Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects.


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:
19 02 2019
Historique:
pubmed: 16 1 2019
medline: 6 5 2019
entrez: 16 1 2019
Statut: ppublish

Résumé

Polyneoptera represents one of the major lineages of winged insects, comprising around 40,000 extant species in 10 traditional orders, including grasshoppers, roaches, and stoneflies. Many important aspects of polyneopteran evolution, such as their phylogenetic relationships, changes in their external appearance, their habitat preferences, and social behavior, are unresolved and are a major enigma in entomology. These ambiguities also have direct consequences for our understanding of the evolution of winged insects in general; for example, with respect to the ancestral habitats of adults and juveniles. We addressed these issues with a large-scale phylogenomic analysis and used the reconstructed phylogenetic relationships to trace the evolution of 112 characters associated with the external appearance and the lifestyle of winged insects. Our inferences suggest that the last common ancestors of Polyneoptera and of the winged insects were terrestrial throughout their lives, implying that wings did not evolve in an aquatic environment. The appearance of the first polyneopteran insect was mainly characterized by ancestral traits such as long segmented abdominal appendages and biting mouthparts held below the head capsule. This ancestor lived in association with the ground, which led to various specializations including hardened forewings and unique tarsal attachment structures. However, within Polyneoptera, several groups switched separately to a life on plants. In contrast to a previous hypothesis, we found that social behavior was not part of the polyneopteran ground plan. In other traits, such as the biting mouthparts, Polyneoptera shows a high degree of evolutionary conservatism unique among the major lineages of winged insects.

Identifiants

pubmed: 30642969
pii: 1817794116
doi: 10.1073/pnas.1817794116
pmc: PMC6386694
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3024-3029

Commentaires et corrections

Type : CommentIn

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

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Auteurs

Benjamin Wipfler (B)

Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-University Jena, 07743 Jena, Germany; benjamin.wipfler@leibniz-zfmk.de sabrina.simon@wur.nl.
Center of Taxonomy and Evolutionary Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, Germany.

Harald Letsch (H)

Department für Botanik und Biodiversitätsforschung, Universität Wien, 1030 Vienna, Austria.

Paul B Frandsen (PB)

Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT 84604.
Data Science Lab, Office of the Chief Information Officer, Smithsonian Institution, Washington, DC 20002.

Paschalia Kapli (P)

The Exelixis Lab, Scientific Computing Group, Heidelberg Institute for Theoretical Studies, 69118 Heidelberg, Germany.
Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom.

Christoph Mayer (C)

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

Daniela Bartel (D)

Department of Integrative Zoology, Universität Wien, 1090 Vienna, Austria.

Thomas R Buckley (TR)

New Zealand Arthropod Collection, Manaaki Whenua - Landcare Research, Auckland 1142, New Zealand.
School of Biological Sciences, The University of Auckland, Auckland 1142, New Zealand.

Alexander Donath (A)

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

Janice S Edgerly-Rooks (JS)

Department of Biology, College of Arts and Sciences, Santa Clara University, Santa Clara, CA 95053.

Mari Fujita (M)

Sugadaira Research Station, Mountain Science Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano 386-2204, Japan.

Shanlin Liu (S)

BGI-Shenzhen, Shenzhen 518083, China.
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350 Copenhagen K, Denmark.

Ryuichiro Machida (R)

Sugadaira Research Station, Mountain Science Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano 386-2204, Japan.

Yuta Mashimo (Y)

Sugadaira Research Station, Mountain Science Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano 386-2204, Japan.

Bernhard Misof (B)

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

Oliver Niehuis (O)

Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert Ludwig University, 79104 Freiburg, Germany.

Ralph S Peters (RS)

Center of Taxonomy and Evolutionary Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, Germany.

Malte Petersen (M)

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

Lars Podsiadlowski (L)

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

Kai Schütte (K)

Tierökologie und Naturschutz, Universität Hamburg, 20146 Hamburg, Germany.

Shota Shimizu (S)

Sugadaira Research Station, Mountain Science Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano 386-2204, Japan.

Toshiki Uchifune (T)

Sugadaira Research Station, Mountain Science Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano 386-2204, Japan.
Yokosuka City Museum, Fukadadai, Kanagawa 238-0016, Japan.

Jeanne Wilbrandt (J)

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

Evgeny Yan (E)

Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-University Jena, 07743 Jena, Germany.
Borissiak Palaeontological Institute, Russian Academy of Sciences, 123 Moscow, Russia.

Xin Zhou (X)

Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100083, China.

Sabrina Simon (S)

Biosystematics Group, Wageningen University and Research, 6708 PB Wageningen, The Netherlands benjamin.wipfler@leibniz-zfmk.de sabrina.simon@wur.nl.

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Classifications MeSH