Genome-wide analysis of hybridization in wild boar populations reveals adaptive introgression from domestic pig

Abstract

The admixture of domestic pig into French wild boar populations has been monitored since the 1980s thanks to the existence of a cytogenetic difference between the two sub-species. The number of chromosomes is 2n = 36 in wild boar and 2n = 38 in pig, respectively. This difference makes it possible to assign the "hybrid" status to wild boar individuals controlled with 37 or 38 chromosomes. However, it does not make it possible to determine the timing of the hybridization(s), nor to guarantee the absence of domestic admixture in an animal with 2n = 36 chromosomes. In order to analyze hybridization in greater detail and to avoid the inherent limitations of the cytogenetic approach, 362 wild boars (WB) recently collected in different French geographical areas and in different environments (farms, free ranging in protected or unprotected areas, animals with 2n = 36, 37 or 38 chromosomes) were genotyped on a 70K SNP chip. Principal component analyses allowed the identification of 13 "outliers" (3.6%), for which the proportion of the genome of "domestic" origin was greater than 40% (Admixture analyses). These animals were probably recent hybrids, having Asian domestic pig ancestry for most of them. For the remaining 349 animals studied, the proportion of the genome of "wild" origin varied between 83% and 100% (median: 94%). This proportion varied significantly depending on how the wild boar populations were managed. Local ancestry analyses revealed adaptive introgression from domestic pig, suggesting a critical role of genetic admixture in improving the fitness and population growth of WB. Overall, our results show that the methods used to monitor the domestic genetic contributions to wild boar populations should evolve in order to limit the level of admixture between the two gene pools.

Keywords: Sus scrofa; Wildlife management; admixture; feral pig; genetic monitoring; genotyping; population genetics.

FIGURE 1

Population structure defined with PCA of 714 pigs from nine European breeds, 37 pigs from two Asian breeds, and 362 French WB. The first (PC1) and second (PC2) principal components are shown. The WBs outside the WB cluster (WB_Outliers) are represented with their respective identification numbers (GISA‐xxx). Letters A, B/B′ and C represent the Asian pig breeds, European pig breeds, and wild boar groups, respectively

FIGURE 2

Estimates of WB ancestry and 95% confidence intervals (CI) for all 362 individuals. Individuals are arranged by Q score following admixture analysis for k = 11. The colors represent the chromosome number of each individual. The first vertical line (on the left side) separates the outliers from animals belonging to the WB cluster (based on PCA). Among the WB_cluster, animals were considered as “unadmixed” if the 95% CI overlapped 0.99 (proportion of WB ancestry)

FIGURE 3

Admixture analysis (K = 11) of wild boar outliers (+ “Vietnamese” DP on the left of the figure). The different colors represent the dominant ancestral proportions of the different breeds (gene pools) considered in this study

FIGURE 4

Average wild boar ancestry estimated over the 349 WB (without outliers) using ELAI, for each position of each autosome. The bold red line represents the mean ancestry, and dotted red lines represent a deviation of three SD and six SD from the mean