Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

The delayed and geographically heterogeneous diversification of flowering plant families

This article has been updated


The Early Cretaceous (145–100 million years ago (Ma)) witnessed the rise of flowering plants (angiosperms), which ultimately lead to profound changes in terrestrial plant communities. However, palaeobotanical evidence shows that the transition to widespread angiosperm-dominated biomes was delayed until the Palaeocene (66–56 Ma). Important aspects of the timing and geographical setting of angiosperm diversification during this period, and the groups involved, remain uncertain. Here we address these aspects by constructing and dating a new and complete family-level phylogeny, which we integrate with 16 million geographic occurrence records for angiosperms on a global scale. We show substantial time lags (mean, 37–56 Myr) between the origin of families (stem age) and the diversification leading to extant species (crown ages) across the entire angiosperm tree of life. In turn, our results show that families with the shortest lags are overrepresented in temperate and arid biomes compared with tropical biomes. Our results imply that the diversification and ecological expansion of extant angiosperms was geographically heterogeneous and occurred long after most of their phylogenetic diversity originated during the Cretaceous Terrestrial Revolution.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Flowering plant dated phylogeny encompassing all currently recognized families.
Fig. 2: Flowering plant family ages through time and across space.

Similar content being viewed by others

Data availability

GenBank accession numbers for sequence data, sequence alignments, phylogenetic trees and fossil information that support the findings of this study are available within the supplementary information files of the paper and at Zenodo with the identifier The fossil calibration list is available at Zenodo with the identifier The geographic data are available from the Global Biodiversity Information Facility with the identifier

Code availability

The code used to process data and perform the analyses is available at Zenodo with the identifier

Change history

  • 09 July 2020

    In the PDF version of the Article, Fig. 2 was incorrectly displayed before Fig. 1. The HTML version was unaffected. The figures are now displayed in the correct order in all versions of the Article.


  1. Magallón, S., Gómez-Acevedo, S., Sanchéz-Reyes, 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 

  2. Barba-Montoya, J., dos Reis, M., Schneider, H., Donoghue, P. C. J. & Yang, Z. Constraining uncertainty in the timescale of angiosperm evolution and the veracity of a Cretaceous Terrestrial Revolution. New Phytol. 218, 819–834 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Coiro, M., Doyle, J. A. & Hilton, J. How deep is the conflict between molecular and fossil evidence on the age of angiosperms? New Phytol. 223, 83–99 (2019).

    Article  PubMed  Google Scholar 

  4. Li, H.-T. et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat. Plants 5, 461–470 (2019).

    Article  PubMed  Google Scholar 

  5. Foster, C. S. P. et al. Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Syst. Biol. 66, 338–351 (2017).

    PubMed  Google Scholar 

  6. Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011).

  7. Herendeen, P. S., Friis, E. M., Pedersen, K. R. & Crane, P. R. Palaeobotanical redux: revisiting the age of the angiosperms. Nat. Plants 3, 17015 (2017).

    Article  PubMed  Google Scholar 

  8. Hughes, N. F. & McDougall, A. B. Records of angiospermid pollen entry into the English Early Cretaceous succession. Rev. Palaeobot. Palynol. 50, 255–272 (1987).

    Article  Google Scholar 

  9. Brenner, G. J. in Flowering Plant Origin, Evolution & Phylogeny (eds Taylor, D. W. & Hickey, L. J.) 91–115 (Springer, 1996).

  10. Magallón, S., Sánchez-Reyes, L. L. & Gómez-Acevedo, S. L. Thirty clues to the exceptional diversification of flowering plants. Ann. Bot. 123, 491–503 (2018).

    Article  PubMed Central  Google Scholar 

  11. Tank, D. C. et al. Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol. 207, 454–467 (2015).

    Article  PubMed  Google Scholar 

  12. Silvestro, D., Cascales-Miñana, B., Bacon, C. D. & Antonelli, A. Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytol. 207, 425–436 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wing, S. L., Hickey, L. J. & Swisher, C. C. Implications of an exceptional fossil flora for Late Cretaceous vegetation. Nature 363, 342–344 (1993).

