From genomes to phenomes: Multi-omics dissection of positive and balancing selection in Jinhua pig

The Jinhua (JH) pig is a renowned Chinese indigenous breed distinguished by their two-end black phenotype, serve as the exclusive genetic resource for producing Jinhua ham. However, there is currently limited knowledge about the genetic structure and characteristics of JH pigs. This study employed whole-genome sequencing of 1238 individuals representing 67 breeds/lines to elucidate the genetic architecture of JH pigs. Population structure analysis revealed five distinct geographic clusters within Chinese indigenous pigs (North China/CCN, Central China/CCN, East China/ECN, South China/SCN, Southwest China/SWCN), with JH forming an early-diverging lineage in the ECN group exhibiting unique ancestry patterns. Genome-wide scans identified 7995 signatures of positive selection (iSAFE; FDR < 0.05). These signals were enriched in pathways related to immunity, neurodevelopment, and lipid metabolism. Key candidate genes (CLEC7A, D2HGDH, NOVA1) demonstrated breed-specific expression. Balancing selection analysis detected 4630 signals converging on PLA2G2A, a metabolic hub gene influencing intramuscular fat deposition. Two haplotypes (Hap1:41%; Hap2:59%) exhibited antagonistic pleiotropy: Hap1 was associated with enhanced growth performance, whereas Hap2 correlated with superior carcass quality. Our integrative analysis demonstrates that germplasm traits of JH pigs, including tender marbling, disease resilience, and roughage utilization efficiency, result from synergistic effects of directional selection on metabolic/immune genes and balancing selection maintaining fitness trade-offs. This study establishes a framework for delineating adaptive mechanisms in indigenous livestock, providing critical insights for genomic conservation and precision breeding.