Phylogenomics and the rise of the angiosperms

Alexandre Zuntini (1) , Tom Carruthers (1) , Olivier Maurin (1) , Paul Bailey (1) , Kevin Leempoel (1) , Grace Brewer (1) , Niroshini Epitawalage (1) , Elaine Françoso , Berta Gallego-Paramo , Catherine Mcginnie , Raquel Negrão , Shyamali Roy , Lalita Simpson , Eduardo Toledo Romero , Vanessa Barber , Laura Botigué , James Clarkson , Robyn Cowan , Steven Dodsworth , Matthew Johnson , Jan Kim , Lisa Pokorny , Norman Wickett , Guilherme Antar , Lucinda Debolt , Karime Gutierrez , Kasper Hendriks , Alina Hoewener , Ai-Qun Hu , Elizabeth Joyce , Izai Kikuchi , Isabel Larridon , Drew Larson , Elton John de Lírio , Jing-Xia Liu , Panagiota Malakasi , Natalia Przelomska , Toral Shah , Juan Viruel , Theodore Allnutt , Gabriel Ameka , Rose Andrew , Marc Appelhans , Montserrat Arista , María Jesús Ariza , Juan Arroyo , Watchara Arthan , Julien Bachelier , C. Donovan Bailey , Helen Barnes , Matthew Barrett , Russell Barrett , Randall Bayer , Michael Bayly , Ed Biffin , Nicky Biggs , Joanne Birch , Diego Bogarín , Renata Borosova , Alexander Bowles , Peter Boyce , Gemma Bramley , Marie Briggs , Linda Broadhurst , Gillian Brown , Jeremy Bruhl , Anne Bruneau , Sven Buerki , Edie Burns , Margaret Byrne , Stuart Cable , Ainsley Calladine , Martin Callmander , Ángela Cano , David Cantrill , Warren Cardinal-Mcteague , Mónica Carlsen , Abigail Carruthers , Alejandra de Castro Mateo , Mark Chase , Lars Chatrou , Martin Cheek , Shilin Chen , Maarten Christenhusz , Pascal-Antoine Christin , Mark Clements , Skye Coffey , John Conran , Xavier Cornejo , Thomas Couvreur , Ian Cowie , Laszlo Csiba , Iain Darbyshire , Gerrit Davidse , Nina Davies , Aaron Davis , Kor-Jent van Dijk , Stephen Downie , Marco Duretto , Melvin Duvall , Sara Edwards , Urs Eggli , Roy Erkens , Marcial Escudero , Manuel de la Estrella , Federico Fabriani , Michael Fay , Paola de L. Ferreira , Sarah Ficinski , Rachael Fowler , Sue Frisby , Lin Fu , Tim Fulcher , Mercè Galbany-Casals , Elliot Gardner , Dmitry German , Augusto Giaretta , Marc Gibernau , Lynn Gillespie , Cynthia González , David Goyder , Sean Graham , Aurélie Grall , Laura Green , Bee Gunn , Diego Gutiérrez , Jan Hackel , Thomas Haevermans (2) , Anna Haigh , Jocelyn Hall , Tony Hall , Melissa Harrison , Sebastian Hatt , Oriane Hidalgo , Trevor Hodkinson , Gareth Holmes , Helen Hopkins , Christopher Jackson , Shelley James , Richard Jobson , Gudrun Kadereit , Imalka Kahandawala , Kent Kainulainen , Masahiro Kato , Elizabeth Kellogg , Graham King , Beata Klejevskaja , Bente Klitgaard , Ronell Klopper , Sandra Knapp , Marcus Koch , James Leebens-Mack , Frederic Lens , Christine Leon , Étienne Léveillé-Bourret , Gwilym Lewis , De-Zhu Li , Lan Li , Sigrid Liede-Schumann , Tatyana Livshultz , David Lorence , Meng Lu , Patricia Lu-Irving , Jaquelini Luber , Eve Lucas , Manuel Luján , Mabel Lum , Terry Macfarlane , Carlos Magdalena , Vidal Mansano , Lizo Masters , Simon Mayo , Kristina Mccoll , Angela Mcdonnell , Andrew Mcdougall , Todd Mclay , Hannah Mcpherson , Rosa Meneses , Vincent Merckx , Fabián Michelangeli , John Mitchell , Alexandre Monro , Michael Moore , Taryn Mueller , Klaus Mummenhoff , Jérôme Munzinger (3) , Priscilla Muriel , Daniel Murphy , Katharina Nargar , Lars Nauheimer , Francis Nge , Reto Nyffeler , Andrés Orejuela , Edgardo Ortiz , Luis Palazzesi , Ariane Luna Peixoto , Susan Pell , Jaume Pellicer , Darin Penneys , Oscar Perez-Escobar , Claes Persson , Marc Pignal (2) , Yohan Pillon (4, 5) , José Pirani , Gregory Plunkett , Robyn Powell , Ghillean Prance , Carmen Puglisi , Ming Qin , Richard Rabeler , Paul Rees , Matthew Renner , Eric Roalson , Michele Rodda , Zachary Rogers , Saba Rokni , Rolf Rutishauser , Miguel de Salas , Hanno Schaefer , Rowan Schley , Alexander Schmidt-Lebuhn , Alison Shapcott , Ihsan Al-Shehbaz , Kelly Shepherd , Mark Simmons , André Simões , Ana Rita G. Simões , Michelle Siros , Eric Smidt , James Smith , Neil Snow , Douglas Soltis , Pamela Soltis , Robert Soreng , Cynthia Sothers , Julian Starr , Peter Stevens , Shannon Straub , Lena Struwe , Jennifer Taylor , Ian Telford , Andrew Thornhill , Ifeanna Tooth , Anna Trias-Blasi , Frank Udovicic , Timothy Utteridge , Jose del Valle , G. Anthony Verboom , Helen Vonow , Maria Vorontsova , Jurriaan de Vos , Noor Al-Wattar , Michelle Waycott , Cassiano Welker , Adam White , Jan Wieringa , Luis Williamson , Trevor Wilson , Sin Yeng Wong , Lisa Woods , Roseina Woods , Stuart Worboys , Martin Xanthos , Ya Yang , Yu-Xiao Zhang , Meng-Yuan Zhou , Sue Zmarzty , Fernando Zuloaga , Alexandre Antonelli , Sidonie Bellot , Darren Crayn , Olwen Grace , Paul Kersey , Ilia Leitch , Hervé Sauquet , Stephen Smith , Wolf Eiserhardt , Félix Forest , William Baker (1)

1 Royal Botanic Gardens [Kew]
2 ISYEB - Institut de Systématique, Evolution, Biodiversité
3 UMR AMAP - Botanique et Modélisation de l'Architecture des Plantes et des Végétations
4 IRD - Institut de Recherche pour le Développement
5 UMR DIADE - Diversité, adaptation, développement des plantes

Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods 1,2 . 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 genome 3,4 . Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins 5–7 . 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 genes 8 . This 15-fold increase in genus-level sampling relative to comparable nuclear studies 9 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: Phylogenetics; Phylogenomics; Plant evolution; Speciation

Domains: Biodiversity and Ecology

Alexandre Zuntini, Tom Carruthers, Olivier Maurin, Paul Bailey, Kevin Leempoel, et al.. Phylogenomics and the rise of the angiosperms. Nature, In press, ⟨10.1038/s41586-024-07324-0⟩. ⟨hal-04560060⟩