Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus

Abstract

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.

Key words:

• Fagaceae
• gene tree
• outgroup
• phylogenetics
• Quercus
• species tree

Acknowledgements

Thomas Denk is acknowledged for insights into the fossil record of oaks and most valuable discussions. We are grateful to all the colleagues that contributed to the collections of samples throughout the worldwide distribution of oaks: Guylaine Blanc, Catherine Bodénès, Frédéric Brisson, Henri Caron, Béatrice Chassé, Bruno Fady, Silvia Fineschi, Reiner Finkeldey, Antonio Gonzalez, Riina Jalonen, Zeky Kaya, Jarkko Koskela, Thierry Lamant, Hervé Le Bouler, Richard Michalet, Huang Min-Ren, Carlos Navarro, Greuk Pakkad, Dominique Piou, Hui-MinLiu, Ken Oyama, Hui-Xin Pan, Juan Manuel Penaloza, Gabriel Schiller, Nasrin Seyedi, Jean Timbal, Jozef Turok, Susana Valencia, Yann Vitasse, Li-An Xu, Wu-Yuan Yin, Roghayed Zolfaghari and Hui-Yu Zou. We are also grateful to Pauline Garnier-Géré for providing the gene sequences, which were obtained within a resequencing project conducted within the EU-supported EVOLTREE network of excellence (FP7, project #016322).

Associate Editor: Nadia Bystriakova

Supplemental data

Supplemental data for this article can be accessed here.

Additional information

Funding

This research was supported by the ANR (Agence Nationale de la Recherche) project PHYLOSPACE (‘Integrating cophylogenies, area shifts and palaeomaps for inferring history of associations under climate change’). GWG was financed by the Swedish Research Council (VR-grant 2008–3726).