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

The social environment encountered early during development can temporarily or permanently influence life history decisions and behaviour of individuals and correspondingly shape molecular pathways. In the highly social cichlid fish Neolamprologus pulcher, deprivation of brood care permanently affects social behaviour and alters the expression of stress axis genes in juveniles and adults. It is unclear when gene expression patterns change during early life depending on social experience, and which genes are involved. We compared brain gene expression of N. pulcher at two time points during the social experience phase when juveniles were reared either with or without brood care, and one time point shortly afterwards. We compared (a) whole transcriptomes and (b) expression of 79 genes related to stress regulation, in order to define a neurogenomic state of stress for each fish. At developmental day 75, that is, after the social experience phase, 43 genes were down-regulated in fish having experienced social deprivation, while two genes involved in learning and memory and in post-translational modifications of proteins (PTM), respectively, were up-regulated. Down-regulated genes were mainly associated with immunity, PTM and brain function. In contrast, during the experience phase no genes were differentially expressed when assessing the whole transcriptome. When focusing on the neurogenomic state associated with the stress response, we found that individuals from the two social treatments differed in how their brain gene expression profiles changed over developmental stages. Our results indicate that the early social environment influences the transcriptional activation in fish brains, both during and after an early social experience, possibly affecting plasticity, immune system function and stress axis regulation.

Divergence of developmental trajectories is triggered interactively by early social and ecological experience in a cooperative breeder.

Cooperative breeders feature the highest level of social complexity among vertebrates. Environmental constraints foster the evolution of this form of social organization, selecting for both well-developed social and ecological competences. Cooperative breeders pursue one of two alternative social trajectories: delaying reproduction to care for the offspring of dominant breeders or dispersing early to breed independently. It is yet unclear which ecological and social triggers determine the choice between these alternatives and whether diverging developmental trajectories exist in cooperative vertebrates predisposing them to dispersal or philopatry. Here we experimentally reared juveniles of cooperatively breeding cichlid fish by varying the social environment and simulated predation threat in a two-by-two factorial long-term experiment. First, we show that individuals develop specialized behavioral competences, originating already in the early postnatal phase. Second, these specializations predisposed individuals to pursue different developmental trajectories and either to disperse early or to extend philopatry in adulthood. Thus, our results contrast with the proposition that social specializations in early ontogeny should be restricted to eusocial species. Importantly, social and ecological triggers were both required for the generation of divergent life histories. Our results thus confirm recent predictions from theoretical models that organisms should combine relevant information from different environmental cues to develop integrated phenotypes.

Evolutionary conserved neural signature of early life stress affects animal social competence.

In vertebrates, the early social environment can persistently influence behaviour and social competence later in life. However, the molecular mechanisms underlying variation in animal social competence are largely unknown. In rats, high-quality maternal care causes an upregulation of hippocampal glucocorticoid receptors (gr) and reduces offspring stress responsiveness. This identifies gr regulation as a candidate mechanism for maintaining variation in animal social competence. We tested this hypothesis in a highly social cichlid fish, Neolamprologus pulcher, reared with or without caring parents. We find that the molecular pathway translating early social experience into later-life alterations of the stress axis is homologous across vertebrates: fish reared with parents expressed the glucocorticoid receptor gr1 more in the telencephalon. Furthermore, expression levels of the transcription factor egr-1 (early growth response 1) were associated with gr1 expression in the telencephalon and hypothalamus. When blocking glucocorticoid receptors (GR) with an antagonist, mifepristone (RU486), parent-reared individuals showed more socially appropriate, submissive behaviour when intruding on a larger conspecific's territory. Remarkably, mifepristone-treated fish were less attacked by territory owners and had a higher likelihood of territory takeover. Our results indicate that early social-environment effects on stress axis programming are mediated by an evolutionary conserved molecular pathway, which is causally involved in environmentally induced variation of animal social competence.

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

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.