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

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.

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

Version history

  1. Received: May 13, 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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  1. Philipp Brand
  2. Hugh M Robertson
  3. Wei Lin
  4. Ratnasri Pothula
  5. William E Klingeman
  6. Juan Luis Jurat-Fuentes
  7. Brian R Johnson
(2018)
The origin of the odorant receptor gene family in insects
eLife 7:e38340.
https://doi.org/10.7554/eLife.38340

Share this article

https://doi.org/10.7554/eLife.38340

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