Large-scale phylogenomics reveals ancient introgression in Asian Hepatica and new insights into the origin of the insular endemic Hepatica maxima

Hepatica maxima is native to Ulleungdo, which is one of the oceanic islands in Korea, and it likely originated via anagenetic speciation from the Korean mainland species H. asiatica. However, the relationships among the Asian lineages remain unresolved. Phylogenomics based on plant genomes can provide new insights into the evolutionary history of plants. We first generated plastid, mitochondrial and transcriptome sequences of the insular endemic species H. maxima. Using the genomic data for H. maxima, we obtained a phylogenomic dataset consisting of 76 plastid, 37 mitochondrial and 413 nuclear genes from Asian Hepatica and two outgroups. Coalescent- and concatenation-based methods revealed cytonuclear and organellar discordance in the lineage. The presence of gynodioecy with cytoplasmic male sterility in Asian Hepatica suggests that the discordance is correlated with potential disruption of linkage disequilibrium between the organellar genomes. Species network analyses revealed a deep history of hybridization and introgression in Asian Hepatica. We discovered that ancient and recent introgression events occurred throughout the evolutionary history of the insular endemic species H. maxima. The introgression may serve as an important source of genetic variation to facilitate adaptation to the Ulleungdo environment.

大花獐耳细辛（Hepatica maxima）原产于韩国海洋性岛屿之一郁陵岛，其可能由朝鲜大陆物种亚洲獐耳细辛（H. asiatica）通过前进演化成种（anagenetic speciation）形成。然而，亚洲獐耳细辛属支系间的系统发育关系仍未厘清。基于植物基因组的系统基因组学（Phylogenomics）研究可为解析植物演化历史提供全新视角。本研究首先对该岛屿特有种大花獐耳细辛的质体（plastid）、线粒体（mitochondrial）及转录组（transcriptome）序列进行了测序与组装。依托大花獐耳细辛的基因组数据，我们构建了一套系统基因组数据集，涵盖来自亚洲獐耳细辛类群及2个外类群的76个质体基因、37个线粒体基因与413个核基因。基于溯祖法（coalescent-based method）与串联法（concatenation-based method）的分析结果显示，该支系存在质核基因组与细胞器基因组的演化冲突。亚洲獐耳细辛类群中存在伴随细胞质雄性不育（cytoplasmic male sterility）的雌全异株（gynodioecy）现象，这暗示该基因组冲突或与细胞器基因组间连锁不平衡（linkage disequilibrium）的潜在破坏存在关联。物种网络分析（species network analyses）揭示了亚洲獐耳细辛属类群拥有悠久的杂交与基因渐渗（introgression）演化历史。研究发现，从古至今的基因渐渗事件贯穿了大花獐耳细辛的完整演化历程。该基因渐渗事件或可作为重要的遗传变异来源，助力其适应郁陵岛的特有生境。