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Phylogenomics and the rise of the angiosperms

Alexandre R. Zuntini, Tom Carruthers, Olivier Maurin, Paul C. Bailey, Kevin Leempoel, Grace E. Brewer, Niroshini Epitawalage, Elaine Françoso, Berta Gallego-Paramo, Catherine McGinnie, Raquel Negrão, Shyamali R. Roy, Lalita Simpson, Eduardo Toledo Romero, Vanessa M. A. Barber, Laura Botigué, James J. Clarkson, Robyn S. Cowan, Steven Dodsworth, Matthew G. Johnson, Jan T. Kim, Lisa Pokorny, Norman J. Wickett, Guilherme M. Antar, Lucinda DeBolt, Karime Gutierrez, Kasper P. Hendriks, Alina Hoewener, Ai-Qun Hu, Elizabeth M. Joyce, Izai A. B. S. Kikuchi, Isabel Larridon, Drew A. Larson, Elton John Lírio, Jing-Xia Liu, Panagiota Malakasi, Natalia A. S. Przelomska, Toral Shah, Juan Viruel, Theodore R. Allnutt, Gabriel K. Ameka, Rose L. Andrew, Marc S. Appelhans, Montserrat Arista, María Jesús Ariza, Juan Arroyo, Watchara Arthan, Julien B. Bachelier, C. Donovan Bailey, Helen F. Barnes, Matthew D. Barrett, Russell L. Barrett, Randall J. Bayer, Michael J. Bayly, Ed Biffin, Nicky Biggs, Joanne L. Birch, Diego Bogarín, Renata Borosova, Alexander M. C. Bowles, Peter C. Boyce, Gemma L. C. Bramley, Marie Briggs, Linda Broadhurst, Gillian K. Brown, Jeremy J. Bruhl, Anne Bruneau, Sven Buerki, Edie Burns, Margaret Byrne, Stuart Cable, Ainsley Calladine, Martin W. Callmander, Ángela Cano, David J. Cantrill, Warren M. Cardinal-McTeague, Mónica M. Carlsen, Abigail J. A. Carruthers, Alejandra Castro Mateo, Mark W. Chase, Lars W. Chatrou, Martin Cheek, Shilin Chen, Maarten J. M. Christenhusz, Pascal-Antoine Christin, Mark A. Clements, Skye C. Coffey, John G. Conran, Xavier Cornejo, Thomas L. P. Couvreur, Ian D. Cowie, Laszlo Csiba, Iain Darbyshire, Gerrit Davidse, Nina M. J. Davies, Aaron P. Davis, Kor-jent Dijk, Stephen R. Downie, Marco F. Duretto, Melvin R. Duvall, Sara L. Edwards, Urs Eggli, Roy H. J. Erkens, Marcial Escudero, Manuel Estrella, Federico Fabriani, Michael F. Fay, Paola de L. Ferreira, Sarah Z. Ficinski, Rachael M. Fowler, Sue Frisby, Lin Fu, Tim Fulcher, Mercè Galbany-Casals, Elliot M. Gardner, Dmitry A. German, Augusto Giaretta, Marc Gibernau, Lynn J. Gillespie, Cynthia C. González, David J. Goyder, Sean W. Graham, Aurélie Grall, Laura Green, Bee F. Gunn, Diego G. Gutiérrez, Jan Hackel, Thomas Haevermans, Anna Haigh, Jocelyn C. Hall, Tony Hall, Melissa J. Harrison, Sebastian A. Hatt, Oriane Hidalgo, Trevor R. Hodkinson, Gareth D. Holmes, Helen C. F. Hopkins, Christopher J. Jackson, Shelley A. James, Richard W. Jobson, Gudrun Kadereit, Imalka M. Kahandawala, Kent Kainulainen, Masahiro Kato, Elizabeth A. Kellogg, Graham J. King, Beata Klejevskaja, Bente B. Klitgaard, Ronell R. Klopper, Sandra Knapp, Marcus A. Koch, James H. Leebens-Mack, Frederic Lens, Christine J. Leon, Étienne Léveillé-Bourret, Gwilym P. Lewis, Li De-Zhu, Lan Li, Sigrid Liede-Schumann, Tatyana Livshultz, David Lorence, Meng Lu, Patricia Lu-Irving, Jaquelini Luber, Eve J. Lucas, Manuel Luján, Mabel