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. 2019 Feb 19;116(8):3024-3029.
doi: 10.1073/pnas.1817794116. Epub 2019 Jan 14.

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

Benjamin Wipfler  1   2 , Harald Letsch  3 , Paul B Frandsen  4   5 , Paschalia Kapli  6   7 , Christoph Mayer  8 , Daniela Bartel  9 , Thomas R Buckley  10   11 , Alexander Donath  8 , Janice S Edgerly-Rooks  12 , Mari Fujita  13 , Shanlin Liu  14   15 , Ryuichiro Machida  13 , Yuta Mashimo  13 , Bernhard Misof  8 , Oliver Niehuis  16 , Ralph S Peters  2 , Malte Petersen  8 , Lars Podsiadlowski  8 , Kai Schütte  17 , Shota Shimizu  13 , Toshiki Uchifune  13   18 , Jeanne Wilbrandt  8 , Evgeny Yan  19   20 , Xin Zhou  21 , Sabrina Simon  22
Affiliations

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

Benjamin Wipfler et al. Proc Natl Acad Sci U S A. .

Abstract

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.

Keywords: Neoptera; Polyneoptera; Pterygota; lower winged insects; phylogenomics.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Phylogenetic relationships among the major lineages of Polyneoptera, inferred from analyzing a decisive dataset comprising 909,873 amino acids sites and applying protein domain-based partitioning scheme (DAA,decisive). Circles on nodes indicate bootstrap support values. Outgroup taxa are drawn in gray.
Fig. 2.
Fig. 2.
(A–F) Reconstructed evolution of selected characters in Polyneoptera and related lineages (full list in Dataset S11). Pie charts indicate the ML results for the respective hypothesis at that node. Black lines and white pie charts imply ambiguous results or characters that are not applicable. Dotted lines indicate changes within the terminal taxa. Acer., Acercaria; Der., Dermaptera (earwigs); Dic., Dictyoptera (mantids, roaches, and termites); Emb., Embioptera (webspinners); Ephe., Ephemeroptera (mayflies); Gryl., Grylloblattodea (ice crawlers); Holo., Holometabola; Man., Mantophasmatodea (heelwalkers); Neop., Neoptera; Odo., Odonata (damsel- and dragonflies); Orth., Orthoptera (crickets, katydids, and grasshoppers); Phas., Phasmatodea (stick and leaf insects); Ple., Plecoptera (stoneflies); Poly., Polyneoptera; Ptery., Pterygota (winged insects); Zor., Zoraptera (ground lice); Zyg., Zygentoma (silverfish).
Fig. 3.
Fig. 3.
Virtual model of the last common ancestor of Polyneoptera, inferred from analyzing 112 morphological characters. SI Appendix, Fig. S17 illustrates which parts of the model are based on results of the present analyses.
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