，恶疫木层孔菌的跨区域扩散发生在数千世代之前，这与此前学界认为该病原物是近期入侵多个地理区域的假设相互矛盾。本研究结果揭示，东亚、澳大利亚及太平洋岛屿地区恶疫木层孔菌的近期暴发，大概率由人为活动与自然扰动共同驱动，具体包括森林砍伐、土地利用变化、极端天气事件，以及/或外来植物的引入。本研究为应用全基因组等位基因频率数据，解析生态系统变化背景下病原物暴发动态提供了全新的研究范例。
方法
本数据集包含3份输入文件，均由原始RADseq测序读段通过Stacks v.2软件处理得到，用于生成本论文的分析结果。此外，数据集还包含5次DIYABC分析的配置文件，此类分析通过DIYABC Random Forest v.1软件完成。