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 A.R. 0000-0003-0705-8902 [1] Carruthers T. [1] Maurin O. 0000-0002-4151-6164 [1] Bailey P. 0000-0002-4650-9668 [1] Leempoel K. 0000-0001-7335-7930 [1] Brewer G. [1] Epitawalage N. [1] Francoso E. 0000-0002-6464-1240 [1] [2] Gallego-Paramo B. 0000-0002-2016-7161 [1] McGinnie C. [1] Negrao R. 0000-0002-4758-8038 [1] Roy S. [1] Simpson L. Toledo Romero E. [1] Barber V. [1] Botigue L.R. 0000-0001-7114-5168 [3] Clarkson J.J. [1] Cowan R.S. [1] Dodsworth S. 0000-0001-6531-3540 [4] Johnson M.G. 0000-0002-1958-6334 [5] Kim J.T. [6] Pokorny L. 0000-0002-2478-8555 [1] [7] Wickett N.J. 0000-0003-0944-1956 [8] Antar G.M. 0000-0001-8109-4544 [9] [10] DeBolt L. [11] Gutierrez K. [11] Hendriks K.P. 0000-0003-0245-8368 [12] [13] Hoewener A. 0009-0001-6938-9312 [14] Hu A.-Q. 0000-0001-9564-878X [1] Joyce E.M. 0000-0001-8291-8058 [15] Kikuchi I.A.B.S. 0000-0002-0258-1537 [16] Larridon I. 0000-0003-0285-722X [1] Larson D.A. 0000-0002-7557-9999 [17] de Lirio E.J. 0000-0002-9986-9640 [10] Liu J.-X. [18] Malakasi P. [1] Przelomska N.A.S. 0000-0001-9207-4565 [1] [4] Shah T. [1] Viruel J. 0000-0001-5658-8411 [1] Allnutt T.R. 0000-0002-8258-0058 [19] Ameka G.K. 0000-0001-6659-9982 [20] Andrew R.L. 0000-0003-0099-8336 [21] Appelhans M.S. [22] Arista M. 0000-0003-0914-9525 [23] Ariza M.J. [23] Arroyo J. [23] Arthan W. 0000-0002-6941-2199 [1] Bachelier J.B. [24] Bailey C.D. [25] Barnes H.F. [19] Barrett M.D. 0000-0002-2926-4291 Barrett R.L. 0000-0003-0360-8321 Bayer R.J. 0000-0002-7827-5886 Bayly M.J. 0000-0001-6836-5493 [26] Biffin E. 0000-0002-6582-716X [27] Biggs N. [1] Birch J.L. 0000-0002-8226-6085 [26] Bogarin D. 0000-0002-8408-8841 [13] [28] Borosova R. 0000-0002-3691-5005 [1] Bowles A.M.C. 0000-0002-7487-3811 [29] Boyce P.C. [30] Bramley G.L.C. [1] Briggs M. 0000-0003-2988-0032 [1] Broadhurst L. 0000-0002-9853-3328 [31] Brown G. [32] Bruhl J.J. [21] Bruneau A. 0000-0001-5547-0796 [33] Buerki S. 0000-0002-8299-6539 [34] Burns E. [1] Byrne M. 0000-0002-7197-5409 [35] Cable S. [1] Calladine A. 0000-0003-4724-8110 [27] Callmander M.W. 0000-0003-3641-112X Cano A. 0000-0002-5090-7730 [36] Cantrill D. 0000-0002-1185-4015 [19] Cardinal-McTeague W.M. 0000-0003-3558-9794 [16] Carlsen M.M. 0000-0002-1663-0475 [37] Carruthers A.J.A. 0000-0003-2586-9733 [1] de Castro Mateo A. [23] Chase M.W. 0000-0002-9927-4938 [1] [38] Chatrou L.W. 0000-0003-0131-0302 [39] Cheek M. [1] Chen S. 0000-0002-0449-236X [40] [41] Christenhusz M.J.M. 0000-0003-1398-8743 [1] [38] Christin P.-A. 0000-0001-6292-8734 [42] Clements M.A. [31] Coffey S.C. 0000-0001-8211-5546 [43] Conran J. 0000-0003-2268-2703 [44] Cornejo X. [45] Couvreur T.L.P. 0000-0002-8509-6587 [46] Cowie I.D. Csiba L. [1] Darbyshire I. 0000-0002-5514-9561 [1] Davidse G. [37] Davies N.M.J. 0009-0007-0395-6250 [1] Davis A.P. 0000-0001-9213-4353 [1] van Dijk K.