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      Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths

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          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.

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          Most cited references50

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          Butterflies and Plants: A Study in Coevolution

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            BUTTERFLIES AND PLANTS: A STUDY IN COEVOLUTION

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              Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny.

              The fossil record suggests a rapid radiation of placental mammals following the Cretaceous-Paleogene (K-Pg) mass extinction 65 million years ago (Ma); nevertheless, molecular time estimates, while highly variable, are generally much older. Early molecular studies suffer from inadequate dating methods, reliance on the molecular clock, and simplistic and over-confident interpretations of the fossil record. More recent studies have used Bayesian dating methods that circumvent those issues, but the use of limited data has led to large estimation uncertainties, precluding a decisive conclusion on the timing of mammalian diversifications. Here we use a powerful Bayesian method to analyse 36 nuclear genomes and 274 mitochondrial genomes (20.6 million base pairs), combined with robust but flexible fossil calibrations. Our posterior time estimates suggest that marsupials diverged from eutherians 168-178 Ma, and crown Marsupialia diverged 64-84 Ma. Placentalia diverged 88-90 Ma, and present-day placental orders (except Primates and Xenarthra) originated in a ∼20 Myr window (45-65 Ma) after the K-Pg extinction. Therefore we reject a pre K-Pg model of placental ordinal diversification. We suggest other infamous instances of mismatch between molecular and palaeontological divergence time estimates will be resolved with this same approach.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                5 November 2019
                21 October 2019
                21 October 2019
                : 116
                : 45
                : 22657-22663
                Affiliations
                [1] aMcGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida , Gainesville, FL 32611;
                [2] bEntomology and Nematology Department, University of Florida , Gainesville, FL 32611;
                [3] cArthropoda Department, Alexander Koenig Zoological Research Museum , D-53113 Bonn, Germany;
                [4] dDepartment of Evolutionary Biology and Ecology, Institute for Biology I (Zoology), University of Freiburg , D-79104 Freiburg, Germany;
                [5] eCenter for Molecular Biodiversity Research, Alexander Koenig Zoological Research Museum , D-53113 Bonn, Germany;
                [6] fAustralian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation , Canberra, Acton, ACT 2601, Australia;
                [7] gDepartment of Entomology, Natural History Museum of Geneva , 1208 Geneva, Switzerland;
                [8] hPlant and Wildlife Sciences, Brigham Young University , Provo, UT 84602;
                [9] iData Science Lab, Smithsonian Institution , Washington, DC 20002;
                [10] jSchool of Biological and Chemical Sciences, Queen Mary University of London , London E1 4NS, United Kingdom;
                [11] kDepartment of Biological Sciences, Boise State University , Boise, ID 83725;
                [12] lChina National GeneBank , BGI-Shenzhen, 518083 Guangdong, China;
                [13] mDepartment of Entomology, College of Plant Protection, China Agricultural University , 100193 Beijing, China;
                [14] nDepartment of Biology, Carleton University , Ottawa, ON, Canada K1S 5B6;
                [15] oBioinformatics & Data Analysis Division, RAPiD Genomics , Gainesville, FL 32601
                Author notes
                1To whom correspondence may be addressed. Email: kawahara@ 123456flmnh.ufl.edu .

                Edited by Douglas Futuyma, Stony Brook University, Stony Brook, NY, and approved September 16, 2019 (received for review May 29, 2019)

                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.

                2Present address: Division of Bioinformatics, Intermountain Healthcare, Precision Genomics, St. George, UT 84790.

                Author information
                http://orcid.org/0000-0002-3724-4610
                http://orcid.org/0000-0002-2339-655X
                http://orcid.org/0000-0002-8439-1285
                http://orcid.org/0000-0001-5618-0547
                http://orcid.org/0000-0001-9514-3976
                http://orcid.org/0000-0001-5104-6621
                Article
                201907847
                10.1073/pnas.1907847116
                6842621
                31636187
                40888dae-1550-407b-a95e-03b9a73e0df4
                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).

                History
                Page count
                Pages: 7
                Funding
                Funded by: NSF | BIO | Division of Environmental Biology (DEB) 100000155
                Award ID: 1541500
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse W Breinholt
                Funded by: NSF | BIO | Division of Environmental Biology (DEB) 100000155
                Award ID: 1557007
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse W Breinholt
                Funded by: NSF | BIO | Division of Environmental Biology (DEB) 100000155
                Award ID: 1354585
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse W Breinholt
                Funded by: NSF | BIO | Division of Integrative Organismal Systems (IOS) 100000154
                Award ID: 1121739
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse R Barber
                Funded by: NSF | BIO | Division of Integrative Organismal Systems (IOS) 100000154
                Award ID: 1121807
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse R Barber
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: NI 1387/ 1-1
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: MI 649/6
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: MI 649/10
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: RE 345/1-2
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: BE 1789/8-1
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: BE 1789/10-1
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: STA 860/4
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: Heisenberg grant WA 1496/8-1
                Award Recipient : Karen Meusemann Award Recipient : Ralph S Peters Award Recipient : Bernhard Misof
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: 1920895
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse R Barber
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: 1920936
                Award Recipient : Akito Y Kawahara Award Recipient : Jesse R Barber
                Categories
                Biological Sciences
                Evolution

                lepidoptera,coevolution,phylogeny,angiosperms,bats
                lepidoptera, coevolution, phylogeny, angiosperms, bats

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