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Phylogenomics and the rise of the angiosperms

Zuntini AR 1 , Carruthers T 1 , Maurin O 1 , Bailey PC 1 , Leempoel K 1 , Brewer GE 1 Show all authors , Epitawalage N 1 , Françoso E 1 , Gallego-Paramo B 1 , McGinnie C 1 , Negrão R 1 , Roy SR 1 , Simpson L 2 , Toledo Romero E 1 , Barber VMA 1 , Botigué L 3 , Clarkson JJ 1 , Cowan RS 1 , Dodsworth S 4 , Johnson MG 5 , Kim JT 6 , Pokorny L 1 , Wickett NJ 7 , Antar GM 8 , DeBolt L 9 , Gutierrez K 9 , Hendriks KP 10 , Hoewener A 11 , Hu AQ 1 , Joyce EM 2 , Kikuchi IABS 12 , Larridon I 1 , Larson DA 13 , de Lírio EJ 8 , Liu JX 14 , Malakasi P 1 , Przelomska NAS 1 , Shah T 1 , Viruel J 1 , Allnutt TR 15 , Ameka GK 16 , Andrew RL 17 , Appelhans MS 18 , Arista M 19 , Ariza MJ 20 , Arroyo J 19 , Arthan W 1 , Bachelier JB 21 , Bailey CD 22 , Barnes HF 15 , Barrett MD 2 , Barrett RL 23 , Bayer RJ 24 , Bayly MJ 25 , Biffin E 26 , Biggs N 1 , Birch JL 25 , Bogarín D 27 , Borosova R 1 , Bowles AMC 28 , Boyce PC 29 , Bramley GLC 1 , Briggs M 1 , Broadhurst L 30 , Brown GK 31 , Bruhl JJ 17 , Bruneau A 32 , Buerki S 33 , Burns E 1 , Byrne M 34 , Cable S 1 , Calladine A 26 , Callmander MW 35 , Cano Á 36 , Cantrill DJ 15 , Cardinal-McTeague WM 37 , Carlsen MM 38 , Carruthers AJA 1 , de Castro Mateo A 19 , Chase MW 1 , Chatrou LW 39 , Cheek M 1 , Chen S 40 , Christenhusz MJM 1 , Christin PA 41 , Clements MA 30 , Coffey SC 42 , Conran JG 43 , Cornejo X 44 , Couvreur TLP 45 , Cowie ID 46 , Csiba L 1 , Darbyshire I 1 , Davidse G 38 , Davies NMJ 1 , Davis AP 1 , van Dijk KJ 47 , Downie SR 48 , Duretto MF 23 , Duvall MR 49 , Edwards SL 1 , Eggli U 50 , Erkens RHJ 27 , Escudero M 19 , de la Estrella M 51 , Fabriani F 39 , Fay MF 1 , Ferreira PL 52 , Ficinski SZ 1 , Fowler RM 25 , Frisby S 1 , Fu L 53 , Fulcher T 1 , Galbany-Casals M 54 , Gardner EM 55 , German DA 56 , Giaretta A 57 , Gibernau M 58 , Gillespie LJ 59 , González CC 60 , Goyder DJ 1 , Graham SW 12 , Grall A 1 , Green L 1 , Gunn BF 15 , Gutiérrez DG 61 , Hackel J 1 , Haevermans T 62 , Haigh A 1 , Hall JC 63 , Hall T 1 , Harrison MJ 2 , Hatt SA 1 , Hidalgo O 64 , Hodkinson TR 65 , Holmes GD 15 , Hopkins HCF 1 , Jackson CJ 15 , James SA 42 , Jobson RW 23 , Kadereit G 66 , Kahandawala IM 1 , Kainulainen K 67 , Kato M 68 , Kellogg EA 69 , King GJ 70 , Klejevskaja B 71 , Klitgaard BB 1 , Klopper RR 72 , Knapp S 73 , Koch MA 74 , Leebens-Mack JH 75 , Lens F 27 , Leon CJ 1 , Léveillé-Bourret É 76 , Lewis GP 1 , Li DZ 14 , Li L 77 , Liede-Schumann S 78 , Livshultz T 79 , Lorence D 80 , Lu M 1 , Lu-Irving P 23 , Luber J 81 , Lucas EJ 1 , Luján M 1 , Lum M 82 , Macfarlane TD 42 , Magdalena C 1 , Mansano VF 81 , Masters LE 1 , Mayo SJ 1 , McColl K 23 , McDonnell AJ 83 , McDougall AE 47 , McLay TGB 15 , McPherson H 23 , Meneses RI 84 , Merckx VSFT 27 , Michelangeli FA 85 , Mitchell JD 85 , Monro AK 1 , Moore MJ 86 , Mueller TL 87 , Mummenhoff K 10 , Munzinger J 88 , Muriel P 89 , Murphy DJ 15 , Nargar K 2 , Nauheimer L 2 , Nge FJ 26 , Nyffeler R 90 , Orejuela A 91 , Ortiz EM 11 , Palazzesi L 61 , Peixoto AL 81 , Pell SK 92 , Pellicer J 64 , Penneys DS 93 , Perez-Escobar OA 1 , Persson C 94 , Pignal M 62 , Pillon Y 95 , Pirani JR 8 , Plunkett GM 85 , Powell RF 1 , Prance GT 1 , Puglisi C 1 , Qin M 53 , Rabeler RK 13 , Rees PEJ 1 , Renner M 23 , Roalson EH 96 , Rodda M 97 , Rogers ZS 98 , Rokni S 1 , Rutishauser R 90 , de Salas MF 99 , Schaefer H 11 , Schley RJ 100 , Schmidt-Lebuhn A 30 , Shapcott A 101 , Al-Shehbaz I 38 , Shepherd KA 42 , Simmons MP 102 , Simões AO 103 , Simões ARG 1 , Siros M 1 , Smidt EC 104 , Smith JF 33 , Snow N 105 , Soltis DE 106 , Soltis PS 106 , Soreng RJ 107 , Sothers CA 1 , Starr JR 108 , Stevens PF 38 , Straub SCK 109 , Struwe L 110 , Taylor JM 77 , Telford IRH 17 , Thornhill AH 17 , Tooth I 23 , Trias-Blasi A 1 , Udovicic F 15 , Utteridge TMA 1 , Del Valle JC 19 , Verboom GA 111 , Vonow HP 26 , Vorontsova MS 1 , de Vos JM 112 , Al-Wattar N 1 , Waycott M 26 , Welker CAD 113 , White AJ 114 , Wieringa JJ 27 , Williamson LT 47 , Wilson TC 23 , Wong SY 115 , Woods LA 23 , Woods R 1 , Worboys S 2 , Xanthos M 1 , Yang Y 116 , Zhang YX 117 , Zhou MY 14 , Zmarzty S 1 , Zuloaga FO 118 , Antonelli A 1 , Bellot S 1 , Crayn DM 2 , Grace OM 1 , Kersey PJ 1 , Leitch IJ 1 , Sauquet H 23 , Smith SA 13 , Eiserhardt WL 1 , Forest F 1 , Baker WJ 119

