Social descent with territory loss causes rapid behavioral, endocrine, and transcriptional changes in the brain

Abstract

SUMMARYIn social species that form hierarchies where only dominant males reproduce, lower-ranking individuals may challenge higherranking ones, often resulting in changes in relative social status. How does a losing animal respond to loss of status? Here, using the African cichlid fish Astatotilapia burtoni, we manipulated the social environment, causing males to descend in rank, and then examined changes in behavior, circulating steroids and immediate early gene (IEG) expression (cfos, egr-1) in micro-dissected brain regions as a proxy for neuronal activation. In particular, we examined changes in the conserved 'social behavior network' (SBN), a collection of brain nuclei known to regulate social behaviors across vertebrates. Astatotilapia burtoni has rapidly reversible dominant-subordinate male phenotypes, so that within minutes, descending males lost their bright body coloration, switched to submissive behaviors and expressed higher plasma cortisol levels compared with non-descending and control males. Descending males had higher IEG expression throughout the SBN, but each brain region showed a distinct IEG-specific response in either cfos or egr-1 levels, but not both. Overall, SBN IEG patterns in descending males were distinctly different from the pattern observed in males ascending (subordinate to dominant) in social status. These results reveal that the SBN rapidly coordinates the perception of social cues about status that are of opposite valence, and translates them into appropriate phenotypic changes. This shows for the first time in a non-mammalian vertebrate that dropping in social rank rapidly activates specific socially relevant brain nuclei in a pattern that differs from when males rise to a higher status position.

Social interactions elicit rapid shifts in functional connectivity in the social decision-making network of zebrafish

“…These results are coincident with those reported for another fish species, the African cichlid Astatotilapia burtoni, where stable dominant and stable subordinate males express different status-specific behavioural profiles, which are also not paralleled by differences in either c-fos or egr-1 expression in any of the studied nodes of the SDM network-which in this case also included, the anterior (ATn) and the ventral tuberal nuclei (VTn) [37]. However, in another study with the same species winners and losers of an acute agonistic interaction show different expression profiles across the network, with localized higher expression of c-fos in the POA and the ATn, and of egr-1 in Dm, Dl, Vv, Vs and VTn of losers [38]. Together these results suggest that socially driven changes in neuronal activation in the SDM network are transient, and that stable social behaviour states do not rely on localized differences in brain activity.…”

The mechanosensory lateral line is used to assess opponents and mediate aggressive behaviors during territorial interactions in an African cichlid fish

“…Fight onset was defined as the first reciprocal exchange of aggressive behaviors, and fights had to last a minimum of 30 s. The fight was allowed to continue until a clear winner and loser was established based on criteria similar to those used previously in a study on social defeat (Maruska et al, 2013). Specifically, the winner fish had to fulfill two of the following characteristics: (1) enter the shelter >3 times within a 1 min period, (2) enter and stay in the shelter for >10 consecutive seconds, (3) perform at least three dominance behaviors within 1 min, and (4) chase or bite the other male.…”

Social status differences regulate the serotonergic system of a cichlid fish, Astatotilapia burtoni

“…Slides were placed on a frozen stage (BFS-30MP, Physitemp, Clifton, NJ, USA) and visualized under a dissecting microscope. Brain nuclei were microdissected by a single experimenter over a 2 day period with a modified 23 gauge needle (inner diameter ~390 μm) as described elsewhere (Maruska et al, 2013) to isolate the VTn, POA and raphe nucleus. Microdissected samples were placed into 200 μl of perchloric acid on dry ice and centrifuged at 13,200 rpm at 4°C for 10 min.…”