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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 de 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 de 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 van Dijk, Stephen R. Downie, Marco F. Duretto, Melvin R. Duvall, Sara L. Edwards, Urs Eggli, Roy H.J. Erkens, Marcial Escudero, Manuel de la 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, De Zhu Li, 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. de 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. Del Valle, G. Anthony Verboom, Helen P. Vonow, Maria S. Vorontsova, Jurriaan M. de 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, William J. Baker*
*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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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.

Original languageEnglish
Pages (from-to)843-850
Number of pages8
JournalNature
Volume629
Issue number8013
DOIs
StatePublished - 23 May 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

Funding

The PAFTOL project was funded by grants from the Calleva Foundation to the Royal Botanic Gardens, Kew. Data were also contributed by the Genomics for Australian Plants Framework Initiative consortium funded by Bioplatforms Australia (enabled by the National Collaborative Research Infrastructure Strategy) and partner organizations. The work was further supported by research grants from VILLUM FONDEN (grant no. 00025354) and the Aarhus University Research Foundation (grant no. AUFF-E-2017-7-19) to W.L.E. and from grant nos NSF DBI 1930030 and DEB 1917146 to S.A.S. Computational resources and technical support were provided by the Research/Scientific Computing teams at The James Hutton Institute and the National Institute of Agricultural Botany (NIAB) through the ‘UK’s Crop Diversity Bioinformatics HPC’ (BBSRC grant no. BB/S019669/1). The following provided technical assistance to the project at various stages: O. Berry, N. Black, M. Corcoran, S. Dequiret, I. Fairlie, L. Frankel, T. Freeth, A. Gilbert, B. Lepschi, D. Lewis, L. May, A. McArdle, E. O’Loughlin, S. Phillips, T. Sarkinen, L. Simmons, N. Walsh and M.-H. Weech. We thank all institutions who made their biological collections available and the many botanists and co-workers in the field who have collected, identified and curated the specimens used in this project. Specifically, we thank the following herbaria and their staff for providing samples for genomic analysis and/or for housing voucher specimens associated with analysed samples: A, ABH, AD, ALTB, APSC, B, BA, BC, BCN, BCRU, BG, BH, BHCB, BISH, BJFC, BKF, BM, BNRH, BOL, BONN, BR, BRI, BRIT, BRLU, BRUN, C, CAN, CANB, CAS, CBG, CNS, COL, CONC, CORD, CS, CTES, CUVC, DNA, E, EA, F, FI, FLAS, FMB, FTG, G, GB, GC, GENT, GH, GOET, GUAY, GZU, HAW, HEID, HITBC, HNG, HO, HPUJ, HRCB, HTW, HUA, HUAL, HUAZ, HUB, HUEFS, HUFU, IBSC, IBUG, ICN, IEB, INB, INPA, JBB, JBL, JRAU, K, KAS, KLU, KRB, KUN, L, LE, LISC, LP, LPB, LYJB, M, MA, MAU, MBA, MBML, MEDEL, MEL, MELU, MHA, MICH, MIN, MJG, MO, MSUN, MT, MY, N, NBG, NCU, NCY, NE, NH, NHM, NHMR, NMNL, NOU, NSW, NU, NY, OS, OSBU, P, PERTH, PG, PH, PRE, PTBG, QBG, QCA, QRS, RB, REU, S, SALA, SAR, SEV, SGO, SI, SING, SP, SPF, SPFR, SUVA, TCD, TEX, TNS, TUH, TUM, U, UAPC, UB, UBT, UDW, UEC, UPCB, UPR, UPS, UPTC, US, USM, W, WAG, WS, WTU, YA and ZSS; acronyms follow Index Herbariorum ( https://sweetgum.nybg.org/science/ih/ ). We also thank the Millennium Seed Bank Partnership for supporting access to samples. We acknowledge all national, state and regional authorities who authorized and facilitated the sourcing of these specimens. See also extended acknowledgements in the .

FundersFunder number
National Institute of Agricultural Botany
The James Hutton Institute
DEB 1917146, DBI 1930030
AUFF-E-2017-7-19
1930030
00025354
BB/S019669/1

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