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.
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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 https://doi.org/10.5281/zenodo.382087855. The fossil calibration list is available at Zenodo with the identifier https://doi.org/10.5281/zenodo.382807156. The geographic data are available from the Global Biodiversity Information Facility with the identifier https://doi.org/10.15468/dl.iftsjs.
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).
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).
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).
Li, H.-T. et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat. Plants 5, 461–470 (2019).
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).
Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011).
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).
Hughes, N. F. & McDougall, A. B. Records of angiospermid pollen entry into the English Early Cretaceous succession. Rev. Palaeobot. Palynol. 50, 255–272 (1987).
Brenner, G. J. in Flowering Plant Origin, Evolution & Phylogeny (eds Taylor, D. W. & Hickey, L. J.) 91–115 (Springer, 1996).
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).
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).
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).
Wing, S. L., Hickey, L. J. & Swisher, C. C. Implications of an exceptional fossil flora for Late Cretaceous vegetation. Nature 363, 342–344 (1993).
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).
Wing, S. L. et al. Floral and environmental gradients on a Late Cretaceous landscape. Ecol. Monogr. 82, 23–47 (2011).
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).
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).
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).
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).
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).
Sauquet, H. & Magallón, S. Key questions and challenges in angiosperm macroevolution. New Phytol. 219, 1170–1187 (2018).
Wiens, J. J. & Donoghue, M. J. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 19, 639–644 (2004).
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).
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).
Stevens, P. F. Angiosperm Phylogeny Website Version 14 (MOBOT, accessed February 2018); http://www.mobot.org/MOBOT/Research/APweb/welcome.html
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).
Parham, J. F. et al. Best practices for justifying fossil calibrations. Syst. Biol. 61, 346–359 (2012).
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).
Doyle, J. A. Molecular and fossil evidence on the origin of angiosperms. Annu. Rev. Earth Planet. Sci. 40, 301–326 (2012).
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).
Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379–421 (1998).
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).
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).
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).
Cooper, A. & Fortey, R. Evolutionary explosions and the phylogenetic fuse. Trends Ecol. Evol. 13, 151–156 (1998).
Crepet, W. L. The fossil record of angiosperms: requiem or renaissance? Ann. Mo. Bot. Gard. 95, 3–33 (2008).
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).
Budd, G. E. & Mann, R. P. The dynamics of stem and crown groups. Sci. Adv. 6, eaaz1626 (2020).
Igea, J. & Tanentzap, A. J. Angiosperm speciation speeds up near the poles. Ecol. Lett. 23, 692–700 (2020).
Donoghue, M. J. & Sanderson, M. J. Confluence, synnovation, and depauperons in plant diversification. New Phytol. 207, 260–274 (2015).
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).
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
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).
Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).
Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).
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).
Massoni, J., Doyle, J. & Sauquet, H. Fossil calibration of Magnoliidae, an ancient lineage of angiosperms. Palaeontol. Electron. 18.1.2FC, 1–25 (2015).
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).
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).
Helmus, M. R., Bland, T. J., Williams, C. K. & Ives, A. R. Phylogenetic measures of biodiversity. Am. Nat. 169, E68–E83 (2007).
Tucker, C. M. et al. A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol. Rev. 92, 698–715 (2017).
Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51, 933–938 (2001).
Sauquet, H. et al. The ancestral flower of angiosperms and its early diversification. Nat. Commun. 8, 16047 (2017).
Ramírez-Barahona, S., Sauquet, H. & Magallón, S. The delayed and geographically heterogenous diversification of flowering plant families (version 1.0). Zenodo https://doi.org/10.5281/zenodo.3820878 (2020).
Sauquet, H., Ramírez-Barahona, S. & Magallón, S. A revised list of fossil calibrations to constrain molecular dating of angiosperms (version 1.0). Zenodo https://doi.org/10.5281/zenodo.3828071 (2020).
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.
The authors declare no competing interests.
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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).
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.
a–c, 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.
a–c, 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. d–f, 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.
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 methods, Tables 1–3, Figs. 1–9 and a list of supplementary data files (provided separately in a zipped folder).
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Ramírez-Barahona, S., Sauquet, H. & Magallón, S. The delayed and geographically heterogeneous diversification of flowering plant families. Nat Ecol Evol 4, 1232–1238 (2020). https://doi.org/10.1038/s41559-020-1241-3
Proceedings of the National Academy of Sciences (2020)