A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins

Akito Kawahara; Caroline Storer; Ana Paula S Carvalho; David Plotkin; Fabien Condamine; Mariana Braga; Emily Ellis; Ryan St Laurent; Xuankun Li; Vijay Barve; Liming Cai; Chandra Earl; Paul Frandsen; Hannah Owens; Wendy Valencia-Montoya; Kwaku Aduse-Poku; Emmanuel Toussaint; Kelly Dexter; Tenzing Doleck; Amanda Markee; Rebeccah Messcher; Y-Lan Nguyen; Jade Aster T Badon; Hugo Benítez; Michael Braby; Perry Buenavente; Wei-Ping Chan; Steve Collins; Richard Rabideau Childers; Even Dankowicz; Rod Eastwood; Zdenek Fric; Riley Gott; Jason Hall; Winnie Hallwachs; Nate Hardy; Rachel Sipe; Alan Heath; Jomar Hinolan; Nicholas Homziak; Yu-Feng Hsu; Yutaka Inayoshi; Micael Itliong; Daniel Janzen; Ian Kitching; Krushnamegh Kunte; Gerardo Lamas; Michael Landis; Elise Larsen; Torben Larsen; Jing Leong; Vladimir Lukhtanov; Crystal Maier; Jose Martinez; Dino Martins; Kiyoshi Maruyama; Sarah Maunsell; Nicolás Oliveira Mega; Alexander Monastyrskii; Ana Morais; Chris Müller; Mark Arcebal K Naive; Gregory Nielsen; Pablo Sebastián Padrón; Djunijanti Peggie; Helena Piccoli Romanowski; Szabolcs Sáfián; Motoki Saito; Stefan Schröder; Vaughn Shirey; Doug Soltis; Pamela Soltis; Andrei Sourakov; Gerard Talavera; Roger Vila; Petr Vlasanek; Houshuai Wang; Andrew Warren; Keith Willmott; Masaya Yago; Walter Jetz; Marta Jarzyna; Jesse Breinholt; Marianne Espeland; Leslie Ries; Robert Guralnick; Naomi Pierce; David Lohman; Ana Paula S. Carvalho; Jade Aster T. Badon; Mark Arcebal K. Naive

doi:10.1038/s41559-023-02041-9

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A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins

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A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins

Akito Kawahara, Caroline Storer, Ana Paula S Carvalho, David Plotkin, Fabien Condamine, Mariana Braga, Emily Ellis, Ryan St Laurent, Xuankun Li, Vijay Barve, …

Nature Ecology & Evolution, Vol.7(6), pp.903-913

06/2023

DOI: https://doi.org/10.1038/s41559-023-02041-9

PMCID: PMC10250192

PMID: 37188966

Abstract

Animals

Phylogeny

Biological Evolution

Butterflies

Butterflies are a diverse and charismatic insect group that are thought to have evolved with plants and dispersed throughout the world in response to key geological events. However, these hypotheses have not been extensively tested because a comprehensive phylogenetic framework and datasets for butterfly larval hosts and global distributions are lacking. We sequenced 391 genes from nearly 2,300 butterfly species, sampled from 90 countries and 28 specimen collections, to reconstruct a new phylogenomic tree of butterflies representing 92% of all genera. Our phylogeny has strong support for nearly all nodes and demonstrates that at least 36 butterfly tribes require reclassification. Divergence time analyses imply an origin ~100 million years ago for butterflies and indicate that all but one family were present before the K/Pg extinction event. We aggregated larval host datasets and global distribution records and found that butterflies are likely to have first fed on Fabaceae and originated in what is now the Americas. Soon after the Cretaceous Thermal Maximum, butterflies crossed Beringia and diversified in the Palaeotropics. Our results also reveal that most butterfly species are specialists that feed on only one larval host plant family. However, generalist butterflies that consume two or more plant families usually feed on closely related plants.

