Effect of the early social environment on behavioural and genomic responses to a social challenge in a cooperatively breeding vertebrate

Abstract

The early social environment can have substantial, lifelong effects on vertebrate social behaviour, which can be mediated by developmental plasticity of brain gene expression. Early-life effects can influence immediate behavioural responses towards later-life social challenges and can activate different gene expression responses. However, while genomic responses to social challenges have been reported frequently, how developmental experience influences the shape of these genomic reaction norms remains largely unexplored. We tested how manipulating the early social environment of juvenile cooperatively breeding cichlids, Neolamprologus pulcher, affects their behavioural and brain genomic responses when competing over a resource. Juveniles were reared either with or without a breeder pair and a helper. Fish reared with family members behaved more appropriately in the competition than when reared without. We investigated whether the different social rearing environments also affected the genomic responses to the social challenge. A set of candidate genes, coding for hormones and receptors influencing social behaviour, were measured in the telencephalon and hypothalamus. Social environment and social challenge both influenced gene expression of egr-1 (early growth response 1) and gr1 (glucocorticoid receptor 1) in the telencephalon and of bdnf (brain-derived neurotrophic factor) in the hypothalamus. A global analysis of the 11 expression patterns in the two brain areas showed that neurogenomic states diverged more strongly between intruder fish and control fish when they had been reared in a natural social setting. Our results show that same molecular pathways may be used differently in response to a social challenge depending on early-life experiences.

Transcriptomic signatures of social experience during early development in a highly social cichlid fish

“…Future studies will reveal whether the observed expression differences are also causally related to age‐dependent social behavioural changes during early development, and whether these gene expression differences are transient or permanent. Previous studies in N. pulcher established that the early social environment affects molecular mechanisms of stress regulation much later in life and that the effects on stress axis programming are mediated by an evolutionary conserved molecular pathway in these fish (Nyman et al, , ; Taborsky et al, ). These studies, however, treated molecular processes during the important social experience phase essentially as a black box.…”

“…N. pulcher possess a large and refined repertoire of affiliative, submissive and aggressive social behaviours used to navigate the complexities of their social environment (Taborsky & Oliveira, ), helping to resolve within‐group conflict and to maintain group stability (Taborsky, ; Taborsky & Taborsky, ). The early social environment during the first two months after reaching the fry stage strongly influences the ability to express this behavioural repertoire in an appropriate, context‐specific manner (Arnold & Taborsky, ; Fischer et al, ; Nyman et al, , ; Taborsky et al, ).…”

“…Through developmental plasticity, the social environment experienced during the early life of an individual can persistently shape its phenotype (Adkins‐Regan & Krakauer, ; Arnold & Taborsky, ; Feng et al, ; Francis, Diorio, Liu, & Meaney, ; Liu et al, ; Nyman, Fischer, Aubin‐Horth, & Taborsky, ; Taborsky, Arnold, Junker, & Tschopp, ; see review Taborsky, ). For instance, early social experience can influence individual life history decisions (Fischer, Bohn, Oberhummer, Nyman, & Taborsky, ), maternal behaviour (Francis et al, ), learning and memory (Champagne et al, ), mate choice decisions (Adkins‐Regan & Krakauer, ), alcohol abuse (Higley, Hasert, Suomi, & Linnoila, ) and fitness (reviewed in Taborsky, ).…”

“…In vertebrates, the hypothalamus–pituitary–adrenal/interrenal (HPA/HPI) axis has been proposed as a central mechanism responsible for long‐term effects of early social experience (Arnold & Taborsky, ; Banerjee, Arterbery, Fergus, & Adkins‐Regan, ; Fischer et al, ; Francis et al, ; Liu et al, ; Nyman et al, ; Nyman, Fischer, Aubin‐Horth, & Taborsky, ; Taborsky, Tschirren, Meunier, & Aubin‐Horth, ). Hippocampal glucocorticoid receptors (GRs) are implicated in the negative feedback loop controlling glucocorticoid production, which promotes termination of the stress response (de Kloet, ).…”

“…In rat pups, gene expression of gr in the hippocampus is increased with higher quality of maternal care (Liu et al, ) resulting in more stress‐resilient individuals. Likewise, in the highly social cichlid fish Neolamprologus pulcher, individuals reared with (vs. without) brood caring group members are less neophobic (Bannier, Tebbich, & Taborsky, ) and more socially competent as juveniles (Arnold & Taborsky, ; Nyman et al, ) and adults (Taborsky et al, ) and feature a persistently altered stress gene expression in the brain (Nyman et al, , ; Taborsky et al, ). In Japanese quails, pharmacologically activating the stress response causes large‐scale changes in gene expression in adults, including hormone receptors implicated in the regulation of serotonin, somatostatin and corticotrophin‐releasing factor (Marasco et al, ).…”