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. 2021 Aug 23;38(9):3832-3846.
doi: 10.1093/molbev/msab023.

Expansion and Accelerated Evolution of 9-Exon Odorant Receptors in Polistes Paper Wasps

Andrew W Legan  1 , Christopher M Jernigan  1 , Sara E Miller  1 , Matthieu F Fuchs  1 , Michael J Sheehan  1
Affiliations

Expansion and Accelerated Evolution of 9-Exon Odorant Receptors in Polistes Paper Wasps

Andrew W Legan et al. Mol Biol Evol. .

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 OR 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 (dN/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 (relaxed 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.

Keywords: antennal lobe glomeruli; birth-and-death process; comparative genomics; olfaction; social insect; tandem array.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.
Phylogeny of five Polistes species considered in this study: P. fuscatus, P. metricus, P. dorsalis, P. canadensis, and P. dominula. The photo to the right of the phylogeny shows P. fuscatus foundresses on a nest. Phylogenetic tree based on the 16S ribosomal RNA gene and the cytochrome oxidase subunit I gene.
Fig. 2.
Fig. 2.
The number of functional ORs is correlated with the number of antennal lobe glomeruli across insect species (50 glomeruli and 62 ORs in the genome of the common fruit fly D. melanogaster, Fishilevich and Vosshall 2005; 166 glomeruli in the worker and 163 intact ORs in the genome of the honey bee A. mellifera, Arnold et al. 1985, Robertson and Wanner 2006; ∼200 glomeruli in females and 225 intact ORs in the genome of the parasitic wasp N. vitripennis, Groothuis et al. 2019, Robertson et al. 2010; ∼434 glomeruli in the worker and 352 functional ORs in the genome of the ant C. floridanus, Zube and Rössler 2008, Zhou et al. 2012; 493 glomeruli in the worker and 503 intact ORs in the genome of the ant O. biroi, McKenzie et al. 2016; McKenzie and Kronauer 2018). The diagonal line represents a line of equality with slope of 1.
<sc>Fig</sc>. 3.
Fig. 3.
Maximum likelihood OR protein tree constructed using data from four Hymenopterans (Apis mellifera, Robertson and Wanner 2006; Camponotus floridanus, Zhou et al. 2012; Nasonia vitripennis, Robertson et al. 2010). Branches are colored by species (Red: C. floridanus; Light blue: A. mellifera; Green: P. fuscatus; Purple: N. vitripennis). The L and 9-exon OR subfamilies are highlighted. Scale bar represents 0.5 mean substitutions per site.
<sc>Fig</sc>. 4.
Fig. 4.
Cladogram of Hymenoptera species showing estimated number of OR gene gain and loss events along branches and estimated size of ancestral and extant species OR repertoires in boxes. To the right is a bar chart showing numbers of ORs broken down by subfamily. Non-Polistine OR data are from Robertson et al. (2010) and Zhou et al. (2012, 2015). The set of intact ORs that were longer than 300 amino acids was used except for C. floridanus in the bar chart, where only ORs considered putatively functional by Zhou et al. (2012) were used.
Fig. 5.
Fig. 5.
(A) Maximum likelihood OR protein tree with branches colored by species (Green: Polistes fuscatus; Yellow: P. metricus; Orange: P. dorsalis; Magenta: P. canadensis; Blue: P. dominula). The L and 9-exon subfamilies are highlighted. Scale bar represents 0.4 mean substitutions per site. (B) Stacked bar chart showing the number of Polistes species (x-axis) represented in each orthologous group (y-axis), and whether or not each orthologous group is single copy (shaded bottom portion of bar) or contains an expansion in at least one species (top-striped portion of bar). Orthologous groups are split into two categories: non-9-exon orthologous groups (“non-9e” left bar) and 9-exon orthologous groups (right bar).
Fig. 6.
Fig. 6.
(A) Frequency of OR gene singletons and tandem arrays in the Polistes fuscatus genome. 62% of ORs in P. fuscatus occur in tandem arrays of six or more genes. The longest tandem array is a 44 gene cluster on scaffold 13 (s13) containing 9-exon subfamily ORs. The first row of x-axis labels is the number of OR genes in a tandem array cluster, and the second row labels the OR subfamily and scaffold number (abbreviated s# in parentheses) of the six longest tandem arrays. (B) Genome alignments of four loci containing tandem arrays of OR genes in all Polistes species examined. Each alignment is labeled with the corresponding OR subfamily and P. fuscatus scaffold number. Black boxes represent putatively functional genes (≥300 amino acids) and gray boxes represent pseudogenes. Directionality of genes is denoted by curved corners at the 3' (tail) end. Black lines connect orthologous genes between species. Genomic scaffolds are represented by horizontal, gray lines, and scaffold ends are represented by vertical gray lines. Scale bars beneath each alignment represent 5 kb.
<sc>Fig</sc>. 7.
Fig. 7.
Percent amino acid identity between neighboring genes at eight loci containing the longest OR gene tandem arrays in the P. fuscatus genome. Arrays are ordered by length in gene number, from longest (44 9-exon subfamily ORs in the s13 tandem array) to shortest (6 H subfamily ORs in the s6 tandem array and 6 V subfamily ORs in the s19 tandem array).
<sc>Fig</sc>. 8.
Fig. 8.
The values of dS (x-axis) and dN (y-axis) from pairwise alignments of Polistes fuscatus and P. dorsalis 1:1 orthologs. Values of dN are elevated in the 9-exon OR subfamily (data points represented by red triangles) relative to other OR subfamilies (data points represented by circles). The diagonal line represents a line of equality with slope of 1.
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