Characterizing breed-shared and breed-specific genetic regulatory effects of gene expression across three pig breeds

Background Differences across breeds in adaptation to various environments and performance on complex traits such as growth rate are very common in livestock animals. These differences have been attributed to various factors, including genetic variation, selection, and environmental influences. Gene expression regulation, serving as a critical intermediary mechanism that bridges genotypes and phenotypes, may play a pivotal role in driving these differences across breeds. Hence, we characterized the breed-shared and breed-specific pattern in genetic regulatory effects on gene expression via expression quantitative trait loci (eQTL) mapping in three pig breeds (Duroc, Landrace, and Yorkshire), aiming to gain a deeper understanding of the molecular basis underlying complex trait differences across breeds. Results We observed breed differentiation at both the single-nucleotide polymorphism (SNP) and gene expression levels. By eQTL mapping, within each tissue, an average of 71.1% of the eGenes identified in each breed were breed-shared, while the remaining 28.9% were breed-specific. We found that some regulatory effects are relevant to either the difference in average gene expression or expression variance among populations. Breed-shared eGenes were more abundant and showed larger effect sizes and lower evolutionary conservation, and vice versa. Enrichment analysis showed that the genome-wide association studies (GWAS) loci were significantly enriched in the cis-eQTLs of eGenes for an average of 12 of 19 complex traits per breed. These loci exhibited higher enrichment in breed-specific eGenes than breed-shared eGenes. Through colocalization analyses with GWAS loci, we observed 220 colocalization events (PP.H4 > 0.8) with breed-specific eGenes and 758 events with breed-shared eGenes. Conclusions Our study reveals breed-shared and breed-specific effects and characteristics of genetic regulation on gene expression in three pig breeds. Both breed-shared and breed-specific eGenes contribute to the genetic regulation of complex traits, while breed-specific eGenes explain regulatory variation unique to each breed. These findings together improved our understanding of breed-dependent genetic regulation and their contribution to complex traits.