open access publication

Article, 2024

Phylogenomics and the rise of the angiosperms

Nature, ISSN 0028-0836, 1476-4687, Volume 629, 8013, Pages 843-850, 10.1038/s41586-024-07324-0

Contributors

Zuntini, Alexandre Rizzo 0000-0003-0705-8902 [1] Carruthers, Tom [1] Maurin, Olivier 0000-0002-4151-6164 [1] Bailey, Paul C. [1] Leempoel, Kevin 0000-0001-7335-7930 [1] Brewer, Grace E [1] Epitawalage, Niroshini [1] Françoso, Elaine Aparecida 0000-0002-6464-1240 [1] [2] Gallego-Paramo, Berta [1] Mcginnie, Catherine [1] Negrão, Raquel 0000-0002-4758-8038 [1] Roy, Shyamali R. [1] Simpson, Lalita [3] Toledo Romero, Eduardo [1] Barber, Vanessa M A [1] Botigué, Laura R 0000-0001-7114-5168 [4] Clarkson, James J [1] Cowan, Robyn S [1] Dodsworth, Steven 0000-0001-6531-3540 [5] Johnson, Matthew G. [6] Kim, Jan T. [7] Pokorny, Lisa 0000-0002-2478-8555 [1] [8] Wickett, Norman J 0000-0003-0944-1956 [9] Antar, Guilherme Medeiros 0000-0001-8109-4544 [10] [11] DeBolt, Lucinda [12] Gutierrez, Karime 0000-0002-1748-8108 [12] Hendriks, Kasper P 0000-0003-0245-8368 [13] [14] Hoewener, Alina [15] Hu, Ai-Qun 0000-0001-9564-878X [1] Joyce, Elizabeth Marie 0000-0001-8291-8058 [3] [16] Kikuchi, Izai Alberto Bruno Sabino [17] Larridon, Isabel 0000-0003-0285-722X [1] Larson, Drew A. [18] De Lírio, Elton John 0000-0002-9986-9640 [11] Liu, Jing-Xia [19] Malakasi, Panagiota [1] Przelomska, Natalia A S 0000-0001-9207-4565 [1] [5] Shah, Toral [1] Viruel, Juan 0000-0001-5658-8411 [1] Allnutt, Theodore Richard [20] Ameka, Gabriel Komla 0000-0001-6659-9982 [21] Andrew, Rose L 0000-0003-0099-8336 [22] Appelhans, Marc Sebastian [23] Arista, Montserrat 0000-0003-0914-9525 [24] Ariza, María Jesús [24] Arroyo, Juan [24] Arthan, Watchara 0000-0002-6941-2199 [1] Bachelier, Julien B 0000-0001-9472-1615 [25] Bailey, C Donovan [26] Barnes, Helen F. [20] Barrett, Matthew D. [3] Barrett, Russell Lindsay 0000-0003-0360-8321 [27] Bayer, Randall J 0000-0002-7827-5886 [28] Bayly, Michael J. [29] Biffin, Edward 0000-0002-6582-716X [30] Biggs, Nicky [1] Birch, Joanne L. [29] Bogarín, Diego 0000-0002-8408-8841 [14] [31] Borosova, Renata 0000-0002-3691-5005 [1] Bowles, Alexander M C 0000-0002-7487-3811 [32] Boyce, Peter C. [33] Bramley, Gemma L C 0000-0003-0893-6789 [1] Briggs, Marie [1] Broadhurst, Linda M 0000-0002-9853-3328 [34] Brown, Gillian K. [35] Bruhl, Jeremy James 0000-0001-9112-4436 [22] Bruneau, Anne [36] Buerki, Sven 0000-0002-8299-6539 [37] Burns, Edie [1] Byrne, Margaret [38] Cable, Stuart [1] Calladine, Ainsley 0000-0003-4724-8110 [30] Callmander, Martin W [39] Cano, Ángela [40] Cantrill, David J. [20] Cardinal-Mcteague, Warren M 0000-0003-3558-9794 [17] Carlsen, Mónica M [41] Carruthers, Abigail J. A. [1] de Castro Mateo, Alejandra [24] Chase, Mark W 0000-0002-9927-4938 [1] [42] Chatrou, Lars Willem 0000-0003-0131-0302 [43] Cheek, Martin [1] Chen, Shilin [44] [45] Christenhusz, Maarten J M 0000-0003-1398-8743 [1] [42] [46] Christin, Pascal-Antoine-John-Luc 0000-0001-6292-8734 [47] Clements, Mark A [34] Coffey, Skye C. [38] Conran, John Godfrey [48] Cornejo, Xavier [49] Couvreur, Thomas L P 0000-0002-8509-6587 [50] Cowie, Ian D [51] Csiba, Laszlo [1] Darbyshire, Iain A [1] Davidse, Gerrit [41] Davies, Nina M J [1] Davis, Aaron P. [1] Van Dijk, Kor-Jent 0000-0002-6521-2843 [48] Downie, Stephen R. [52] Duretto, Marco Fillipo 0000-0003-1013-4291 [27] Duvall, Melvin R R [53] Edwards, Sara L. [1] Eggli, Urs 0000-0002-8842-8188 [54] Erkens, Roy H J 0000-0002-1093-0370 [14] [55] Escudero, Marcial 0000-0002-2541-5427 [24] De La Estrella, Manuel 0000-0002-4484-3566 [56] Fabriani, Federico [43] Fay, Michael F 0000-0003-3491-9093 [1] Ferreira, Paola De Lima [11] [57] Ficinski, Sarah Z [1] Fowler, Rachael M. [29] Frisby, Sue [1] Fu, Lin [58] Fulcher, Tim K [1] Galbany-Casals, Mercè 0000-0002-7267-3330 [59] Gardner, Elliot M. [60] German, Dmitry A 0000-0001-7951-1644 [61] Giaretta, Augusto 0000-0002-8263-9806 [62] Gibernau, Marc [63] Gillespie, Lynn Judith 0000-0003-3129-434X [64] González, Cynthia C [65] Goyder, David J 0000-0002-3449-7313 [1] Graham, Sean W. [17] Grall, Aurélie 0000-0002-1613-4703 [1] Green, Laura [1] Gunn, Bee F 0000-0002-9591-3085 [20] Gutiérrez, Diego Germán 0000-0001-9292-235X [66] Hackel, Jan [1] [67] Haevermans, Thomas 0000-0001-8934-4544 [68] Haigh, Anna L 0000-0003-3435-3501 [1] Hall, Jocelyn C. [69] Hall, Tony [1] Harrison, Melissa J. [3] Hatt, Sebastian A 0000-0003-4887-3508 [1] Hidalgo, Oriane 0000-0002-1547-8627 [70] Hodkinson, Trevor Roland 0000-0003-1384-7270 [71] Holmes, Gareth D. [20] Hopkins, Helen C Fortune [1] Jackson, Christopher J. [20] James, Shelley Anne 0000-0003-1105-1850 [38] Jobson, Richard W. [27] Kadereit, Gudrun 0000-0003-0094-8769 [16] Kahandawala, Imalka M. [1] Kainulainen, Kent 0000-0003-4271-1778 [72] Kato, Masahiro [73] Kellogg, Elizabeth Anne 0000-0003-1671-7447 [74] King, Graham John 0000-0002-5975-6051 [75] Klejevskaja, Beata [76] Klitgaard, Bente Bang 0000-0002-8509-0556 [1] Klopper, Ronell Renett 0000-0002-0948-5038 [77] [78] Knapp, Sandra [79] Koch, Marcus A 0000-0002-1693-6829 [80] Leebens-Mack, James H 0000-0003-4811-2231 [81] Lens, Frederic 0000-0002-5001-0149 [14] Leon, Christine J [1] Léveillé-Bourret, Étienne 0000-0002-0069-0430 [36] Lewis, Gwilym Peter [1] Li, De-Zhu 0000-0002-4990-724X [19] Li, Lan [82] Liede-Schumann, Sigrid 0000-0003-2707-0335 [83] Livshultz, Tatyana [84] Lorence, David Harold 0000-0002-6735-9531 [85] Lu, Meng 0000-0002-2921-1632 [1] Lu-Irving, Patricia [27] Luber, Jaquelini 0000-0002-6662-1710 [86] Lucas, Eve Jane 0000-0002-7603-435X [1] Luján, Manuel [1] Lum, Mabel 0000-0002-4712-0603 [87] Macfarlane, Terry D. [38] Magdalena, Carlos [1] Mansano, Vidal Freitas 0000-0002-7204-0744 [86] Masters, Lizo E 0000-0001-8632-0758 [1] Mayo, Simon Joseph 0000-0002-1969-4984 [1] McColl, Kristina [27] McDonnell, Angela J. [88] McDougall, Andrew E. [48] Mclay, Todd G B 0000-0001-6405-8007 [20] McPherson, Hannah [27] Meneses, Rosa Isela 0000-0001-8779-2757 [89] Merckx, Vincent S F T 0000-0002-3959-8623 [14] Michelangeli, Fabián Armando 0000-0001-7348-143X [90] Mitchell, John D. [90] Monro, Alexandre K 0000-0003-4013-3804 [1] Moore, Michael J. [91] Mueller, Taryn L. [92] Mummenhoff, Klaus 0000-0002-8449-1593 [13] Munzinger, Jérôme [93] Muriel, Priscilla 0000-0002-7874-8057 [94] Murphy, Daniel John 0000-0002-8358-363X [20] Nargar, Katharina 