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.近一个世纪以来，新兴植物病原物的数量呈指数级增长。为应对这一问题，明确这些病原物是否为本土生态系统原有物种，或是近期传入的外来物种，是至关重要的。解析促成本病原物暴发的生态与演化过程，有助于管控其扩散并预测流行病与植物流行病（epiphytotics）。本研究利用限制性酶切位点相关DNA测序（restriction site-associated DNA sequencing, RAD-seq）数据，针对东亚、澳大利亚及太平洋群岛地区一种起源不明的新兴根腐真菌——恶生木层孔菌（Phellinus noxius），解析其遗传亲缘关系、扩散路径与演化历史。我们采用贝叶斯推断、最大似然系统发育分析、基于等位基因频率相关性与遗传漂变测算的群体拆分与混合分析，并结合近似贝叶斯计算（Approximate Bayesian computation, ABC）与监督机器学习方法，基于溯祖理论解析其遗传变异模式。群体结构分析结果显示，该真菌存在5个遗传类群，且呈现出复杂的近期与远古迁移历史特征。最可能的远古病原物扩散场景为：从一个未被采样的群体传播至马来西亚与太平洋群岛，随后进一步扩散至中国台湾地区与澳大利亚。此外，近似贝叶斯计算分析结果表明，恶生木层孔菌的扩散发生于数千代之前，这与此前认为该病原物近期才传入多个地理区域的假设相悖。本研究结果显示，东亚、澳大利亚及太平洋群岛地区恶生木层孔菌的近期暴发，可能由人为与自然干扰活动驱动，例如森林砍伐、土地利用变化、极端天气事件，以及/或外来植物引种。本研究为在生态系统动态变化的背景下，利用全基因组等位基因频率数据解析病原物暴发动态提供了全新范例。