Early experience affects learning performance and neophobia in a cooperatively breeding cichlid

Abstract

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.

The Influence of Rearing on Behavior, Brain Monoamines, and Gene Expression in Three-Spined Sticklebacks

“…More specifically, based on previous work on sticklebacks and other animals, we predicted neophobia would decrease for fish raised with increased simulated predator stress, habitat complexity, or social stress [e.g., Elvidge et al, 2016;Christensen and Nielsen, 2004;Naguib et al, 2011;Bannier et al, 2017]. We found that fish raised in complex physical or socially stressful environments were less neophobic, confirming our predictions and matching findings also in birds [Christensen and Nielsen, 2004].…”

“…We found that fish raised in complex physical or socially stressful environments were less neophobic, confirming our predictions and matching findings also in birds [Christensen and Nielsen, 2004]. Numerous other studies have found that early social environment matters: birds raised in "dynamic" flocks with varying individuals had larger singing networks and had greater mating success than individuals raised in stable flocks [White et al, 2010], rodents raised in social groups were less anxious [Curley et al, 2009;Cirulli et al, 2010], and social aspects of group composition during rearing influenced fish neophobia and cognition [Bannier et al, 2017]. Additionally, many psychological studies using the reverse of our treatment (exposing individuals to negative or no early environmental stimulus) found comparable results: primates with negative early social experience were less explorative and more neophobic [Fairbanks and McGuire, 1988], and rodents with no early social experience showed reduced overall attention [Lovic et al, 2011].…”

“…Sticklebacks are a mobile species and exploration is required to find both food and mates; aggression is likely important for both social interactions and for males to establish breeding burrows and attract females; and neophobia is important for avoiding predators [e.g., Ostlund-Nilsson et al, 2007]. Based on previous work, we predict that exposure to predation stress increases aggressiveness [Lima and Dill, 1990;Bell and Sih, 2007] and neophobia [e.g., Elvidge et al, 2016], and decreases exploration [e.g., Abbey- Lee et al, 2016;Moses and Sih, 1998;Hedrick and Kortet, 2006]; exposure to habitat complexity increases exploration behavior and decreases neophobia [e.g., Christensen and Nielsen, 2004]; and exposure to variable social environment increases aggression and decreases neophobia [e.g., Bannier et al, 2017;Naguib et al, 2011]. Additionally, we predict that monoamine levels, their metabolites, and the expression of genes related to monoaminergic transmission will vary in the brain depending on early environmental treatment, but, as the relationship between the environment and monoaminergic systems is not well understood, we have no directional predictions [Winberg and Nilsson, 1992;Carere and Maestripieri, 2013].…”

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

“…This finding contrasts previous work in N. pulcher, which showed a significant influence of early-life social experience on stress gene expression [17,36] and on the behaviour of both owners and intruders in the same asymmetric competition paradigm [9,16]. In these studies, N. pulcher reared with parents and other older group members (helpers) (i) had a higher expression of the gr1 gene in the telencephalon, (ii) when in the role of intruders, showed more submissive behaviour per received opponent aggression, and (iii) were less neophobic [90] compared to juveniles reared in a socially deprived setting with the same-aged siblings only. Thus, these previous findings also involved a re-programming of the stress axis, but with significant differences from the current study.…”

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

“…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, ).…”