Cross-population meta-analysis and colocalisation analysis reveal novel and pleiotropic genes associated with rib and teat number in pigs.

Total rib number (TRN) and total teat number (TTN) are key anatomical and economic traits in pigs, linked to carcass yield and reproductive performance, respectively, and are genetically correlated. However, the shared genetic basis underlying these traits remains incompletely understood. This study aimed to dissect the genetic architecture of TRN and TTN and to identify pleiotropic genes affecting both traits. Single-population genome-wide association studies (GWASs), multi-population meta-analysis, and multi-trait meta-analysis were conducted using phenotypic and genotypic data from three pig populations: Yorkshire (YY, n = 413), Suhuai (SH, n = 655), and Landrace × Yorkshire (LY, n = 678). Significant genetic and phenotypic correlations were observed between TRN and TTN, with genetic correlations of 0.82 in YY, 0.46 in SH, and 0.35 in LY. Ten quantitative trait loci (QTLs) associated with TRN were identified, including novel loci on SSC2 (39.38-40.49 Mb), SSC3 (123.79-125.58 Mb), SSC6 (103.40-104.53 Mb), SSC12 (53.30-54.84 Mb), and SSC18 (45.29-46.91 Mb). For TTN, eight QTLs were detected, including three newly discovered regions on SSC13 (142.82-143.99 Mb), SSC14 (7.26-8.54 Mb), and SSC16 (10.19-12.18 Mb). Candidate genes were identified through functional annotation and phenome-wide association analysis. For TRN, the prioritised genes included GREB1, SMCHD1, HES7, VRTN, ABCD4, NTN1, and members of the HOX gene family, whereas for TTN, the identified genes included FRMD4A, STC1, GREB1, and ABCD4. Colocalisation analysis integrating GWAS and multi-tissue expression QTL data suggested shared genetic signals for several genes, including EMILIN2, PTGR2, PSEN1, and ABCD4 for TRN, and PTGR2 and ENSSSCG00000033037 for TTN. Notably, GREB1, PTGR2, and ABCD4 were identified as pleiotropic genes potentially regulating both traits. These results clarify the shared genetic architecture of rib and teat number and provide candidate genes for future functional validation and genetic improvement in pig breeding.