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Title: A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins
Creators - without role: Akito Kawahara - Florida Museum of Natural History
Caroline Storer - Florida Museum of Natural History
Ana Paula S Carvalho - Florida Museum of Natural History
David Plotkin - Florida Museum of Natural History
Fabien Condamine - Université de Montpellier, Institut des Sciences de l'Evolution - Montpellier - ISEM
Mariana Braga - Swedish University of Agricultural Sciences
Emily Ellis - Florida Museum of Natural History [Gainesville]
Ryan St Laurent - Smithsonian Institution
Xuankun Li - Florida Museum of Natural History
Vijay Barve - Florida Museum of Natural History
Liming Cai - Harvard University
Chandra Earl - University of Florida
Paul Frandsen - Brigham Young University
Hannah Owens - University of Florida
Wendy Valencia-Montoya - Harvard University
Kwaku Aduse-Poku - City College of New York
Emmanuel Toussaint - Natural History Museum [Geneva]
Kelly Dexter - University of Florida
Tenzing Doleck - City College of New York
Amanda Markee - University of Florida
Rebeccah Messcher - University of Florida
Y-Lan Nguyen
Jade Aster T Badon - University of the Philippines Los Baños
Hugo Benítez - Catholic University of the Maule
Michael Braby - Australian National University
Perry Buenavente
Wei-Ping Chan - Harvard University
Steve Collins
Richard Rabideau Childers
Even Dankowicz - Harvard University
Rod Eastwood - Harvard University
Zdenek Fric - Czech Academy of Sciences, Biology Centre
Riley Gott - University of Florida
Jason Hall
Winnie Hallwachs - University of Pennsylvania
Nate Hardy - Auburn University
Rachel Sipe
Alan Heath - Harvard University
Jomar Hinolan - National Museum of the Philippines
Nicholas Homziak - University of Florida
Yu-Feng Hsu
Yutaka Inayoshi
Micael Itliong
Daniel Janzen - University of Pennsylvania
Ian Kitching - Natural History Museum
Krushnamegh Kunte - Tata Institute of Fundamental Research
Gerardo Lamas - National University of San Marcos
Michael Landis - Washington University in St. Louis
Elise Larsen - Georgetown University
Torben Larsen - Georgetown University
Jing Leong - City College of New York
Vladimir Lukhtanov - Zoological Institute
Crystal Maier - Harvard University
Jose Martinez - University of Florida
Dino Martins - Stony Brook University
Kiyoshi Maruyama
Sarah Maunsell - Harvard University
Nicolás Oliveira Mega - Universidade Federal do Rio Grande do Sul
Alexander Monastyrskii
Ana Morais
Chris Müller - Australian Museum
Mark Arcebal K Naive - Xishuangbanna Tropical Botanical Garden
Gregory Nielsen
Pablo Sebastián Padrón - Universidad del Azuay
Djunijanti Peggie
Helena Piccoli Romanowski - Universidade Federal do Rio Grande do Sul
Szabolcs Sáfián - University of Sopron
Motoki Saito - Research Institutue of Evolutionary Biology
Stefan Schröder
Vaughn Shirey - Georgetown University
Doug Soltis - Florida Museum of Natural History
Pamela Soltis - Florida Museum of Natural History
Andrei Sourakov - Florida Museum of Natural History
Gerard Talavera - Institut Botànic de Barcelona
Roger Vila - Institut de Biologia Evolutiva
Petr Vlasanek - T. G. Masaryk Water Research Institute
Houshuai Wang - South China Agricultural University
Andrew Warren - University of Florida
Keith Willmott - University of Florida
Masaya Yago - The University of Tokyo
Walter Jetz - Yale University
Marta Jarzyna - Yale University
Jesse Breinholt - Florida Museum of Natural History
Marianne Espeland - Zoological Research Museum Alexander Koenig
Leslie Ries - Georgetown University
Robert Guralnick - University of Florida
Naomi Pierce - Harvard University
David Lohman - National Museum of the Philippines
Ana Paula S. Carvalho - Florida Museum of Natural History
Jade Aster T. Badon - University of the Philippines Los Baños
Mark Arcebal K. Naive - Xishuangbanna Tropical Botanical Garden
Publication Details: Nature Ecology & Evolution, Vol.7(6), pp.903-913
Grant note: High-performance clusters at Brigham Young University, Harvard University, Smithsonian Institution, University of Florida and Zoological Research Museum Alexander Koenig provided computational support. Funding came from the US National Science Foundation (NSF) GoLife ‘ButterflyNet’ collaborative grant (DEB-1541500, 1541557, 1541560) to A.Y.K., R.P.G., D.J.L. and N.E.P. Specimen collection and preservation was funded by NSF DBI-1349345, 1601369, DEB-1557007 and IOS-1920895 (A.Y.K.), NSF DEB-1120380 (D.J.L.), grants 9285-13 and WW-227R-17 from the National Geographic Society (D.J.L.), NSF DBI-1256742 (A.Y.K. and K.R.W.), NSF DEB-0639861 (K.R.W.) and NSF SES-0750480, DEB-0447244 and DEB-9615760 (N.E.P.). M.E. was supported by the Research Council of Norway (no. 204308) and the Hintelmann Scientific Award for Zoological Systematics. F.L.C. was supported by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (project GAIA, no. 851188). M.P.B. was supported by the Swedish Research Council (IPG no. 2020‐06422). R.V. was supported by the Spanish Ministry of Science and Innovation grant PID2019-107078GB-I00/AEI/10.13039/501100011033. G.T. was supported by the Spanish Ministry of Science and Innovation (grants PID2020-117739GA-I00/AEI/10.13039/501100011033 and RYC2018-025335-I). V.L. was supported by the Russian Science Foundation (grant 19-14-00202) and by the Ministry of Science and Higher Education of the Russian Federation (grant 075-15-2021-1069). M.Y. was supported by MEXT KAKENHI no. 19916010 and JSPS KAKENHI grants 13010131, 23570111, 26440207, 17K07528 and 21H02215. A.B.B.M., H.P.R. and N.O.M. were supported by CNPQ grants proc 563332/2010-7 and 304273/2014-7. We are thankful for the continuous support from the Museum of Comparative Zoology for fieldwork (Putnam Expedition Grants), and providing funds to support Open Access (Wetmore-Colles Fund).
Identifiers: 9935952609311
Academic Unit: Institut des Sciences de l'Evolution - Montpellier - ISEM
Language: English
Resource Type: Journal article
Local Fields: hal-04262510