0000-0002-0459-5991 [3] [34] Nauheimer, Lars 0000-0002-2847-0966 [3] Nge, Francis Jason 0000-0002-0361-8709 [30] Nyffeler, Reto 0000-0002-9293-5967 [95] Orejuela, Andrés 0000-0002-3511-1478 [96] [97] Ortiz, Edgardo M 0000-0001-8052-1671 [15] Palazzesi, Luis 0000-0001-8026-4679 [66] Peixoto, Ariane Luna 0000-0003-1959-8543 [86] Pell, Susan K. [98] Pellicer, Jaume 0000-0001-7632-9775 [70] Penneys, Darin S [99] Pérez-Escobar, Oscar Alejandro [1] Persson, Claes [100] Pignal, Marc 0000-0002-6772-9299 [68] Pillon, Yohan 0000-0003-1760-329X [93] Pirani, José R. [11] Plunkett, Gregory M 0000-0002-0751-4309 [90] Powell, Robyn Faye [1] Prance, Ghillean Tolmie 0000-0002-5999-3591 [1] Puglisi, Carmen [1] [41] Qin, Ming [58] Rabeler, Richard K [18] Rees, Paul E. J. [1] Renner, Matthew [27] Roalson, Eric H 0000-0003-1655-3681 [101] Rodda, Michele 0000-0002-4130-6685 [102] Rogers, Zachary S [26] Rokni, Saba [1] Rutishauser, Rolf [95] De Salas, Miguel F [103] Schaefer, Hanno 0000-0001-7231-3987 [15] Schley, Rowan J 0000-0003-1532-5353 [104] Schmidt-Lebuhn, Alexander Nikolai 0000-0002-7402-8941 [34] Shapcott, Alison [105] Al-Shehbaz, Ihsan Ali [41] Shepherd, Kelly A. [38] Simmons, Mark P. [106] Simões, André Olmos 0000-0001-6555-8759 [107] Simões, Ana Rita Giraldes 0000-0001-7267-8353 [1] Siros, Michelle R [1] [108] Smidt, Eric Camargo [109] Smith, James F. [37] Snow, Neil W [110] Soltis, Douglas Edward [111] Soltis, Pamela S 0000-0001-9310-8659 [111] Soreng, Robert John 0000-0002-8358-4915 [112] Sothers, Cynthia A 0000-0002-8052-9590 [1] Starr, Julian R. [113] Stevens, Peter F [41] Straub, Shannon C K [114] Struwe, Lena 0000-0001-6074-5758 [115] Taylor, Jennifer M. [82] Telford, Ian R H 0000-0002-3570-0053 [22] Thornhill, Andrew H 0000-0002-0325-5725 [22] [30] [48] Tooth, Ifeanna [27] Trias-Blasi, Anna 0000-0001-9745-3222 [1] Udovicic, Frank [20] Utteridge, Timothy Michael Arthur 0000-0003-2823-0337 [1] Del Valle, José Carlos 0000-0001-6023-6208 [24] Verboom, George Anthony 0000-0002-1363-9781 [116] Vonow, Helen P. [30] Vorontsova, Maria Sergeevna [1] De Vos, Jurriaan M 0000-0001-6428-7774 [117] Al-Wattar, Noor [1] Waycott, Michelle 0000-0002-0822-0564 [30] [48] Welker, Cassiano Aimberê Dorneles 0000-0001-6347-341X [118] White, Adam J. [119] Wieringa, Jan J 0000-0003-0566-372X [14] Williamson, Luis T. [48] Wilson, Trevor C. [27] Wong, Sin Yeng 0000-0003-4042-9672 [120] Woods, Lisa A. [27] Woods, Roseina [1] Worboys, Stuart 0000-0001-6706-4509 [3] Xanthos, Martin D 0000-0002-5378-8757 [1] Yang, Ya [92] Zhang, Yu-Xiao [121] Zhou, Meng-Yuan [19] Zmarzty, Sue [1] Zuloaga, Fernando Omar 0000-0003-2794-539X [122] Antonelli, Alexandre Marcos 0000-0003-1842-9297 [1] [100] [123] Bellot, Sidonie 0000-0001-6355-237X [1] Crayn, Darren Michael 0000-0001-6614-4216 [3] Grace, Olwen Megan 0000-0003-1431-2761 [1] [97] Kersey, Paul Julian 0000-0002-7054-800X [1] Leitch, Ilia Judith 0000-0002-3837-8186 [1] Sauquet, Hervé 0000-0001-8305-3236 [27] Smith, Stephen Andrew 0000-0003-2035-9531 [18] Eiserhardt, Wolf Lukas Tilmann 0000-0002-8136-5233 [1] [57] Forest, Félix 0000-0002-2004-433X [1] Baker, William J 0000-0001-6727-1831 (Corresponding author) [1] [57]

