Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain

Abstract

Group living animals must be able to express different behavior profiles depending on their social status. Therefore, the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. However, how social information is translated into a neurogenomic response and what are the specific cues in a social interaction that signal a change in social status are questions that have remained unanswered. Here, we show for the first time, to our knowledge, that the switch between status-specific neurogenomic states relies on the assessment of fight outcome rather than just on self- or opponent-only assessment of fighting ability. For this purpose, we manipulated the perception of fight outcome in male zebrafish and measured its impact on the brain transcriptome using a zebrafish whole genome gene chip. Males fought either a real opponent, and a winner and a loser were identified, or their own image on a mirror, in which case, despite expressing aggressive behavior, males did not experience either a victory or a defeat. Massive changes in the brain transcriptome were observed in real opponent fighters, with losers displaying both a higher number of differentially expressed genes and of coexpressed gene modules than winners. In contrast, mirror fighters expressed a neurogenomic state similar to that of noninteracting fish. The genes that responded to fight outcome included immediate early genes and genes involved in neuroplasticity and epigenetic modifications. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on mutual assessment of fighting ability.

Social Control of Hypothalamus-Mediated Male Aggression

“…The use of a mirror was prompted by previous work showing that fish show aggressive displays to a mirror image (Desjardins and Fernald, 2010; Oliveira et al, 2016; Tinbergen, 1951). Strikingly, males given CNO did not physically attack the mirror but they reliably tail rattled to it (Figure 2D, Movies S1, S2).…”

Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks

“…(Oldfield et al, 2015). Other differentially expressed candidate genes related to aggressiveness from other studies include bdnf (Muhie et al, 2015; Oliveira et al, 2016), cnot3b (Schunter et al, 2014), chga (Renn et al, 2008), dmrt3a (Edwards et al, 2006), igf2a (Aubin-Horth et al, 2005; Kroes et al, 2006), syt14b (Feldker et al, 2003; Aubin-Horth et al, 2005), TLN2 (Muhie et al, 2015), and wnt8a (Rittschof et al, 2014). …”

Transcriptome analysis of genes and gene networks involved in aggressive behavior in mouse and zebrafish

“…The zebrafish data was obtained from the Gene Expression Omnibus (GEO) repository (GEO accession number: GSE56549) from a study conducted previously at the Oliveira lab [Oliveira et al, ]. All animals were wild‐type (AB) male zebrafish ( Danio rerio ) and were acquired from the Zebrafish International Resource Center (ZIRC).…”