Genome-wide association and selection signature analyses reveal the genetic basis of swimming performance in large yellow croaker (Larimichthys crocea)

The large yellow croaker ( Larimichthys crocea ), a cornerstone of China’s marine aquaculture, faces survival challenges in offshore farming due to intensified water currents. To elucidate the genetic basis of swimming performance, a key adaptive trait, we integrated meta-analysis of genome-wide association studies (meta-GWAS) with selection signature analysis across three populations. A genomic selection (GS) program targeting critical swimming speed (U crit ) was implemented, in which parents with the highest and lowest genomic estimated breeding values (GEBVs) formed selective (SL) and control (CL) lines, respectively. Three populations were analyzed: juveniles from SL (JS) and CL (JT), and adults from SL (AS). Swimming tests showed that JS exhibited 19.5% higher absolute U crit than JT (27.99 vs. 23.43 cm·s⁻¹, p < 0.05), with adult U crit reaching 61.80 cm·s⁻¹ . Despite genetic differentiation between JS and JT (supported by phylogenetic and linkage disequilibrium analyses), meta-GWAS identified two quantitative trait loci (QTLs), SPC4_1 and SPC4_2 , on chromosome 4. Selection scans revealed 97 regions under positive selection, with SPC4_1 showing signatures of recent artificial selection and harboring key genes such as CACNA1E (calcium signaling), GNA11/GNA15 (G-protein coupling), LPL (lipid metabolism), and PODN (connective tissue development). Enriched KEGG pathways included metabolic, biosynthetic, and signal transduction processes, underscoring their potential involvement in swimming performance. This study pioneers the integration of meta-GWAS and selection signature analysis in marine fish, highlights candidate genomic regions responsive to short-term GS. The identified QTLs and candidate genes represent promising targets for future functional validation, providing a foundation for subsequent improvements in offshore aquaculture performance.