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Transition of survival strategies under global climate shifts in the grape family

Nature Plants volume 10, pages 1100–1111 (2024)Cite this article

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Abstract

Faced with environmental changes, plants may either move to track their ancestral niches or evolve to adapt to new niches. Vitaceae, the grape family, has evolved diverse adaptive traits facilitating a global expansion in wide-ranging habitats, making it ideal for investigating transition between move and evolve strategies and exploring the underlying mechanisms. Here we inferred the patterns of biogeographic diversification and trait evolution in Vitaceae based on a robust phylogeny with dense sampling including 495 species (~52% of Vitaceae species). Vitaceae probably originated from Asia—the diversity centre of extant genera and the major source of dispersals. Boundaries of the Eocene, Oligocene and Miocene were identified as turning points in shifting strategies. A significant decrease in move strategy was identified during the Oligocene, followed by increases in move and evolve. After the Miocene, evolve began to dominate, during which increased niche opportunities and key trait innovations played important roles.

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Fig. 1: Major habitats and global distributions of the grape family.
Fig. 2: Biogeographic history reconstruction of the grape family.
Fig. 3: Biogeographic diversification patterns of the grape family.
Fig. 4: Niche shifts and dispersal events in the grape family.

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Data availability

The newly generated short reads for phylogeny reconstruction have been deposited in NCBI BioProject PRJNA1051838. Voucher information and accession numbers for all of the sampled species are provided in Supplementary Table 1. The phylogenetic tree and time tree are available via GitHub at https://github.com/logysnail/Vitaceae-global-diversification. The assembled fossil records are available in Supplementary Table 2 and information on biogeographic regions, niches and traits for all of the sampled species is provided in Supplementary Table 5.

Code availability

All of the codes and scripts used in the analyses are available via GitHub at https://github.com/logysnail/Vitaceae-global-diversification.

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Acknowledgements

We thank B. Liu, J. Ye, Z. Shan, C. Fu, P. Li, X. Zhou, L. Yuan, X. Zhu, M. Huang, C. Huang, Y. Liang, B. Jackes, D. Crayn, A. Trias-Blasi, V. H. Dang, V. D. Nguyen, J. Gerrath, Q. Luke, X. Ma, Y. Meng, T. Yang, M. Sun, B. Dao, F. Li, J. Guo, W. Xu and C. Zhao for field assistance and/or sample collection, G. Parmar for collecting morphological traits of the genus Causonis, J. Li and S. Manchester for helpful comments on an earlier version of the manuscript and the staff at the herbaria of A, BM, CAL, CANB, CNS, E, EA, G, HN, IBSC, K, KUN, L, LE, LISU, MEL, MO, NGB, NY, P, PE, PH, PRE, TAN, U and US for help and for the loan of or access to specimens. This work was supported by the National Natural Science Foundation of China (31870197, 32270230 and 32122009 to L.L. and 32060055 to Z.N.), National Key Research Development Program of China (2022YFC2601200 to L.L. and 2023YFF0805800 to Z.C.), International Partnership Program of the Chinese Academy of Sciences (CAS) (151853KYSB20190027 to Z.C.), Youth Innovation Promotion Association of CAS (2020080 to L.L.), Sino-Africa Joint Research Center and CAS International Research and Education Development Program (SAJC202101 to Z.C.). R.N.R was supported by the CAS-TWAS President’s Fellowship for International PhD Students. R.L.B. acknowledges support from the CAS President’s International Fellowship Initiative.

Author information

Author notes

  1. These authors contributed equally: Yichen You, Jinren Yu, Zelong Nie.

Authors and Affiliations

  1. State Key Laboratory of Plant Diversity and Specialty Crops and Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Yichen You, Jinren Yu, Danxiao Peng, Romer Narindra Rabarijaona, Yangjun Lai, Yujie Zhao, Zhiduan Chen & Limin Lu

  2. China National Botanical Garden, Beijing, China

    Yichen You, Jinren Yu, Danxiao Peng, Romer Narindra Rabarijaona, Yangjun Lai, Yujie Zhao, Zhiduan Chen & Limin Lu

  3. University of Chinese Academy of Sciences, Beijing, China

    Yichen You, Jinren Yu & Yujie Zhao

  4. Hunan Provincial Key Laboratory of Ecological Conservation and Sustainable Utilization of Wulingshan Resources and Key Laboratory of Plant Resources Conservation and Utilization, College of Biology and Environmental Sciences, Jishou University, Jishou, China

    Zelong Nie

  5. Botanic Gardens of Sydney, National Herbarium of New South Wales, Australian Botanic Garden, Sydney, New South Wales, Australia

    Russell L. Barrett

  6. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia

    Russell L. Barrett

  7. University of Medicine and Pharmacy, Vietnam National University, Hanoi, Vietnam

    Viet-Cuong Dang

  8. Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China

    Youhua Chen

  9. Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, China

    Zhiduan Chen

  10. Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

    Jun Wen

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  1. Yichen You
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  11. Zhiduan Chen
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  12. Jun Wen
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Contributions

L.L., J.W. and Z.C. conceived of the project and designed the research. Z.C., J.W., L.L., R.N.R., Y.L., R.L.B. and V.-C.D. conducted field collection. J.Y., Y.Y. and V.-C.D. performed DNA laboratory work and phylogenetic reconstruction. Y.Y., D.P., J.Y., Y.C and Z.N. conducted the biogeographic and diversification-related analyses. L.L., Y.Y. and R.N.R. collected trait data. Y.L. and Y.Z. assembled and cleaned the fossil data. J.Y., Y.Y. and L.L. drafted the paper. All authors revised and approved the paper.

