Biological basis of social hierarchy in fish: hormones, genes, and behavioral interaction mechanism

Social hierarchy, a widespread social structure in aquatic ecosystems, plays a crucial role in optimizing resource allocation and individual fitness. In vertebrates, fish serve as ideal models for investigating the evolutionary origins and internal mechanisms of social behavior due to their rich species diversity and clear dominance structures. However, while behavioral descriptions of dominance-subordination relationships are well established, the complete regulatory pathway from genes to hormones and complex social behaviors remains fragmented. This review integrates findings from neuroendocrinology, behavioral ecology, and molecular genetics to systematically elucidate the biological mechanisms governing fish social hierarchy. The objective of this study is to construct a comprehensive “hormone-gene-behavior” interaction framework, aiming to clarify the bidirectional feedback loops that regulate social rank and behavioral plasticity. By synthesizing literature across disciplines, the review analyzes key signaling molecules, dynamic feedback mechanisms, and genetic bases. The results reveal a complex interplay of regulatory factors. Stress hormones are critical markers: subordinate rainbow trout (Oncorhynchus mykiss) show significantly elevated plasma cortisol and POMC mRNA expression, indicating chronic stress, whereas dominant individuals exhibit transient spikes that stabilize at low levels once status is established. Sex hormones are pivotal for dominance; plasma 11-ketotestosterone (11-KT) in dominant Amphiprion species is significantly higher than in subordinates and decreases with rank. Experimental evidence confirms this causality: 11-KT supplementation increased aggressive behavior in bluegill sunfish (Lepomis macrochirus) by 64%, while flutamide (an androgen receptor antagonist) decreased it by 7%. Furthermore, the “winner effect” is mediated by androgens; treatment with the anti-androgen cyproterone acetate in tilapia completely blocked this effect, reducing win rates to 44% (random levels). Neurotransmitters also modulate status, with subordinate salmonids exhibiting elevated serotonin metabolism ratios (5-HIAA/5-HT). Neuroplasticity provides a structural basis for long-term strategies; 28 days of 11-KT treatment in female tilapia increased GnRH3 neuron numbers by approximately 30%. Social status also remodels gene expression, with hundreds of genes in the social decision-making network showing differential expression, including upregulation of dopamine synthesis genes (th) in dominants. Additionally, social experiences induce epigenetic changes in chromatin modification genes (epc1, jdp2), facilitating long-term behavioral adaptation. In conclusion, fish social hierarchy is governed by a precise dynamic feedback network involving hormones, genes, and behavior. This review emphasizes that behavioral strategies are flexible adaptations driven by neuroendocrine states and genetic backgrounds. These insights provide theoretical guidance for aquaculture, advocating for “hierarchy-friendly” strategies such as environmental enrichment to provide visual barriers and physiological phenotype selection to mitigate chronic stress, thereby improving fish welfare and production efficiency.