Lum, Terry D. Macfarlane, Carlos Magdalena, Vidal F. Mansano, Lizo E. Masters, Simon J. Mayo, Kristina McColl, Angela J. McDonnell, Andrew E. McDougall, Todd G. B. McLay, Hannah McPherson, Rosa I. Meneses, Vincent S. F. T. Merckx, Fabián A. Michelangeli, John D. Mitchell, Alexandre K. Monro, Michael J. Moore, Taryn L. Mueller, Klaus Mummenhoff, Jérôme Munzinger, Priscilla Muriel, Daniel J. Murphy, Katharina Nargar, Lars Nauheimer, Francis J. Nge, Reto Nyffeler, Andrés Orejuela, Edgardo M. Ortiz, Luis Palazzesi, Ariane Luna Peixoto, Susan K. Pell, Jaume Pellicer, Darin S. Penneys, Oscar A. Perez-Escobar, Claes Persson, Marc Pignal, Yohan Pillon, José R. Pirani, Gregory M. Plunkett, Robyn F. Powell, Ghillean T. Prance, Carmen Puglisi, Ming Qin, Richard K. Rabeler, Paul E. J. Rees, Matthew Renner, Eric H. Roalson, Michele Rodda, Zachary S. Rogers, Saba Rokni, Rolf Rutishauser, Miguel F. Salas, Hanno Schaefer, Rowan J. Schley, Alexander Schmidt-Lebuhn, Alison Shapcott, Ihsan Al-Shehbaz, Kelly A. Shepherd, Mark P. Simmons, André O. Simões, Ana Rita G. Simões, Michelle Siros, Eric C. Smidt, James F. Smith, Neil Snow, Douglas E. Soltis, Pamela S. Soltis, Robert J. Soreng, Cynthia A. Sothers, Julian R. Starr, Peter F. Stevens, Shannon C. K. Straub, Lena Struwe, Jennifer M. Taylor, Ian R. H. Telford, Andrew H. Thornhill, Ifeanna Tooth, Anna Trias-Blasi, Frank Udovicic, Timothy M. A. Utteridge, Jose C. Valle, G. Anthony Verboom, Helen P. Vonow, Maria S. Vorontsova, Jurriaan M. Vos, Noor Al-Wattar, Michelle Waycott, Cassiano A. D. Welker, Adam J. White, Jan J. Wieringa, Luis T. Williamson, Trevor C. Wilson, Sin Yeng Wong, Lisa A. Woods, Roseina Woods, Stuart Worboys, Martin Xanthos, Ya Yang, Yu-Xiao Zhang, Meng-Yuan Zhou, Sue Zmarzty, Fernando O. Zuloaga, Alexandre Antonelli, Sidonie Bellot, Darren M. Crayn, Olwen M. Grace, Paul J. Kersey, Ilia J. Leitch, Hervé Sauquet, Stephen A. Smith, Wolf L. Eiserhardt, Félix Forest and William J. Baker ()
Additional contact information
Alexandre R. Zuntini: Royal Botanic Gardens, Kew
Tom Carruthers: Royal Botanic Gardens, Kew
Olivier Maurin: Royal Botanic Gardens, Kew
Paul C. Bailey: Royal Botanic Gardens, Kew
Kevin Leempoel: Royal Botanic Gardens, Kew
Grace E. Brewer: Royal Botanic Gardens, Kew
Niroshini Epitawalage: Royal Botanic Gardens, Kew
Elaine Françoso: Royal Botanic Gardens, Kew
Berta Gallego-Paramo: Royal Botanic Gardens, Kew
Catherine McGinnie: Royal Botanic Gardens, Kew
Raquel Negrão: Royal Botanic Gardens, Kew
Shyamali R. Roy: Royal Botanic Gardens, Kew
Lalita Simpson: James Cook University
Eduardo Toledo Romero: Royal Botanic Gardens, Kew
Vanessa M. A. Barber: Royal Botanic Gardens, Kew
Laura Botigué: Campus UAB
James J. Clarkson: Royal Botanic Gardens, Kew
Robyn S. Cowan: Royal Botanic Gardens, Kew
Steven Dodsworth: University of Portsmouth
Matthew G. Johnson: Texas Tech University
Jan T. Kim: University of Hertfordshire
Lisa Pokorny: Royal Botanic Gardens, Kew
Norman J. Wickett: Clemson University
Guilherme M. Antar: Universidade de São Paulo
