Highlights
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Single-cell RNA-seq identifies hormone-degrading esterase CfJhe localized to ant BBB
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CfJhe expression is high in non-foraging Major-worker BBB cells leading to low JH3
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Ectopic expression of CfJhe in fly leads to loss of foraging-like behavior
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KD of CfJhe leads to acquisition of foraging in Major workers
Summary
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.
Ju, L. et al. Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants. Cell https://doi.org/10.1016/j.cell.2023.08.002 (2023)
See also:
Epigenetic control of caste-specific foraging
In carpenter ants, separate behavioral classes, known as castes, are determined by the epigenetic regulation of genes. Simola et al. treated ants of different castes with drugs that affected histone acetylation. Reducing histone acetylation stimulated scouting and foraging behavior. The foraging and scouting behaviors of young ants were permanently changed by directly injecting their brains with histone acetylation inhibitors.
SCIENCE, 1 Jan 2016 Vol 351, Issue 6268, DOI: 10.1126/science.aac6633
