Single-nucleus profiling of social behaviour in a mutualistic reef fish

Complex social decision-making in vertebrates relies on a conserved network within the forebrain. However, the precise neural cell populations and gene regulatory networks that orchestrate these sophisticated social behaviours remain largely unresolved. Here, we present the first single-nucleus transcriptome atlas of the telencephalon in the cleaner wrasse Labroides dimidiatus, a remarkable model for advanced social cognition. Profiling ~67,000 telencephalic nuclei, we mapped the neural architecture of the teleost forebrain and identified highly conserved cell populations including a cholinergic-GABAergic neuron population implicated in social behaviours and cells resembling mammalian striatal medium spiny neurons and hippocampal cell types. By comparing distinct behavioural states, we found that socially interacting fish expanded radial glial subclusters, and associative learning co-expression networks, whereas social observers exhibited gene expression signatures for motivation and behavioural preparedness. Ultimately, the resolved telencephalon atlas reveals the evolutionarily conserved cellular and molecular substrates that may govern complex social behaviour across vertebrates.