Phylogenomic Analyses Reveal Widespread Gene Flow During the Early Radiation of Oaks and Relatives (Fagaceae: Quercoideae)
Phylogenomic Analyses Reveal Widespread Gene Flow During the Early Radiation of Oaks and Relatives (Fagaceae: Quercoideae)
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DOI：
10.1101/2023.04.25.538215
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发表时间：
2023-04
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通讯作者：
Shuiyin Liu;Yingying Yang;Qin Tian;Zhiyun Yang;Shufeng Li;P. Valdes;A. Farnsworth;H. Kates;C. Siniscalchi;R. Guralnick;D. Soltis;P. Soltis;Gregory W. Stull;R. Folk;T. Yi
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作者：
Shuiyin Liu;Yingying Yang;Qin Tian;Zhiyun Yang;Shufeng Li;P. Valdes;A. Farnsworth;H. Kates;C. Siniscalchi;R. Guralnick;D. Soltis;P. Soltis;Gregory W. Stull;R. Folk;T. Yi
橡树（栎属）是北半球物种最丰富、生态优势最大的木本植物分支之一，众所周知，它们具有杂交和形成合子的倾向，等位基因很容易在密切相关的物种之间交换。虽然杂交已经在橡树系统发育的尖端得到了广泛的研究，但在橡树及其相关属（栎科）的早期辐射中，杂交的程度、时间和进化情景仍然知之甚少。利用一个庞大的核和叶绿体序列新数据集（包括多达431种），我们对栎进行了多方面的系统基因组研究，旨在表征基因树和细胞核（叶绿体-核）不一致性，并确定该群体早期进化中的古代网状结构。我们在栎科和栎科的深层节点上发现了广泛的核基因树和细胞核不一致，在叶绿体系统发育中发现栎属非单系植物。在不完全谱系分类的背景下，分析恢复了基因流动的清晰特征，基因流动在栎科和栎科的主要谱系中最普遍，可追溯到始新世早期中期。包括化石资料在内的祖先重建表明，Castanea+Castanopsis、Lithocarpus和旧世界栎枝的祖先共同出现在北美和欧亚大陆，而Chrysolepis、Notholithocarpus和新世界栎枝的祖先共同出现在北美，这为每个地区的杂交提供了充足的机会。在辐射和网状化的初始阶段，我们发现了栎科和其他栎科属的多次生态位转移，这可能有助于它们在始新世后的气候变化中向新的栖息地扩张。我们的研究表明，在橡树及其近亲的进化史上，杂交——也许是以类似于今天所看到的古老合成子的形式——是一个普遍而重要的过程。
Oaks (Quercus), one of the most species-rich and ecologically dominant woody plant clades in the Northern Hemisphere, are well known for their propensity to hybridize and form syngameons, complexes where alleles are readily exchanged among closely related species. While hybridization has been extensively studied towards the tips of the oak phylogeny, the extent, timeline, and evolutionary scenarios of hybridization during the early radiation of oaks and related genera (Quercoideae) remain poorly known. Using an expansive new dataset of nuclear and chloroplast sequences (including up to 431 spp.), we conducted a multifaceted phylogenomic investigation of Quercus aimed at characterizing gene-tree and cytonuclear (chloroplast-nuclear) discordance and identifying ancient reticulation in the early evolution of the group. We document extensive nuclear gene-tree and cytonuclear discordance at deep nodes in Quercus and Quercoideae, with Quercus recovered as non-monophyletic in the chloroplast phylogeny. Analyses recovered clear signatures of gene flow against a backdrop of incomplete lineage sorting, with gene flow most prevalent among major lineages of Quercus and Quercoideae during their initial radiation, dated to the early-middle Eocene. Ancestral reconstructions including fossil data suggest that the ancestors of Castanea+Castanopsis, Lithocarpus, and the Old World oak clade co-occurred in North America and Eurasia, while the ancestors of Chrysolepis, Notholithocarpus, and the New World oak clade co-occurred in North America, offering ample opportunity for hybridization in each region. Following this initial phase of radiation and reticulation, we detected multiple niche shifts in Quercus and other Quercoideae genera that likely facilitated their expansion into new habitats arising from post-Eocene climatic changes. Our study shows that hybridization—perhaps in the form of ancient syngameons similar to those seen today—has been a common and important process throughout the evolutionary history of oaks and their close relatives.