Evolutionary history of the angiosperm flora of China

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Patterns of the MDTs for Chinese angiosperm genera.
Figure 2: Spatio-temporal divergence patterns of the Chinese angiosperm flora.
Figure 3: Angiosperm divergence pattern and conservation priorities in western and eastern China.
Figure 4: Regression analyses between MDT and two environmental variables for the Chinese angiosperm genera.

References

  1. 1

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

    Article  ADS  CAS  PubMed  Google Scholar 

  2. 2

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

    Article  PubMed  Google Scholar 

  3. 3

    Blackmore, S., Hong, D.-Y., Raven, P. H. & Wortley, A. H. in Plants of China: A Companion to the Flora of China (eds Hong, D.-Y. & Blackmore, S. ) 1–6 (Science Press, 2013)

    Google Scholar 

  4. 4

    Sun, G., Dilcher, D. L., Zheng, S.-L. & Zhou, Z.-K. In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science 282, 1692–1695 (1998)

    Article  ADS  CAS  PubMed  Google Scholar 

  5. 5

    Wen, J., Zhang, J.-Q., Nie, Z.-L., Zhong, Y. & Sun, H. Evolutionary diversifications of plants on the Qinghai–Tibetan Plateau. Front. Genet. 5, 4 (2014)

    PubMed  PubMed Central  Google Scholar 

  6. 6

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

    Article  CAS  PubMed  Google Scholar 

  7. 7

    Klak, C., Reeves, G. & Hedderson, T. Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427, 63–65 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  8. 8

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

    Article  ADS  CAS  PubMed  Google Scholar 

  9. 9

    Richardson, J. E., Pennington, R. T., Pennington, T. D. & Hollingsworth, P. M. Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293, 2242–2245 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  10. 10

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

    Article  ADS  CAS  PubMed  Google Scholar 

  11. 11

    Verboom, G. A. 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)

    Article  PubMed  Google Scholar 

  12. 12

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

    Article  Google Scholar 

  13. 13

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

    Article  ADS  PubMed  Google Scholar 

  14. 14

    Svenning, J.-C., Eiserhardt, W. L., Normand, S., Ordonez, A. & Sandel, B. The influence of paleoclimate on present-day patterns in biodiversity and ecosystems. Annu. Rev. Ecol. Evol. Syst. 46, 551–572 (2015)

    Article  Google Scholar 

  15. 15

    Wu, Z.-Y., Raven, P. H. & Hong, D.-Y. (eds) Flora of China, Vol. 1–25 (Science Press & Missouri Botanical Garden Press, 1994–2013)

  16. 16

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

    Article  PubMed  Google Scholar 

  17. 17

    López-Pujol, J., Zhang, F.-M., Sun, H.-Q., Ying, T.-S. & Ge, S. Centres of plant endemism in China: places for survival or for speciation? J. Biogeogr. 38, 1267–1280 (2011)

    Article  Google Scholar 

  18. 18

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

    Wang, Z.-H., Fang, J.-Y., Tang, Z.-Y. & Lin, X. Patterns, determinants and models of woody plant diversity in China. Proc. R. Soc. Lond. B 278, 2122–2132 (2011)

    Article  Google Scholar 

  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

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

    Article  PubMed  Google Scholar 

  22. 22

    Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L. L. & Hernández-Hernández, T. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207, 437–453 (2015)

    Article  PubMed  Google Scholar 

  23. 23

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

    Article  ADS  CAS  PubMed  Google Scholar 

  24. 24

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

    Article  Google Scholar 

  25. 25

    Favre, A. 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)

    Article  PubMed  Google Scholar 

  26. 26

    Axelrod, D. I., Al-Shehbaz, I. A. & Raven, P. H. in Floristic Characteristics and Diversity of East Asian Plants (eds Zhang, A.-L. & Wu, S.-G. ) 43–55 (China Higher Education, 1996)

    Google Scholar 

  27. 27

    Benton, M. J. The Fossil Record 2 (Chapman & Hall, 1993)

  28. 28

    Wu, Z.-Y., Sun, H., Zhou, Z.-K., Li, D.-Z. & Peng, H. Floristics of Seed Plants from China (Science Press, 2010)

  29. 29

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

    Article  Google Scholar 

  30. 30

    Zhang, Z.-J., He, J.-S., Li, J.-S. & Tang, Z.-Y. Distribution and conservation of threatened plants in China. Biol. Conserv. 192, 454–460 (2015)

    Article  Google Scholar 

  31. 31

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

    Article  Google Scholar 

  32. 32

    Smith, S. A. & O’Meara, B. C. treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28, 2689–2690 (2012)

