Genomic signatures of adaptive introgression from European mouflon into domestic sheep

Abstract

Mouflon (Ovis aries musimon) became extinct from mainland Europe after the Neolithic, but remnant populations from the Mediterranean islands of Corsica and Sardinia have been used for reintroductions across Europe since the 19^th-century. Mouflon x sheep hybrids are larger-bodied than mouflon, potentially showing increased male reproductive success, but little is known about genomic levels of admixture, or about the adaptive significance of introgression between resident mouflon and local sheep breeds. Here we analysed Ovine medium-density SNP array genotypes of 92 mouflon from six geographic regions, along with data from 330 individuals of 16 domestic sheep breeds. We found lower levels of genetic diversity in mouflon than in domestic sheep, consistent with past bottlenecks in mouflon. Introgression signals were bidirectional and affected most mouflon and sheep populations, being strongest in one Sardinian mouflon population. Developing and using a novel approach to identify chromosomal regions with consistent introgression signals, we infer adaptive introgression from mouflon to domestic sheep related to immunity mechanisms, but not in the opposite direction. Further, we infer that Soay and Sarda sheep carry introgressed mouflon alleles involved in bitter taste perception and/or innate immunity. Our results illustrate the potential for adaptive introgression even among recently diverged populations.

Figure 1

Sampling location. Geographic origin of mouflon and domestic sheep samples. For population abbreviations see Table 1. Map was generated in Inkscape v 0.91 (https://inkscape.org/).

Figure 2

Admixture plot. Admixture plot comprising the first 24 clustering solutions of all the 422 individuals analysed in this work. The analysis is based on 36,961 SNPs from the Ovine SNP50BeadChip. For population abbreviations see Table 1.

Figure 3

Treemix plot. (a) Phylogenetic network inferred by Treemix of the relationships between mouflon and domestic sheep populations. The first four migration edges between populations are shown with arrows pointing in the direction toward the recipient group, and coloured according to the ancestry percentage received from the donor. The numbers associated with each vector identify the identification order. (b) The inset shows the f index representing the fraction of the variance in the sample covariance matrix ($\widehat{W}$) accounted for by the model covariance matrix ($W$), as a function of the number of modelled migration events. For population abbreviations see Table 1.

Figure 4

Graphical exemplification of the CIWI approach. Graphical representation of the inferred local ancestry for a domestic sheep breed (SAR) according to PCAdmix. (a) The 10 focal diploid individuals belonging to SAR are represented by the 10 numbered lines. Each line represents a diploid individual of the SAR population, and extends for the total length of the ovine chromosome 2 (249.99 Mb). The colour scheme indicates the assignment of each block to one of the three reference populations. (b) PCAdmix results for one individual (number 2) of the SAR population, obtained from comparison with four different reference populations for domestic sheep (CAS, ASM, LAC, SAB_p). Genomic regions not analysed by the software due to the absence of SNPs are visible as white gaps. (c) Within-analysis concordance scores (A-scores) are calculated along the chromosome to represent the concordance of ancestry assignment among the 10 focal SAR individuals. The A-scores relative to the four reference populations are represented by coloured segments. The CIWI score is then calculated from the A-scores and is represented by the black solid line. The inset expands the genomic region within chromosome 2, where genes related to the citrullination function are located. (d) Comparison between PCAdmix results for a portion of chromosome 4 in the same individual when compared to four different domestic sheep reference populations. Regions of discordance (i) and concordance (ii; a CIWI) are highlighted by dashed boxes.