Egg-mediated maternal effects in a cooperatively breeding cichlid fish.

Mothers can influence offspring phenotype through egg-mediated maternal effects, which can be influenced by cues mothers obtain from their environment during offspring production. Developing embryos use these components but have mechanisms to alter maternal signals. Here we aimed to understand the role of mothers and embryos in how maternal effects might shape offspring social phenotype. In the cooperatively breeding fish Neolamprologus pulcher different social phenotypes develop in large and small social groups differing in predation risk and social complexity. We manipulated the maternal social environment of N. pulcher females during egg laying by allocating them either to a small or a large social group. We compared egg mass and clutch size and the concentration of corticosteroid metabolites between social environments, and between fertilized and unfertilized eggs to investigate how embryos deal with maternal signalling. Mothers in small groups produced larger clutches but neither laid smaller eggs nor bestowed eggs differently with corticosteroids. Fertilized eggs scored lower on a principal component representing three corticosteroid metabolites, namely 11-deoxycortisol, cortisone, and 11-deoxycorticosterone. We did not detect egg-mediated maternal effects induced by the maternal social environment. We discuss that divergent social phenotypes induced by different group sizes may be triggered by own offspring experience.

Stress axis programming generates long-term effects on cognitive abilities in a cooperative breeder.

The ability to flexibly adjust behaviour to social and non-social challenges is important for successfully navigating variable environments. Social competence, i.e. adaptive behavioural flexibility in the social domain, allows individuals to optimize their expression of social behaviour. Behavioural flexibility outside the social domain aids in coping with ecological challenges. However, it is unknown if social and non-social behavioural flexibility share common underlying cognitive mechanisms. Support for such shared mechanism would be provided if the same neural mechanisms in the brain affected social and non-social behavioural flexibility similarly. We used individuals of the cooperatively breeding fish Neolamprologus pulcher that had undergone early-life programming of the hypothalamic-pituitary-interrenal axis by exposure to (i) cortisol, (ii) the glucocorticoid receptor antagonist mifepristone, or (iii) control treatments, and where effects of stress-axis programming on social flexibility occurred. One year after the treatments, adults learned a colour discrimination task and subsequently, a reversal-learning task testing for behavioural flexibility. Early-life mifepristone treatment marginally enhanced learning performance, whereas cortisol treatment significantly reduced behavioural flexibility. Thus, early-life cortisol treatment reduced both social and non-social behavioural flexibility, suggesting a shared cognitive basis of behavioural flexibility. Further our findings imply that early-life stress programming affects the ability of organisms to flexibly cope with environmental stressors.

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.

Early-life manipulation of cortisol and its receptor alters stress axis programming and social competence.

In many vertebrate species, early social experience generates long-term effects on later life social behaviour. These effects are accompanied by persistent modifications in the expression of genes implicated in the stress axis. It is unknown, however, whether stress axis programming can affect the development of social competence, and if so, by which mechanism(s). Here, we used pharmacological manipulations to persistently reprogramme the hypothalamic-pituitary-interrenal axis of juvenile cooperatively breeding cichlids, Neolamprologus pulcher. During the first two months of life, juveniles were repeatedly treated with cortisol, mifepristone or control treatments. Three months after the last manipulation, we tested for treatment effects on (i) social competence, (ii) the expression of genes coding for corticotropin-releasing factor ( crf), glucocorticoid receptor ( gr1) and mineralocorticoid receptor ( mr) in the telencephalon and hypothalamus and (iii) cortisol levels. Social competence in a social challenge was reduced in cortisol-treated juveniles, which is in accordance with previous work applying early-life manipulations using different social experiences. During early life, both cortisol and mifepristone treatments induced a persistent downregulation of crf and upregulation of mr in the telencephalon. We suggest that these persistent changes in stress gene expression may represent an effective physiological mechanism for coping with stress. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.