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Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths.
Proc Natl Acad Sci U S A. 2019 11 05; 116(45):22657-22663.PN

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.

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Authors+Show Affiliations

Kawahara AY
McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611; kawahara@flmnh.ufl.edu.
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.
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.
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.
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.
Donath A
Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
Gimnich F
Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
Frandsen PB
Plant and Wildlife Sciences, Brigham Young University, Provo, UT 84602. Data Science Lab, Smithsonian Institution, Washington, DC 20002.
Zwick A
Australian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation, Canberra, Acton, ACT 2601, Australia.
Dos Reis M
School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom.
Barber JR
Department of Biological Sciences, Boise State University, Boise, ID 83725.
Peters RS
Arthropoda Department, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
Liu S
China National GeneBank, BGI-Shenzhen, 518083 Guangdong, China. Department of Entomology, College of Plant Protection, China Agricultural University, 100193 Beijing, China.
Zhou X
Department of Entomology, College of Plant Protection, China Agricultural University, 100193 Beijing, China.
Mayer C
Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
Podsiadlowski L
Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
Storer C
McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611.
Yack JE
Department of Biology, Carleton University, Ottawa, ON, Canada K1S 5B6.
Misof B
Center for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum, D-53113 Bonn, Germany.
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.

MeSH

AnimalsButterfliesEvolution, MolecularMothsPhylogeny

Pub Type(s)

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

Language

eng

PubMed ID

31636187

Citation

Kawahara, Akito Y., et al. "Phylogenomics Reveals the Evolutionary Timing and Pattern of Butterflies and Moths." Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 45, 2019, pp. 22657-22663.
Kawahara AY, Plotkin D, Espeland M, et al. Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proc Natl Acad Sci U S A. 2019;116(45):22657-22663.
Kawahara, A. Y., Plotkin, D., Espeland, M., Meusemann, K., Toussaint, E. F. A., Donath, A., Gimnich, F., Frandsen, P. B., Zwick, A., Dos Reis, M., Barber, J. R., Peters, R. S., Liu, S., Zhou, X., Mayer, C., Podsiadlowski, L., Storer, C., Yack, J. E., Misof, B., & Breinholt, J. W. (2019). Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proceedings of the National Academy of Sciences of the United States of America, 116(45), 22657-22663. https://doi.org/10.1073/pnas.1907847116
Kawahara AY, et al. Phylogenomics Reveals the Evolutionary Timing and Pattern of Butterflies and Moths. Proc Natl Acad Sci U S A. 2019 11 5;116(45):22657-22663. PubMed PMID: 31636187.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. AU - Kawahara,Akito Y, AU - Plotkin,David, AU - Espeland,Marianne, AU - Meusemann,Karen, AU - Toussaint,Emmanuel F A, AU - Donath,Alexander, AU - Gimnich,France, AU - Frandsen,Paul B, AU - Zwick,Andreas, AU - Dos Reis,Mario, AU - Barber,Jesse R, AU - Peters,Ralph S, AU - Liu,Shanlin, AU - Zhou,Xin, AU - Mayer,Christoph, AU - Podsiadlowski,Lars, AU - Storer,Caroline, AU - Yack,Jayne E, AU - Misof,Bernhard, AU - Breinholt,Jesse W, Y1 - 2019/10/21/ PY - 2019/10/23/pubmed PY - 2020/5/6/medline PY - 2019/10/23/entrez KW - Lepidoptera KW - angiosperms KW - bats KW - coevolution KW - phylogeny SP - 22657 EP - 22663 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc Natl Acad Sci U S A VL - 116 IS - 45 N2 - 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. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/31636187/Phylogenomics_reveals_the_evolutionary_timing_and_pattern_of_butterflies_and_moths_ DB - PRIME DP - Unbound Medicine ER -