Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus

Phylogenetic relationships among 108 oak species (genus Quercus L.) were inferred using DNA sequences of six nuclear genes selected from the existing genomic resources of the genus. Previous phylogenetic reconstructions based on traditional molecular markers are inconclusive at the deeper nodes. Overall, weak phylogenetic signals were obtained for each individual gene analysis, but stronger signals were obtained when gene sequences were concatenated. Our data support the recognition of six major intrageneric groups Cyclobalanopsis, Cerris, Ilex, Quercus, Lobatae and Protobalanus. Our analyses provide resolution at deeper nodes but with moderate support and a more robust infrageneric classification within the two major clades, the ‘Old World Oaks’ (Cyclobalanopsis, Cerris, Ilex) and ‘New World Oaks’ (Quercus, Lobatae, Protobalanus). However, depending on outgroup choice, our analysis yielded two alternative placements of the Cyclobalanopsis clade within the genus Quercus. When Castanea Mill. was chosen as outgroup, our data suggested that the genus Quercus comprised two clades corresponding to two subgenera as traditionally recognized by Camus: subgenus Euquercus Hickel and Camus and subgenus Cyclobalanopsis Øersted (Schneider). However, when Notholithocarpus Manos, Cannon and S. Oh was chosen as an outgroup subgenus Cyclobalanopsis clustered with Cerris and Ilex groups to form the Old World clade. To assess the placement of the root, we complemented our dataset with published data of ITS and CRC sequences. Based on the concatenated eight gene sequences, the most likely root position is at the split between the ‘Old World Oaks’ and the ‘New World Oaks’, which is one of the alternative positions suggested by our six gene analysis. Using a dating approach, we inferred an Eocene age for the primary divergences in Quercus and a root age of about 50–55 Ma, which agrees with palaeobotanical evidence. Finally, irrespective of the outgroup choice, our data boost the topology within the New World clade, where (Protobalanus + Quercus) is a sister clade of Lobatae. Inferred divergence ages within this clade and the Cerris–Ilex clade are generally younger than could be expected from the fossil record, indicating that morphological differentiation pre-dates genetic isolation in this clade.

通过对来自该属现有基因组资源的六个核基因的DNA序列进行分析，推断出108种栎属（Quercus L.）物种的进化关系。与传统分子标记的基于以往的系统发育重建相比，在较深的节点上结果并不明确。总体而言，对单个基因的分析均获得了较弱的系统发育信号，但将基因序列拼接后，信号则更为明显。我们的数据支持将六种主要属内群组——即青冈属（Cyclobalanopsis）、刺槐属（Cerris）、冬青属（Ilex）、栎属（Quercus）、楔栎属（Lobatae）和原栎属（Protobalanus）——予以认可。我们的分析在较深的节点上提供了更高的分辨率，但支持度适中，并在两个主要类群——即‘旧世界栎树’（Cyclobalanopsis、Cerris、Ilex）和‘新世界栎树’（Quercus、Lobatae、Protobalanus）——的属内分类上表现出更强的稳健性。然而，根据外群的选择，我们的分析在栎属（Quercus）的青冈属（Cyclobalanopsis）类群中产生了两种不同的位置排列。当以Castanea Mill.作为外群时，我们的数据表明栎属（Quercus）包含两个类群，分别对应于Camus所传统认定的两个亚属：欧栎亚属（Euquercus Hickel和Camus）和青冈亚属（Cyclobalanopsis Øersted，Schneider）。然而，当选择Notholithocarpus Manos、Cannon和S. Oh作为外群亚属时，青冈亚属（Cyclobalanopsis）与刺槐属（Cerris）和冬青属（Ilex）类群聚集，形成了旧世界类群。为了评估根的位置，我们补充了已发表的ITS和CRC序列数据。基于拼接的八个基因序列，最可能的根位置位于‘旧世界栎树’和‘新世界栎树’的分歧点，这是我们六基因分析所提出的替代位置之一。通过年代学方法，我们推断栎属（Quercus）的主要分歧发生在始新世，其根的年龄约为50-55百万年，这与古植物学证据相符。最后，无论外群选择如何，我们的数据增强了新世界类群内部的拓扑结构，其中（Protobalanus + Quercus）是楔栎属（Lobatae）的姐妹类群。在此类群和刺槐属-冬青属类群中的推断分歧年龄通常比化石记录所预期的要年轻，这表明形态学分化先于该类群中的遗传隔离。