Runs of Homozygosity Preliminary Investigation in Pig Breeds

Abstract

Runs of homozygosity (ROH) are contiguous homozygous genomic segments that provide valuable insights into population history, selection pressures, and inbreeding levels. However, the global distribution of ROH and their implications for pig domestication and breeding are not yet fully understood. In this study, we analyzed whole-genome resequencing data from 1203 pigs across 49 breeds to characterize ROH patterns worldwide. European commercial pigs exhibited longer and more numerous ROH segments than Asian indigenous breeds, indicative of stronger artificial selection and higher inbreeding. Crossbreeding led to a reduction in ROH burden, with greater reductions observed when parental genetic divergence was larger. Notably, Asian and European pigs displayed distinct ROH islands, reflecting divergent selection pressures. Functional analysis revealed that these ROH islands were associated with growth, immunity, and reproduction. These findings enhance our understanding of the genetic diversity and selection history of global pig populations, providing valuable insights for future breeding strategies.

Keywords: breeding strategies; crossbreeding effects; domestication; genetic diversity.

Figure 1

Individual patterns of ROH. The distributions of ROH statistics per individual for 49 pig breeds. We divided the population into four groups (ASD: Asian domestic pigs, ASW: Asian wild boars, EUD: European domestic pigs, EUW: European wild boars) corresponding to the four colors based on geographic location, with the name of the breeds and the number of groups indicated in the horizontal coordinates of the figure. The diamonds indicate the mean value of the population. (A) The length of ROH per individual. (B) The number of ROH per individual. (C) ROH length category distribution. Stacked bar charts depicting the proportion of ROH by length (0.5–2 Mb: short, 2–5 Mb: medium, >5 Mb: long) across the 49 pig breeds, with colors corresponding to ROH categories, and each column representing a breed. Netherlands is a local pig breed originating from the Netherlands. TBT refers to Tibetan pigs from the Qinghai–Tibet Plateau of China. TBTGanSu denotes Tibetan pigs from the Gansu Province, China. TBTSiChuan represents Tibetan pigs from the Sichuan Province, China. TBTYunNan indicates Tibetan pigs from the Yunnan Province, China.

Figure 2

ROH patterns and pairwise Fst in individuals of hybrid and parental populations. (A) Boxplot comparing cumulative ROH length per individual (MB) between the hybrid population DD (Diannanxiaoer × Duroc) and its parental populations (Diannanxiaoer [DNXE] and Duroc [D]). (B) Cumulative ROH length comparison for the hybrid population DLY (Duroc × Landrace × Yorkshire) against its parental populations (Duroc [D], Landrace [L], and Yorkshire [Y]). (C) Boxplot showing cumulative ROH number per individual in hybrid population DD versus parental populations DNXE and D. (D) Cumulative ROH number comparison for hybrid population DLY versus parental populations D, L, and Y. In (A–D) plots, where diamonds represent mean values, significance levels are indicated by *, **, *** and **** at p < 0.05, 0.01, 0.001 and 0.0001, respectively. (E) Heatmap of pairwise F_ST values among five populations: Diannanxiaoer (DNXE), Duroc (D), Landrace (L), Yorkshire (Y), and hybrids DD and DLY. Color gradient (blue to red) reflects genetic differentiation intensity, with red indicating higher divergence.

Figure 3

Comparative analysis of selective pressures between ROH-enriched genomic regions and randomly sampled non-ROH island SNPs revealed significantly heightened selection pressures within ROH islands. Significance levels for cohort boxplots were determined using *** for p < 0.001.

Figure 4

(A) Manhattan plot of the distribution of ROH island in the Asian pig (top) and European pig (bottom), where the red line is the top 1% threshold line. (B) Significant biological pathways (p < 0.01) for GO and KEGG enrichment analysis of candidate genes identified in ROH islands of Asian pig (top) and European pig (bottom) populations.

Figure 5

The FSTL5 gene suffers different selective pressures in European and Asian pig populations. (A) The point plot shows the association between FSTL5 gene and 298 complex traits. (B) The point plot shows significant association TWAS results between FSTL5 gene and traits in muscle tissue. (A,B) Data obtained from PigBiobank (http://pigbiobank.farmgtex.org, accessed on 11 January 2025). (C) Haplotype heat map of Asian and European pigs in the FSTL5 gene region (50.26–51.05 Mb).