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.

Early social experience has life-long effects on baseline but not stress-induced cortisol levels in a cooperatively breeding fish.

In cooperatively breeding cichlid fish, the early social environment has lifelong effects on the offspring's behaviour, life-history trajectories and brain gene expression. Here, we asked whether the presence or absence of parents and subordinate helpers during early life also shapes fluctuating levels of cortisol, the major stress hormone in the cichlid Neolamprologus pulcher. To non-invasively characterize baseline and stress-induced cortisol levels, we adapted the 'static' holding-water method often used to collect waterborne steroid hormones in aquatic organisms by including a flow-through system allowing for repeated sampling without handling of the experimental subjects. We used 8-year-old N. pulcher either raised with (+F) or without (-F) parents and helpers in early life. We found that N. pulcher have a peak of their circadian cortisol cycle in the early morning, and that they habituated to the experimental procedure after four days. Therefore, we sampled the experimental fish in the afternoon after four days of habituation. -F fish had significantly lower baseline cortisol levels, whereas stress-induced cortisol levels did not differ between treatments. Thus, we show that the early social environment has life-long effects on aspects of the physiological stress system of the Hypothalamic-Pituitary-Interrenal (HPI) axis. We discuss how these differences in physiological state may have contributed to the specialization in different social and life-history trajectories of this species.

The role of serotonin in modulating social competence in a cooperatively breeding fish.

Behavioural interactions between conspecifics rely on the appreciation of social cues, which is achieved through biochemical switching of pre-existing neurophysiological pathways. Serotonin is one of the major neurotransmitters in the central nervous system responsible for the modulation of physiological and behavioural traits, in particular social behaviour. The relative importance of serotonin in modulating optimal social responses to the available social information (i.e., social competence) is yet unknown. Here we investigate how serotonin and the serotonin 1 A receptor (5-HT1A) modulate social competence in a competitive context. In the cooperatively breeding cichlid Neolamprologus pulcher, we pharmacologically manipulated the serotonin availability and 5-HT1A activity to test their effects on social behaviours during an asymmetric contest between the owner of a defended territory containing a shelter and an intruder devoid of a territory. In this contest, the adequate response by the intruders, the focal individuals in our study, is to show submissive behaviour in order to avoid eviction from the vicinity of the shelter. While the serotonin enhancer Fluoxetine did not affect the frequency of submission towards territory owners, reducing serotonin by a low dosage of 4-Chloro-DL-phenylalanine (PCPA) increased submissive behaviour. Furthermore, threat displays towards territory owners were reduced at high dosages of Fluoxetine and also at the lowest dosage of PCPA. 5-HT1A activation increased threat displays by intruders, indicating that this receptor may not be involved in regulating social competence. We conclude that serotonin, but not its receptor 5-HT1A plays an important role in the regulation of social competence.

Dopamine modulates social behaviour in cooperatively breeding fish.

Dopamine is part of the reward system triggering the social decision-making network in the brain. It has hence great potential importance in the regulation of social behaviour, but its significance in the control of behaviour in highly social animals is currently limited. We studied the role of the dopaminergic system in social decision-making in the cooperatively breeding cichlid fish, Neolamprologus pulcher, by blocking or stimulating the dopaminergic D1-like and D2-like receptors. We first tested the effects of different dosages and timing of administration on subordinate group members' social behaviour within the group in an unchallenging environment. In a second experiment we pharmacologically manipulated D1-like and D2-like receptors while experimentally challenging N. pulcher groups by presenting an egg predator, and by increasing the need for territory maintenance through digging out sand from the shelter. Our results show that the D1-like and D2-like receptor pathways are differently involved in the modulation of aggressive, submissive and affiliative behaviours. Interestingly, the environmental context seems particularly crucial regarding the role of the D2-like receptors in behavioural regulation of social encounters among group members, indicating a potential pathway in agonistic and cooperative interactions in a pay-to-stay scenario. We discuss the importance of environmental information in mediating the role of dopamine for the modulation of social behaviour.

Early social and ecological experience triggers divergent reproductive investment strategies in a cooperative breeder.

Unlike eusocial systems, which are characterized by reproductive division of labour, cooperative breeders were predicted not to exhibit any reproductive specialization early in life. Nevertheless, also cooperative breeders face a major life-history decision between dispersal and independent breeding vs staying as helper on the natal territory, which might affect their reproductive strategies. In the cooperatively-breeding cichlid Neolamprologus pulcher early-life social and predator experiences induce two behavioural types differing in later-life social and dispersal behaviour. We performed a long-term breeding experiment to test whether the two early-life behavioural types differ in their reproductive investment. We found that the early-dispersing type laid fewer and smaller eggs, and thus invested overall less in reproduction, compared to the philopatric type. Thus N. pulcher had specialised already shortly after birth for a dispersal and reproductive strategy, which is in sharp contrast to the proposition that reproductively totipotent cooperative breeders should avoid reproductive specialization before adulthood.