    Article  CAS  PubMed  Google Scholar 

  33. 33

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Miller, M. A ., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop, IEEE. http://ieeexplore.ieee.org/document/5676129/ (2010)

  35. 35

    Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    Britton, T., Anderson, C. L., Jacquet, D., Lundqvist, S. & Bremer, K. Estimating divergence times in large phylogenetic trees. Syst. Biol. 56, 741–752 (2007)

    Article  PubMed  Google Scholar 

  37. 37

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

  38. 38

    R Core Team. R: a language and environment for statistical computing. http://R-project.org/ (2014)

  39. 39

    Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001)

    Article  ADS  CAS  Google Scholar 

  40. 40

    Smith, S. A. & Donoghue, M. J. Rates of molecular evolution are linked to life history in flowering plants. Science 322, 86–89 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  41. 41

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

    Article  ADS  CAS  PubMed  Google Scholar 

  42. 42

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

    Article  Google Scholar 

  43. 43

    Lennon, J. J., Koleff, P., Greenwood, J. J. D. & Gaston, K. J. Contribution of rarity and commonness to patterns of species richness. Ecol. Lett. 7, 81–87 (2004)

    Article  Google Scholar 

  44. 44

    Iglewicz, B. & Hoaglin, D. How to Detect and Handle Outliers (ASQC Quality, 1993)

  45. 45

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

    Article  MathSciNet  MATH  Google Scholar 

  46. 46

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

    Article  PubMed  Google Scholar 

  47. 47

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

    Article  Google Scholar 

  48. 48

    Rodrigues, A. S. L., Brooks, T. M. & Gaston, K. J. in Phylogeny and Conservation (eds Purvis, A., Gittleman, J. L., & Brooks, T. ) 101–119 (Cambridge Univ. Press, 2005)

    Google Scholar 

  49. 49

    Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002)

    Article  Google Scholar 

  50. 50

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005)

    Article  Google Scholar 

  51. 51

    Qian, H. & Jin, Y. 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)

    Article  Google Scholar 

  52. 52

    Kuhn, T. S., Mooers, A. Ø. & Thomas, G. H. A simple polytomy resolver for dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011)

    Article  Google Scholar 

  53. 53

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

    Article  PubMed  PubMed Central  Google Scholar 

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

Affiliations

Authors

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.

Corresponding author

Correspondence to Zhi-Duan Chen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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 figures and tables

Extended Data Figure 1 Dated megaphylogeny of the Chinese angiosperms.

Major clades, including magnoliids, monocots, superrosids and superasterids, as well as the basal eudicot grade, are indicated with different colours. Divergence times were estimated using treePL.

Extended Data Figure 2 The 95% confidence intervals of divergence times and the Spearman’s rank correlation between our dating and those of recent publications.

a, b, Plots of divergence times and 95% confidence intervals (grey bars) for each family (a, n = 273) and genus (b, n = 2,909). The centre values are ages calculated based on the optimal maximum likelihood tree. c, Correlation of nodal ages between treePL and PATHd8 in this study (n = 5,863; r = 0.94, P = 0). d, Correlation of family ages between treePL and ref. 22 (n = 236, r = 0.68, P = 1.17 × 10−33). e, Correlation of family ages between treePL and ref. 23 (n = 257; r = 0.55, P = 4.54 × 10−22). f, Correlation of family ages between ref. 22 and ref. 23 (n = 235; r = 0.75, P = 2.11 × 10−43). The solid line is y = x.

Extended Data Figure 3 Number of angiosperm genera that originated during specified geological timespans.

Column with three colours shows the number of woody (grey), herbaceous (yellow) and mixed genera (light blue) that originated within a specific geological timespan. Number of woody genera, n = 995; number of herbaceous genera, n = 1,569; mixed genera (genera with both woody and herbaceous species), n = 101. The dashed line indicates the accumulated percentage of genera that have originated since the Early Cretaceous. Global temperature changes that have occurred since the Palaeogene are shown by the red curve (from ref. 39; reprinted with permission from AAAS). The x axis indicates the geological period and time in millions of years. The left y axis shows the total number of genera that have originated by any given time period; the right y-axis represents the accumulated percentage of genera that originated within a geological time period.

Extended Data Figure 4 Plot of divergence times of the Chinese angiosperm genera in each grid cell.

Mean and median values of the divergence times are indicated.

