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

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.

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Publication Details

Journal
Journal of Integrative Plant Biology
Published
2024-09-19
DOI
https://doi.org/10.1111/jipb.13773
Citations
18
Primary Topic
Plant Diversity and Evolution
Type
article
Field-Weighted Citation Impact
18.52

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article

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

Pamela S. Soltis, Ryan A. Folk, Robert Guralnick, Shui‐Yin Liu et al.
18 citations
Journal of Integrative Plant Biology
Plant Diversity and Evolution
18.52
article

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

Pamela S. Soltis, Ryan A. Folk, Robert Guralnick, Shui‐Yin Liu, Ting‐Shuang Yi, Heather R. Kates, Gregory W. Stull, Alex Farnsworth, Carolina M. Siniscalchi, Paul J. Valdes, Shufeng Li, Zhiyun Yang, Yingying Yang, Qin Tian, Douglas E. Soltis
article en
18 citations

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.

Journal of Integrative Plant BiologyVol. 67(4)
Florida Museum of Natural History (US), Kunming Institute of Botany (CN), Chinese Academy of Sciences (CN), Xishuangbanna Tropical Botanical Garden (CN), University of Florida (US), University of Bristol (GB), Institute of Tibetan Plateau Research (CN), University of Chinese Academy of Sciences (CN), Mississippi State University (US)
National Science Foundation, Smithsonian Institution, U.S. Department of Energy, Ohio State University, Harvard University, Leverhulme Trust, Sight Research UK, National Natural Science Foundation of China, Chinese Academy of Sciences, Natural Environment Research Council, Kunming Institute of Botany, Chinese Academy of Sciences, Institute of Botany, Chinese Academy of Sciences
Openalex Percentile: Top 1%
Plant Diversity and Evolution
18.52
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