Abstract

High species diversity may result from recent rapid speciation in a ‘cradle’ and/or the gradual accumulation and preservation of species over time in a ‘museum’1,2. China harbours nearly 10% of angiosperm species worldwide and has long been considered as both a museum, owing to the presence of many species with hypothesized ancient origins3,4, and a cradle, as many lineages have originated as recent topographic changes and climatic shifts—such as the formation of the Qinghai–Tibetan Plateau and the development of the monsoon—provided new habitats that promoted remarkable radiation5. However, no detailed phylogenetic study has addressed when and how the major components of the Chinese angiosperm flora assembled to form the present-day vegetation. Here we investigate the spatio-temporal divergence patterns of the Chinese flora using a dated phylogeny of 92% of the angiosperm genera for the region, a nearly complete species-level tree comprising 26,978 species and detailed spatial distribution data. We found that 66% of the angiosperm genera in China did not originate until early in the Miocene epoch (23 million years ago (Mya)). The flora of eastern China bears a signature of older divergence (mean divergence times of 22.04–25.39 Mya), phylogenetic overdispersion (spatial co-occurrence of distant relatives) and higher phylogenetic diversity. In western China, the flora shows more recent divergence (mean divergence times of 15.29–18.86 Mya), pronounced phylogenetic clustering (co-occurrence of close relatives) and lower phylogenetic diversity. Analyses of species-level phylogenetic diversity using simulated branch lengths yielded results similar to genus-level patterns. Our analyses indicate that eastern China represents a floristic museum, and western China an evolutionary cradle, for herbaceous genera; eastern China has served as both a museum and a cradle for woody genera. These results identify areas of high species richness and phylogenetic diversity, and provide a foundation on which to build conservation efforts in China.

  • Subscribe to Nature for full access:

    $199

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    & Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proc. Natl Acad. Sci. USA 103, 10947–10951 (2006)

  2. 2.

    & Testing the museum versus cradle tropical biological diversity hypothesis: phylogeny, diversification, and ancestral biogeographic range evolution of the ants. Evolution 67, 2240–2257 (2013)

  3. 3.

    , , & in Plants of China: A Companion to the Flora of China (eds & ) 1–6 (Science Press, 2013)

  4. 4.

    , , & In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science 282, 1692–1695 (1998)

  5. 5.

    , , , & Evolutionary diversifications of plants on the Qinghai–Tibetan Plateau. Front. Genet. 5, 4 (2014)

  6. 6.

    & Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc. Natl Acad. Sci. USA 114, E3444–E3451 (2017)

  7. 7.

    , & Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427, 63–65 (2004)

  8. 8.

    et al. Phylogenetic measures of biodiversity and neo- and paleo-endemism in Australian Acacia. Nat. Commun. 5, 4473 (2014)

  9. 9.

    , , & Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293, 2242–2245 (2001)

  10. 10.

    et al. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760 (2007)

  11. 11.

    et al. Origin and diversification of the Greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? Mol. Phylogenet. Evol. 51, 44–53 (2009)

  12. 12.

    et al. Continental-scale spatial phylogenetics of Australian angiosperms provides insights into ecology, evolution and conservation. J. Biogeogr. 43, 2085–2098 (2016)

  13. 13.

    A phylogenetic perspective on the distribution of plant diversity. Proc. Natl Acad. Sci. USA 105, 11549–11555 (2008)

  14. 14.

    , , , & The influence of paleoclimate on present-day patterns in biodiversity and ecosystems. Annu. Rev. Ecol. Evol. Syst. 46, 551–572 (2015)

  15. 15.

    , & (eds) Flora of China, Vol. 1–25 (Science Press & Missouri Botanical Garden Press, 1994–2013)

  16. 16.

    & A comparison of the taxonomic richness of vascular plants in China and the United States. Am. Nat. 154, 160–181 (1999)

  17. 17.

    , , , & Centres of plant endemism in China: places for survival or for speciation? J. Biogeogr. 38, 1267–1280 (2011)

  18. 18.

    Environmental determinants of woody plant diversity at a regional scale in China. PLoS ONE 8, e75832 (2013)

  19. 19.

    , , & Patterns, determinants and models of woody plant diversity in China. Proc. R. Soc. Lond. B 278, 2122–2132 (2011)

  20. 20.

