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      The timescale of early land plant evolution

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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.

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          A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

          Phylogenies are usually dated by calibrating interior nodes against the fossil record. This relies on indirect methods that, in the worst case, misrepresent the fossil information. Here, we contrast such node dating with an approach that includes fossils along with the extant taxa in a Bayesian total-evidence analysis. As a test case, we focus on the early radiation of the Hymenoptera, mostly documented by poorly preserved impression fossils that are difficult to place phylogenetically. Specifically, we compare node dating using nine calibration points derived from the fossil record with total-evidence dating based on 343 morphological characters scored for 45 fossil (4--20 complete) and 68 extant taxa. In both cases we use molecular data from seven markers (∼5 kb) for the extant taxa. Because it is difficult to model speciation, extinction, sampling, and fossil preservation realistically, we develop a simple uniform prior for clock trees with fossils, and we use relaxed clock models to accommodate rate variation across the tree. Despite considerable uncertainty in the placement of most fossils, we find that they contribute significantly to the estimation of divergence times in the total-evidence analysis. In particular, the posterior distributions on divergence times are less sensitive to prior assumptions and tend to be more precise than in node dating. The total-evidence analysis also shows that four of the seven Hymenoptera calibration points used in node dating are likely to be based on erroneous or doubtful assumptions about the fossil placement. With respect to the early radiation of Hymenoptera, our results suggest that the crown group dates back to the Carboniferous, ∼309 Ma (95% interval: 291--347 Ma), and diversified into major extant lineages much earlier than previously thought, well before the Triassic. [Bayesian inference; fossil dating; morphological evolution; relaxed clock; statistical phylogenetics.]
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            Estimating the rate of evolution of the rate of molecular evolution.

            A simple model for the evolution of the rate of molecular evolution is presented. With a Bayesian approach, this model can serve as the basis for estimating dates of important evolutionary events even in the absence of the assumption of constant rates among evolutionary lineages. The method can be used in conjunction with any of the widely used models for nucleotide substitution or amino acid replacement. It is illustrated by analyzing a data set of rbcL protein sequences.
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              GEOCARB III: A revised model of atmospheric CO2 over Phanerozoic time

              R. Berner (2001)
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                6 March 2018
                20 February 2018
                20 February 2018
                : 115
                : 10
                : E2274-E2283
                Affiliations
                [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
                Author notes
                2To whom correspondence may be addressed. Email: Phil.Donoghue@ 123456bristol.ac.uk or harald@ 123456xtbg.ac.cn .

                Edited by Peter R. Crane, Oak Spring Garden Foundation, Upperville, VA, and approved January 17, 2018 (received for review November 10, 2017)

                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.

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

                Author information
                http://orcid.org/0000-0002-1011-3442
                http://orcid.org/0000-0002-3626-5460
                http://orcid.org/0000-0001-7511-0464
                http://orcid.org/0000-0003-3351-7981
                Article
                201719588
                10.1073/pnas.1719588115
                5877938
                29463716
                121839df-8a65-4460-b5cb-5bb1cae0bc6b
                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).

                History
                Page count
                Pages: 10
                Funding
                Funded by: RCUK | Natural Environment Research Council (NERC) 501100000270
                Award ID: NE/N002067/1
                Funded by: RCUK | Biotechnology and Biological Sciences Research Council (BBSRC) 501100000268
                Award ID: BB/N000919/1
                Funded by: Royal Society 501100000288
                Award ID: Wolfson Merit Award
                Categories
                PNAS Plus
                Biological Sciences
                Evolution
                Physical Sciences
                Earth, Atmospheric, and Planetary Sciences
                PNAS Plus

                plant,evolution,timescale,phylogeny,embryophyta
                plant, evolution, timescale, phylogeny, embryophyta

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