-J. 0000-0002-6521-2843 [44] Downie S.R. 0000-0002-4772-0625 [47] Duretto M.F. 0000-0003-1013-4291 Duvall M.R. [48] Edwards S.L. [1] Eggli U. 0000-0002-8842-8188 Erkens R.H.J. 0000-0002-1093-0370 [13] [49] Escudero M. 0000-0002-2541-5427 [23] de la Estrella M. 0000-0002-4484-3566 [50] Fabriani F. 0000-0002-5844-7484 [39] Fay M.F. 0000-0003-3491-9093 [1] de Lima Ferreira P. 0000-0002-6957-4243 [10] [51] Ficinski S.Z. [1] Fowler R.M. 0000-0002-8953-7036 [26] Frisby S. [1] Fu L. 0000-0003-4933-221X [52] Fulcher T. [1] Galbany-Casals M. 0000-0002-7267-3330 [53] Gardner E.M. 0000-0003-1133-5167 [54] German D.A. 0000-0001-7951-1644 [55] Giaretta A. [56] Gibernau M. 0000-0003-3866-3099 [57] Gillespie L.J. 0000-0003-3129-434X [58] Gonzalez C.C. 0009-0003-3797-1249 [59] Goyder D. 0000-0002-3449-7313 [1] Graham S.W. 0000-0001-8209-5231 [16] Grall A. [1] Green L. 0000-0003-0774-9498 [1] Gunn B.F. 0000-0002-9591-3085 [19] Gutierrez D.G. [60] Hackel J. 0000-0002-9657-5372 [1] [61] Haevermans T. 0000-0001-8934-4544 [62] Haigh A. 0000-0003-3435-3501 [1] Hall J.C. 0000-0002-5279-4346 [63] Hall T. [1] Harrison M.J. Hatt S.A. [1] Hidalgo O. 0000-0002-1547-8627 [64] Hodkinson T.R. 0000-0003-1384-7270 [65] Holmes G.D. 0000-0003-1120-8731 [19] Hopkins H.C.F. 0000-0003-4984-8224 [1] Jackson C.J. [19] James S.A. 0000-0003-1105-1850 [43] Jobson R.W. 0000-0002-1822-9634 Kadereit G. [66] Kahandawala I.M. [1] Kainulainen K. 0000-0003-4271-1778 [67] Kato M. 0000-0001-7752-2745 [68] Kellogg E.A. 0000-0003-1671-7447 [69] King G.J. 0000-0002-5975-6051 [70] Klejevskaja B. Klitgaard B. 0000-0002-8509-0556 [1] Klopper R.R. 0000-0002-0948-5038 [71] [72] Knapp S. 0000-0001-7698-3945 [73] Koch M.A. 0000-0002-1693-6829 [74] Leebens-Mack J.H. 0000-0003-4811-2231 [75] Lens F. 0000-0002-5001-0149 [13] Leon C.J. [1] Leveille-Bourret E. 0000-0002-0069-0430 [33] Lewis G.P. 0000-0003-2599-4577 [1] Li D.-Z. 0000-0002-4990-724X [18] Li L. [31] Liede-Schumann S. 0000-0003-2707-0335 [76] Livshultz T. 0009-0000-7244-5955 [77] Lorence D. [78] Lu M. 0000-0002-2921-1632 [1] Lu-Irving P. 0000-0003-1116-9402 Luber J. [79] Lucas E.J. 0000-0002-7603-435X [1] Lujan M. [1] Lum M. 0000-0002-4712-0603 Macfarlane T.D. 0000-0002-7023-9231 [43] Magdalena C. [1] Mansano V.F. [79] Masters L.E. 0000-0001-8632-0758 [1] Mayo S.J. [1] McColl K. McDonnell A.J. 0000-0002-2549-9253 [80] McDougall A.E. 0000-0001-7713-2800 [44] McLay T.G.B. 0000-0001-6405-8007 [19] McPherson H. 0000-0003-0254-4573 Meneses R.I. 0000-0001-8779-2757 [81] Merckx V.S.F.T. 0000-0002-3959-8623 [13] Michelangeli F.A. 0000-0001-7348-143X [82] Mitchell J.D. [82] Monro A.K. 0000-0003-4013-3804 [1] Moore M.J. 0000-0003-2222-8332 [83] Mueller T.L. 0000-0003-3148-4776 [84] Mummenhoff K. 0000-0002-8449-1593 [12] Munzinger J. 0000-0001-5300-2702 [85] Muriel P. 0000-0002-7874-8057 [86] Murphy D.J. 0000-0002-8358-363X [19] Nargar K. 0000-0002-0459-5991 [31] Nauheimer L. 0000-0002-2847-0966 Nge F.J. 0000-0002-0361-8709 [27] Nyffeler R. 0000-0002-9293-5967 [87] Orejuela A. 0000-0002-3511-1478 [88] Ortiz E.M. 0000-0001-8052-1671 [14] Palazzesi L. 0000-0001-8026-4679 [60] Peixoto A.L. [79] Pell S.K. 0000-0002-7214-3225 Pellicer J. 0000-0001-7632-9775 [64] Penneys D.S. 0000-0003-0727-2829 [89] Perez-Escobar O.A. 0000-0001-9166-2410 [1] Persson C. [90] Pignal M. 0000-0002-6772-9299 [62] Pillon Y. 0000-0003-1760-329X [91] Pirani J.R. 0000-0001-7984-4457 [10] Plunkett G.M. 0000-0002-0751-4309 [82] Powell R.F. [1] Prance G.T. [1] Puglisi C. 0000-0003-0304-1812 [1] [37] Qin M. [52] Rabeler R.K. 0000-0002-6765-0353 [17] Rees P.E.J. [1] Renner M.A.M. 0000-0003-2286-7257 Roalson E.H. 0000-0003-1655-3681 [92] Rodda M. 0000-0002-4130-6685 [93] Rogers Z.S. 0000-0003-1136-0960 [25] Rokni S. [1] Rutishauser R. [87] De Salas M. 0000-0002-7148-639X [94] Schaefer H. 0000-0001-7231-3987 [14] Schley R. 0000-0003-1532-5353 [95] Schmidt-Lebuhn A. 0000-0002-7402-8941 [31] Shapcott A. 0000-0003-3734-052X [96] Al-Shehbaz I. [37] Shepherd K.A. 0000-0003-1627-7891 [43] Simmons M.P. [97] Simoes A.O. [98] Simoes A.R.G. 0000-0001-7267-8353 [1] Siros M. 0000-0002-4275-1641 [1] [99] Smidt E.C. 0000-0002-1177-1682 [100] Smith J.F. [34] Snow N. [101] Soltis D.E. 0000-0001-8638-4137 [102] Soltis P.S. 0000-0001-9310-8659 [102] Soreng R.J. 0000-0002-8358-4915 [103] Sothers C.A. 0000-0002-8052-9590 [1] Starr J.R. [104] Stevens P.F. [37] Straub S.C.K. 0000-0001-7506-9043 [105] Struwe L. [106] Taylor J.M. [31] Telford I.R.H. [21] Thornhill A.H. 0000-0002-0325-5725 [21] [27] [44] Tooth I. Trias-Blasi A. [1] Udovicic F. 0000-0003-1697-8444 [19] Utteridge T.M.A. 0000-0003-2823-0337 [1] Del Valle J.C. 0000-0001-6023-6208 [23] Verboom G.A. [107] Vonow H.P. 0000-0002-3507-4101 [27] Vorontsova M.S. 0000-0003-0899-1120 [1] de Vos J.M. 0000-0001-6428-7774 [108] Al-Wattar N. [1] Waycott M. 0000-0002-0822-0564 [27] [44] Welker C.A.D. 0000-0001-6347-341X [109] White A.J. [31] Wieringa J.J. 0000-0003-0566-372X [13] Williamson L.T. 0000-0002-0172-6773 [44] Wilson T.C. 0000-0002-9026-0521 Wong S.Y. 0000-0003-4042-9672 [110] Woods L.A. Woods R. [1] Worboys S. 0000-0001-6706-4509 Xanthos M. [1] Yang Y. 0000-0001-6221-0984 [84] Zhang Y.-X. [111] Zhou M.-Y. 0000-0003-1492-8494 [18] Zmarzty S. [1] Zuloaga F.O. [112] Antonelli A. 0000-0003-1842-9297 [1] [90] [113] Bellot S. 0000-0001-6355-237X [1] Crayn D.M. 0000-0001-6614-4216 Grace O.M. 0000-0003-1431-2761 [1] [88] Kersey P.J. 0000-0002-7054-800X [1] Leitch I.J. 0000-0002-3837-8186 [1] Sauquet H. 0000-0001-8305-3236 Smith S.A. 0000-0003-2035-9531 [17] Eiserhardt W.L. 0000-0002-8136-5233 [1] [51] Forest F. 0000-0002-2004-433X [1] Baker W.J. 0000-0001-6727-1831 (Corresponding author) [1] [51]

Affiliations

  1. [1] Royal Botanic Gardens
    2. [NORA names: United Kingdom; Europe, Non-EU; OECD];
  2. [2] Department of Physics
    3. [NORA names: United Kingdom; Europe, Non-EU; OECD];
  3. [3] Centre for Research in Agricultural Genomics (CRAG)
    4. [NORA names: Spain; Europe, EU; OECD];
  4. [4] University of Portsmouth
    5. [NORA names: United Kingdom; Europe, Non-EU; OECD];
  5. [5] Texas Tech University
    6. [NORA names: United States; America, North; OECD];

Abstract

Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods. 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 genome. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins. 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 genes. This 15-fold increase in genus-level sampling relative to comparable nuclear studies 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.

Funders

  • Bioplatforms Australia
  • Villum Fonden
  • Calleva Foundation
  • Biotechnology and Biological Sciences Research Council
  • Aarhus Universitets Forskningsfond
  • James Hutton Institute
  • Neurosciences Foundation
  • National Institute of Agricultural Botany

Data Provider: Elsevier

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