Early social deprivation shapes neuronal programming of the social decision‐making network in a cooperatively breeding fish

The early social environment an animal experiences may have pervasive effects on its behaviour. The social decision‐making network (SDMN), consisting of interconnected brain nuclei from the forebrain and midbrain, is involved in the regulation of behaviours during social interactions. In species with advanced sociality such as cooperative breeders, offspring are exposed to a large number and a great diversity of social interactions every day of their early life. This diverse social environment may have life‐long consequences on the development of several neurophysiological systems within the SDMN, although these effects are largely unknown. We studied these life‐long effects in a cooperatively breeding fish, Neolamprologus pulcher, focusing on the expression of genes involved in the monoaminergic and stress response systems in the SDMN. N. pulcher fry were raised until an age of 2 months either with their parents, subordinate helpers and same‐clutch siblings (+F), or with same‐clutch siblings only (−F). Analysis of the expression of glucocorticoid receptor, mineralocorticoid receptor, corticotropin releasing factor, dopamine receptors 1 and 2, serotonin transporter and DNA methyltransferase 1 genes showed that early social experiences altered the neurogenomic profile of the preoptic area. Moreover, the dopamine receptor 1 gene was up‐regulated in the preoptic area of −F fish compared to +F fish. −F fish also showed up‐regulation of GR1 expression in the dorsal medial telencephalon (functional equivalent to the basolateral amygdala), and in the dorsolateral telencephalon (functional equivalent to the hippocampus). Our results suggest that early social environment has life‐long effects on the development of several neurophysiological systems within the SDMN.