    Article  Google Scholar 

  14. Wing, S. L. et al. Late Paleocene fossils from the Cerrejón Formation, Colombia, are the earliest record of neotropical rainforest. Proc. Natl Acad. Sci. USA 106, 18627–18632 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wing, S. L. et al. Floral and environmental gradients on a Late Cretaceous landscape. Ecol. Monogr. 82, 23–47 (2011).

    Article  Google Scholar 

  16. Lupia, R., Lidgard, S. & Crane, P. R. Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25, 305–340 (1999).

    Article  Google Scholar 

  17. Eriksson, O., Friis, E. M. & Löfgren, P. Seed size, fruit size, and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. Am. Nat. 156, 47–58 (2000).

    Article  PubMed  Google Scholar 

  18. Manchester, S. R., Grímsson, F. & Zetter, R. Assessing the fossil record of asterids in the context of our current phylogenetic framework. Ann. Mo. Bot. Gard. 100, 329–363 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Collinson, M. E. in Biotic Responses to Global Change: The Last 145 Million Years (eds Culver, S. J. & Rawson, P. F.) 223–243 (Cambridge Univ. Press, 2000).

  20. Lupia, R., Crane, P. R. & Lidgard, S. in Biotic Responses to Global Change: The Last 145 Million Years (eds Culver, S. J. & Rawson, P. F.) 207–222 (Cambridge Univ. Press, 2000).

  21. Sauquet, H. & Magallón, S. Key questions and challenges in angiosperm macroevolution. New Phytol. 219, 1170–1187 (2018).

    Article  PubMed  Google Scholar 

  22. Wiens, J. J. & Donoghue, M. J. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 19, 639–644 (2004).

    Article  PubMed  Google Scholar 

  23. Crepet, W. L. & Niklas, K. J. Darwin’s second ‘abominable mystery’: why are there so many angiosperm species? Am. J. Bot. 96, 366–381 (2009).

    Article  PubMed  Google Scholar 

  24. Vamosi, J. C., Magallón, S., Mayrose, I., Otto, S. P. & Sauquet, H. Macroevolutionary patterns of flowering plant speciation and extinction. Annu. Rev. Plant Biol. 69, 685–706 (2018).

    Article  CAS  PubMed  Google Scholar 

  25. Stevens, P. F. Angiosperm Phylogeny Website Version 14 (MOBOT, accessed February 2018);

  26. APG 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).

    Article  Google Scholar 

  27. Parham, J. F. et al. Best practices for justifying fossil calibrations. Syst. Biol. 61, 346–359 (2012).

    Article  PubMed  Google Scholar 

  28. Sauquet, H. et al. Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Syst. Biol. 61, 289–313 (2012).

    Article  PubMed  Google Scholar 

  29. Doyle, J. A. Molecular and fossil evidence on the origin of angiosperms. Annu. Rev. Earth Planet. Sci. 40, 301–326 (2012).

    Article  CAS  Google Scholar 

  30. Friis, E. M., Pedersen, K. R. & Crane, P. R. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 251–293 (2006).

    Article  Google Scholar 

  31. Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379–421 (1998).

    Article  CAS  Google Scholar 

  32. Boucot, A. J., Xu, C., Scotese, C. R. & Morley, R. J. Phanerozoic Paleoclimate: An Atlas of Lithologic Indicators of Climate (SEPM Concepts in Sedimentology and Paleontology No. 11: Map Folio, SEPM Society for Sedimentary Geology, 2013).

  33. Heimhofer, U., Hochuli, P. A., Burla, S., Dinis, J. M. L. & Weissert, H. Timing of Early Cretaceous angiosperm diversification and possible links to major paleoenvironmental change. Geology 33, 141–144 (2005).

