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A Comprehensive and Dated Phylogenomic Analysis of Butterflies.
Curr Biol. 2018 03 05; 28(5):770-778.e5.CB

Abstract

Butterflies (Papilionoidea), with over 18,000 described species [1], have captivated naturalists and scientists for centuries. They play a central role in the study of speciation, community ecology, biogeography, climate change, and plant-insect interactions and include many model organisms and pest species [2, 3]. However, a robust higher-level phylogenetic framework is lacking. To fill this gap, we inferred a dated phylogeny by analyzing the first phylogenomic dataset, including 352 loci (> 150,000 bp) from 207 species representing 98% of tribes, a 35-fold increase in gene sampling and 3-fold increase in taxon sampling over previous studies [4]. Most data were generated with a new anchored hybrid enrichment (AHE) [5] gene kit (BUTTERFLY1.0) that includes both new and frequently used (e.g., [6]) informative loci, enabling direct comparison and future dataset merging with previous studies. Butterflies originated around 119 million years ago (mya) in the late Cretaceous, but most extant lineages diverged after the Cretaceous-Paleogene (K-Pg) mass-extinction 65 mya. Our analyses support swallowtails (Papilionidae) as sister to all other butterflies, followed by skippers (Hesperiidae) + the nocturnal butterflies (Hedylidae) as sister to the remainder, indicating a secondary reversal from diurnality to nocturnality. The whites (Pieridae) were strongly supported as sister to brush-footed butterflies (Nymphalidae) and blues + metalmarks (Lycaenidae and Riodinidae). Ant association independently evolved once in Lycaenidae and twice in Riodinidae. This study overturns prior notions of the taxon's evolutionary history, as many long-recognized subfamilies and tribes are para- or polyphyletic. It also provides a much-needed backbone for a revised classification of butterflies and for future comparative studies including genome evolution and ecology.

Authors+Show Affiliations

Arthropoda Department, Zoological Research Museum Alexander Koenig, Adenauer Allee 160, 53113 Bonn, Germany; Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA; Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA. Electronic address: m.espeland@leibniz-zfmk.de.Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA; RAPiD Genomics 747 SW 2nd Avenue IMB#14, Gainesville, FL 32601, USA.Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.Institut de Biologia Evolutiva (CSIC- Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37, ESP-08003 Barcelona, Spain.Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.Biology Department, City College of New York, New York, NY 10031, USA.Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA; Institut de Biologia Evolutiva (CSIC- Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37, ESP-08003 Barcelona, Spain.Institute for Agricultural Sciences, Biocommunication & Entomology, Eidgenössische Technische Hochschule Zürich (ETHZ), WEV E26.1, Weinbergstrasse 56-58, 8092 Zürich, Switzerland.Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511-8934, USA.Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.Biology Department, City College of New York, New York, NY 10031, USA; PhD Program in Biology, Graduate Center, City University of New York, New York, NY 10016, USA; Entomology Section, National Museum of the Philippines, Manila 1000, Philippines.Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA. Electronic address: kawahara@flmnh.ufl.edu.

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

29456146

Citation

Espeland, Marianne, et al. "A Comprehensive and Dated Phylogenomic Analysis of Butterflies." Current Biology : CB, vol. 28, no. 5, 2018, pp. 770-778.e5.
Espeland M, Breinholt J, Willmott KR, et al. A Comprehensive and Dated Phylogenomic Analysis of Butterflies. Curr Biol. 2018;28(5):770-778.e5.
Espeland, M., Breinholt, J., Willmott, K. R., Warren, A. D., Vila, R., Toussaint, E. F. A., Maunsell, S. C., Aduse-Poku, K., Talavera, G., Eastwood, R., Jarzyna, M. A., Guralnick, R., Lohman, D. J., Pierce, N. E., & Kawahara, A. Y. (2018). A Comprehensive and Dated Phylogenomic Analysis of Butterflies. Current Biology : CB, 28(5), 770-e5. https://doi.org/10.1016/j.cub.2018.01.061
Espeland M, et al. A Comprehensive and Dated Phylogenomic Analysis of Butterflies. Curr Biol. 2018 03 5;28(5):770-778.e5. PubMed PMID: 29456146.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A Comprehensive and Dated Phylogenomic Analysis of Butterflies. AU - Espeland,Marianne, AU - Breinholt,Jesse, AU - Willmott,Keith R, AU - Warren,Andrew D, AU - Vila,Roger, AU - Toussaint,Emmanuel F A, AU - Maunsell,Sarah C, AU - Aduse-Poku,Kwaku, AU - Talavera,Gerard, AU - Eastwood,Rod, AU - Jarzyna,Marta A, AU - Guralnick,Robert, AU - Lohman,David J, AU - Pierce,Naomi E, AU - Kawahara,Akito Y, Y1 - 2018/02/15/ PY - 2017/09/17/received PY - 2017/11/21/revised PY - 2018/01/19/accepted PY - 2018/2/20/pubmed PY - 2019/7/10/medline PY - 2018/2/20/entrez KW - Lepidoptera KW - Papilionoidea KW - ant association KW - evolution KW - fossils KW - hybrid enrichment KW - molecular dating KW - phylogenomics KW - species tree KW - target capture SP - 770 EP - 778.e5 JF - Current biology : CB JO - Curr Biol VL - 28 IS - 5 N2 - Butterflies (Papilionoidea), with over 18,000 described species [1], have captivated naturalists and scientists for centuries. They play a central role in the study of speciation, community ecology, biogeography, climate change, and plant-insect interactions and include many model organisms and pest species [2, 3]. However, a robust higher-level phylogenetic framework is lacking. To fill this gap, we inferred a dated phylogeny by analyzing the first phylogenomic dataset, including 352 loci (> 150,000 bp) from 207 species representing 98% of tribes, a 35-fold increase in gene sampling and 3-fold increase in taxon sampling over previous studies [4]. Most data were generated with a new anchored hybrid enrichment (AHE) [5] gene kit (BUTTERFLY1.0) that includes both new and frequently used (e.g., [6]) informative loci, enabling direct comparison and future dataset merging with previous studies. Butterflies originated around 119 million years ago (mya) in the late Cretaceous, but most extant lineages diverged after the Cretaceous-Paleogene (K-Pg) mass-extinction 65 mya. Our analyses support swallowtails (Papilionidae) as sister to all other butterflies, followed by skippers (Hesperiidae) + the nocturnal butterflies (Hedylidae) as sister to the remainder, indicating a secondary reversal from diurnality to nocturnality. The whites (Pieridae) were strongly supported as sister to brush-footed butterflies (Nymphalidae) and blues + metalmarks (Lycaenidae and Riodinidae). Ant association independently evolved once in Lycaenidae and twice in Riodinidae. This study overturns prior notions of the taxon's evolutionary history, as many long-recognized subfamilies and tribes are para- or polyphyletic. It also provides a much-needed backbone for a revised classification of butterflies and for future comparative studies including genome evolution and ecology. SN - 1879-0445 UR - https://www.unboundmedicine.com/medline/citation/29456146/A_Comprehensive_and_Dated_Phylogenomic_Analysis_of_Butterflies_ DB - PRIME DP - Unbound Medicine ER -