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. 2018 Mar 6;115(10):E2274-E2283.
doi: 10.1073/pnas.1719588115. Epub 2018 Feb 20.

The timescale of early land plant evolution

Jennifer L Morris  1 , Mark N Puttick  1   2 , James W Clark  1 , Dianne Edwards  3 , Paul Kenrick  2 , Silvia Pressel  4 , Charles H Wellman  5 , Ziheng Yang  6   7 , Harald Schneider  8   4   9 , Philip C J Donoghue  8
Affiliations

The timescale of early land plant evolution

Jennifer L Morris et al. Proc Natl Acad Sci U S A. .

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.

Keywords: Embryophyta; evolution; phylogeny; plant; timescale.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The seven alternative hypotheses considered in the dating analyses. (A) Monophyletic bryophytes; (B) liverwort–moss sister clade to tracheophytes; (C) mosses, liverworts, and hornworts as successive sister lineages to tracheophytes; (D) a moss–liverwort sister clade to other embryophytes; (E) hornworts, mosses, and liverworts as successive sister lineages to tracheophytes; (F) mosses, hornworts, and liverworts as successive sister lineages to tracheophytes; and (G) a moss–hornwort sister clade to tracheophytes.
Fig. 2.
Fig. 2.
Age estimates for the seven topologies used in analyses, highlighting the 95% HPD age uncertainty for embryophytes and tracheophytes. Age estimates are shown for (A) monophyletic bryophytes, (B) hornworts−sister, (C) hornworts−liverworts−mosses, (D) liverworts−mosses−sister, (E) liverworts−mosses−hornworts, (F) liverworts−hornworts−mosses, and (G) liverworts−sister.
Fig. 3.
Fig. 3.
Detailed phylogenies showing the congruent age estimates produced using the monophyletic (A) and hornworts−sister (B) topologies.
Fig. 4.
Fig. 4.
Infinite site plots showing the effects of including more sequence data on the precision of age estimates. All ages are plotted using the monophyletic bryophytes topology with (A) datasets including all sites, and datasets trimmed so sequences are complete for (B) 50%, (C) 75%, (D) 95%, and (E) 99.9% of taxa.
Fig. 5.
Fig. 5.
The estimated ages of embryophyte and tracheophyte divergence is more variable due to differences in modeling compared with differences in dataset size or topology. Using the monophyletic topology, the impact on age estimation was tested by using alternative strategies to model substitution rates, age constraints, and by excluding outgroups. An asterisk (*) denotes analysis performed on hornworts−sister topology.
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Comment in

  • Reply to Hedges et al.: Accurate timetrees do indeed require accurate calibrations.
    Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PCJ. Morris JL, et al. Proc Natl Acad Sci U S A. 2018 Oct 9;115(41):E9512-E9513. doi: 10.1073/pnas.1812816115. Epub 2018 Sep 28. Proc Natl Acad Sci U S A. 2018. PMID: 30266794 Free PMC article. No abstract available.
  • Accurate timetrees require accurate calibrations.
    Hedges SB, Tao Q, Walker M, Kumar S. Hedges SB, et al. Proc Natl Acad Sci U S A. 2018 Oct 9;115(41):E9510-E9511. doi: 10.1073/pnas.1812558115. Epub 2018 Sep 28. Proc Natl Acad Sci U S A. 2018. PMID: 30266795 Free PMC article. No abstract available.

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