Analysis of the genetics of boar taint reveals both single SNPs and regional effects

Abstract

Background: Boar taint is an offensive urine or faecal-like odour, affecting the smell and taste of cooked pork from some mature non-castrated male pigs. Androstenone and skatole in fat are the molecules responsible. In most pig production systems, males, which are not required for breeding, are castrated shortly after birth to reduce the risk of boar taint. There is evidence for genetic variation in the predisposition to boar taint.A genome-wide association study (GWAS) was performed to identify loci with effects on boar taint. Five hundred Danish Landrace boars with high levels of skatole in fat (>0.3 μg/g), were each matched with a litter mate with low levels of skatole and measured for androstenone. DNA from these 1,000 non-castrated boars was genotyped using the Illumina PorcineSNP60 Beadchip. After quality control, tests for SNPs associated with boar taint were performed on 938 phenotyped individuals and 44,648 SNPs. Empirical significance thresholds were set by permutation (100,000). For androstenone, a 'regional heritability approach' combining information from multiple SNPs was used to estimate the genetic variation attributable to individual autosomes.

Results: A highly significant association was found between variation in skatole levels and SNPs within the CYP2E1 gene on chromosome 14 (SSC14), which encodes an enzyme involved in degradation of skatole. Nominal significance was found for effects on skatole associated with 4 other SNPs including a region of SSC6 reported previously. Genome-wide significance was found for an association between SNPs on SSC5 and androstenone levels and nominal significance for associations with SNPs on SSC13 and SSC17. The regional analyses confirmed large effects on SSC5 for androstenone and suggest that SSC5 explains 23% of the genetic variation in androstenone. The autosomal heritability analyses also suggest that there is a large effect associated with androstenone on SSC2, not detected using GWAS.

Conclusions: Significant SNP associations were found for skatole on SSC14 and for androstenone on SSC5 in Landrace pigs. The study agrees with evidence that the CYP2E1 gene has effects on skatole breakdown in the liver. Autosomal heritability estimates can uncover clusters of smaller genetic effects that individually do not exceed the threshold for GWAS significance.

Figure 1

Visualization of population structure. Scree plot showing best fit shown by bend in curve is 3 clusters for the data (top). Plot of three clusters using co-ordinates from multi-dimensional scaling (bottom). Clusters are shown in green, red and blue. Individuals are assigned to clusters or groups based on degree of genetic relatedness.

Figure 2

Manhattan plots for genome-wide association analysis for associations with skatole (top) and androstenone (bottom). Grammar method applied to eighteen autosomes plus unassigned SNPs (far right in dark blue). Genome-wide significance thresholds dashed line 5% FDR cut off. Dotted line is genome-wide significance threshold set by 100,000 permutations. Results are based on corrected P values using lambda statistic to account for systematic bias.

Figure 3

LD decay from SNP H3G000016037 plotted against significance of effect on androstenone, pairwise LD in the region and genes located within the region. Sscrofa genome build 10.2.

Figure 4

Autosomal heritability or proportion of phenotypic variance explained for androstenone. *estimate of heritability is larger than standard error. All 18 autosomes were fitted simultaneously in a mixed linear model.

Figure 5

Likelihood ratio test (LRT) for significance of autosomal heritability or proportion of phenotypic variance explained for androstenone using three different linear mixed models. LRTind is comparing a model fitting an individual autosome with a null model, LRTdrop is where all autosomes are fitted and compared with a model which drops each autosome in turn, LRTpoly is comparing a model fitting an individual autosome plus a polygenic effect with a model containing only a polygenic effect.

Figure 6

LD decay from SNP SIRI0000194 plotted against significance of effect on Skatole, pairwise LD in the region and genes located within the region. Sscrofa genome build 10.2.