Phylogeny and biogeography of East Asian evergreen oaks (Quercus section Cyclobalanopsis; Fagaceae): Insights into the Cenozoic history of evergreen broad-leaved forests in subtropical Asia.

The evolutionary history of Quercus section Cyclobalanopsis, a dominant lineage in East Asian evergreen broadleaved forests (EBLFs), has not been comprehensively studied using molecular tools. In this study, we reconstruct the first comprehensive phylogeny of this lineage using a genomic approach (restriction-site associated DNA sequencing, RAD-seq), sampling 35 of the ca. 90 species currently recognized, representing all main morphological groups of section Cyclobalanopsis. In addition, 10 other species of Quercus and two outgroups were also sampled. Divergence times were estimated using a relaxed clock model and two fossil calibrations. Ancestral areas and dispersal routes were inferred using statistical dispersal-vicariance analysis and the dispersal-extinction-cladogenesis (DEC) model. The phylogeny of Quercus section Cyclobalanopsis demonstrates the section to be monophyletic, comprising two main lineages and six subclades that are well supported by anatomical traits. Biogeographical reconstructions indicate that the wide northern hemisphere distribution of Quercus was disrupted in the Late Eocene, leading to the main extant groups at about 33 Ma. The earliest divergences in section Cyclobalanopsis correspond to the phased uplift of the Himalayas and lateral extrusion of Indochina at the transition of the Oligocene and Miocene, where the highest rate of diversification occurred in the late Miocene. Dispersal from Sino-Himalaya and the Palaeotropics to Sino-Japan in the Miocene was facilitated by the increased intensity of East Asian summer monsoons and by the Middle Miocene Climatic Optimum. Our results highlight the importance of climatic changes and Indo-Eurasian collision-induced tectonic activities from the Neogene onward to the spatial-temporal diversification patterns of Asian EBLF lineages.