Corresponding authors

Correspondence to Zhiduan Chen, Jun Wen or Limin Lu.

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The authors declare no competing interests.

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Nature Plants thanks Ryan Folk and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Illustrations showing biogeographic events and survival strategies involved in this study.

a, A shift event characterized by the change of node states. b, Biogeographic events involved in this study, including dispersal, extinction, and in-situ diversification. Green blocks represent the distribution regions at a node. Multiple biogeographic events can occur in the same lineage. c, The ‘move’ and ‘evolve’ strategies characterized by niche shifts and biogeographic events.

Extended Data Fig. 2 Spatial and temporal distribution of Vitaceae fossils.

a, The global distribution of all types of fossils. Different symbols represent fossils from different geological periods. The border between North America and South America and that between Asia and Australasia are indicated by dashed lines. b, Number of all types of fossils through geological time. c, Number of pollen/seed/fruit fossils through geological time. Map in a was created with cartopy version 0.20.2 (https://scitools.org.uk/cartopy).

Extended Data Fig. 3 Phylogeny of Vitaceae based on plastid and nuclear datasets.

a, Phylogram of Vitaceae based on the 505-taxa plastid dataset, using the maximum likelihood method. Internal branches with higher bootstrap support values were colored with brighter red, and those with support values below 80% were colored with grey. Tip branches are colored with grey. Vertical bars on the right of different colors indicate 16 genera of Vitaceae (Species of Pterisanthes were included in Ampelocissus, which deserve further taxonomic treatment), with the number of species in each genus denoted. b, Conflicts of intergeneric relationships in Vitaceae based on plastid and nuclear phylogenies, highlighted by blue boxes. The plastid phylogeny was constructed in this study and the nuclear topology was adapted from the tree of 346 nuclear sequences in Ma et al.25.

Extended Data Fig. 4 Plots of lineages with dispersal and in-situ diversification events through geological time.

a, Number of lineages with dispersal events through geological time, with different colors representing different dispersal sinks. b, Number of lineages with in-situ diversification events in each biogeographic region through time.

Extended Data Fig. 5 Accumulation of dispersal events to Australasia or Indian subcontinent through geological time.

a, Dispersals to Australasia. b, Dispersals to Indian subcontinent. Dots indicate the median heights of the ancestral nodes of lineages where dispersal events happened. Different colors show different dispersal source areas. Blue bars represent the 95% highest posterior density of node heights (tree replications: n = 1,000) in the treePL maximum clade credibility tree. Maps in a and b were created by the ODSN Plate Tectonic Reconstruction Service (http://www.odsn.de/odsn/services/paleomap/paleomap.html).

Extended Data Fig. 6 Emergence of different types of trait-state shifts through geological time.

The lines mark the number of lineages shifting to specific trait states.

Extended Data Fig. 7 Heatmap showing correlation among traits supported by Bayesian factor (BF).

Red boxes represent that the correlation between the trait-state transition and the state of other trait is substantially supported (log10(BF) > 0.5, marked by red dotted line above). Blue boxes represent that the independence between the trait-state transition and the state of other trait is substantially supported (log10(BF) < –0.5, marked by red dotted line below).

Extended Data Fig. 8 Niche states and niche shifts in each biogeographic region through geological time.

The lines indicate the proportions of lineages shifting to a specific niche (to forest, to savanna, or to desert or rocky area). The background colors show the proportions of lineages in different niche types (forest, savanna, and desert or rocky area) through geological time. Grey bars represent the time period of major climatic or geological events for each region (see Supplementary Table 9 for references). Europe-central Asia and Indian subcontinent were not shown as no niche shift has been detected for the two regions. Maps were created with cartopy version 0.20.2 (https://scitools.org.uk/cartopy).

Extended Data Fig. 9 Null model test for ‘move’ and ‘evolve’ patterns in Vitaceae.

a–b, The proportion of lineages with ‘move’ (dispersal, a) or ‘evolve’ (niche shift, b) events to the total lineages through geological time. The red line represents the observed pattern based on the median node heights of the treePL time tree, the yellow lines represent observed patterns from 100 empirical dated bootstrap trees, and the blue lines represent simulated patterns from random simulated data. c–d, The distributions of Pearson correlation coefficient for observed and simulated patterns of ‘move’ (c) and ‘evolve’ (d) events. The yellow bars represent the distributions of Pearson correlation coefficient between each pair of observed patterns, while green bars represent those between the observed and simulated patterns.

Extended Data Fig. 10 The seed/fruit fossil records of five Vitaceae tribes through geological time.

The bars represent the number of fossils within every two million years.

Supplementary information

Supplementary Information

Supplementary Sections 1–5 and Figs. 1–15.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–11.

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You, Y., Yu, J., Nie, Z. et al. Transition of survival strategies under global climate shifts in the grape family. Nat. Plants 10, 1100–1111 (2024). https://doi.org/10.1038/s41477-024-01726-8

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