Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression

Abstract

The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics. During the Industrial Revolution, Chinese breeds were imported to Europe to improve commercial traits in European breeds. Here we demonstrate the presence of introgressed Asian haplotypes in European domestic pigs and selection signatures on some loci in these regions, using whole genome sequence data. The introgression signatures are widespread and the Asian haplotypes are rarely fixed. The Asian introgressed haplotypes are associated with regions harbouring genes involved in meat quality, development and fertility. We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines. These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.

Figure 1. Experimental setup for the introgression detection.

Arrows indicate the comparisons between groups that are used for the IBD detection. Individuals from the LW breed are used for all pairwise comparisons with individuals from two geographical and functional groups: EUWB and ASDom. The blue arrow indicates the human-mediated introgression from ASDom in to LW.

Figure 2. Distribution of regions in the genome where the LW contain introgressed haplotypes from ASDom.

(a) The x axis shows the full length of all chromosomes, and the y axis represents the relative frequency of LW haplotypes IBD with ASDom or EUWB, ranging from 1 (all haplotypes are IBD with ASDom, and none with EUWB) to −1. The two longest regions of consecutive introgression are indicated with arrows. (b) Distribution of the relative proportion of IBD haplotypes in LW and the EUWB (green, IBDEUWB, 0 to −1) or ASDom (blue, IBDASDom, 0 to 1) in bins of 10 Kbp. (c) Distribution of the rIBD scores for the LW haplotypes (rIBD=IBDEUWB–IBDASDom). (d) Z-transformed distribution of rIBD.

Figure 3. Levels of differentiation between LW and ASDom or EUWB in regions of introgression.

(a) Relative introgression fraction (rIBD) over the full length of chromosome 8 and 9. The longest regions of introgression are indicated with purple and blue. (b) Boxplot of D-statistics for the full genome (red) and the two longest regions of introgression as indicated in a on chr8 (purple) and chr9 (blue). The minimum, first quartile, median, third quartile and maximum are indicated with the box and whiskers with outliers >1.5*IQR. D-statistics are computed for each possible trio with LW=P1, ASDom=P2 and EUWB=P3, with the Sumatran S. scrofa as outgroup (O) resulting in 378 trios. (c–e) Distribution of Fst between LW-ASDom (blue) and LW-EUWB (red) in bins of 10 Kbp. The left histogram shows the Fst distributions based on the full genome (c), and the other two show the Fst distribution for the regions of introgression on chr8 (d) and chr9 (e).