Evaluating the impact of thirty years of directional genetic selection on shaping the population genomic structures of Italian pig breeds

The breeding programs for the Italian heavy pig breeds (Italian Duroc, Italian Landrace and Italian Large White) began in 1990, with the goal of meeting the specific needs of the Italian dry-cured ham protected designation of origin (PDO) value chain. This directional selection focused on improving performance, reproduction and meat quality traits, involving specific traits for improving dry-cured ham seasoning like ham weight loss at first salting, visible intermuscular fat content of the legs, and fat coverage. As a result of this selection, the genetic background of the three breeds diverged from the corresponding cosmopolitan breeds, more widely used in other production systems, i.e. Duroc (D), Landrace (L) and Large White (LW). This study aimed to track how this selection influenced the genomic profiles of the Italian heavy pig breeds over a span of approximately three decades. We genotyped with a high-density SNP array a total of approximately 1800 Italian Duroc pigs (ID), 6900 Italian Large White pigs (ILW) and 3400 Italian Landrace pigs (IL) born over the last 30 years, as well as 101, 151 and 154 pigs from their cosmopolitan counterpart, collected from the european nucleotide archive (ENA), which we collected to evaluate population structure differentiation. After quality control and filtering, about 28000 autosomal SNP were phased and used to build haplotypes. Within each breed, SNPs and haplotypes were evaluated independently using a combination of two methods: logistic regression, for evaluating each genotype as response with the year as predictor, and Mann-Kendall test for monotonicity, with allele frequencies over the years as input. The results were ranked by p-value and filtered, keeping the first percentile only. By intersecting the filtered results of the two methods, a stringently validated set of haplotypes and SNPs was identified, which significantly changed over the analyzed time period. Additionally, the absolute difference of the median allele frequency over the first and last five year intervals was computed to evaluate the magnitude of change. A total of 133, 88 and 25 SNP and 127, 105 and 62 haplotypes were selected in ILW, ID and IL, respectively, with no overlap between breeds. Frequency change of selected SNP ranged from 0.21 to 0.68. MDS plots supported population structure changes over the years, with increasing divergence between cosmopolitan and Italian breeds. The selected haplotypes covered 265, 248 and 134 genes in ILW, ID and IL respectively, indirectly suggesting that these changes may have affected specific biological functions associated with relevant phenotypes under selection. These results provide a picture of the effect of the directional artificial selection programs operating over the last decades in shaping the population genomic structure of three pig breeds that differentiated from their corresponding cosmopolitan counterparts.