Aggression is a key component of the behavioral repertoire of animals that impacts on their Darwinian fitness. The available genetic tools in zebrafish make this species a promising vertebrate neurogenetic model for the study of neural circuits underlying aggressive behavior. For this purpose, a detailed characterization of the aggressive behavior and its behavioral consequences is first needed. In this article we establish a simple protocol that reliably elicits the expression of fighting behavior in zebrafish dyads and characterized it. The agonistic behavior expressed during dyadic fighting behavior has a temporal structure, indicating the existence of an underlying architecture prone to genetic manipulation. Social interactions have consequences for subsequent behavior with a potential fitness impact, which stresses the validity of this species for the study of aggression. These effects of experience seem to be mediated by different mechanisms in winners and losers. Winners increase the probability of winning subsequent fights without changing their fighting behavior, suggesting the existence of social status cues. On the other hand, losers decrease the probability of winning subsequent fights by decreasing their motivation to escalate fights. Together, these results are a first step to the development of a quantitative framework for the study of aggressive behavior in zebrafish.

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.