Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
05 11 2019
Historique:
pubmed: 23 10 2019
medline: 6 5 2020
entrez: 23 10 2019
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 31636187
pii: 1907847116
doi: 10.1073/pnas.1907847116
pmc: PMC6842621
doi:

Banques de données

Dryad
['10.5061/dryad.j477b40']

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

22657-22663

Informations de copyright

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

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Akito Y Kawahara (AY)

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611; kawahara@flmnh.ufl.edu.

David Plotkin (D)

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.
Entomology and Nematology Department, University of Florida, Gainesville, FL 32611.

Marianne Espeland (M)

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.
Arthropoda Department, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

Karen Meusemann (K)

Department of Evolutionary Biology and Ecology, Institute for Biology I (Zoology), University of Freiburg, D-79104 Freiburg, Germany.
Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
Australian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation, Canberra, Acton, ACT 2601, Australia.

Emmanuel F A Toussaint (EFA)

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.
Department of Entomology, Natural History Museum of Geneva, 1208 Geneva, Switzerland.

Alexander Donath (A)

Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

France Gimnich (F)

Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

Paul B Frandsen (PB)

Plant and Wildlife Sciences, Brigham Young University, Provo, UT 84602.
Data Science Lab, Smithsonian Institution, Washington, DC 20002.

Andreas Zwick (A)

Australian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation, Canberra, Acton, ACT 2601, Australia.

Mario Dos Reis (M)

School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom.

Jesse R Barber (JR)

Department of Biological Sciences, Boise State University, Boise, ID 83725.

Ralph S Peters (RS)

Arthropoda Department, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

Shanlin Liu (S)

China National GeneBank, BGI-Shenzhen, 518083 Guangdong, China.
Department of Entomology, College of Plant Protection, China Agricultural University, 100193 Beijing, China.

Xin Zhou (X)

Department of Entomology, College of Plant Protection, China Agricultural University, 100193 Beijing, China.

Christoph Mayer (C)

Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

Lars Podsiadlowski (L)

Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

Caroline Storer (C)

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.

Jayne E Yack (JE)

Department of Biology, Carleton University, Ottawa, ON, Canada K1S 5B6.

Bernhard Misof (B)

Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.

Jesse W Breinholt (JW)

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.
Bioinformatics & Data Analysis Division, RAPiD Genomics, Gainesville, FL 32601.

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