Role of the gut-brain axis in marine fish behavior

[eng] Introduction Consistent behavioral differences among individuals are well documented across animal taxa and are recognized as key contributors to ecological and evolutionary processes. However, the mechanisms underlying the emergence and persistence of such differences remain poorly understood. While genetic and environmental influences have traditionally been considered the main drivers of behavioral variation, recent research highlights the potential involvement of additional factors. In this context, the gut-brain axis (GBA) and the gut microbiome have emerged as promising modulators of animal behavior. This bidirectional communication system links the central nervous system with the gastrointestinal tract and is increasingly acknowledged for its role in behavioral modulation. Nevertheless, its specific contribution to behavior in marine fish remains largely unexplored. Research Content The main objective of this thesis is to expand current knowledge of the GBA and its role in behavioral regulation in marine fish by investigating the relationship between individual behavior and the gut microbiome. To this end, two marine teleost species were used as model organisms: the pearly razorfish (Xyrichtys novacula) and the gilthead seabream (Sparus aurata). Chapter 1 explores interindividual variation in behavior in gilthead seabream and compares behavioral differences between wild and captive-reared individuals. The results reveal consistent behavioral types among individuals and significant differences between the two groups, providing valuable insights into behavioral variability in natural versus rearing environments. Chapter 2 builds on the behavioral dataset from Chapter 1 by integrating gut microbiome analyses in the same individuals. The findings reveal marked differences in gut microbiome composition between wild and reared seabream, as well as distinct patterns in core and non-core microbiome components. In addition, correlations are identified between specific microbial characteristics and behavioral types, pointing to potentially behaviorally relevant bacterial taxa. Chapter 3 investigates these behavior–microbiome relationships in a wild population of Xyrichtys novacula. This study leverages novel high-resolution tracking technologies to reconstruct the social network of free-living individuals and combines these behavioral data with gut microbiome sequencing. The findings provide key insights, including the influence of environmental variables on microbiome composition, a greater similarity of gut microbiomes among individuals belonging to the same harem, and evidence suggesting microbial transmission via social interactions. Conclusion The results of this thesis open new avenues for understanding the origins of animal behavior and highlight the potential role of the gut-brain axis in modulating behavior in marine teleosts. Future research should consider microbial manipulation experiments combined with behavioral assessments, both in aquaculture and under controlled conditions in the wild, to further elucidate causal relationships. Based on the findings, the implementation of fasting periods and sampling at multiple time points is also recommended to account for microbiome dynamics over time and improve study design. Overall, this thesis contributes novel perspectives to the study of animal behavior, emphasizing the ecological and evolutionary relevance of host–microbiome interactions in marine ecosystems.