    The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1–20 (2016)

  21. 21.

    et al. Angiosperm phylogeny: 17 genes, 640 taxa. Am. J. Bot. 98, 704–730 (2011)

  22. 22.

    , , & A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207, 437–453 (2015)

  23. 23.

    et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014)

  24. 24.

    & How old is the Asian monsoon system?—Palaeobotanical records from China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 222, 181–222 (2005)

  25. 25.

    et al. The role of the uplift of the Qinghai–Tibetan Plateau for the evolution of Tibetan biotas. Biol. Rev. Camb. Philos. Soc. 90, 236–253 (2015)

  26. 26.

    , & in Floristic Characteristics and Diversity of East Asian Plants (eds & ) 43–55 (China Higher Education, 1996)

  27. 27.

    The Fossil Record 2 (Chapman & Hall, 1993)

  28. 28.

    , , , & Floristics of Seed Plants from China (Science Press, 2010)

  29. 29.

    & Life history influences rates of climatic niche evolution in flowering plants. Proc. R. Soc. Lond. B 276, 4345–4352 (2009)

  30. 30.

    , , & Distribution and conservation of threatened plants in China. Biol. Conserv. 192, 454–460 (2015)

  31. 31.

    et al. Tree of life for the genera of Chinese vascular plants. J. Syst. Evol. 54, 277–306 (2016)

  32. 32.

    & C. treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28, 2689–2690 (2012)

  33. 33.

    RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014)

  34. 34.

    ., & Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop, IEEE. (2010)

  35. 35.

    , , & Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012)

  36. 36.

    , , , & Estimating divergence times in large phylogenetic trees. Syst. Biol. 56, 741–752 (2007)

  37. 37.

    Dating Divergence Times in Phylogenies. PhD thesis, Uppsala Univ. (2007)

  38. 38.

    R Core Team. R: a language and environment for statistical computing. (2014)

  39. 39.

    , , , & Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001)

  40. 40.

    & Rates of molecular evolution are linked to life history in flowering plants. Science 322, 86–89 (2008)

  41. 41.

    & Geographic range size and determinants of avian species richness. Science 297, 1548–1551 (2002)

  42. 42.

    . et al. Predicting continental-scale patterns of bird species richness with spatially explicit models. Proc. R. Soc. Lond. B 274, 165–174 (2007)

  43. 43.

    , , & Contribution of rarity and commonness to patterns of species richness. Ecol. Lett. 7, 81–87 (2004)

  44. 44.

    & How to Detect and Handle Outliers (ASQC Quality, 1993)

  45. 45.

    & Alternatives to the median absolute deviation. J. Am. Stat. Assoc. 88, 1273–1283 (1993)

  46. 46.

    Clinical trials: robust tests are wonderful for imperfect data. Am. J. Ther. 22, e1–e5 (2015)

  47. 47.

    Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992)

  48. 48.

    , & in Phylogeny and Conservation (eds , , & ) 101–119 (Cambridge Univ. Press, 2005)

  49. 49.

    , , & Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002)

  50. 50.

    , , , & Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005)

  51. 51.

    & An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J. Plant Ecol. 9, 233–239 (2016)

  52. 52.

    , & A simple polytomy resolver for dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011)

  53. 53.

    et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012)

Download references

Acknowledgements

We thank J.-Y. Fang, D.-Z. Li, K.-P. Ma, S.-Z. Zhang, H. Sun, J.-Q. Liu, Z.-H. Wang, X.-Q. Wang and H.-Z. Kong for help initiating this study. This research was supported by the National Key Basic Research Program of China (2014CB954100), the National Natural Science Foundation of China (31590822), the Chinese Academy of Sciences International Institution Development Program (SAJC201613), the National Natural Science Foundation of China and US National Science Foundation Dimensions Collaboration Project (31461123001), the US National Science Foundation (Open Tree of Life: DEB-1207915, DEB-1208428; ABI DBI-1458466 and DBI-1458640; iDigBio: EF-1115210 and DBI-1547229; US–China Dimensions of Biodiversity: DEB-1442280) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Author notes

    • Li-Min Lu
    • , Ling-Feng Mao
    • , Tuo Yang
    • , Jian-Fei Ye
    • , Bing Liu
    • , Hong-Lei Li
    •  & Miao Sun

    These authors contributed equally to this work.

