Stable reprogramming of brain transcription profiles by the early social environment in a cooperatively breeding fish

Abstract

Adult social behaviour can be persistently modified by early-life social experience. In rodents, such effects are induced by tactile maternal stimulation resulting in neuroendocrine modifications of the hypothalamicpituitary -adrenal axis involved in stress responsiveness. Whether similar long-term alterations can occur in the hypothalamic -pituitary -interrenal (HPI) axis of poikilothermic vertebrates is unknown. We compared the expression of four genes of the HPI axis in adults of the cooperatively breeding cichlid Neolamprologus pulcher, which had been exposed to two early-life social treatments 1.5 years prior to brain sampling. Fish reared with parents and siblings had less brain expression of corticotropin-releasing factor and of the functional homologue of the mammalian glucocorticoid receptor (GR1) than individuals reared with same-age siblings only. Expression of the mineralocorticoid receptors (MR) did not differ between treatments, but the MR/GR1 expression ratio was markedly higher in fish reared with parents and siblings. Thus, we show here that early social experience can alter the programming of the stress axis in poikilothermic vertebrates, suggesting that this mechanism is deeply conserved within vertebrates. Moreover, we show for the first time that reprogramming of the stress axis of a vertebrate can be induced without tactile stimulation by parents.

Using an integrative approach to investigate the evolution of behaviour

“…Using quantitative real‐time PCR, we showed that the expression level of the candidate genes involved in the stress response (glucocorticoid receptors, corticotropin releasing factor) was permanently altered in the brain of these fish when they reached the adult stage (Taborsky et al. ). Our results suggest that the early rearing environment can thus induce permanent reprogramming that may directly affect social behaviour in a fish, as found in mammals.…”

Effects of social conditions during adolescence on courtship and aggressive behavior are not abolished by adult social experience

“…Influences of social conditions during early and adolescent development on adult behavior, morphology, physiology and gene expression have been described frequently (e.g., birds : Holveck, Geberzahn, & Riebel, 2011;Mariette, Cathaud, Chambon, & Vignal, 2013;Riebel, Naguib, & Gil, 2009;White, Gros-Louis, King, Papakhian, & West, 2007;fish: Arnold & Taborsky, 2010;Chapman, Ward, & Krause, 2008;Taborsky, Arnold, Junker, & Tschopp, 2012;Taborsky, Tschirren, Meunier, & Aubin-Horth, 2013;mammals: Branchi, 2009;Delville, Melloni, & Ferris, 1998;Ferris, Messenger, & Sullivan, 2005;Sachser, Hennessy, & Kaiser, 2011;Sachser, Kaiser, & Hennessy, 2013). Influences of social conditions during early and adolescent development on adult behavior, morphology, physiology and gene expression have been described frequently (e.g., birds : Holveck, Geberzahn, & Riebel, 2011;Mariette, Cathaud, Chambon, & Vignal, 2013;Riebel, Naguib, & Gil, 2009;White, Gros-Louis, King, Papakhian, & West, 2007;fish: Arnold & Taborsky, 2010;Chapman, Ward, & Krause, 2008;Taborsky, Arnold, Junker, & Tschopp, 2012;Taborsky, Tschirren, Meunier, & Aubin-Horth, 2013;mammals: Branchi, 2009;Delville, Melloni, & Ferris, 1998;Ferris, Messenger, & Sullivan, 2005;Sachser, Hennessy, & Kaiser, 2011;Sachser, Kaiser, & Hennessy, 2013).…”

“…Therefore, organisms should ideally remain plastic throughout their whole life. Lorenz (1935) coined the term "imprinting" for this type of learning, to point to the stability of behaviors established in the course of sensitive periods and it has been shown later that song learning, which had been named an "imprinting like process" in the early learning literature, shared almost every feature with the originally described process of sexual and filial imprinting (Bischof, 1997;ten Cate, Vos, & Mann, 1993). Lorenz (1935) coined the term "imprinting" for this type of learning, to point to the stability of behaviors established in the course of sensitive periods and it has been shown later that song learning, which had been named an "imprinting like process" in the early learning literature, shared almost every feature with the originally described process of sexual and filial imprinting (Bischof, 1997;ten Cate, Vos, & Mann, 1993).…”

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

“…In vertebrates, the hypothalamus–pituitary–adrenal/interrenal (HPA/HPI) axis has been proposed as a central mechanism responsible for long‐term effects of early social experience (Arnold & Taborsky, ; Banerjee, Arterbery, Fergus, & Adkins‐Regan, ; Fischer et al, ; Francis et al, ; Liu et al, ; Nyman et al, ; Nyman, Fischer, Aubin‐Horth, & Taborsky, ; Taborsky, Tschirren, Meunier, & Aubin‐Horth, ). Hippocampal glucocorticoid receptors (GRs) are implicated in the negative feedback loop controlling glucocorticoid production, which promotes termination of the stress response (de Kloet, ).…”

“…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, ).…”