Lucinda DeBolt: Smith College
Karime Gutierrez: Smith College
Kasper P. Hendriks: University of Osnabrück
Alina Hoewener: Technical University Munich
Ai-Qun Hu: Royal Botanic Gardens, Kew
Elizabeth M. Joyce: James Cook University
Izai A. B. S. Kikuchi: University of British Columbia
Isabel Larridon: Royal Botanic Gardens, Kew
Drew A. Larson: University of Michigan
Elton John Lírio: Universidade de São Paulo
Jing-Xia Liu: Chinese Academy of Sciences
Panagiota Malakasi: Royal Botanic Gardens, Kew
Natalia A. S. Przelomska: Royal Botanic Gardens, Kew
Toral Shah: Royal Botanic Gardens, Kew
Juan Viruel: Royal Botanic Gardens, Kew
Theodore R. Allnutt: Royal Botanic Gardens Victoria
Gabriel K. Ameka: University of Ghana
Rose L. Andrew: University of New England
Marc S. Appelhans: University of Göttingen
Montserrat Arista: Universidad de Sevilla
María Jesús Ariza: Universidad de Sevilla
Juan Arroyo: Universidad de Sevilla
Watchara Arthan: Royal Botanic Gardens, Kew
Julien B. Bachelier: Freie Universität
C. Donovan Bailey: New Mexico State University
Helen F. Barnes: Royal Botanic Gardens Victoria
Matthew D. Barrett: James Cook University
Russell L. Barrett: Botanic Gardens of Sydney
Randall J. Bayer: University of Memphis
Michael J. Bayly: The University of Melbourne
Ed Biffin: Botanic Gardens and State Herbarium
Nicky Biggs: Royal Botanic Gardens, Kew
Joanne L. Birch: The University of Melbourne
Diego Bogarín: Naturalis Biodiversity Center
Renata Borosova: Royal Botanic Gardens, Kew
Alexander M. C. Bowles: University of Bristol
Peter C. Boyce: University of Florence
Gemma L. C. Bramley: Royal Botanic Gardens, Kew
Marie Briggs: Royal Botanic Gardens, Kew
Linda Broadhurst: National Research Collections Australia, CSIRO
Gillian K. Brown: Brisbane Botanic Gardens
Jeremy J. Bruhl: University of New England
Anne Bruneau: University of Montreal
Sven Buerki: Boise State University
Edie Burns: Royal Botanic Gardens, Kew
Margaret Byrne: Department of Biodiversity, Conservation and Attractions, Government of Western Australia
Stuart Cable: Royal Botanic Gardens, Kew
Ainsley Calladine: Botanic Gardens and State Herbarium
Martin W. Callmander: Conservatoire et Jardin Botaniques de Genève
Ángela Cano: Cambridge University Botanic Garden
David J. Cantrill: Royal Botanic Gardens Victoria
Warren M. Cardinal-McTeague: University of British Columbia
Mónica M. Carlsen: Missouri Botanical Garden
Abigail J. A. Carruthers: Royal Botanic Gardens, Kew
Alejandra Castro Mateo: Universidad de Sevilla
Mark W. Chase: Royal Botanic Gardens, Kew
Lars W. Chatrou: Ghent University
Martin Cheek: Royal Botanic Gardens, Kew
Shilin Chen: Chengdu University of Traditional Chinese Medicine
Maarten J. M. Christenhusz: Royal Botanic Gardens, Kew
Pascal-Antoine Christin: University of Sheffield
Mark A. Clements: National Research Collections Australia, CSIRO
Skye C. Coffey: Government of Western Australia
John G. Conran: The University of Adelaide
Xavier Cornejo: Universidad de Guayaquil