Affiliations 

  • 1 Royal Botanic Gardens, Kew, Richmond, UK
  • 2 Australian Tropical Herbarium, James Cook University, Smithfield, Queensland, Australia
  • 3 Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Barcelona, Spain
  • 4 School of Biological Sciences, University of Portsmouth, Portsmouth, UK
  • 5 Texas Tech University, Lubbock, TX, USA
  • 6 School of Physics, Engineering and Computer Science, University of Hertfordshire, Hatfield, UK
  • 7 Department of Biological Sciences, Clemson University, Clemson, SC, USA
  • 8 Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil
  • 9 Smith College, Northampton, MA, USA
  • 10 Department of Biology, University of Osnabrück, Osnabrück, Germany
  • 11 Plant Biodiversity, Technical University Munich, Freising, Germany
  • 12 Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada
  • 13 Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA
  • 14 Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
  • 15 Royal Botanic Gardens Victoria, Melbourne, Victoria, Australia
  • 16 Department of Plant and Environmental Biology, University of Ghana, Accra, Ghana
  • 17 Botany and N.C.W. Beadle Herbarium, University of New England, Armidale, New South Wales, Australia
  • 18 Department of Systematics, Biodiversity and Evolution of Plants, Albrecht-von-Haller Institute of Plant Sciences, University of Göttingen, Göttingen, Germany
  • 19 Departamento de Biología Vegetal y Ecología, Facultad de Biología, Universidad de Sevilla, Seville, Spain
  • 20 General Research Services, Herbario SEV, CITIUS, Universidad de Sevilla, Seville, Spain
  • 21 Institute of Biology, Freie Universität, Berlin, Germany
  • 22 Department of Biology, New Mexico State University, Las Cruces, NM, USA
  • 23 National Herbarium of NSW, Botanic Gardens of Sydney, Mount Annan, New South Wales, Australia
  • 24 Department of Biological Sciences, University of Memphis, Memphis, TN, USA
  • 25 School of BioSciences, The University of Melbourne, Parkville, Victoria, Australia
  • 26 State Herbarium of South Australia, Botanic Gardens and State Herbarium, Adelaide, South Australia, Australia
  • 27 Naturalis Biodiversity Center, Leiden, The Netherlands
  • 28 School of Geographical Sciences, University of Bristol, Bristol, UK
  • 29 Centro Studi Erbario Tropicale, Dipartimento di Biologia, University of Florence, Florence, Italy
  • 30 Centre for Australian National Biodiversity Research, National Research Collections Australia, CSIRO, Canberra, Australian Capital Territory, Australia
  • 31 Queensland Herbarium and Biodiversity Science, Brisbane Botanic Gardens, Toowong, Queensland, Australia
  • 32 Institut de Recherche en Biologie Végétale and Département de Sciences Biologiques, University of Montreal, Montreal, Quebec, Canada
  • 33 Department of Biological Sciences, Boise State University, Boise, ID, USA
  • 34 Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Government of Western Australia, Kensington, Western Australia, Australia
  • 35 Conservatoire et Jardin Botaniques de Genève, Chambésy, Switzerland
  • 36 Cambridge University Botanic Garden, Cambridge, UK
  • 37 Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, British Columbia, Canada
  • 38 Missouri Botanical Garden, St. Louis, MO, USA
  • 39 Department of Biology, Ghent University, Ghent, Belgium
  • 40 Institute of Herbgenomics, Chengdu University of Traditional Chinese Medicine, Chengdu, China
  • 41 Ecology and Evolutionary Biology, School of Biosciences, University of Sheffield, Sheffield, UK
  • 42 Western Australian Herbarium, Department of Biodiversity, Conservation and Attractions, Government of Western Australia, Kensington, Western Australia, Australia
