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Research Article

Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths

View ORCID ProfileAkito Y. Kawahara, View ORCID ProfileDavid Plotkin, Marianne Espeland, Karen Meusemann, View ORCID ProfileEmmanuel F. A. Toussaint, View ORCID ProfileAlexander Donath, France Gimnich, Paul B. Frandsen, Andreas Zwick, View ORCID ProfileMario dos Reis, Jesse R. Barber, Ralph S. Peters, Shanlin Liu, Xin Zhou, View ORCID ProfileChristoph Mayer, Lars Podsiadlowski, Caroline Storer, Jayne E. Yack, Bernhard Misof, and Jesse W. Breinholt
PNAS November 5, 2019 116 (45) 22657-22663; first published October 21, 2019; https://doi.org/10.1073/pnas.1907847116
Akito Y. Kawahara
aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
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  • ORCID record for Akito Y. Kawahara
  • For correspondence: kawahara@flmnh.ufl.edu
David Plotkin
aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
bEntomology and Nematology Department, University of Florida, Gainesville, FL 32611;
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Marianne Espeland
aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
cArthropoda Department, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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Karen Meusemann
dDepartment of Evolutionary Biology and Ecology, Institute for Biology I (Zoology), University of Freiburg, D-79104 Freiburg, Germany;
eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
fAustralian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation, Canberra, Acton, ACT 2601, Australia;
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Emmanuel F. A. Toussaint
aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
gDepartment of Entomology, Natural History Museum of Geneva, 1208 Geneva, Switzerland;
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  • ORCID record for Emmanuel F. A. Toussaint
Alexander Donath
eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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  • ORCID record for Alexander Donath
France Gimnich
eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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Paul B. Frandsen
hPlant and Wildlife Sciences, Brigham Young University, Provo, UT 84602;
iData Science Lab, Smithsonian Institution, Washington, DC 20002;
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Andreas Zwick
fAustralian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation, Canberra, Acton, ACT 2601, Australia;
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Mario dos Reis
jSchool of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom;
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Jesse R. Barber
kDepartment of Biological Sciences, Boise State University, Boise, ID 83725;
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Ralph S. Peters
cArthropoda Department, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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Shanlin Liu
lChina National GeneBank, BGI-Shenzhen, 518083 Guangdong, China;
mDepartment of Entomology, College of Plant Protection, China Agricultural University, 100193 Beijing, China;
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Xin Zhou
mDepartment of Entomology, College of Plant Protection, China Agricultural University, 100193 Beijing, China;
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Christoph Mayer
eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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Lars Podsiadlowski
eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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Caroline Storer
aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
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Jayne E. Yack
nDepartment of Biology, Carleton University, Ottawa, ON, Canada K1S 5B6;
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Bernhard Misof
eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany;
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Jesse W. Breinholt
aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611;
oBioinformatics & Data Analysis Division, RAPiD Genomics, Gainesville, FL 32601
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  1. Edited by Douglas Futuyma, Stony Brook University, Stony Brook, NY, and approved September 16, 2019 (received for review May 29, 2019)

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Significance

Lepidoptera play key roles in many biological systems. Butterflies are hypothesized to have evolved contemporaneously with flowering plants, and moths are thought to have gained anti-bat defenses in response to echolocating predatory bats, but these hypotheses have largely gone untested. Using a transcriptomic, dated evolutionary tree of Lepidoptera, we demonstrate that the most recent common ancestor of Lepidoptera is considerably older than previously hypothesized. The oldest moths in crown Lepidoptera were present in the Carboniferous, some 300 million years ago, and began to diversify largely in synchrony with angiosperms. We show that multiple lineages of moths independently evolved hearing organs well before the origin of bats, rejecting the hypothesis that lepidopteran hearing organs arose in response to these predators.