Thomas L. P. Couvreur: Université Montpellier, CIRAD IRD
Ian D. Cowie: Northern Territory Herbarium Department of Environment Parks & Water Security, Northern Territory Government
Laszlo Csiba: Royal Botanic Gardens, Kew
Iain Darbyshire: Royal Botanic Gardens, Kew
Gerrit Davidse: Missouri Botanical Garden
Nina M. J. Davies: Royal Botanic Gardens, Kew
Aaron P. Davis: Royal Botanic Gardens, Kew
Kor-jent Dijk: The University of Adelaide, North Terrace Campus
Stephen R. Downie: University of Illinois at Urbana-Champaign
Marco F. Duretto: Botanic Gardens of Sydney
Melvin R. Duvall: Northern Illinois University
Sara L. Edwards: Royal Botanic Gardens, Kew
Urs Eggli: Sukkulenten-Sammlung Zürich/ Grün Stadt Zürich
Roy H. J. Erkens: Naturalis Biodiversity Center
Marcial Escudero: Universidad de Sevilla
Manuel Estrella: Universidad de Córdoba
Federico Fabriani: Ghent University
Michael F. Fay: Royal Botanic Gardens, Kew
Paola de L. Ferreira: Universidade de São Paulo
Sarah Z. Ficinski: Royal Botanic Gardens, Kew
Rachael M. Fowler: The University of Melbourne
Sue Frisby: Royal Botanic Gardens, Kew
Lin Fu: Chinese Academy of Sciences
Tim Fulcher: Royal Botanic Gardens, Kew
Mercè Galbany-Casals: Universitat Autònoma de Barcelona
Elliot M. Gardner: Case Western Reserve University
Dmitry A. German: Altai State University
Augusto Giaretta: Universidade Federal da Grande Dourados
Marc Gibernau: Université de Corse
Lynn J. Gillespie: Canadian Museum of Nature
Cynthia C. González: Universidad Nacional de la Patagonia San Juan Bosco
David J. Goyder: Royal Botanic Gardens, Kew
Sean W. Graham: University of British Columbia
Aurélie Grall: Royal Botanic Gardens, Kew
Laura Green: Royal Botanic Gardens, Kew
Bee F. Gunn: Royal Botanic Gardens Victoria
Diego G. Gutiérrez: Museo Argentino de Ciencias Naturales (MACN-CONICET)
Jan Hackel: Royal Botanic Gardens, Kew
Thomas Haevermans: Muséum National d’Histoire Naturelle
Anna Haigh: Royal Botanic Gardens, Kew
Jocelyn C. Hall: University of Alberta
Tony Hall: Royal Botanic Gardens, Kew
Melissa J. Harrison: James Cook University
Sebastian A. Hatt: Royal Botanic Gardens, Kew
Oriane Hidalgo: Institut Botànic de Barcelona (IBB CSIC-Ajuntament de Barcelona)
Trevor R. Hodkinson: The University of Dublin
Gareth D. Holmes: Royal Botanic Gardens Victoria
Helen C. F. Hopkins: Royal Botanic Gardens, Kew
Christopher J. Jackson: Royal Botanic Gardens Victoria
Shelley A. James: Government of Western Australia
Richard W. Jobson: Botanic Gardens of Sydney
Gudrun Kadereit: Botanischer Garten München-Nymphenburg
Imalka M. Kahandawala: Royal Botanic Gardens, Kew
Kent Kainulainen: Gothenburg Botanical Garden
Masahiro Kato: National Museum of Nature and Science
Elizabeth A. Kellogg: Donald Danforth Plant Science Center
Graham J. King: Southern Cross University
Beata Klejevskaja: Synergy SRG
Bente B. Klitgaard: Royal Botanic Gardens, Kew
Ronell R. Klopper: South African National Biodiversity Institute
Sandra Knapp: Natural History Museum
Marcus A. Koch: Heidelberg University
