Whole-genome sequencing of Berkshire (European native pig) provides insights into its origin and domestication

Abstract

Domesticated organisms have experienced strong selective pressures directed at genes or genomic regions controlling traits of biological, agricultural or medical importance. The genome of native and domesticated pigs provide a unique opportunity for tracing the history of domestication and identifying signatures of artificial selection. Here we used whole-genome sequencing to explore the genetic relationships among the European native pig Berkshire and breeds that are distributed worldwide, and to identify genomic footprints left by selection during the domestication of Berkshire. Numerous nonsynonymous SNPs-containing genes fall into olfactory-related categories, which are part of a rapidly evolving superfamily in the mammalian genome. Phylogenetic analyses revealed a deep phylogenetic split between European and Asian pigs rather than between domestic and wild pigs. Admixture analysis exhibited higher portion of Chinese genetic material for the Berkshire pigs, which is consistent with the historical record regarding its origin. Selective sweep analyses revealed strong signatures of selection affecting genomic regions that harbor genes underlying economic traits such as disease resistance, pork yield, fertility, tameness and body length. These discoveries confirmed the history of origin of Berkshire pig by genome-wide analysis and illustrate how domestication has shaped the patterns of genetic variation.

Figure 1. Phylogenetic relationship and gene introgression.

(a) Two-way PCA plot of pig breeds. The fraction of the variance explained is 33.56% for eigenvector 1 and 9.56% for eigenvector 2 with a Tracy-Widom P value < 10⁻⁶ (Supplementary Table S5). (b) NJ phylogenetic tree of pig breeds. The scale bar represents p distance. (c) Four-taxon ABBA/BABA test of introgression. First panel from the left: ABBA and BABA nucleotide sites employed in the test are derived (- - B -) in Chinese domestic pigs compared with the warthog outgroup (- - - A), but differ among Berkshire and other 5 European domestic pigs (either ABBA or BABA). As this almost exclusively restricts attention to sites polymorphic in the ancestor of Chinese domestic pigs, Berkshire and other 5 European domestic pigs, equal numbers of ABBA and BABA sites are expected under a null hypothesis of no introgression, as depicted in the two gene genealogies. Second to last panel from the left: Distribution among chromosomes of D-statistic (± s.e.), which measures excess of ABBA sites over BABA sites, here for the comparison: Other 5 European domestic pigs (i.e. Duroc, Landrace, Pietrain, Large white and Hampshire), Berkshire, Chinese domestic pigs, African warthog.

Figure 2. Identification of genomic regions with strong selective sweep signals in Berkshire pigs.

(a) LD patterns of Berkshire and European wild boars. (b) Distribution of log₂ (θ_π ratio (θ_{π, wild boar}/θ_{π, Berkshire})) and F_ST, which are calculated in 100 kb windows sliding in 10 kb steps. Data points located to the right of the vertical lines (corresponding to 10% right tails of the empirical log₂ (θ_π ratio) distribution, where log₂ (θ_π ratio) is 3.14) and above the horizontal line (10% right tail of the empirical F_ST distribution, where F_ST is 0.71) were identified as selected regions for Berkshire pigs (red points). (c) Violin plot of θ_π ratio and F_ST values for regions of Berkshire pigs that have undergone positive selection versus the whole genome. Each “violin” with the width depicting a 90°-rotated kernel density trace and its reflection. Vertical black boxes denote the interquartile range (IQR) between the first and third quartiles (25^th and 75^th percentiles, respectively) and the white point inside denotes the median. Vertical black lines denote the lowest and highest values within 1.5 times IQR from the first and third quartiles, respectively. The statistical significance was calculated by the Mann-Whitney U test.

Figure 3. Genes related to body length with strong selective sweep signals in Berkshire pigs.

(a) Log₂ (θ_π ratio (θ_{π, wild boar}/θ_{π, Berkshire})) and F_ST values are plotted using a 10 kb sliding window for genes embedded in selected regions. Genomic regions located above the upper horizontal blue line (corresponding to a 10% significance level of F_ST, where F_ST = 0.71) and above the lower horizontal red line (a 10% significance level of θ_π ratio, where log₂ (θ_π ratio) = 3.14) were termed as regions with strong selective sweep signals (green regions). Genome annotations are shown at the bottom (black bar: coding sequences, blue bar: genes). The boundary of ten genes related to body length is marked in red. (b) NR6A1 gene with strong selective sweep signals. Out of 482 genes embedded in selected regions which crossed 1,144 windows of 100 kb in length sliding in 10 kb steps, only one gene (i.e. NR6A1) is embedded in the most significantly (1% right tail log₂ (θ_π ratio and F_ST values) selected regions (log₂ (θ_π ratio) = 6.72; F_ST = 0.91).