Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?

Viet Dai Dang, Amir B. Cohanim, Silvia Fontana, Eyal Privman, John Wang

Research output: Contribution to journalArticlepeer-review

Abstract

Queen discrimination behavior in the fire ant Solenopsis invicta maintains its two types of societies: colonies with one (monogyne) or many (polygyne) queens, yet the underlying genetic mechanism is poorly understood. This behavior is controlled by two supergene alleles, SB and Sb, with ~600 genes. Polygyne workers, having either the SB/SB or SB/Sb genotype, accept additional SB/Sb queens into their colonies but kill SB/SB queens. In contrast, monogyne workers, all SB/SB, reject all additional queens regardless of genotype. Because the SB and Sb alleles have suppressed recombination, determining which genes within the supergene mediate this differential worker behavior is difficult. We hypothesized that the alternate worker genotypes sense queens differently because of the evolution of differential expression of key genes in their main sensory organ, the antennae. To identify such genes, we sequenced RNA from four replicates of pooled antennae from three classes of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb. We identified 81 differentially expressed protein-coding genes with 13 encoding potential chemical metabolism or perception proteins. We focused on the two odorant perception genes: an odorant receptor SiOR463 and an odorant-binding protein SiOBP12. We found that SiOR463 has been lost in the Sb genome. In contrast, SiOBP12 has an Sb-specific duplication, SiOBP12b′, which is expressed in the SB/Sb worker antennae, while both paralogs are expressed in the body. Comparisons with another fire ant species revealed that SiOBP12b′ antennal expression is specific to S. invicta and suggests that queen discrimination may have evolved, in part, through expression neofunctionalization.

Original languageEnglish
Pages (from-to)12754-12766
Number of pages13
JournalEcology and Evolution
Volume9
Issue number22
DOIs
StatePublished - 1 Nov 2019

Bibliographical note

Publisher Copyright:
© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Keywords

  • RNA-Seq
  • Solenopsis invicta
  • fire ant
  • neofunctionalization
  • odorant-binding protein
  • worker antennae

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Ecology
  • Nature and Landscape Conservation

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