James H. Leebens-Mack: University of Georgia
Frederic Lens: Naturalis Biodiversity Center
Christine J. Leon: Royal Botanic Gardens, Kew
Étienne Léveillé-Bourret: University of Montreal
Gwilym P. Lewis: Royal Botanic Gardens, Kew
Li De-Zhu: Chinese Academy of Sciences
Lan Li: CSIRO
Sigrid Liede-Schumann: University of Bayreuth
Tatyana Livshultz: Drexel University
David Lorence: National Tropical Botanical Garden
Meng Lu: Royal Botanic Gardens, Kew
Patricia Lu-Irving: Botanic Gardens of Sydney
Jaquelini Luber: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro
Eve J. Lucas: Royal Botanic Gardens, Kew
Manuel Luján: Royal Botanic Gardens, Kew
Mabel Lum: Bioplatforms Australia Ltd
Terry D. Macfarlane: Government of Western Australia
Carlos Magdalena: Royal Botanic Gardens, Kew
Vidal F. Mansano: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro
Lizo E. Masters: Royal Botanic Gardens, Kew
Simon J. Mayo: Royal Botanic Gardens, Kew
Kristina McColl: Botanic Gardens of Sydney
Angela J. McDonnell: Saint Cloud State University
Andrew E. McDougall: The University of Adelaide, North Terrace Campus
Todd G. B. McLay: Royal Botanic Gardens Victoria
Hannah McPherson: Botanic Gardens of Sydney
Rosa I. Meneses: Universidad Católica del Norte
Vincent S. F. T. Merckx: Naturalis Biodiversity Center
Fabián A. Michelangeli: New York Botanical Garden
John D. Mitchell: New York Botanical Garden
Alexandre K. Monro: Royal Botanic Gardens, Kew
Michael J. Moore: Oberlin College
Taryn L. Mueller: University of Minnesota
Klaus Mummenhoff: University of Osnabrück
Jérôme Munzinger: Université Montpellier, IRD, CIRAD, CNRS INRAE
Priscilla Muriel: Pontificia Universidad Católica del Ecuador
Daniel J. Murphy: Royal Botanic Gardens Victoria
Katharina Nargar: James Cook University
Lars Nauheimer: James Cook University
Francis J. Nge: Botanic Gardens and State Herbarium
Reto Nyffeler: University of Zürich
Andrés Orejuela: Royal Botanic Garden Edinburgh
Edgardo M. Ortiz: Technical University Munich
Luis Palazzesi: Museo Argentino de Ciencias Naturales (MACN-CONICET)
Ariane Luna Peixoto: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro
Susan K. Pell: US Botanic Garden
Jaume Pellicer: Institut Botànic de Barcelona (IBB CSIC-Ajuntament de Barcelona)
Darin S. Penneys: University of North Carolina Wilmington
Oscar A. Perez-Escobar: Royal Botanic Gardens, Kew
Claes Persson: University of Gothenburg
Marc Pignal: Muséum National d’Histoire Naturelle
Yohan Pillon: LSTM Université Montpellier, CIRADIRD
José R. Pirani: Universidade de São Paulo
Gregory M. Plunkett: New York Botanical Garden
Robyn F. Powell: Royal Botanic Gardens, Kew
Ghillean T. Prance: Royal Botanic Gardens, Kew
Carmen Puglisi: Royal Botanic Gardens, Kew
Ming Qin: Chinese Academy of Sciences
Richard K. Rabeler: University of Michigan
Paul E. J. Rees: Royal Botanic Gardens, Kew
Matthew Renner: Botanic Gardens of Sydney
Eric H. Roalson: Washington State University
Michele Rodda: Singapore Botanic Gardens
Zachary S. Rogers: New Mexico State University
