Phylogenomic conflict analyses in the apple genus Malus s.l. reveal widespread hybridization and allopolyploidy driving diversification, with insights into the complex biogeographic history in the Northern Hemisphere

Phylogenomic evidence from an increasing number of studies has demonstrated that different data sets and analytical approaches often reconstruct strongly supported but conflicting relationships. In this study, 785 single-copy nuclear genes and 75 complete plastomes were used to infer the phylogenetic relationships and estimate the historical biogeography of the apple genus Malus sensu lato, an economically important lineage disjunctly distributed in the Northern Hemisphere and involved in known and suspected hybridization and allopolyploidy events. The nuclear phylogeny recovered the monophyly of Malus s.l. (including Docynia); however, the genus was supported to be biphyletic in the plastid phylogeny. An ancient chloroplast capture event in the Eocene in western North America best explains the cytonuclear discordance. Our conflict analysis demonstrated that ILS, hybridization, and allopolyploidy could explain the widespread nuclear gene tree discordance. One deep hybridization event (Malus doumeri) and one recent event (Malus coronaria) were detected in Malus s.l. Furthermore, our historical biogeographic analysis integrating living and fossil data supported a widespread East Asian-western North American origin of Malus s.l. in the Eocene, followed by several extinction and dispersal events in the Northern Hemisphere. We also propose a general workflow for assessing phylogenomic discordance and biogeographic analysis using deep genome skimming datasets.

越来越多的研究通过系统发育基因组学 (Phylogenomic) 证据表明，不同数据集与分析方法往往会重建出支持度极高但彼此冲突的系统发育关系。本研究选取785个单拷贝核基因与75个完整质体基因组 (plastome)，对广义苹果属 (Malus sensu lato) 的系统发育关系进行推断，并重建其历史生物地理学格局。广义苹果属是一类具有重要经济价值的支系，间断分布于北半球，且已知存在或疑似存在杂交与异源多倍化 (allopolyploidy) 事件。核基因系统发育树支持广义苹果属（包括栘[木衣]属 (Docynia)）为单系群；但质体系统发育树则显示该属为双系群 (biphyletic)。发生于始新世 (Eocene) 北美西部的一次古老叶绿体捕获事件，可最佳解释核质系统发育不一致 (cytonuclear discordance) 现象。本研究的冲突分析表明，不完全谱系分选 (Incomplete Lineage Sorting, ILS)、杂交与异源多倍化可解释广泛存在的核基因树冲突现象。在广义苹果属中，检测到一次深度杂交事件 (Malus doumeri) 与一次近期杂交事件 (Malus coronaria)。此外，整合现生与化石数据的历史生物地理学分析表明，广义苹果属起源于始新世的东亚-北美西部广布区域，随后在北半球经历了多次灭绝与扩散事件。本研究还提出了一套通用流程，可用于基于深度基因组浅测序 (deep genome skimming) 数据集评估系统发育基因组学冲突与开展生物地理学分析。