Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants

Linyang Ju, Karl M. Glastad, Lihong Sheng, Janko Gospocic, Callum J. Kingwell, Shawn M. Davidson, Sarah D. Kocher, Roberto Bonasio, Shelley L. Berger

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Here, we reveal an unanticipated role of the blood-brain barrier (BBB) in regulating complex social behavior in ants. Using scRNA-seq, we find localization in the BBB of a key hormone-degrading enzyme called juvenile hormone esterase (Jhe), and we show that this localization governs the level of juvenile hormone (JH3) entering the brain. Manipulation of the Jhe level reprograms the brain transcriptome between ant castes. Although ant Jhe is retained and functions intracellularly within the BBB, we show that Drosophila Jhe is naturally extracellular. Heterologous expression of ant Jhe into the Drosophila BBB alters behavior in fly to mimic what is seen in ants. Most strikingly, manipulation of Jhe levels in ants reprograms complex behavior between worker castes. Our study thus uncovers a remarkable, potentially conserved role of the BBB serving as a molecular gatekeeper for a neurohormonal pathway that regulates social behavior.

Original languageEnglish (US)
Pages (from-to)4289-4309.e23
JournalCell
Volume186
Issue number20
DOIs
StatePublished - Sep 28 2023

All Science Journal Classification (ASJC) codes

  • General Biochemistry, Genetics and Molecular Biology

Keywords

  • blood-brain barrier
  • gene regulation
  • hormones
  • plasticity
  • scRNA-seq
  • social behavior
  • social insects

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