Abstract

Butterflies and moths (Lepidoptera) are one of the major superradiations of insects, comprising nearly 160,000 described extant species. As herbivores, pollinators, and prey, Lepidoptera play a fundamental role in almost every terrestrial ecosystem. Lepidoptera are also indicators of environmental change and serve as models for research on mimicry and genetics. They have been central to the development of coevolutionary hypotheses, such as butterflies with flowering plants and moths’ evolutionary arms race with echolocating bats. However, these hypotheses have not been rigorously tested, because a robust lepidopteran phylogeny and timing of evolutionary novelties are lacking. To address these issues, we inferred a comprehensive phylogeny of Lepidoptera, using the largest dataset assembled for the order (2,098 orthologous protein-coding genes from transcriptomes of 186 species, representing nearly all superfamilies), and dated it with carefully evaluated synapomorphy-based fossils. The oldest members of the Lepidoptera crown group appeared in the Late Carboniferous (∼300 Ma) and fed on nonvascular land plants. Lepidoptera evolved the tube-like proboscis in the Middle Triassic (∼241 Ma), which allowed them to acquire nectar from flowering plants. This morphological innovation, along with other traits, likely promoted the extraordinary diversification of superfamily-level lepidopteran crown groups. The ancestor of butterflies was likely nocturnal, and our results indicate that butterflies became day-flying in the Late Cretaceous (∼98 Ma). Moth hearing organs arose multiple times before the evolutionary arms race between moths and bats, perhaps initially detecting a wide range of sound frequencies before being co-opted to specifically detect bat sonar. Our study provides an essential framework for future comparative studies on butterfly and moth evolution.

  • Lepidoptera
  • coevolution
  • phylogeny
  • angiosperms
  • bats

Footnotes

  • ↵1To whom correspondence may be addressed. Email: kawahara{at}flmnh.ufl.edu.
  • ↵2Present address: Division of Bioinformatics, Intermountain Healthcare, Precision Genomics, St. George, UT 84790.

  • Author contributions: A.Y.K., R.S.P., and B.M. designed research; A.Y.K., D.P., M.E., K.M., E.F.A.T., A.D., F.G., P.B.F., A.Z., M.d.R., S.L., X.Z., C.M., L.P., C.S., J.E.Y., B.M., and J.W.B. performed research; A.Y.K., K.M., P.B.F., A.Z., J.R.B., R.S.P., J.E.Y., B.M., and J.W.B. collected or provided samples; A.Y.K., D.P., M.E., K.M., E.F.A.T., A.D., F.G., P.B.F., A.Z., M.d.R., C.M., L.P., C.S., J.E.Y., B.M., and J.W.B. analyzed data; and A.Y.K., D.P., M.E., K.M., E.F.A.T., A.D., F.G., P.B.F., A.Z., M.d.R., J.R.B., R.S.P., S.L., X.Z., C.M., L.P., C.S., J.E.Y., B.M., and J.W.B. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Transcriptome assemblies for the newly sequenced transcriptomes used in this study either have been deposited in the National Center for Biotechnology Information Transcriptome Shotgun Assembly archive (all accession nos. provided in Dataset S1) or in a DRYAD digital repository (https://doi.org/10.5061/dryad.j477b40, Supplementary Archive 1). Other data files have also been archived in the same DRYAD repository. The contents of these archives are listed in the SI Appendix.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1907847116/-/DCSupplemental.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths
Akito Y. Kawahara, David Plotkin, Marianne Espeland, Karen Meusemann, Emmanuel F. A. Toussaint, Alexander Donath, France Gimnich, Paul B. Frandsen, Andreas Zwick, Mario dos Reis, Jesse R. Barber, Ralph S. Peters, Shanlin Liu, Xin Zhou, Christoph Mayer, Lars Podsiadlowski, Caroline Storer, Jayne E. Yack, Bernhard Misof, Jesse W. Breinholt
Proceedings of the National Academy of Sciences Nov 2019, 116 (45) 22657-22663; DOI: 10.1073/pnas.1907847116

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Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths
Akito Y. Kawahara, David Plotkin, Marianne Espeland, Karen Meusemann, Emmanuel F. A. Toussaint, Alexander Donath, France Gimnich, Paul B. Frandsen, Andreas Zwick, Mario dos Reis, Jesse R. Barber, Ralph S. Peters, Shanlin Liu, Xin Zhou, Christoph Mayer, Lars Podsiadlowski, Caroline Storer, Jayne E. Yack, Bernhard Misof, Jesse W. Breinholt
Proceedings of the National Academy of Sciences Nov 2019, 116 (45) 22657-22663; DOI: 10.1073/pnas.1907847116
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