J Integr Plant Biol ›› 2025, Vol. 67 ›› Issue (4): 1119-1141.DOI: 10.1111/jipb.13773  cstr: 32098.14.jipb.13773

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  • 收稿日期:2023-12-20 接受日期:2024-08-16 出版日期:2025-04-01 发布日期:2025-04-28

An integrative framework reveals widespread gene flow during the early radiation of oaks and relatives in Quercoideae (Fagaceae)

Shui-Yin Liu1,2, Ying-Ying Yang1, Qin Tian1,2, Zhi-Yun Yang1, Shu-Feng Li3, Paul J. Valdes4,5, Alex Farnsworth4,5, Heather R. Kates6, Carolina M. Siniscalchi7, Robert P. Guralnick6, Douglas E. Soltis6,8, Pamela S. Soltis6, Gregory W. Stull1,*, Ryan A. Folk9,*, Ting-Shuang Yi1,2,*   

  1. 1. Germplasm Bank of Wild Species, Yunnan Key Laboratory of Crop Wild Relatives Omics, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
    2. University of Chinese Academy of Sciences, Beijing 100049, China;
    3. Chinese Academy of Sciences Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China;
    4. School of Geographical Sciences, University of Bristol, Bristol BS8 1SS, UK;
    5. State Key Laboratory of Tibetan Plateau Earth System, Environment and Resources, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China;
    6. Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA;
    7. Mississippi State University Libraries, Mississippi State University, Mississippi State, Mississippi 39762, USA;
    8. Department of Biology, University of Florida, Gainesville, Florida 32611, USA;
    9. Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA
  • Received:2023-12-20 Accepted:2024-08-16 Online:2025-04-01 Published:2025-04-28
  • Contact: *Gregory W. Stull (gwstull@gmail.com); Ryan A. Folk (rfolk@biology.msstate.edu); Ting-Shuang Yi (tingshuangyi@mail.kib.ac.cn; Dr. Yi is fully responsible for the distribution of all the materials associated with this article)
  • Supported by:
    National Natural Science Foundation of China with a key international (regional) cooperative research project (No. 31720103903 to T.-S.Y. and D.E.S), the Strategic Priority Research Program of the Chinese Academy of Sciences (CAS) (grant No. XDB31000000 to D.-Z.L.), the Science and Technology Basic Resources Investigation Program of China (2019FY100900 to H.-L.L.), the National Natural Science Foundation of China (No. 32270247 to R.Z.), the Yunling International High-end Experts Program of Yunnan Province, China (grant No. YNQR-GDWG-2017-002 to P.S.S. and T.-S. Y. and YNQR-GDWG-2018-012 to D.E.S. and T.- S.Y.), the USA Department of Energy (grant DE-SC0018247 to P.S.S., D.E.S., R.P.G., and R.A.F.), the USA National Science Foundation (grant DEB-1916632 to R.A.F., R.P.G., D.E.S., and P.S.S.), the Natural Environment Research Council of the UK (grant No. NE/X015505/1 to A.F. and P.J.V.), and Leverhulme Research Project (grant RPG-2019-365 to A.F. and P.J.V.).

Abstract: Although the frequency of ancient hybridization across the Tree of Life is greater than previously thought, little work has been devoted to uncovering the extent, timeline, and geographic and ecological context of ancient hybridization. Using an expansive new dataset of nuclear and chloroplast DNA sequences, we conducted a multifaceted phylogenomic investigation to identify ancient reticulation in the early evolution of oaks (Quercus). We document extensive nuclear gene tree and cytonuclear discordance among major lineages of Quercus and relatives in Quercoideae. Our analyses recovered clear signatures of gene flow against a backdrop of rampant incomplete lineage sorting, with gene flow most prevalent among major lineages of Quercus and relatives in Quercoideae during their initial radiation, dated to the Early-Middle Eocene. Ancestral reconstructions including fossils suggest ancestors of Castanea + Castanopsis, Lithocarpus, and the Old World oak clade probably 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. Our study shows that hybridization—perhaps in the form of ancient syngameons like those seen today—has been a common and important process throughout the evolutionary history of oaks and their relatives. Concomitantly, this study provides a methodological framework for detecting ancient hybridization in other groups.

Key words: ancient reticulation, biogeography, cytonuclear discordance, Fagaceae, fossils, niche evolution, phylogenomics, Quercus

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