  • 43 School of Biological Sciences, The University of Adelaide, Adelaide, South Australia, Australia
  • 44 Herbario GUAY, Facultad de Ciencias Naturales, Universidad de Guayaquil, Guayaquil, Ecuador
  • 45 DIADE, Université Montpellier, CIRAD IRD, Montpellier, France
  • 46 Northern Territory Herbarium Department of Environment Parks & Water Security, Northern Territory Government, Palmerston, Northern Territory, Australia
  • 47 The University of Adelaide, North Terrace Campus, Adelaide, South Australia, Australia
  • 48 Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
  • 49 Department of Biological Sciences and Institute for the Study of the Environment, Sustainability and Energy, Northern Illinois University, DeKalb, IL, USA
  • 50 Sukkulenten-Sammlung Zürich/ Grün Stadt Zürich, Zürich, Switzerland
  • 51 Departamento de Botánica, Ecología y Fisiología Vegetal, Facultad de Ciencias, Universidad de Córdoba, Córdoba, Spain
  • 52 Departamento de Biologia, Faculdade de Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, Brazil
  • 53 South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
  • 54 Systematics and Evolution of Vascular Plants (UAB)-Associated Unit to CSIC by IBB, Departament de Biologia Animal, Biologia Vegetal i Ecologia, Facultat de Biociències, Universitat Autònoma de Barcelona, Bellaterra, Spain
  • 55 Department of Biology, Case Western Reserve University, Cleveland, OH, USA
  • 56 Altai State University, Barnaul, Russia
  • 57 Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Dourados, Brazil
  • 58 Laboratoire Sciences Pour l'Environnement, Université de Corse, Ajaccio, France
  • 59 Canadian Museum of Nature, Ottawa, Ontario, Canada
  • 60 Herbario Trelew, Universidad Nacional de la Patagonia San Juan Bosco, Trelew, Argentina
  • 61 Museo Argentino de Ciencias Naturales (MACN-CONICET), Buenos Aires, Argentina
  • 62 Institut de Systématique, Evolution, Biodiversité, Muséum National d'Histoire Naturelle, Paris, France
  • 63 Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
  • 64 Institut Botànic de Barcelona (IBB CSIC-Ajuntament de Barcelona), Barcelona, Spain
  • 65 Botany, School of Natural Sciences, Trinity College Dublin, The University of Dublin, Dublin, Ireland
  • 66 Prinzessin Therese von Bayern-Lehrstuhl für Systematik, Biodiversität & Evolution der Pflanzen, Ludwig-Maximilians-Universität München, Botanische Staatssammlung München, Botanischer Garten München-Nymphenburg, Munich, Germany
  • 67 Gothenburg Botanical Garden, Gothenburg, Sweden
  • 68 National Museum of Nature and Science, Tsukuba, Japan
  • 69 Donald Danforth Plant Science Center, St. Louis, MO, USA
  • 70 Southern Cross University, Lismore, New South Wales, Australia
  • 71 Synergy SRG, Luton, UK
  • 72 Foundational Biodiversity Science Division, South African National Biodiversity Institute, Pretoria, South Africa
  • 73 Natural History Museum, London, UK
  • 74 Centre for Organismal Studies, Biodiversity and Plant Systematics, Heidelberg University, Heidelberg, Germany
  • 75 Department of Plant Biology, University of Georgia, Athens, GA, USA
  • 76 Institut de Recherche en Biologie Végétale, University of Montreal, Montreal, Quebec, Canada
  • 77 CSIRO, Canberra, Australian Capital Territory, Australia
  • 78 Department of Plant Systematics, University of Bayreuth, Bayreuth, Germany
  • 79 Department of Biodiversity, Earth and Environmental Sciences, Drexel University, Philadelphia, PA, USA
  • 80 National Tropical Botanical Garden, Kalaheo, HI, USA
  • 81 Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brazil
  • 82 Bioplatforms Australia Ltd, Sydney, New South Wales, Australia
  • 83 Department of Biological Sciences, Saint Cloud State University, Saint Cloud, MN, USA
  • 84 Instituto de Arqueología y Antropología, Universidad Católica del Norte, San Pedro de Atacama, Chile
  • 85 New York Botanical Garden, Bronx, NY, USA
  • 86 Department of Biology, Oberlin College, Oberlin, OH, USA
  • 87 Department of Ecology, Evolution & Behavior, University of Minnesota, St. Paul, MN, USA
