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      Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record

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          Summary

          • Plants have a long evolutionary history, during which mass extinction events dramatically affected Earth's ecosystems and its biodiversity. The fossil record can shed light on the diversification dynamics of plant life and reveal how changes in the origination–extinction balance have contributed to shaping the current flora.

          • We use a novel Bayesian approach to estimate origination and extinction rates in plants throughout their history. We focus on the effect of the ‘Big Five’ mass extinctions and on estimating the timing of origin of vascular plants, seed plants and angiosperms.

          • Our analyses show that plant diversification is characterized by several shifts in origination and extinction rates, often matching the most important geological boundaries. The estimated origin of major plant clades predates the oldest macrofossils when considering the uncertainties associated with the fossil record and the preservation process.

          • Our findings show that the commonly recognized mass extinctions have affected each plant group differently and that phases of high extinction often coincided with major floral turnovers. For instance, after the Cretaceous–Paleogene boundary we infer negligible shifts in diversification of nonflowering seed plants, but find significantly decreased extinction in spore‐bearing plants and increased origination rates in angiosperms, contributing to their current ecological and evolutionary dominance.

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          Mass extinctions in the marine fossil record.

          A new compilation of fossil data on invertebrate and vertebrate families indicates that four mass extinctions in the marine realm are statistically distinct from background extinction levels. These four occurred late in the Ordovician, Permian, Triassic, and Cretaceous periods. A fifth extinction event in the Devonian stands out from the background but is not statistically significant in these data. Background extinction rates appear to have declined since Cambrian time, which is consistent with the prediction that optimization of fitness should increase through evolutionary time.
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            The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary.

            The Cretaceous-Paleogene boundary approximately 65.5 million years ago marks one of the three largest mass extinctions in the past 500 million years. The extinction event coincided with a large asteroid impact at Chicxulub, Mexico, and occurred within the time of Deccan flood basalt volcanism in India. Here, we synthesize records of the global stratigraphy across this boundary to assess the proposed causes of the mass extinction. Notably, a single ejecta-rich deposit compositionally linked to the Chicxulub impact is globally distributed at the Cretaceous-Paleogene boundary. The temporal match between the ejecta layer and the onset of the extinctions and the agreement of ecological patterns in the fossil record with modeled environmental perturbations (for example, darkness and cooling) lead us to conclude that the Chicxulub impact triggered the mass extinction.
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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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                Author and article information

                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                26 January 2015
                July 2015
                : 207
                : 2 , Evolutionary plant radiations ( doiID: 10.1111/nph.2015.207.issue-2 )
                : 425-436
                Affiliations
                [ 1 ] Department of Biological and Environmental SciencesUniversity of Gothenburg Carl Skottsbergs gata 22B SE‐413 19 GöteborgSweden
                [ 2 ] CNRSUMR Botanique et Bioinformatique de l'Architecture des Plantes (AMAP) Montpellier F‐34000France
                [ 3 ] Laboratório de Biología Molecular (CINBIN) Department of BiologyUniversidad Industrial de Santander BucaramangaColombia
                [ 4 ]Gothenburg Botanical Garden Carl Skottsbergs gata 22A SE‐413 19 GöteborgSweden
                [ 5 ]Present address: PPP Département de GéologieUniversité de Liège Allée du 6 Août B18 Sart Tilman B4000 LiègeBelgium
                Author notes
                [*] [* ] Authors for correspondence:

                Daniele Silvestro

                Tel: +41 21 692 4186

                Email: silvestro.daniele@ 123456gmail.com

                Alexandre Antonelli

                Tel: +46 703 989570

                Email: alexandre.antonelli@ 123456bioenv.gu.se

                [†]

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0003-0100-0961
                Article
                NPH13247 2014-18240
                10.1111/nph.13247
                4949670
                25619401
                b4c1287b-896a-42c9-a1ff-a27106bc4e73
                © 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 August 2014
                : 23 November 2014
                Page count
                Pages: 12
                Funding
                Funded by: Carl Tryggers stiftelse and Wenner‐Gren foundation
                Award ID: ANR‐2010‐BLAN‐607‐02
                Funded by: TERRES
                Funded by: Swedish Research Council
                Award ID: B0569601
                Funded by: European Research Council under the European Union's Seventh Framework Programme
                Award ID: FP/2007‐2013
                Award ID: 331024
                Categories
                Full Paper
                Research
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                Custom metadata
                2.0
                nph13247
                July 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.2 mode:remove_FC converted:19.07.2016

                Plant science & Botany
                biodiversity changes,diversification,floristic turnover,mass extinction,plant fossils,pyrate

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