The delayed and geographically heterogeneous diversification of flowering plant families

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Abstract

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

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 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.

Code availability

The code used to process data and perform the analyses is available at Zenodo with the identifier https://doi.org/10.5281/zenodo.382087855.

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.

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Acknowledgements

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.

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Contributions

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.

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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).

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Supplementary Data

Zipped folder containing the data supporting the findings of this study. Available at Zenodo with the identifiers https://doi.org/10.5281/zenodo.3820878 and https://doi.org/10.5281/zenodo.3828071.

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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

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