The origin of the odorant receptor gene family in insects

AbstractThe sense of smell enables the detection and discrimination of airborne chemicals via chemosensory receptors that have evolved independently multiple times throughout the tree of life. In insects, the odorant receptor (OR) gene family is the major chemosensory gene family involved in olfaction and its origin has been hypothesized to coincide with the evolution of a terrestrial lifestyle in hexapods. Missbach et al. (2014) challenged this view and suggested that ORs evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality, hypothesizing that the OR/Orco system is an adaptation to winged flight in insects instead. Building upon this work, we investigated the genomes of basal hexapod and insect lineages including Collembola, Diplura, Archaeognatha, Zygentoma, Odonata, and Ephemeroptera in an effort to identify the origin of the insect OR gene family. While absent from all non-insect hexapod lineages analyzed, ORs are present in all insect genomes. Orco is absent only in the most ancient insect lineage Archaeognatha. A fully functional OR/Orco system was present in our newly generated genome data of the Zygentoma Thermobia domestica. We suggest that ORs did evolve as adaptation to a terrestrial lifestyle outside high-humidity habitats, and not winged flight, representing a key evolutionary novelty in the ancestor of all insects. The OR family is therefore the first known molecular synapomorphy for the Class Insecta.

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The origin of the odorant receptor gene family in insects

eLife ◽

10.7554/elife.38340 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 36

Author(s):

Philipp Brand ◽

Hugh M Robertson ◽

Wei Lin ◽

Ratnasri Pothula ◽

William E Klingeman ◽

...

Keyword(s):

Gene Family ◽

Genome Sequence ◽

Odorant Receptor ◽

Receptor Gene ◽

Evolutionary Novelty ◽

Thermobia Domestica ◽

Or Gene ◽

Receptor Gene Family

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.

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Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family

10.1101/604389 ◽

2019 ◽

Author(s):

Michael Thoma ◽

Christine Missbach ◽

Melissa D. Jordan ◽

Ewald Grosse-Wilde ◽

Richard D. Newcomb ◽

...

Keyword(s):

Gene Family ◽

Odorant Receptor ◽

Receptor Gene ◽

Expression Patterns ◽

Cellular Expression ◽

Flying Insects ◽

Highly Sensitive ◽

Or Gene ◽

And Function ◽

Receptor Gene Family

AbstractThe insect odorant receptor (Or) gene family is among the largest multigene families in insect genomes, but its evolutionary origin and mode of expansion is still a matter of debate. We performed transcriptomic surveys of two wingless insect species, the silverfishLepisma saccharinaandTricholepidion gertschi, and identified multiple Or gene family members in both species. A phylogenetic analysis suggests that the silverfish Ors do not fall into the clade comprised of more derived flying insect ligand-binding Ors, but, along with bristletail, firebrat and some mayfly Ors, are consistently resolved as a distinct set of genes that may constitute an evolutionary intermediate between gustatory receptors and the more derived Ors of flying insects. We propose to consider these “primitive Ors” separately from higher insect Ors until their cellular expression patterns and function are resolved and suggest a multistep evolutionary scenario ultimately leading to the highly sensitive, rapidly evolving and physiologically diverse Or gene family observed in higher insects.

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Expansion and accelerated evolution of 9-exon odorant receptors in Polistes paper wasps

Molecular Biology and Evolution ◽

10.1093/molbev/msab023 ◽

2021 ◽

Author(s):

Andrew W Legan ◽

Christopher M Jernigan ◽

Sara E Miller ◽

Matthieu F Fuchs ◽

Michael J Sheehan

Keyword(s):

Gene Family ◽

Odorant Receptor ◽

Receptor Gene ◽

Gene Tree ◽

Gene Family Evolution ◽

Paper Wasp ◽

Gene Copy ◽

Evolutionary Divergence ◽

Wasp Species ◽

Or Gene

Abstract Independent origins of sociality in bees and ants are associated with independent expansions of particular odorant receptor (OR) gene subfamilies. In ants, one clade within the OR gene family, the 9-exon subfamily, has dramatically expanded. These receptors detect cuticular hydrocarbons (CHCs), key social signaling molecules in insects. It is unclear to what extent 9-exon OR subfamily expansion is associated with the independent evolution of sociality across Hymenoptera, warranting studies of taxa with independently derived social behavior. Here we describe odorant receptor gene family evolution in the northern paper wasp, Polistes fuscatus, and compare it to four additional paper wasp species spanning ∼40 million years of evolutionary divergence. We find 200 putatively functional OR genes in P. fuscatus, matching predictions from neuroanatomy, and more than half of these are in the 9-exon subfamily. Most OR gene expansions are tandemly arrayed at orthologous loci in Polistes genomes, and microsynteny analysis shows species-specific gain and loss of 9-exon ORs within tandem arrays. There is evidence of episodic positive diversifying selection shaping ORs in expanded subfamilies. Values of omega (d N/dS) are higher among 9-exon ORs compared to other OR subfamilies. Within the Polistes OR gene tree, branches in the 9-exon OR clade experience relaxed negative (purifying) selection relative to other branches in the tree. Patterns of OR evolution within Polistes are consistent with 9-exon OR function in CHC perception by combinatorial coding, with both natural selection and neutral drift contributing to interspecies differences in gene copy number and sequence.

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