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

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

10.1101/2020.09.04.283903 ◽

2020 ◽

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 Family Evolution ◽

Paper Wasp ◽

Wasp Species ◽

Accelerated Evolution ◽

Evolution Of Sociality ◽

Or Gene ◽

Or Genes

ABSTRACTIndependent 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 divergence. We find 200 functional OR genes in P. fuscatus matching predictions from neuroanatomy, and more than half of these are in the 9-exon subfamily. Lineage-specific expansions of 9-exon subfamily ORs are tandemly arrayed in Polistes genomes and exhibit a breakdown in microsynteny relative to tandem arrays in other OR subfamilies. There is evidence of episodic positive diversifying selection shaping ORs in expanded subfamilies, including 9-exon, E, H, and L, but 9-exon ORs do not stand out as selectively diversified among Polistes species. Accelerated evolution has resulted in lower amino acid similarity and high dN/dS among 9-exon ORs compared to other OR subfamilies. Patterns of OR evolution within Polistes are consistent with 9-exon OR function in CHC perception by combinatorial coding, with both selection and drift contributing to interspecies differences in copy number and sequence.

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The Multilocus Multispecies Coalescent: A Flexible New Model of Gene Family Evolution

Systematic Biology ◽

10.1093/sysbio/syaa084 ◽

2020 ◽

Author(s):

Qiuyi Li ◽

Celine Scornavacca ◽

Nicolas Galtier ◽

Yao-Ban Chan

Keyword(s):

Gene Family ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Gene Family Evolution ◽

Gene Copy ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

New Model ◽

Multispecies Coalescent

Abstract Incomplete lineage sorting (ILS), the interaction between coalescence and speciation, can generate incongruence between gene trees and species trees, as can gene duplication (D), transfer (T) and loss (L). These processes are usually modelled independently, but in reality, ILS can affect gene copy number polymorphism, i.e., interfere with DTL. This has been previously recognised, but not treated in a satisfactory way, mainly because DTL events are naturally modelled forward-in-time, while ILS is naturally modelled backwards-in-time with the coalescent. Here we consider the joint action of ILS and DTL on the gene tree/species tree problem in all its complexity. In particular, we show that the interaction between ILS and duplications/transfers (without losses) can result in patterns usually interpreted as resulting from gene loss, and that the realised rate of D, T and L becomes non-homogeneous in time when ILS is taken into account. We introduce algorithmic solutions to these problems. Our new model, the multilocus multispecies coalescent (MLMSC), which also accounts for any level of linkage between loci, generalises the multispecies coalescent model and offers a versatile, powerful framework for proper simulation and inference of gene family evolution.

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The origin of the odorant receptor gene family in insects

10.1101/259424 ◽

2018 ◽

Cited By ~ 1

Author(s):

Philipp Brand ◽

Hugh M. Robertson ◽

Wei Lin ◽

Ratnasri Pothula ◽

William E. Klingeman ◽

...

Keyword(s):

Gene Family ◽

Odorant Receptor ◽

Receptor Gene ◽

Evolutionary Novelty ◽

Thermobia Domestica ◽

Genome Data ◽

Chemosensory Gene ◽

Or Gene ◽

Airborne Chemicals ◽

Receptor Gene Family

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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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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The Multilocus Multispecies Coalescent: A Flexible New Model of Gene Family Evolution

10.1101/2020.05.07.081836 ◽

2020 ◽

Author(s):

Qiuyi Li ◽

Celine Scornavacca ◽

Nicolas Galtier ◽

Yao-Ban Chan

Keyword(s):

Gene Family ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Gene Family Evolution ◽

Gene Copy ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

New Model ◽

Multispecies Coalescent

AbstractIncomplete lineage sorting (ILS), the interaction between coalescence and speciation, can generate incongruence between gene trees and species trees, as can gene duplication (D), transfer (T) and loss (L). These processes are usually modelled independently, but in reality, ILS can affect gene copy number polymorphism, i.e., interfere with DTL. This has been previously recognised, but not treated in a satisfactory way, mainly because DTL events are naturally modelled forward-in-time, while ILS is naturally modelled backwards-in-time with the coalescent. Here we consider the joint action of ILS and DTL on the gene tree/species tree problem in all its complexity. In particular, we show that the interaction between ILS and duplications/transfers (without losses) can result in patterns usually interpreted as resulting from gene loss, and that the realised rate of D, T and L becomes non-homogeneous in time when ILS is taken into account. We introduce algorithmic solutions to these problems. Our new model, the multilocus multispecies coalescent (MLMSC), which also accounts for any level of linkage between loci, generalises the multispecies coalescent model and offers a versatile, powerful framework for proper simulation and inference of gene family evolution.

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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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Olfactory receptor gene family evolution in stickleback and medaka fishes

Science China Life Sciences ◽

10.1007/s11427-010-0025-4 ◽

2010 ◽

Vol 53 (2) ◽

pp. 257-266 ◽

Cited By ~ 4

Author(s):

Ming Chen ◽

ZuoGang Peng ◽

ShunPing He

Keyword(s):

Gene Family ◽

Olfactory Receptor ◽

Receptor Gene ◽

Gene Family Evolution ◽

Olfactory Receptor Gene ◽

Receptor Gene Family

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Repellency Mechanism of Natural Guar Gum-Based Film Incorporated with Citral against Brown Planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae)

International Journal of Molecular Sciences ◽

10.3390/ijms23020758 ◽

2022 ◽

Vol 23 (2) ◽

pp. 758

Author(s):

Xiubing Gao ◽

Xianfeng Hu ◽

Feixu Mo ◽

Yi Ding ◽

Ming Li ◽

...

Keyword(s):

Differential Expression ◽

Guar Gum ◽

Defense Mechanism ◽

Insect Pests ◽

Odorant Receptor ◽

Receptor Gene ◽

Insect Pest ◽

Brown Planthopper ◽

Sequencing Analysis ◽

Or Gene

Using of plant essential oil that coevolved as a defense mechanism against agriculture insects is an alternative means of controlling many insect pests. In order to repel brown planthoppers (BPHs), the most notorious rice insect pest, a new film based on guar gum incorporated with citral (GC film) was formulated, which was effective while being environmentally friendly. In this paper, the effect and mechanism of GC film repellency against BPHs were determined. Repellent activity test and olfactory reaction analysis showed that GC film had repellency effect against BPHs, with repellency of 60.00% and 73.93%, respectively. The result of olfactory reaction indicated that GC film repellency against BPHs relied on smell. EPG analysis showed the proportion and mean duration of np waveform were significantly higher than in CK and increased following the treatment concentration, which indicated that GC film affected the recognition of BPHs to rice. Further analysis by RNA sequencing analysis showed a total of 679 genes were significantly upregulated and 284 genes were significantly downregulated in the BPHs fed on the rice sprayed with GC film compared to control. Odorant-binding protein (OBP) gene 797 and gustatory receptor gene (GR)/odorant receptor (OR) gene 13110 showed a significant decrease in differential expression and significant increase in differential expression, respectively. There were 0.66 and 2.55 differential expression multiples between treated BPHs and control, respectively. According to the results described above, we reasoned that GC film repellency against BPHs due to smell, by release of citral, caused the recognition difficulties for BPHs to rice, and OBP gene 797 and GR/OR gene 13110 appeared to be the crucial candidate genes for GC film repellency against BPHs. The present study depicted a clear and consistent repellency effect for GC film against BPHs and preliminarily clarified the mechanism of GC film as a repellent against BPHs, which might offer an alternative approach for control of BPHs in the near future. Our results could also help in the development and improvement of GC films.

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