Elsevier

Hormones and Behavior

Volume 61, Issue 1, January 2012, Pages 140-146
Hormones and Behavior

Natural variation in the molecular stress network correlates with a behavioural syndrome

https://doi.org/10.1016/j.yhbeh.2011.11.008Get rights and content

Abstract

In several species, individuals from the same population behave differently from each other. A functional link between variation in personality traits and the stress response has been suggested by studies in artificial selection lines in fish, birds and mammals. The aim of this study was to test whether the expression of genes involved in the stress response co-varies with personality traits in a natural population. Four personality traits, excreted cortisol level and brain expression of six candidate genes (CRF, CRF-R2, POMC1, GR1, GR2, MR) were measured in non-stressed wild-caught threespine sticklebacks (Gasterosteus aculeatus). We found correlations between variation in personality traits and variation in the expression of genes involved in the stress response. Aggressiveness was negatively correlated with cortisol levels. Boldness and aggressiveness formed a behavioural syndrome and were both positively correlated with brain expression of glucocorticoid receptors (GR1 and GR2). Boldness and exploration were positively correlated with expression of POMC1 but not with each other. Our results are compatible with a model that suggests that the aggressiveness–boldness behavioural syndrome could be the consequence of a physiological pleiotropic effect of glucocorticoid receptors, which are involved in the stress response and behaviour variation.

Highlights

► Link between personality traits and the stress response in a natural population. ► Negative correlation between aggressiveness and cortisol levels. ► Covariation of the molecular stress network and personality traits. ► Positive correlation of personality with brain expression of glucocorticoid receptors.

Introduction

Wild individuals from the same population behave differently from each other (Koolhaas et al., 1999). These among-individual differences are defined as personality traits when they are consistent in time and/or across contexts. Five main personality traits that can have significant impact on fitness and ultimately on the ecology and evolution of populations have been defined: boldness, aggressiveness, activity, exploration and sociability (Reale et al., 2007). These personality traits sometimes co-vary at the population level to form what is called a behavioural syndrome, as shown for boldness and aggressiveness in a wide range of species (Huntingford, 1976). These syndromes are found in some natural populations and not in others (Dingemanse et al., 2007). The presence of behavioural syndromes can be explained by different mechanisms (Bergmüller, 2010): genetic linkage, where two genes are located at very near loci and are often inherited together; resource allocation trade-off, where investing in one trait (growth) affects another negatively (survival) and results in differences in personality; correlational selection, where certain behaviour combinations are selected; and finally genetic pleiotropy and physiological pleiotropy, where the same gene or hormone influences two behaviours. It is crucial to uncover the mechanisms that underlie personality traits and behavioural syndromes to understand how they have evolved, are maintained and could evolve in the future (Bell and Aubin-Horth, 2010).

Studies in various vertebrates suggest that baseline or post-stress levels of glucocorticoid hormones involved in the stress response are correlated with personality variation, such as in rodents where aggressive and actively coping individuals have a low glucocorticoid stress response (Koolhaas et al., 1999). This covariation could be the result of physiological pleiotropy. This model is supported by artificial selection of a high or low cortisol response following a stress, which leads to behavioural divergence between the selection lines in fish and birds (Martins et al., 2007, Overli et al., 2005). Moreover, selecting lines for differences in personality traits causes changes in glucocorticoid levels in mammals and birds (Albert et al., 2008, Stowe et al., 2010). Finally, the stress response is the result of a hormonal cascade composed of genes coding for proteins that act as hormones and their receptors that are themselves implicated in behaviour variation (Bernier et al., 2009). Corticotropin-releasing factor (CRF, in fish) is secreted in the hypothalamus. It stimulates the synthesis of proopiomelanocortin (POMC) in the pituitary through its receptor (CRF-R), has been implicated in variation in anxiety in fish (Backström et al., 2011) and its mammalian homologue has been implicated in variation in fearfulness in primates (Kalin et al., 2000). POMC is a hormone precursor that results in different active peptides following enzymatic cleavage, including corticotropin (ACTH), which binds the MC2R receptor in the interrenal cells of the head kidney in fish to activate the synthesis and secretion of a glucocorticoid steroid hormone into the general circulation. Glucocorticoids, such as cortisol, in turn activate glucocorticoid receptors (GR1 and GR2 in several fish species) and mineralocorticoid receptors (MR) in different tissues (Arterbery et al., 2011, Bury and Sturm, 2007, Prunet et al., 2006). The GRs and MR have been related to anxiety in mammals (Brinks et al., 2009, Liu et al., 1997) and in fish (Piato et al., 2011). GRs have also been implicated in variation in aggressiveness in fish (Dunlap et al., 2011, Schjolden et al., 2009). Variation in the brain expression of genes involved in the stress response has been shown between artificial lines selected for divergent stress responses in fish (Johansen et al., 2011) and birds (Hodgson et al., 2007). In order to test whether variation in expression is present for genes involved in the stress response in nature and whether there is co-variation between personality traits and the expression of the molecular stress network, a within-population study of wild individuals is needed.

We therefore set out to test whether personality traits are correlated with differences in cortisol level and expression of six candidate genes involved in the stress response in wild-caught threespine sticklebacks (Gasterosteus aculeatus).

Section snippets

Animals and housing

We collected threespine sticklebacks during their breeding season in the St. Lawrence River (Québec, Canada, 46.729 N, 71.432 W) using a beach seine. Fish were brought back to the Laboratoire Régional de Sciences Aquatiques aquatic laboratory (Université Laval, Québec, Canada). Experimental procedures were approved by the Ministère du développement durable de l'environnement et des parcs du Québec and the Comité de protection des animaux of Université de Montréal. We studied 20 sexually mature

Behavioural syndrome

Boldness in the presence of a human observer had a repeatability of 57%, and boldness under the threat of predation had a repeatability of 56% (Lessells and Boag, 1987), suggesting that consistent differences exist among individuals for both measures. The two boldness measures were not significantly correlated (Pearson correlation, r = 0.29, p = 0.11, n = 20). Due to the lack of correlation of boldness under the threat of predation with other behaviours (see below), we only used boldness towards a

Discussion

We tested whether natural variation in expression of genes involved in the stress response is present in wild-caught threespine sticklebacks and whether personality traits are correlated with these transcription differences. Based on previous studies (Liu et al., 1997, Schjolden et al., 2009), we predicted that a positive correlation would be present between the expression of glucocorticoid receptors and the boldness–aggressiveness behavioural syndrome. We did find a significant covariation

Acknowledgments

The authors would like to thank S. McCairns, S. Higgins and the LARSA personnel at Université Laval, the Hofmann Laboratory and R. Earley for help with the solid-phase extraction protocol and J. Lacasse for technical help. We thank members of the Aubin-Horth lab, A. Reddon, M. Morris, S. Renn and C.R. Landry for comments on previous versions of this manuscript. Funding was provided to NAH by a NSERC Discovery grant, a FQRNT Nouveau chercheur grant and a Canadian Foundation for Innovation Leader

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