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Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms

Abstract

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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Fig. 1: Transcriptome species tree showing major genomic events.
Fig. 2: Gene duplications versus phenotypic innovation.
Fig. 3: Gene-tree conflict versus phenotypic rates.
Fig. 4: Climatic and diversification shifts across gymnosperms.

Data availability

The newly generated raw sequence data are available at the NCBI Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra) under BioProject PRJNA726756 (transcriptomic samples) and PRJNA726638 (genome skimming samples). The newly assembled plastid genomes are also available at NCBI (https://www.ncbi.nlm.nih.gov); see Supplementary Table 2 for sample accession numbers. Sequence alignments, phylogenies, Ks plots, phenotypic trait data and other data analysed (chromosome counts, C-values) are available on figshare (https://doi.org/10.6084/m9.figshare.14547354).

Code availability

The code used to calculate and plot rates and levels of phenotypic evolution can be found on figshare (https://figshare.com/articles/dataset/pf_stull_smith_tgz/13190816/2).

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Acknowledgements

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.

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Contributions

G.W.S., D.-Z.L., S.A.S. and T.-S.Y. conceived the study; X.-J.Q., Y.-Y.Y., T.-S.Y., Y.H., J.-B.Y., Z.-Y.Y. and H.M. collected and prepared samples for transcriptome and plastome sequencing; G.W.S. generated the trait dataset and compiled publicly available data for the supermatrix and comparative analyses; G.W.S. conducted analyses with help from C.P.-F., S.A.S. and X.-J.Q; G.W.S, C.P.-F., P.S.S., D.E.S., S.A.S. and T.-S.Y. interpreted the results; G.W.S. wrote the manuscript, with contributions from C.P.-F., P.S.S., D.E.S., S.A.S. and T.-S.Y. All authors approved the manuscript.

Corresponding authors

Correspondence to De-Zhu Li, Stephen A. Smith or Ting-Shuang Yi.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Plots of synonymous substitutions per site (Ks) for within-taxon paralog pairs (black lines) and between-taxon orthologue pairs (blue lines).

The relative positions of orthologue vs. paralog Ks spikes help clarify the phylogenetic positions of possible WGD events. The seed plant WGD event (GINK-α) is labelled. Ks peaks corresponding to an inferred WGD for gymnosperms are highlighted with an asterisk. The taxa compared capture the root nodes of (A, B) seed plants and gymnosperms, (C) the ‘ginkad’ clade, (D) conifers, (E) the cupressophyte clade, and (F) the Taxaceae-Cupressaceae clade. Orthologue and paralog Ks plots were generated using the pipelines of Walker et al.84 and Yang et al.28, respectively.

Extended Data Fig. 2 Plots of synonymous substitutions per site (Ks) for within-taxon paralog pairs of representatives of the ‘ginkad’ clade.

The seed plant WGD event (GINK-α) is labelled. Ks peaks corresponding to an inferred WGD for gymnosperms are highlighted with an asterisk.

Extended Data Fig. 3 Genome size evolution in gymnosperms.

Ancestral reconstruction of genome size (C-value) on the pruned supermatrix phylogeny, showing BAMM rate shifts (red circles) and jumps (that is, extreme differences in ancestor-descendent values; transparent circles) in genome size evolution, as well as BAMM diversification shifts (larger black circles). Supplementary Fig. 15 shows this figure with species tip labels.

Supplementary information

Supplementary Information

Supplementary Methods, Tables 1 and 3, results and discussion, and Figs. 1–35.

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Stull, G.W., Qu, XJ., Parins-Fukuchi, C. et al. Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms. Nat. Plants 7, 1015–1025 (2021). https://doi.org/10.1038/s41477-021-00964-4

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  • DOI: https://doi.org/10.1038/s41477-021-00964-4

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