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

Andrew W. Legan, Christopher . M Jernigan, Sara Miller, Matthieu F Fuchs, Michael J. Sheehan

Research output: Contribution to journalArticlepeer-review

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 ( d N / d S ) 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.
Original languageAmerican English
JournalMolecular Biology and Evolution
Volume38
DOIs
StatePublished - Sep 2021

Keywords

  • antennal lobe glomeruli
  • birth-and-death process
  • comparative genomics
  • olfaction
  • social insect
  • tandem array

Disciplines

  • Biology

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