Phylogenomic Analysis of Target Enrichment and Transcriptome Data Uncovers Rapid Radiation and Extensive Hybridization in Slipper Orchid Genus Cypripedium L

IF 3.6 2区 生物学 Q1 PLANT SCIENCES Annals of botany Pub Date : 2024-09-09 DOI:10.1093/aob/mcae161
Loudmila Jelinscaia Lagou, Gudrun Kadereit, Diego F Morales-Briones
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Abstract

Background and Aims Cypripedium is the most widespread and morphologically diverse genus of slipper orchids. Despite several published phylogenies, the topology and monophyly of its infrageneric taxa remained uncertain. Here, we aimed to reconstruct a robust section-level phylogeny of Cypripedium and explore its evolutionary history using target capture data for the first time. Methods We used the orchid-specific bait set Orchidaceae963 in combination with transcriptomic data to reconstruct the phylogeny of Cypripedium based on 913 nuclear loci, covering all 13 sections. Subsequently, we investigated discordance among nuclear and chloroplast trees, estimated divergence times and ancestral ranges, searched for anomaly zones, polytomies, and diversification rate shifts, and identified potential gene (genome) duplication and hybridization events. Key Results All sections were recovered as monophyletic, contrary to the two subsections within sect. Cypripedium. The two subclades within this section did not correspond to its subsections but matched the geographic distribution of their species. Additionally, we discovered high levels of discordance in the short backbone branches of the genus and within sect. Cypripedium, which can be attributed to hybridization events detected based on phylogenetic network analyses, and incomplete lineage sorting caused by rapid radiation. Our biogeographic analysis suggested a Neotropical origin of the genus during the Oligocene (~30 Ma), with a lineage of potentially hybrid origin spreading to the Old World in the Early Miocene (~22 Ma). The rapid radiation at the backbone likely occurred in Southeast Asia around the Middle Miocene Climatic Transition (~15–13 Ma), followed by several independent dispersals back to the New World. Moreover, the Pliocene-Quaternary glacial cycles may have contributed to further speciation and reticulate evolution within Cypripedium. Conclusions Our study provided novel insights into the evolutionary history of Cypripedium based on high-throughput molecular data, shedding light on the dynamics of its distribution and diversity patterns from its origin to the present.
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目标富集和转录组数据的系统发生组分析揭示了拖鞋兰属 Cypripedium L 的快速辐射和广泛杂交
背景和目的 蕙兰是分布最广、形态最多样的拖鞋兰属。尽管已发表了几个系统发生,但其下属类群的拓扑结构和单系仍不确定。在此,我们首次利用目标捕获数据重建了一个稳健的虎皮兰科级系统发育,并探索了其进化历史。方法 我们利用兰花特异性诱饵集 Orchidaceae963 和转录组数据,基于 913 个核位点重建了 Cypripedium 的系统发育,涵盖了所有 13 个部分。随后,我们研究了核树和叶绿体树之间的不一致性,估计了分化时间和祖先范围,寻找了异常区、多态性和分化率变化,并确定了潜在的基因(基因组)重复和杂交事件。主要结果 所有的科都被恢复为单系,与Cypripedium科中的两个亚科相反。Cypripedium。该节中的两个亚支系与其子节不一致,但与其物种的地理分布相匹配。此外,我们还发现该属的短骨干分支与该科内的短骨干分支存在高度不一致。这可归因于根据系统发生网络分析检测到的杂交事件,以及快速辐射导致的不完全世系分类。我们的生物地理学分析表明,该属起源于渐新世(约 30 Ma)的新热带地区,在中新世早期(约 22 Ma),一个可能是杂交起源的品系扩散到了旧大陆。骨干的快速辐射很可能发生在中新世气候转变前后(约 15-13 Ma)的东南亚地区,随后又有几个独立的种群扩散回新大陆。此外,上新世-第四纪冰川周期也可能促进了鱼腥草的进一步物种分化和网状演化。结论 我们的研究以高通量分子数据为基础,为了解青鱼草的进化历史提供了新的视角,揭示了青鱼草从起源至今的分布动态和多样性模式。
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来源期刊
Annals of botany
Annals of botany 生物-植物科学
CiteScore
7.90
自引率
4.80%
发文量
138
审稿时长
3 months
期刊介绍: Annals of Botany is an international plant science journal publishing novel and rigorous research in all areas of plant science. It is published monthly in both electronic and printed forms with at least two extra issues each year that focus on a particular theme in plant biology. The Journal is managed by the Annals of Botany Company, a not-for-profit educational charity established to promote plant science worldwide. The Journal publishes original research papers, invited and submitted review articles, ''Research in Context'' expanding on original work, ''Botanical Briefings'' as short overviews of important topics, and ''Viewpoints'' giving opinions. All papers in each issue are summarized briefly in Content Snapshots , there are topical news items in the Plant Cuttings section and Book Reviews . A rigorous review process ensures that readers are exposed to genuine and novel advances across a wide spectrum of botanical knowledge. All papers aim to advance knowledge and make a difference to our understanding of plant science.
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