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J Integr Plant Biol.

• Research Article •    

Genome duplications, genomic conflict, and rapid phenotypic evolution characterize the Cretaceous radiation of Fagales

Ying‐Ying Yang1,2,3,4†, Gregory W. Stull5†, Xiao‐Jian Qu6, Min Deng7, Lei Zhao1, Yi Hu8, Zhi‐Heng Wang3, Hong Ma8, De‐Zhu Li1,2,9*, Stephen A. Smith10* and Ting‐Shuang Yi1,2,4*   

  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 100864, China
    3. Institute of Ecology and Key Laboratory for Earth Surface Processes of the Ministry of Education, College of Urban and Environmental Sciences, Peking University, Beijing 100871, China
    4. Key Laboratory of Plant Diversity and Specialty Crops, Chinese Academy of Sciences, Beijing 10093, China
    5. Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA
    6. Shandong Provincial Key Laboratory of Plant Stress Research, College of Life Sciences, Shandong Normal University, Jinan 250358, China
    7. School of Ecology and Environmental Sciences, Yunnan University, Kunming 650500, China
    8. Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA
    9. Center for Interdisciplinary Biodiversity Research & College of Forestry, Shandong Agricultural University, Tai'an, Shandong 271018, China
    10. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA

    †These authors contributed equally to this work.
    *Correspondences: De‐Zhu Li (DZL@mail.kib.ac.cn); Stephen A. Smith (eebsmith@umich.edu); Ting‐Shuang Yi (tingshuangyi@mail.kib.ac.cn, Dr. Yi is fully responsible for the distribution of all materials associated with this article)
  • Received:2024-12-25 Accepted:2025-07-13 Online:2025-08-13
  • Supported by:
    This work was funded by the and the Science and Technology Basic Resources Investigation Program of China (2019FY100900), the Major Program for Basic Research Project of Yunnan Province (202401BC070001), the Yunnan Revitalization Talent Support Program: Yunling Scholar Project, the National Natural Science Foundation of China [key international (regional) cooperative research project no. 31720103903]. G.W.S. acknowledges funding from the CAS President's International Fellowship Initiative (no. 2020PB0009) and the China Postdoctoral Science Foundation (CPSF) International Postdoctoral Exchange Program. S.A.S. acknowledges support from the United States National Science Foundation (DEB 1917146 and DBI 1930030).

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Abstract: While many plant lineages display remarkable diversity in morphological form, our understanding of how phenotypic diversity, or disparity, arises in relation to genomic evolution over geologic scales remains poorly understood. Here, we investigated the relationship between phenotypic and genomic evolution in the Fagales, a lineage of woody plants that has been a dominant component of temperate and subtropical forests since the Late Cretaceous. We examine newly generated transcriptomic and trait datasets representing most extant genera and a rich diversity of Cretaceous fossil representatives. Our phylogenomic analyses identify recurrent hotspots of gene duplication and genomic conflict across the order. Our phenotypic analyses showed that the morphospace occupied by Fagales was largely filled by the early Cenozoic, and rates of evolution were highest during the early radiation of the Fagales crown and its major families. These results suggest that Fagales conforms to an “early-burst” model of disparification, with morphospace being filled early in the order's diversification history, and that elevated levels of phenotypic evolution also often correspond to hotspots of gene duplication. Species diversification appears decoupled from patterns of both phenotypic and genomic evolution, highlighting the multidimensional nature of the evolution of plant diversity across geological timescales.

Key words: evolutionary rates, Fagales, phenotypic disparity, phylogenomics, transcriptome analysis, whole‐genome duplication

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