Phylogenomics and the rise of the angiosperms

Zuntini, A.R. and Carruthers, T. and Maurin, O. and Bailey, P.C. and Leempoel, K. and Brewer, G.E. and Epitawalage, N. and Françoso, E. and Gallego-Paramo, B. and McGinnie, C. and Negrão, R. and Roy, S.R. and Simpson, L. and Toledo Romero, E. and Barber, V.M.A. and Botigué, L. and Clarkson, J.J. and Cowan, R.S. and Dodsworth, Steven and Johnson, M.G. and Kim, J.T. and Pokorny, L. and Wickett, N.J. and Antar, G.M. and DeBolt, L. and Gutierrez, K. and Hendriks, K.P. and Hoewener, A. and Hu, A.-Q. and Joyce, E.M. and Kikuchi, I.A.B.S. and Larridon, I. and Larson, D.A. and de Lírio, E.J. and Liu, J.-X. and Malakasi, P. and Przelomska, N.A.S. and Shah, T. and Viruel, J. and Allnutt, T.R. and Ameka, G.K. and Andrew, R.L. and Appelhans, M.S. and Arista, M. and Ariza, M.J. and Arroyo, J. and Arthan, W. and Bachelier, J.B. and Bailey, C.D. and Barnes, H.F. and Barrett, M.D. and Barrett, R.L. and Bayer, R.J. and Bayly, M.J. and Biffin, E. and Biggs, N. and Birch, J.L. and Bogarín, D. and Borosova, R. and Bowles, A.M.C. and Boyce, P.C. and Bramley, G.L.C. and Briggs, M. and Broadhurst, L. and Brown, G.K. and Bruhl, J.J. and Bruneau, A. and Buerki, S. and Burns, E. and Byrne, M. and Cable, S. and Calladine, A. and Callmander, M.W. and Cano, Á. and Cantrill, D.J. and Cardinal-McTeague, W.M. and Carlsen, M.M. and Carruthers, A.J.A. and de Castro Mateo, A. and Chase, M.W. and Chatrou, L.W. and Cheek, M. and Chen, S. and Christenhusz, M.J.M. and Christin, P.-A. and Clements, M.A. and Coffey, S.C. and Conran, J.G. and Cornejo, X. and Couvreur, T.L.P. and Cowie, I.D. and Csiba, L. and Darbyshire, I. and Davidse, G. and Davies, N.M.J. and Davis, A.P. and van Dijk, K.-j. and Downie, S.R. and Duretto, M.F. and Duvall, M.R. and Edwards, S.L. and Eggli, U. and Erkens, R.H.J. and Escudero, M. and de la Estrella, M. and Fabriani, F. and Fay, M.F. and Ferreira, P. de L. and Ficinski, S.Z. and Fowler, R.M. and Frisby, S. and Fu, L. and Fulcher, T. and Galbany-Casals, M. and Gardner, E.M. and German, D.A. and Giaretta, A. and Gibernau, M. and Gillespie, L.J. and González, C.C. and Goyder, D. J. and Graham, S.W. and Grall, A. and Green, L. and Gunn, B.F. and Gutiérrez, D.G. and Hackel, J. and Haevermans, T. and Haigh, A. and Hall, J.C. and Hall, T. and Harrison, M.J. and Hatt, S.A. and Hidalgo, O. and Hodkinson, T.R. and Holmes, G.D. and Hopkins, H.C.F. and Jackson, C.J. and James, S.A. and Jobson, R.W. and Kadereit, G. and Kahandawala, I.M. and Kainulainen, K. and Kato, M. and Kellogg, E.A. and King, G.J. and Klejevskaja, B. and Klitgaard, B.B. and Klopper, R.R. and Knapp, S. and Koch, M.A. and Leebens-Mack, J.H. and Lens, F. and Leon, C.J. and Léveillé-Bourret, É. and Lewis, G.P. and Li, De-Z. and Li, L. and Liede-Schumann, S. and Livshultz, T. and Lorence, D. and Lu, M. and Lu-Irving, P. and Luber, J. and Lucas, E.J. and Luján, M. and Lum, M. and Macfarlane, T.D. and Magdalena, C. and Mansano, V.F. and Masters, L.E. and Mayo, S.J. and McColl, K. and McDonnell, A.J. and McDougall, A.E. and McLay, T.G.B. and McPherson, H. and Meneses, R.I. and Merckx, V.S.F.T. and Michelangeli, F.A. and Mitchell, J.D. and Monro, A.K. and Moore, M.J. and Mueller, T.L. and Mummenhoff, K. and Munzinger, J. and Muriel, P. and Murphy, D.J. and Nargar, K. and Nauheimer, L. and Nge, F.J. and Nyffeler, R. and Orejuela, A. and Ortiz, E.M. and Palazzesi, L. and Peixoto, A.L. and Pell, S.K. and Pellicer, J. and Penneys, D.S. and Perez-Escobar, O.A. and Persson, C. and Pignal, M. and Pillon, Y. and Pirani, J.R. and Plunkett, G.M. and Powell, R.F. and Prance, G.T. and Puglisi, C. and Qin, M. and Rabeler, R.K. and Rees, P.E.J. and Renner, M. and Roalson, E.H. and Rodda, M. and Rogers, Z.S. and Rokni, S. and Rutishauser, R. and de Salas, M.F. and Schaefer, H. and Schley, R.J. and Schmidt-Lebuhn, A. and Shapcott, A. and Al-Shehbaz, I. and Shepherd, K.A. and Simmons, M.P. and Simões, A.O. and Simões, A.R.G. and Siros, M. and Smidt, E.C. and Smith, J.F. and Snow, N. and Soltis, D.E. and Soltis, P.S. and Soreng, R. J. and Sothers, C.A. and Starr, J.R. and Stevens, P.F. and Straub, S.C.K. and Struwe, L. and Taylor, J.M. and Telford, I.R.H. and Thornhill, A.H. and Tooth, I. and Trias-Blasi, A. and Udovicic, F. and Utteridge, T.M.A. and Del Valle, J.C. and Verboom, G.A. and Vonow, H.P. and Vorontsova, M.S. and de Vos, J.M. and Al-Wattar, N. and Waycott, M. and Welker, C.A.D. and White, A.J. and Wieringa, J.J. and Williamson, L.T. and Wilson, T.C. and Wong, S. Y. and Woods, L.A. and Woods, R. and Worboys, S. and Xanthos, M. and Yang, Y. and Zhang, Y.-X. and Zhou, M.-Y. and Zmarzty, S. and Zuloaga, F.O. and Antonelli, A. and Bellot, S. and Crayn, D.M. and Grace, O.M. and Kersey, P.J. and Leitch, Ilia J. and Sauquet, H. and Smith, S.A. and Eiserhardt, W.L. and Forest, F. and Baker, W.J. (2024) Phylogenomics and the rise of the angiosperms. Nature 629 (8013), pp. 843-850. ISSN 0028-0836.

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 origins5,6,7. 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.

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