Extended Data Figure 5 Histograms and distribution of skewness and kurtosis for divergence times in each grid cell.

ac, Range of skewness for all genera (a), woody genera (b) and herbaceous genera (c). df, Range of kurtosis (computed as the fourth standardized moment) for all genera (d), woody genera (e) and herbaceous genera (f). gi, Spatial distribution of skewness for all genera (g), woody genera (h) and herbaceous genera (i). jl, Spatial distribution of kurtosis for all genera (j), woody genera (k) and herbaceous genera (l). Skewness values in most grid cells are positive and around 1–2, which implies that divergence times of genera are slightly right-skewed (there are more young ages in each grid cell). Kurtosis values in most grid cells are within a range of 4–8, larger than the value (3) for a normal distribution, which implies that the distribution of divergence times has more extreme outliers than the normal distribution. For eastern China, kurtosis values of approximately 4 for all genera are consistent with grid cells having a range of divergence times—including very young and very old ages—as expected for an area that is both a cradle and a museum.

Extended Data Figure 6 Geographic patterns of median ages for the Chinese angiosperm genera.

ai, Median ages for all genera, woody genera and herbaceous genera (from left to right), based on all sampled genera (ac), the youngest 25% of genera (df), and the oldest 25% of genera (gi) in each grid cell. jl, Null-model test to identify recent (blue grid cells) and ancient (red grid cells) divergence centres for all genera (j), woody genera (k) and herbaceous genera (l). The analyses include 2,592 angiosperm genera (woody genera, n = 925; herbaceous genera, n = 1,501; genera with both woody and herbaceous species, n = 166). Maps adapted from National Administration of Surveying, Mapping and Geoinformation of China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).

Extended Data Figure 7 Spatial distribution of MDTs based on geographic range-size quartiles and the youngest 25% and oldest 25% of genera in China.

ad, MDT patterns of the first (a), second (b), third (c) and fourth quartiles (d) of the sampled Chinese angiosperm genera. The first, second, third and fourth quartiles range from the narrowest to the widest geographic distribution, and represent 0.6%, 3.5%, 13.7% and 82.1% of 1,409,239 records, respectively. The Spearman’s rank correlation coefficients between the overall MDT (including all genera) and MDT of the first, second, third and fourth geographic quartile are 0.12 (P = 1.46 × 10−3), 0.59 (P = 1.21 × 10−87), 0.43 (P = 2.51 × 10−43) and 0.99 (P = 0), respectively. e, MDT pattern of the youngest 25% of genera in China, showing that there are young genera in both western and eastern China. f, MDT pattern of the oldest 25% of genera in China, confirming that older genera mainly occur in eastern China. Maps adapted from National Administration of Surveying, Mapping and Geoinformation of China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).

Extended Data Figure 8 Patterns of generic richness, phylogenetic diversity and phylogenetic structure for the Chinese angiosperm genera.

ac, Richness for all genera (a), woody genera (b) and herbaceous genera (c). df, Phylogenetic diversity for all genera (d), woody genera (e) and herbaceous genera (f). gi, SES-PD for all genera (g), woody genera (h) and herbaceous genera (i). jl, NRI for all genera (j), woody genera (k) and herbaceous genera (l). mo, NTI for all genera (m), woody genera (n) and herbaceous genera (o). The analyses include 2,592 angiosperm genera (woody genera, n = 925; herbaceous genera, n = 1,501; genera with both woody and herbaceous species, n = 166). Maps adapted from National Administration of Surveying, Mapping and Geoinformation of China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).

Extended Data Figure 9 Patterns of species-level phylogenetic diversity for all Chinese angiosperms.

al, Observed phylogenetic diversity for all species (a, d, g, j), woody species (b, e, h, k) and herbaceous species (c, f, i, l) based on species trees 210, 30, 174 and 461 (species trees were randomly selected from 1,000 post-burn-in trees). mo, SES-PD for all species (m), woody species (n) and herbaceous species (o) based on species tree 461. The analyses include 26,978 angiosperm species (woody, n = 10,169; herbaceous, n = 16,809). Phylogenetic diversity and SES-PD based on 10 species trees produce similar patterns; Spearman’s rank correlation coefficients, r > 0.99, P < 2.20 × 10−16. Maps adapted from National Administration of Surveying, Mapping and Geoinformation of China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).

Extended Data Table 1 Number of genera that occur only in western or eastern China, with the number of woody, herbaceous and mixed genera in each order indicated

Supplementary information

Supplementary Information

This file contains Supplementary Table 1, Supplementary Text and Supplementary References. (PDF 606 kb)

Life Sciences Reporting Summary (PDF 76 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lu, L., Mao, L., Yang, T. et al. Evolutionary history of the angiosperm flora of China. Nature 554, 234–238 (2018). https://doi.org/10.1038/nature25485

Download citation

Further reading

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.

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing