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Social species rely on acquiring appropriate social skills to navigate their social environment. Developmental plasticity allows individuals to develop an appropriate phenotype by receiving cues from their social and nonsocial environment. However, committing to a specific phenotype early in life may prove maladaptive if there is a mismatch between the early and future environment. To address potential mismatches, multiple or extended sensitive periods provide opportunities for individuals to gather the necessary information in changing and predictable environments. Cooperative breeders, like the highly social cichlid Neolamprologus pulcher , typically experience changing environments especially during dispersal. While we know that early development is critical for the acquisition of social competence, it remains uncertain whether a second or extended sensitive period exists around the time of dispersal decisions in cooperative breeders. Here we manipulated the early and late life social environment of N. pulcher and asked whether individuals retain plasticity to adjust their social phenotype around sexual maturation. Juveniles were raised for 2 months with or without adults and tested for social competence. Shortly before reaching sexual maturity, they were randomly assigned to be housed alone, with siblings or with a social group for an additional 2 months before undergoing further social competence testing. Aggressive and submissive behaviours were assessed in two social contexts. Fish raised with a large group exhibited greater social competence compared to those raised only among siblings, regardless of subsequent social experiences. This suggests that either early life cues reliably predict future environments in nature or that constraints on late life plasticity exist. • We study the acquisition of social competence in cooperatively breeding fish. • We investigate whether sensitive periods exist early and late in life. • Early development is critical in acquiring social competence in Neolamprologus pulcher. • Later development does not influence the social competence in N. pulcher. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Juveniles of the cooperatively breeding cichlid fish Neolamprologus pulcher either consistently provide help in form of alloparental egg care ("cleaners") or consistently abstain from helping ("noncleaners"). These phenotypes are not based on heritable genetic differences. Instead, they arise during ontogeny, which should lead to differences in brain structure or physiology, a currently untested prediction. We compared brain gene expression profiles of cleaners and noncleaners in two experimental conditions, a helping opportunity and a control condition. We aimed to identify (a) expression differences between cleaners and noncleaners in the control, (b) changes in gene expression induced by the opportunity and (c) differences in plasticity of gene expression between cleaners and noncleaners. Control cleaners and noncleaners differed in the expression of a single gene, irx2, which regulates neural differentiation. During the opportunity, cleaners and noncleaners had three upregulated genes in common, which were implicated in neuroplasticity, hormonal signalling and cell proliferation. Thus, the stimulus in the opportunity was sufficiently salient. Cleaners also showed higher expression of seven additional genes that were unique to the opportunity. One of these cleaner‐specific genes is implicated in neuropeptide metabolism, indicating that this process is associated with cleaning performance. This suggests that the two types employed different pathways to integrate social information, preparing them for accelerated reaction to future opportunities. Interestingly, three developmental genes were downregulated between the control and the opportunity in cleaners only. Our results indicate that the two behavioural types responded differently to the helping opportunity and that only cleaners responded by downregulating developmental genes. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

The ability to respond flexibly to environmental challenges, for instance by learning or by responding appropriately to novel stimuli, may be crucial for survival and reproductive success. Experiences made during early ontogeny can shape the degree of behavioural flexibility maintained by individuals during later life. In natural habitats, animals are exposed to a multitude of social and non-social ecological factors during early ontogeny, but their relative influences on future learning ability and behavioural flexibility are only poorly understood. In the cooperatively breeding cichlid Neolamprologus pulcher, we investigated whether early social and predator experiences shape the learning performance, flexibility, and response to novelty of adults. Fish were reared either with or without parents and helpers and with or without perceived predation risk in a full-factorial experiment. We investigated the influence of these treatments on learning performance and flexibility in a spatial acquisition and reversal learning task. To test for response to novelty, we performed a neophobia test. We found that fish reared with predator experience, but without the presence of older group members outperformed fish with other rearing backgrounds in reversal learning and that individuals, which had been reared in a socially more complex environment together with older group members responded less neophobic toward a novel object than individuals reared among siblings only. Comparative evidence from fish and rats suggests that these developmental effects may be driven by the cues of safety perceived in the presence of guarding parents. [ABSTRACT FROM AUTHOR]

Social competence is defined as the ability of an animal to optimize the expression of social behaviour as a function of the available social information. The social environment encountered early in life can affect the expression of various social behaviours later in life. We investigated whether early social experience can affect social competence. In the cooperatively breeding cichlid Neolamprologus pulcher, we tested whether individuals reared with older brood-caring conspecifics persistently perform better in a series of tasks (1) simulating different social contexts, (2) assigning individuals different social roles and (3) exposing them to an unknown social situation. Fish that had been reared together with older conspecifics showed more appropriate behaviours both as winners (more aggressive displays) and as losers (more submissive displays) when aggressively competing with peers over a resource, and when trying to be accepted as subordinate group member and prospective brood care helper by an unfamiliar dominant pair (more submissive displays near shelters), a situation they had never encountered before. In both tasks fish that had grown up with older fish were tolerated better by conspecifics than fish reared with same-age siblings only. We detected effects of the early environment on social behaviour in the juvenile and adult stages of the test fish. Our results suggest that growing up in more complex social groups fosters a general social ability (i.e. social competence) in N. pulcher that improves their performance across different social roles and contexts, and which may provide fitness benefits. [Copyright &y& Elsevier]

Winner and loser effects are widespread among animal taxa and are known to influence hierarchy formation, although it is unclear how rank influences such effects in species organized in social hierarchies. We investigated the existence of winner and loser effects and the effect of social rank on such effects in Neolamprologus pulcher , a cooperatively breeding cichlid fish. Social groups of these fish are organized in strict linear, size-based hierarchies. We successively assigned a dominant or subordinate rank to each of 18 focal individuals in balanced order, followed by an assigned winning or losing experience, respectively, resulting in a two-by-two factorial design. For each of the four treatment combinations, we recorded the performance of the focal fish in contests over a resource with similar-sized, naïve opponents. Assigned winners won subsequent contests more often than losers, were more likely to escalate the contest and showed more overt aggression during a contest. Moreover, individuals with assigned subordinate rank showed more restrained aggression. However, winner and loser effects were not modulated by rank. This study shows that winner–loser effects exist in a highly social fish with linear social hierarchy. Moreover, fighting experience and rank may play complementary roles in conflict resolution. • Whether social hierarchy position influences winner-loser effects is unknown. • In a fully crossed design, we manipulated current rank and winning experience. • Assigned winners showed more aggression and escalated contests more than losers. • Assigned subordinates showed more threat behaviour than dominants. • Rank and winning experience affect contests complementarily but not interactively. [ABSTRACT FROM AUTHOR]

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-HT 1A) modulate social competence in a competitive context. In the cooperatively breeding cichlid Neolamprologus pulcher , we pharmacologically manipulated the serotonin availability and 5-HT 1A 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-HT 1A 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-HT 1A plays an important role in the regulation of social competence. [ABSTRACT FROM AUTHOR]

In many species, aggressive individuals outcompete their less aggressive conspecifics for resources such as food and access to mates. Nevertheless, variation in aggression is maintained in populations, but the underlying mechanisms are not well understood. Here we tested the hypothesis that aggressive behaviours compromise the antipredator behaviour of prey, which would link aggressive behaviours to a cost of predation. We presented computer-animated images of predators to the cooperatively breeding cichlid fish Neolamprologus pulcher either during territorial contests with a group of territory intruders or when the test fish were alone. We investigated their response latencies and the behaviour directed towards predator images. We found that test fish responded to the predator images significantly later during territorial contests than when they were alone. Moreover, during territorial contests, response latencies of test fish increased with increasing levels of aggression towards conspecifics. Test fish also responded more aggressively to the predator images during territorial contests than when they were alone. During territorial contests, fish that responded later to the predator images were more aggressive towards these images. Our findings suggest that territorial contests compromised the ability of prey to respond quickly to predators. However, we propose that increased aggression towards predators might increase survival chances of prey during predator encounters in nature, and it may thus compensate for costs incurred by delayed predator responses during territorial contests. To test this hypothesis experiments under natural predation regimes that examine the relationship between predation risk, territorial and antipredator aggression are required. [ABSTRACT FROM AUTHOR]

The neurotransmitter serotonin (5-HT) reduces aggressive behaviour in a number of vertebrates, and the 5-HT 1A receptor is known to be involved in this regulation. However, the role of this receptor in the modulation of sociopositive behaviour remains largely unknown. Here we investigated the role of the 5-HT 1A receptor in the regulation of aggressive, submissive and affiliative behaviour in the cooperatively-breeding cichlid Neolamprologus pulcher. In two experiments, we performed intramuscular injections of a 5-HT 1A agonist (8-OH-DPAT) and antagonist (Way-100635) followed by recordings of social behaviour of injected fish within their social groups. We determined the concentrations and post-injection times when the drugs had the greatest effect on social behaviour. We recorded spontaneous social behaviour in both experiments. In the second experiment we also recorded behaviour after social groups received a territorial challenge by live presentations of either conspecifics or egg predators. The 5-HT 1A agonist caused an increase in aggression and a decrease in submission and affiliation, whereas the antagonist had the opposite effects. Thus, the 5-HT 1A receptor plays an important regulatory role not only for aggressive but also sociopositive behaviour. • The serotonin 1A receptor is known to modulate aggression in vertebrates. • We show in a cichlid fish that it has important effects on sociopositive behaviour. • The receptor agonist increases aggression and reduces submissive and affiliative behaviour. • The antagonist instead decreases aggressive behaviour and increases affiliation. • The drug effects depend on the social setting and the stressfulness of the context. [ABSTRACT FROM AUTHOR]

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 social experience can program neurophysiological systems for life. • We developed a dynamic holding-water method to non-invasively measure cortisol responses in small fish. • Early social deprivation induced a lifelong reduced cortisol baseline in a highly social cichlid. • The cortisol response to a stressor was not affected by early social experience. • Early socially deprived N. pulcher had higher opercular beat rates OBR response to stressor. [ABSTRACT FROM AUTHOR]