Affiliations

  1. [1] Royal Botanic Gardens
    2. [NORA names: United Kingdom; Europe, Non-EU; OECD];
  2. [2] Royal Holloway University of London
    3. [NORA names: United Kingdom; Europe, Non-EU; OECD];
  3. [3] James Cook University
    4. [NORA names: Australia; Oceania; OECD];
  4. [4] Center for Research in Agricultural Genomics
    5. [NORA names: Spain; Europe, EU; OECD];
  5. [5] University of Portsmouth
    6. [NORA names: United Kingdom; Europe, Non-EU; OECD];

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.

Keywords

Cenozoic, Cenozoic era, Mesozoic, Mesozoic era, analysis, angiosperm diversification, angiosperm evolution, angiosperm genera, angiosperm orders, angiosperm tree of life, angiosperm trees, angiosperms, clade, classification, complex, confidence, conflict, critical test, decreasing global temperatures, deep history, diversification, dominance, ecological dominance, ecosystem, era, evolution, explosive diversification, fossils, foundational work, gene tree conflict, genes, genome, genus, global temperature, group, history, increase, life, megadiverse clades, method, order, phylogenomic methods, phylogenomics, plastid, rate, relationship, results, rosids, samples, sets, standard setting, steady diversification, studies9, study, taxa, temperature, terrestrial ecosystems, test, tree conflict, tree of life, trees, work

Funders

  • Directorate for Biological Sciences
  • Chinese Academy of Agricultural Sciences
  • Biotechnology and Biological Sciences Research Council
  • Chinese Academy of Sciences
  • The Velux Foundations

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