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Research Article

The timescale of early land plant evolution

Jennifer L. Morris, View ORCID ProfileMark N. Puttick, James W. Clark, Dianne Edwards, View ORCID ProfilePaul Kenrick, Silvia Pressel, View ORCID ProfileCharles H. Wellman, View ORCID ProfileZiheng Yang, Harald Schneider, and Philip C. J. Donoghue
  1. aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
  2. bDepartment of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
  3. cSchool of Earth and Ocean Sciences, Cardiff University, Cardiff CF10, United Kingdom;
  4. dDepartment of Life Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
  5. eDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom;
  6. fDepartment of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom;
  7. gRadclie Institute for Advanced Studies, Harvard University, Cambridge, MA 02138;
  8. hCenter of Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Yunnan 666303, China

See allHide authors and affiliations

PNAS March 6, 2018 115 (10) E2274-E2283; first published February 20, 2018; https://doi.org/10.1073/pnas.1719588115
Jennifer L. Morris
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
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Mark N. Puttick
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
bDepartment of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
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  • ORCID record for Mark N. Puttick
James W. Clark
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
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Dianne Edwards
cSchool of Earth and Ocean Sciences, Cardiff University, Cardiff CF10, United Kingdom;
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Paul Kenrick
bDepartment of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
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Silvia Pressel
dDepartment of Life Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
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Charles H. Wellman
eDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom;
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  • ORCID record for Charles H. Wellman
Ziheng Yang
fDepartment of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom;
gRadclie Institute for Advanced Studies, Harvard University, Cambridge, MA 02138;
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  • ORCID record for Ziheng Yang
Harald Schneider
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
dDepartment of Life Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
hCenter of Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Yunnan 666303, China
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  • For correspondence: Phil.Donoghue@bristol.ac.uk harald@xtbg.ac.cn
Philip C. J. Donoghue
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
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  • For correspondence: Phil.Donoghue@bristol.ac.uk harald@xtbg.ac.cn
  1. Edited by Peter R. Crane, Oak Spring Garden Foundation, Upperville, VA, and approved January 17, 2018 (received for review November 10, 2017)

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Significance

Establishing the timescale of early land plant evolution is essential to testing hypotheses on the coevolution of land plants and Earth’s System. Here, we establish a timescale for early land plant evolution that integrates over competing hypotheses on bryophyte−tracheophyte relationships. We estimate land plants to have emerged in a middle Cambrian–Early Ordovocian interval, and vascular plants to have emerged in the Late Ordovician−Silurian. This timescale implies an early establishment of terrestrial ecosystems by land plants that is in close accord with recent estimates for the origin of terrestrial animal lineages. Biogeochemical models that are constrained by the fossil record of early land plants, or attempt to explain their impact, must consider a much earlier, middle Cambrian–Early Ordovician, origin.

Abstract

Establishing the timescale of early land plant evolution is essential for testing hypotheses on the coevolution of land plants and Earth’s System. The sparseness of early land plant megafossils and stratigraphic controls on their distribution make the fossil record an unreliable guide, leaving only the molecular clock. However, the application of molecular clock methodology is challenged by the current impasse in attempts to resolve the evolutionary relationships among the living bryophytes and tracheophytes. Here, we establish a timescale for early land plant evolution that integrates over topological uncertainty by exploring the impact of competing hypotheses on bryophyte−tracheophyte relationships, among other variables, on divergence time estimation. We codify 37 fossil calibrations for Viridiplantae following best practice. We apply these calibrations in a Bayesian relaxed molecular clock analysis of a phylogenomic dataset encompassing the diversity of Embryophyta and their relatives within Viridiplantae. Topology and dataset sizes have little impact on age estimates, with greater differences among alternative clock models and calibration strategies. For all analyses, a Cambrian origin of Embryophyta is recovered with highest probability. The estimated ages for crown tracheophytes range from Late Ordovician to late Silurian. This timescale implies an early establishment of terrestrial ecosystems by land plants that is in close accord with recent estimates for the origin of terrestrial animal lineages. Biogeochemical models that are constrained by the fossil record of early land plants, or attempt to explain their impact, must consider the implications of a much earlier, middle Cambrian–Early Ordovician, origin.

  • plant
  • evolution
  • timescale
  • phylogeny
  • Embryophyta

Footnotes

  • ↵1J.L.M. and M.N.P. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: Phil.Donoghue{at}bristol.ac.uk or harald{at}xtbg.ac.cn.
  • Author contributions: D.E., P.K., S.P., C.H.W., Z.Y., H.S., and P.C.J.D. designed research; J.L.M., M.N.P., J.C., H.S., and P.C.J.D. performed research; J.L.M., M.N.P., J.C., D.E., P.K., S.P., C.H.W., Z.Y., H.S., and P.C.J.D. analyzed data; and J.L.M., M.N.P., D.E., P.K., S.P., C.H.W., Z.Y., H.S., and P.C.J.D. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: All input trees and alignments are available on Figshare (https://dx.doi.org/10.6084/m9.figshare.5573032).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1719588115/-/DCSupplemental.

  • Copyright © 2018 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Timescale of early land plant evolution
Jennifer L. Morris, Mark N. Puttick, James W. Clark, Dianne Edwards, Paul Kenrick, Silvia Pressel, Charles H. Wellman, Ziheng Yang, Harald Schneider, Philip C. J. Donoghue
Proceedings of the National Academy of Sciences Mar 2018, 115 (10) E2274-E2283; DOI: 10.1073/pnas.1719588115

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Timescale of early land plant evolution
Jennifer L. Morris, Mark N. Puttick, James W. Clark, Dianne Edwards, Paul Kenrick, Silvia Pressel, Charles H. Wellman, Ziheng Yang, Harald Schneider, Philip C. J. Donoghue
Proceedings of the National Academy of Sciences Mar 2018, 115 (10) E2274-E2283; DOI: 10.1073/pnas.1719588115
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  • Earth, Atmospheric, and Planetary Sciences

This article has a Letter. Please see:

  • Relationship between Research Article and Letter - September 28, 2018

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Proceedings of the National Academy of Sciences: 115 (10)
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