    • Pamela S. Soltis
    • , Douglas E. Soltis
    • , Jian-Hua Li
    •  & Zhi-Duan Chen

    These authors jointly supervised this work.

Affiliations

  1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

    • Li-Min Lu
    • , Tuo Yang
    • , Jian-Fei Ye
    • , Bing Liu
    • , Hai-Hua Hu
    • , Yan-Ting Niu
    • , Dan-Xiao Peng
    • , Kun-Li Xiang
    • , Chi-Toan Le
    • , Viet-Cuong Dang
    • , An-Ming Lu
    •  & Zhi-Duan Chen
  2. Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China

    • Ling-Feng Mao
  3. University of Chinese Academy of Sciences, Beijing 100049, China

    • Jian-Fei Ye
    • , Hai-Hua Hu
    • , Yan-Ting Niu
    • , Dan-Xiao Peng
    • , Kun-Li Xiang
    • , Chi-Toan Le
    •  & Viet-Cuong Dang
  4. Beijing Botanical Garden, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

    • Jian-Fei Ye
  5. Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan 430074, China

    • Bing Liu
    •  & Zhi-Duan Chen
  6. Chongqing Key Laboratory of Economic Plant Biotechnology/Institute of Special Plants, Chongqing University of Arts and Sciences, Yongchuan 402160, China

    • Hong-Lei Li
  7. Fairylake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen 518004, China

    • Hong-Lei Li
  8. Department of Biology, University of Florida, Gainesville, Florida 32611-7800, USA

    • Miao Sun
    •  & Douglas E. Soltis
  9. Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA

    • Miao Sun
    • , Pamela S. Soltis
    •  & Douglas E. Soltis
  10. CSIRO National Research Collections, Australian National Herbarium, Canberra, Australian Capital Territory 2601, Australia

    • Joseph T. Miller
    •  & Sarah Mathews
  11. Office of International Science and Engineering, National Science Foundation, Alexandria, Virginia 22314, USA

    • Joseph T. Miller
  12. Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China

    • You-Hua Chen
  13. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Stephen A. Smith
  14. Institute of Botany, Jiangsu Province & Chinese Academy of Sciences, Nanjing 210014, China

    • Min Chen
  15. Biology Department, Hope College, Holland, Michigan 49423, USA

    • Jian-Hua Li

Authors

  1. Search for Li-Min Lu in:

  2. Search for Ling-Feng Mao in:

  3. Search for Tuo Yang in:

  4. Search for Jian-Fei Ye in:

  5. Search for Bing Liu in:

  6. Search for Hong-Lei Li in:

  7. Search for Miao Sun in:

  8. Search for Joseph T. Miller in:

  9. Search for Sarah Mathews in:

  10. Search for Hai-Hua Hu in:

  11. Search for Yan-Ting Niu in:

  12. Search for Dan-Xiao Peng in:

  13. Search for You-Hua Chen in:

  14. Search for Stephen A. Smith in:

  15. Search for Min Chen in:

  16. Search for Kun-Li Xiang in:

  17. Search for Chi-Toan Le in:

  18. Search for Viet-Cuong Dang in:

  19. Search for An-Ming Lu in:

  20. Search for Pamela S. Soltis in:

  21. Search for Douglas E. Soltis in:

  22. Search for Jian-Hua Li in:

  23. Search for Zhi-Duan Chen in:

Contributions

Z.-D.C., P.S.S., D.E.S and J.-H.L. conceived the paper. L.-M.L., L.-F.M., T.Y., J.-F.Y., B.L., H.-L.L. and M.S. analysed the data. L.-M.L., L.-F.M., T.Y., J.-F.Y., B.L., J.T.M., S.M., P.S.S., D.E.S., J.-H.L. and Z.-D.C. wrote the first draft and finalized the manuscript. H.-H.H., Y.-T.N., D.-X.P., M.C., K.-L.X., C.-T.L. and V.-C.D. contributed data. J.T.M., A.-M.L., Y.-H.C., S.A.S., P.S.S., D.E.S., J.-H.L. and Z.-D.C. contributed substantially to revisions. All authors commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Zhi-Duan Chen.

Reviewer Information Nature thanks R. Colwell, V. Savolainen and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Table 1, Supplementary Text and Supplementary References.

  2. 2.

    Life Sciences Reporting Summary

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature25485

Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.