Abstract
Social living animals have to adjust their behavior to rapid changes in the social environment. It has been hypothesized that the expression of social behavior is better explained by the activity pattern of a diffuse social decision-making network (SDMN) in the brain than by the activity of a single brain region. In this study, we tested the hypothesis that it is the assessment that individuals make of the outcome of the fights, rather than the expression of aggressive behavior per se, that triggers changes in the pattern of activation of the SDMN which are reflected in socially driven behavioral profiles (e.g., dominant vs. subordinate specific behaviors). For this purpose, we manipulated the perception of the outcome of an agonistic interaction in an African cichlid fish (Oreochromis mossambicus) and assessed if either the perception of outcome or fighting by itself was sufficient to trigger rapid changes in the activity of the SDMN. We have used the expression of immediate early genes (c-fos and egr-1) as a proxy to measure the neuronal activity in the brain. Fish fought their own image on a mirror for 15 min after which they were allocated to one of three conditions for the two last minutes of the trial: (1) they remained fighting the mirror image (no outcome treatment); (2) the mirror was lifted and a dominant male that had just won a fight was presented behind a transparent partition (perception of defeat treatment); and (3) the mirror was lifted and a subordinate male that had just lost a fight was presented behind a transparent partition (perception of victory treatment). Results show that these short-term social interactions elicit distinct patterns in the SDMN and that the perception of the outcome was not a necessary condition to trigger a SDMN response as evidenced in the second treatment (perception of defeat treatment). We suggest that the mutual assessment of relative fighting behavior drives these acute changes in the state of the SDMN.
Highlights
Individuals from social species need to combine information about the social environment they live in with information about their internal state, such as previous social experience and organismal condition, in order to adaptively optimize their responses to changes in the social environment (Taborsky and Oliveira, 2012)
A Principal Component Analysis (PCA) of the behavioral variables resulted in two principal components (PC) that together explained 86.3% of the variance in aggressive behavior (Table 1)
There was an effect of the experimental treatment in ‘‘overt aggression’’ (i.e., PC1 loadings; F(2,17) = 4.87, p = 0.02), with focal fish assigned to the MS condition showing significantly less overt aggression than those in the mirror fights treatment (MM) and MD conditions (Figure 2A)
Summary
Individuals from social species need to combine information about the social environment they live in with information about their internal state, such as previous social experience and organismal condition, in order to adaptively optimize their responses to changes in the social environment (Taborsky and Oliveira, 2012). Different behavioral states should result from divergent transcriptomes of the SDMN, and changes between states, such as acquiring or losing social status should be associated with rapid changes in patterns of gene expression in the SDMN Given their fast and transient response to changes in extra- and intra-cellular environment and their effect as transcription factors, immediate early genes (e.g., c-fos, egr-1) play a key role in orchestrating transcriptomic responses to environmental changes. Several studies have documented changes in immediate early gene (IEG) expression across the SDMN associated with changes in social behavior across different vertebrate taxa (e.g., FaykooMartinez et al, 2018; Kabelik et al, 2018; O’Connell and Hofmann, 2012), including teleost fish and tilapia (e.g., Field and Maruska, 2017; Roleira et al, 2017; Teles et al, 2015). Given that socially-driven changes in the SDMN are expected to produce integrated phenotypic responses, at the behavioral and physiological (hormonal) levels, to the social environment and that androgens have been described to respond to social challenges (challenge hypothesis, Hirschenhauser and Oliveira, 2006; Wingfield et al, 1990), we have characterized the response of the hypothalamic-pituitary-gonadal (HPG) axis to our experimental treatments by measuring the expression of gonadotrophin-releasing hormone (gnrh1) in the preoptic area and circulating androgen levels (testosterone, T, and 11-ketotestosterone, KT)
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