Integrative analysis of population selection signatures and embryonic mammary placode multi-omics reveals the genetic basis of increased teat number in Taihu indigenous pig breeds

Teat number is an important reproductive trait affecting sow lactation capacity, piglet survival, and production efficiency. Erhualian and Jiaxing Black pigs, two representative Taihu indigenous breeds, exhibit exceptionally high teat numbers and provide an ideal model for investigating the genetic basis of this trait. Here, whole-genome resequencing data from 213 pigs were analyzed using Asian wild boars as a common ancestral reference population. Genome-wide selection signatures were identified using complementary approaches, including locus-specific branch length (LSBL), integrated haplotype score (iHS), and cross-population extended haplotype homozygosity (XP-EHH). To prioritize functional candidates, embryonic day 26 (E26) mammary placode RNA-seq and ATAC-seq data were integrated with pig quantitative trait loci (QTL) annotations and the PigGTEx resource. We identified 380 candidate genes under selection, which were significantly enriched in pathways related to mammary placode development, including the TGF-β, WNT, and PI3K-Akt signaling pathways, and were overrepresented in teat number-related QTLs. Integration with transcriptomic data further prioritized 65 candidate genes, of which 37 showed significant associations with teat number in phenome-wide association study (pheWAS). Among these, BMPR1B was consistently supported by selection signatures, differential expression, pathway enrichment, pheWAS, teat number genome-wide association study, haplotype differentiation, and chromatin accessibility. Candidate regulatory variants were further identified within mammary placode-accessible chromatin at the broader BMPR1B locus. Their regulatory effects and target gene remain to be determined. Integration of population genomic, developmental multi-omic, and association evidence provided evidence for a polygenic basis of increased teat number in Taihu pigs and prioritized BMPR1B as a strong candidate gene associated with teat-number variation. These results provide candidate genes and regulatory variants for further functional investigation and genetic improvement of reproductive traits in pigs.