Saba Rokni: Royal Botanic Gardens, Kew
Rolf Rutishauser: University of Zürich
Miguel F. Salas: University of Tasmania
Hanno Schaefer: Technical University Munich
Rowan J. Schley: University of Exeter
Alexander Schmidt-Lebuhn: National Research Collections Australia, CSIRO
Alison Shapcott: University Sunshine Coast
Ihsan Al-Shehbaz: Missouri Botanical Garden
Kelly A. Shepherd: Government of Western Australia
Mark P. Simmons: Colorado State University
André O. Simões: Universidade Estadual de Campinas
Ana Rita G. Simões: Royal Botanic Gardens, Kew
Michelle Siros: Royal Botanic Gardens, Kew
Eric C. Smidt: Universidade Federal do Paraná
James F. Smith: Boise State University
Neil Snow: Pittsburg State University
Douglas E. Soltis: University of Florida
Pamela S. Soltis: University of Florida
Robert J. Soreng: Smithsonian Institution
Cynthia A. Sothers: Royal Botanic Gardens, Kew
Julian R. Starr: University of Ottawa
Peter F. Stevens: Missouri Botanical Garden
Shannon C. K. Straub: Hobart and William Smith Colleges
Lena Struwe: Rutgers University
Jennifer M. Taylor: CSIRO
Ian R. H. Telford: University of New England
Andrew H. Thornhill: University of New England
Ifeanna Tooth: Botanic Gardens of Sydney
Anna Trias-Blasi: Royal Botanic Gardens, Kew
Frank Udovicic: Royal Botanic Gardens Victoria
Timothy M. A. Utteridge: Royal Botanic Gardens, Kew
Jose C. Valle: Universidad de Sevilla
G. Anthony Verboom: University of Cape Town
Helen P. Vonow: Botanic Gardens and State Herbarium
Maria S. Vorontsova: Royal Botanic Gardens, Kew
Jurriaan M. Vos: University of Basel
Noor Al-Wattar: Royal Botanic Gardens, Kew
Michelle Waycott: Botanic Gardens and State Herbarium
Cassiano A. D. Welker: Universidade Federal de Uberlândia
Adam J. White: CSIRO
Jan J. Wieringa: Naturalis Biodiversity Center
Luis T. Williamson: The University of Adelaide, North Terrace Campus
Trevor C. Wilson: Botanic Gardens of Sydney
Sin Yeng Wong: Universiti Malaysia Sarawak
Lisa A. Woods: Botanic Gardens of Sydney
Roseina Woods: Royal Botanic Gardens, Kew
Stuart Worboys: James Cook University
Martin Xanthos: Royal Botanic Gardens, Kew
Ya Yang: University of Minnesota-Twin Cities
Yu-Xiao Zhang: Southwest Forestry University
Meng-Yuan Zhou: Chinese Academy of Sciences
Sue Zmarzty: Royal Botanic Gardens, Kew
Fernando O. Zuloaga: Instituto de Botánica Darwinion
Alexandre Antonelli: Royal Botanic Gardens, Kew
Sidonie Bellot: Royal Botanic Gardens, Kew
Darren M. Crayn: James Cook University
Olwen M. Grace: Royal Botanic Gardens, Kew
Paul J. Kersey: Royal Botanic Gardens, Kew
Ilia J. Leitch: Royal Botanic Gardens, Kew
Hervé Sauquet: Botanic Gardens of Sydney
Stephen A. Smith: University of Michigan
Wolf L. Eiserhardt: Royal Botanic Gardens, Kew
Félix Forest: Royal Botanic Gardens, Kew
William J. Baker: Royal Botanic Gardens, Kew

Nature, 2024, vol. 629, issue 8013, 843-850

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41586-024-07324-0

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