    Article  Google Scholar 

  34. Zachos, J. C., Dickens, G. R. & Zeebe, R. E. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451, 279–283 (2008).

    Article  CAS  PubMed  Google Scholar 

  35. Cooper, A. & Fortey, R. Evolutionary explosions and the phylogenetic fuse. Trends Ecol. Evol. 13, 151–156 (1998).

    Article  CAS  PubMed  Google Scholar 

  36. Crepet, W. L. The fossil record of angiosperms: requiem or renaissance? Ann. Mo. Bot. Gard. 95, 3–33 (2008).

    Article  Google Scholar 

  37. Feild, T. S., Chatelet, D. S. & Brodribb, T. J. Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7, 237–264 (2009).

    Article  CAS  PubMed  Google Scholar 

  38. Budd, G. E. & Mann, R. P. The dynamics of stem and crown groups. Sci. Adv. 6, eaaz1626 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Igea, J. & Tanentzap, A. J. Angiosperm speciation speeds up near the poles. Ecol. Lett. 23, 692–700 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Donoghue, M. J. & Sanderson, M. J. Confluence, synnovation, and depauperons in plant diversification. New Phytol. 207, 260–274 (2015).

    Article  PubMed  Google Scholar 

  41. Hawkins, B. A., Rodríguez, M. Á. & Weller, S. G. Global angiosperm family richness revisited: linking ecology and evolution to climate. J. Biogeogr. 38, 1253–1266 (2011).

    Article  Google Scholar 

  42. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. 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 

  44. Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proc. of the Gateway Computing Environments Workshop (GCE) 1–8 (GCE, 2010).

  45. Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Iles, W. J. D., Smith, S. Y., Gandolfo, M. A. & Graham, S. W. Monocot fossils suitable for molecular dating analyses. Bot. J. Linn. Soc. 178, 346–374 (2015).

    Article  Google Scholar 

  48. Massoni, J., Doyle, J. & Sauquet, H. Fossil calibration of Magnoliidae, an ancient lineage of angiosperms. Palaeontol. Electron. 18.1.2FC, 1–25 (2015).

    Google Scholar 

  49. Wilf, P., Carvalho, M. R., Gandolfo, M. A. & Cúneo, N. R. Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355, 71–75 (2017).

    Article  CAS  PubMed  Google Scholar 

  50. Del Rio, C., Haevermans, T. & De Franceschi, D. First record of an Icacinaceae Miers fossil flower from Le Quesnoy (Ypresian, France) amber. Sci. Rep. 7, 11099 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Helmus, M. R., Bland, T. J., Williams, C. K. & Ives, A. R. Phylogenetic measures of biodiversity. Am. Nat. 169, E68–E83 (2007).

    Article  PubMed  Google Scholar 

  52. Tucker, C. M. et al. A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol. Rev. 92, 698–715 (2017).

    Article  PubMed  Google Scholar 

  53. Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51, 933–938 (2001).

    Article  Google Scholar 

  54. Sauquet, H. et al. The ancestral flower of angiosperms and its early diversification. Nat. Commun. 8, 16047 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ramírez-Barahona, S., Sauquet, H. & Magallón, S. The delayed and geographically heterogenous diversification of flowering plant families (version 1.0). Zenodo (2020).

  56. Sauquet, H., Ramírez-Barahona, S. & Magallón, S. A revised list of fossil calibrations to constrain molecular dating of angiosperms (version 1.0). Zenodo (2020).

