1. Evolutionary Biology
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The origin of the odorant receptor gene family in insects

  1. Philipp Brand  Is a corresponding author
  2. Hugh M Robertson  Is a corresponding author
  3. Wei Lin
  4. Ratnasri Pothula
  5. William E Klingeman
  6. Juan Luis Jurat-Fuentes
  7. Brian R Johnson
  1. University of California, Davis, United States
  2. University of Illinois at Urbana-Champaign, United States
  3. University of Tennessee, United States
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  • Views 3,909
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Cite this article as: eLife 2018;7:e38340 doi: 10.7554/eLife.38340
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Abstract

The origin of the insect odorant receptor (OR) gene family has been hypothesized to have coincided with the evolution of terrestriality in insects. Missbach et al. (2014) suggested that ORs instead evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality and the OR/Orco system is an adaptation to winged flight in insects. We investigated genomes of the Collembola, Diplura, Archaeognatha, Zygentoma, Odonata, and Ephemeroptera, and find ORs present in all insect genomes but absent from lineages predating the evolution of insects. Orco is absent only in the ancestrally wingless insect lineage Archaeognatha. Our new genome sequence of the zygentoman firebrat Thermobia domestica reveals a full OR/Orco system. We conclude that ORs evolved before winged flight, perhaps as an adaptation to terrestriality, representing a key evolutionary novelty in the ancestor of all insects, and hence a molecular synapomorphy for the Class Insecta.

Data availability

Raw genome sequence reads are being submitted to the Sequence Read Archive at the NCBI. The Thermobia domestica genome assembly is available from Dryad under doi:10.5061/dryad.p2t8170. All other data generated and analysed during this study, including all Odorant Receptor protein sequences, are included in the manuscript and supporting file. A detailed version of Figure 2 is provided in the supporting file. All Odorant Receptor protein sequences and the amino acid alignment used for the phylogenetic analysis have also been uploaded to Dryad.

The following data sets were generated
    1. Brand P
    (2018) Thermobia domestica genome assembly v 1.0
    Available at Dryad Digital Repository under a CC0 Public Domain Dedication.
    http://dx.doi.org/10.5061/dryad.p2t8170

Article and author information

Author details

  1. Philipp Brand

    Department of Evolution and Ecology, University of California, Davis, Davis, United States
    For correspondence
    pbrand@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4287-4753

  2. Hugh M Robertson

    Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, United States
    For correspondence
    hughrobe@uiuc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8093-0950

  3. Wei Lin

    Department of Entomology and Nematology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Ratnasri Pothula

    Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. William E Klingeman

    Department of Plant Sciences, University of Tennessee, Knoxville, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Juan Luis Jurat-Fuentes

    Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Brian R Johnson

    Department of Entomology and Nematology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (IOS-1456678)

  • Juan Luis Jurat-Fuentes
  • Brian R Johnson

US Department of Agriculture Hatch (CA-D-ENM 2161-H)

  • Brian R Johnson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Richard Benton, University of Lausanne, Switzerland

Publication history

  1. Received: May 23, 2018
  2. Accepted: July 24, 2018
  3. Accepted Manuscript published: July 31, 2018 (version 1)
  4. Version of Record published: August 7, 2018 (version 2)

Copyright

© 2018, Brand et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Categories and tags

    1. Builds upon

    Evolution of insect olfactory receptors

    Christine Missbach et al.
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    The olfactory sense detects a plethora of behaviorally relevant odor molecules; gene families involved in olfaction exhibit high diversity in different animal phyla. Insects detect volatile molecules using olfactory (OR) or ionotropic receptors (IR) and in some cases gustatory receptors (GRs). While IRs are expressed in olfactory organs across Protostomia, ORs have been hypothesized to be an adaptation to a terrestrial insect lifestyle. We investigated the olfactory system of the primary wingless bristletail Lepismachilis y-signata (Archaeognatha), the firebrat Thermobia domestica (Zygentoma) and the neopteran leaf insect Phyllium siccifolium (Phasmatodea). ORs and the olfactory coreceptor (Orco) are with very high probability lacking in Lepismachilis; in Thermobia we have identified three Orco candidates, and in Phyllium a fully developed OR/Orco-based system. We suggest that ORs did not arise as an adaptation to a terrestrial lifestyle, but evolved later in insect evolution, with Orco being present before the appearance of ORs.

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