An integrated roadmap of European sea bass (Dicentrarchus labrax) spermatogenesis across the annual reproductive cycle.

European sea bass (Dicentrarchus labrax) is a seasonal marine teleost of high aquaculture value, yet a comprehensive, stage-resolved molecular description of its spermatogenic cycle has been lacking. Here, we generated an integrated histology-anchored RNA sequencing atlas covering the six canonical testicular stages (Stages I-VI) to reconstruct the temporal sequence of endocrine, proliferative, meiotic, spermiogenic and regression-related processes across the annual reproductive cycle. Early stages (Stages I-III) were characterised by strong activation of spermatogonial maintenance pathways, hormone-responsive programmes, and circadian regulators, along with robust enrichment of DNA replication, kinetochore assembly, and chromosomal segregation mechanisms that prepare germ cells for meiotic entry. Spermiogenesis (Stage IV) represented the major transcriptional shift, with the coordinated upregulation of axonemal motors, intraflagellar transport and BBSome components, outer dense fibres and microtubule regulators, accompanied by extensive chromatin remodelling involving histone variants, transcription factors, ubiquitin/SUMO pathway enzymes, and heterochromatin-associated proteins. Spermiation (Stage V) showed an enrichment in calcium-dependent signalling, cytokine and chemokine networks, and adhesion and extracellular matrix pathways, consistent with Sertoli-germ cell remodelling and sperm release. Regression (Stage VI) was dominated by immune activation, endocytosis, phagocytosis, and vascular remodelling signatures, indicating an active phase of clearance and tissue reorganisation that preserves the spermatogonial reservoir for the next cycle. From 9,327 differentially expressed genes, we identified 132 distinct temporal expression patterns and curated three translational resources: stage-informative markers, a fertility gene set, and a chromatin-associated compendium. Together, this atlas defines the sequential molecular architecture of spermatogenesis in a seasonal marine fish, conserved vertebrate and species-specific regulatory modules, and provides operational biomarkers for broodstock assessment and the mitigation of precocious maturation in aquaculture.