TY - JOUR
T1 - Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms
AU - Stull, Gregory W.
AU - Qu, Xiao Jian
AU - Parins-Fukuchi, Caroline
AU - Yang, Ying Ying
AU - Yang, Jun Bo
AU - Yang, Zhi Yun
AU - Hu, Yi
AU - Ma, Hong
AU - Soltis, Pamela S.
AU - Soltis, Douglas E.
AU - Li, De Zhu
AU - Smith, Stephen A.
AU - Yi, Ting Shuang
N1 - Funding Information:
We thank the Germplasm Bank of Wild Species at the Kunming Institute of Botany (KIB) for facilitating this study, and the curators and staff of the Kunming Botanical Garden of the Kunming Institute of Botany, the University of California Botanical Garden at Berkeley, the Arnold Arboretum of Harvard University, the Missouri Botanical Garden, the Royal Botanic Garden Edinburgh and the Royal Botanical Gardens Kew for providing fresh and silica-dried leaves and DNA samples. This work was funded by the Strategic Priority Research Program of the Chinese Academy of Sciences (CAS) (grant no. XDB31000000 to D.-Z.L. and T.-S.Y.), CAS’s large-scale scientific facilities (grant no. 2017-LSF-GBOWS-02 to D.-Z.L., J.-B.Y. and T.-S.Y.), the National Natural Science Foundation of China (key international (regional) cooperative research project no. 31720103903 to T.-S.Y. and D.E.S.), the Yunling International High-end Experts Program of Yunnan Province (grant nos. 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.) and the Natural Science Foundation of Shandong Province (ZR2020QC022 to X.-J.Q.). G.W.S. acknowledges support from the CAS President’s International Fellowship Initiative (no. 2020PB0009) and the China Postdoctoral Science Foundation (CPSF) International Postdoctoral Exchange Program.
Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.
PY - 2021/8
Y1 - 2021/8
N2 - Inferring the intrinsic and extrinsic drivers of species diversification and phenotypic disparity across the tree of life is a major challenge in evolutionary biology. In green plants, polyploidy (or whole-genome duplication, WGD) is known to play a major role in microevolution and speciation, but the extent to which WGD has shaped macroevolutionary patterns of diversification and phenotypic innovation across plant phylogeny remains an open question. Here, we examine the relationship of various facets of genomic evolution—including gene and genome duplication, genome size, and chromosome number—with macroevolutionary patterns of phenotypic innovation, species diversification, and climatic occupancy in gymnosperms. We show that genomic changes, such as WGD and genome-size shifts, underlie the origins of most major extant gymnosperm clades, and notably, our results support an ancestral WGD in the gymnosperm lineage. Spikes of gene duplication typically coincide with major spikes of phenotypic innovation, while increased rates of phenotypic evolution are typically found at nodes with high gene-tree conflict, representing historic population-level dynamics during speciation. Most shifts in gymnosperm diversification since the rise of angiosperms are decoupled from putative WGDs and instead are associated with increased rates of climatic occupancy evolution, particularly in cooler and/or more arid climatic conditions, suggesting that ecological opportunity, especially in the later Cenozoic, and environmental heterogeneity have driven a resurgence of gymnosperm diversification. Our study provides critical insight on the processes underlying diversification and phenotypic evolution in gymnosperms, with important broader implications for the major drivers of both micro- and macroevolution in plants.
AB - Inferring the intrinsic and extrinsic drivers of species diversification and phenotypic disparity across the tree of life is a major challenge in evolutionary biology. In green plants, polyploidy (or whole-genome duplication, WGD) is known to play a major role in microevolution and speciation, but the extent to which WGD has shaped macroevolutionary patterns of diversification and phenotypic innovation across plant phylogeny remains an open question. Here, we examine the relationship of various facets of genomic evolution—including gene and genome duplication, genome size, and chromosome number—with macroevolutionary patterns of phenotypic innovation, species diversification, and climatic occupancy in gymnosperms. We show that genomic changes, such as WGD and genome-size shifts, underlie the origins of most major extant gymnosperm clades, and notably, our results support an ancestral WGD in the gymnosperm lineage. Spikes of gene duplication typically coincide with major spikes of phenotypic innovation, while increased rates of phenotypic evolution are typically found at nodes with high gene-tree conflict, representing historic population-level dynamics during speciation. Most shifts in gymnosperm diversification since the rise of angiosperms are decoupled from putative WGDs and instead are associated with increased rates of climatic occupancy evolution, particularly in cooler and/or more arid climatic conditions, suggesting that ecological opportunity, especially in the later Cenozoic, and environmental heterogeneity have driven a resurgence of gymnosperm diversification. Our study provides critical insight on the processes underlying diversification and phenotypic evolution in gymnosperms, with important broader implications for the major drivers of both micro- and macroevolution in plants.
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U2 - 10.1038/s41477-021-00964-4
DO - 10.1038/s41477-021-00964-4
M3 - Article
C2 - 34282286
AN - SCOPUS:85110581148
VL - 7
SP - 1015
EP - 1025
JO - Nature Plants
JF - Nature Plants
SN - 2055-026X
IS - 8
ER -