  • 88 AMAP Lab, Université Montpellier, IRD, CIRAD, CNRS INRAE, Montpellier, France
  • 89 Laboratorio de Ecofisiología, Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Quito, Ecuador
  • 90 Department of Systematic and Evolutionary Botany, University of Zürich, Zürich, Switzerland
  • 91 Royal Botanic Garden Edinburgh, Edinburgh, UK
  • 92 US Botanic Garden, Washington, DC, USA
  • 93 Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA
  • 94 Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden
  • 95 LSTM Université Montpellier, CIRADIRD, Montpellier, France
  • 96 School of Biological Sciences, Washington State University, Pullman, WA, USA
  • 97 National Parks Board, Singapore Botanic Gardens, Singapore, Singapore
  • 98 New Mexico State University, Las Cruces, NM, USA
  • 99 Tasmanian Herbarium, University of Tasmania, Sandy Bay, Tasmania, Australia
  • 100 University of Exeter, Exeter, UK
  • 101 School of Science Technology and Engineering, Center for Bioinnovation, University Sunshine Coast, Sippy Downs, Queensland, Australia
  • 102 Department of Biology, Colorado State University, Fort Collins, CO, USA
  • 103 Departamento de Biologia Vegetal, Universidade Estadual de Campinas, Campinas, Brazil
  • 104 Departamento de Botânica, Universidade Federal do Paraná, Curitiba, Brazil
  • 105 Pittsburg State University, Pittsburg, KS, USA
  • 106 Florida Museum of Natural History, University of Florida, Gainesville, FL, USA
  • 107 Smithsonian Institution, Washington, DC, USA
  • 108 Department of Biology, University of Ottawa, Ottawa, Ontario, Canada
  • 109 Hobart and William Smith Colleges, Geneva, NY, USA
  • 110 Rutgers University, New Brunswick, NJ, USA
  • 111 Department of Biological Sciences and Bolus Herbarium, University of Cape Town, Cape Town, South Africa
  • 112 Department of Environmental Sciences-Botany, University of Basel, Basel, Switzerland
  • 113 Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Brazil
  • 114 Australian National Herbarium, Centre for Australian National Biodiversity Research, National Research Collections Australia, CSIRO, Canberra, Australian Capital Territory, Australia
  • 115 Institute of Biodiversity And Environmental Conservation, Universiti Malaysia Sarawak, Samarahan, Malaysia
  • 116 University of Minnesota-Twin Cities, St. Paul, MN, USA
  • 117 Southwest Forestry University, Kunming, China
  • 118 Instituto de Botánica Darwinion, San Isidro, Argentina
  • 119 Royal Botanic Gardens, Kew, Richmond, UK. w.baker@kew.org
Nature, 2024 May;629(8013):843-850.
PMID: 38658746 DOI: 10.1038/s41586-024-07324-0

Abstract

Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods1,2. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So far, the angiosperm tree of life has been determined primarily by means of analyses of the plastid genome3,4. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins5-7. However, the limited and biased sampling of both taxa and genomes undermines confidence in the tree and its implications. Here, we build the tree of life for almost 8,000 (about 60%) angiosperm genera using a standardized set of 353 nuclear genes8. This 15-fold increase in genus-level sampling relative to comparable nuclear studies9 provides a critical test of earlier results and brings notable change to key groups, especially in rosids, while substantiating many previously predicted relationships. Scaling this tree to time using 200 fossils, we discovered that early angiosperm evolution was characterized by high gene tree conflict and explosive diversification, giving rise to more than 80% of extant angiosperm orders. Steady diversification ensued through the remaining Mesozoic Era until rates resurged in the Cenozoic Era, concurrent with decreasing global temperatures and tightly linked with gene tree conflict. Taken together, our extensive sampling combined with advanced phylogenomic methods shows the deep history and full complexity in the evolution of a megadiverse clade.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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