The origin of the odorant receptor gene family in insects
- University of California, Davis, United States
- University of Illinois at Urbana-Champaign, United States
- 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.
-
Thermobia domestica genome assembly v 1.0Available at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
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
- Richard Benton, University of Lausanne, Switzerland
Version history
- Received: May 13, 2018
- Accepted: July 24, 2018
- Accepted Manuscript published: July 31, 2018 (version 1)
- 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.
Metrics
-
- 5,760
- views
-
- 1,026
- downloads
-
- 101
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
The origin of the odorant receptor gene family in insects
eLife 7:e38340.
https://doi.org/10.7554/eLife.38340
Further reading
-
- Evolutionary Biology
Studies of the starlet sea anemone provide important insights into the early evolution of the circadian clock in animals.
-
- Computational and Systems Biology
- Evolutionary Biology
As the genome encodes the information crucial for cell growth, a sizeable genomic deficiency often causes a significant decrease in growth fitness. Whether and how the decreased growth fitness caused by genome reduction could be compensated by evolution was investigated here. Experimental evolution with an Escherichia coli strain carrying a reduced genome was conducted in multiple lineages for approximately 1000 generations. The growth rate, which largely declined due to genome reduction, was considerably recovered, associated with the improved carrying capacity. Genome mutations accumulated during evolution were significantly varied across the evolutionary lineages and were randomly localized on the reduced genome. Transcriptome reorganization showed a common evolutionary direction and conserved the chromosomal periodicity, regardless of highly diversified gene categories, regulons, and pathways enriched in the differentially expressed genes. Genome mutations and transcriptome reorganization caused by evolution, which were found to be dissimilar to those caused by genome reduction, must have followed divergent mechanisms in individual evolutionary lineages. Gene network reconstruction successfully identified three gene modules functionally differentiated, which were responsible for the evolutionary changes of the reduced genome in growth fitness, genome mutation, and gene expression, respectively. The diversity in evolutionary approaches improved the growth fitness associated with the homeostatic transcriptome architecture as if the evolutionary compensation for genome reduction was like all roads leading to Rome.