Download references


We are grateful to J. Alroy, D. Cantrill, W. Cornwell, L. Eguiarte, F. Forest, S. Graham, S. Ho, R. Lupia, M. Pennell, E. Rebollar, J. Schönenberger and M. von Balthazar for comments on earlier drafts; A. Benitez-Villaseñor, A. López-Martínez and R. Hernández-Gutiérrez for feedback on the dating analyses; A. Antonelli and F. Condamine for early ideas that prompted the development of the fossil calibration dataset; J. Schönenberger and the University of Vienna for funding the eFLOWER server hosting the PROTEUS database; M. A. Vilchis Martínez and G. Ortega Leite for providing original articles for the fossil calibration dataset; L. Eguiarte, Y. Gutierrez Guerrero and R. García Herrera (Scientific Computing Department at Laboratorio Nacional de Ciencias de la Sostenibilidad-Instituto de Ecología, Universidad Nacional Autónoma de México) for setting up and lending the High Throughput Computing infrastructure used for part of the analyses; A. Delgado Salinas for his support. This work was supported by a postdoctoral fellowship from Dirección General de Asuntos del Personal Académico-Universidad Nacional Autónoma de México granted to S.R.-B.

Author information

Authors and Affiliations



S.R.-B., H.S. and S.M. conceived and designed the framework for the analyses. S.R.-B., H.S. and S.M. collected the data. S.R.-B. and H.S. conducted the analyses. S.R.-B. drafted the manuscript and all authors discussed results and revised the manuscript.

Corresponding author

Correspondence to Santiago Ramírez-Barahona.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Extended data

Extended Data Fig. 1 Distribution of fossil calibrations across the flowering plant phylogeny.

White circles represent the conservative set of 45 phylogenetically assigned fossils and black circles represent the remaining fossils in the complete set of 238 fossils. Tree topology is based on a maximum likelihood phylogeny. The colour of branches and outer circle represent the major angiosperm clades depicted in legend (ANA = Amborellales + Nymphaeales + Austrobaileyales).

Extended Data Fig. 2 Distribution of phylogenetic fuse length across the flowering plant phylogeny.

The colour of branches represents the three fuse categories depicted in the caption to the left. Families were classified into the three categories based on the respective length of the phylogenetic fuse. Phylogenetic fuses were calculated from the ages estimated under the relaxed calibration strategy with the complete fossil set. Outer circle represents the major angiosperm clades depicted in Fig. 1 of the main text.

Extended Data Fig. 3 Geographic distribution of flowering plant diversity.

ac, angiosperm (a) family richness, (b) species richness, and (c) phylogenetic diversity estimated from the occurrence of 248,606 species of angiosperms across the globe. Dashed lines in maps mark the limit of tropical latitudes.

Extended Data Fig. 4 Temporal distribution of flowering plant family ages.

ac, frequency histograms showing the distribution of family phylogenetic fuses obtained under the three different calibration strategies using the complete (dark) and the conservative (light) set of fossils. Horizontal dashed lines represent the mean phylogenetic fuse. df, kernel density plots for the 95% highest posterior density intervals of family stem (dark red) and crown (blue) ages obtained under the three different calibration strategies using the complete (solid lines) and the conservative (dashed lines) set of fossils.

Extended Data Fig. 5 Ancestral state reconstruction of super biomes.

Super biomes were recorded from spatial occurrence data and mapped onto the dated phylogeny using maximum likelihood. The colour of branches represents inferred ancestral biomes depicted in the caption to the left. The pie charts at the centre of the tree represent the relative likelihood of the inferred ancestral biome for 15 key nodes of the phylogeny. The dated tree corresponds to the relaxed calibration strategy with the complete fossil set. Outer circle represents the major angiosperm clades depicted in Fig. 1 of the main text.

Supplementary information

Supplementary Information

Supplementary methods, Tables 1–3, Figs. 1–9 and a list of supplementary data files (provided separately in a zipped folder).

Reporting Summary

Supplementary Data

Zipped folder containing the data supporting the findings of this study. Available at Zenodo with the identifiers and

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramírez-Barahona, S., Sauquet, H. & Magallón, S. The delayed and geographically heterogeneous diversification of flowering plant families. Nat Ecol Evol 4, 1232–1238 (2020).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

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