An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants

Hua Yan, Comzit Opachaloemphan, Giacomo Mancini, Huan Yang, Matthew Gallitto, Jakub Mlejnek, Alexandra Leibholz, Kevin Haight, Majid Ghaninia Tabarestani, Lucy Huo, Michael Perry, Jesse Slone, Xiaofan Zhou, Maria Traficante, Clint Penick, Kelly Dolezal, Kaustubh Gokhale, Kelsey Stevens, Ingrid Fetter-Pruneda, Roberto BonasioLaurence J. Zwiebel, Shelley L. Berger, Juergen Liebig, Danny Reinberg, Claude Desplan

Research output: Contribution to journalArticle

62 Scopus citations

Abstract

Ants exhibit cooperative behaviors and advanced forms of sociality that depend on pheromone-mediated communication. Odorant receptor neurons (ORNs) express specific odorant receptors (ORs) encoded by a dramatically expanded gene family in ants. In most eusocial insects, only the queen can transmit genetic information, restricting genetic studies. In contrast, workers in Harpegnathos saltator ants can be converted into gamergates (pseudoqueens) that can found entire colonies. This feature facilitated CRISPR-Cas9 generation of germline mutations in orco, the gene that encodes the obligate co-receptor of all ORs. orco mutations should significantly impact olfaction. We demonstrate striking functions of Orco in odorant perception, reproductive physiology, and social behavior plasticity. Surprisingly, unlike in other insects, loss of OR functionality also dramatically impairs development of the antennal lobe to which ORNs project. Therefore, the development of genetics in Harpegnathos establishes this ant species as a model organism to study the complexity of eusociality.

Original languageEnglish (US)
Pages (from-to)736-747.e9
JournalCell
Volume170
Issue number4
DOIs
StatePublished - Aug 10 2017

Keywords

  • CRISPR
  • Harpegnathos saltator
  • Orco
  • ant
  • eusocial insect
  • glomerulus
  • neural development
  • odorant receptor
  • odorant receptor neurons
  • pheromone
  • reproduction
  • social behavior

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

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    Yan, H., Opachaloemphan, C., Mancini, G., Yang, H., Gallitto, M., Mlejnek, J., Leibholz, A., Haight, K., Ghaninia Tabarestani, M., Huo, L., Perry, M., Slone, J., Zhou, X., Traficante, M., Penick, C., Dolezal, K., Gokhale, K., Stevens, K., Fetter-Pruneda, I., ... Desplan, C. (2017). An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants. Cell, 170(4), 736-747.e9. https://doi.org/10.1016/j.cell.2017.06.051