Runs of homozygosity in Swiss goats reveal genetic changes associated with domestication and modern selection

Abstract

Background: The domestication of goat (Capra hircus) started 11,000 years ago in the fertile crescent. Breed formation in the nineteenth century, establishment of herd books, and selection for specific traits resulted in 10 modern goat breeds in Switzerland. We analyzed whole-genome sequencing (WGS) data from 217 modern goats and nine wild Bezoar goats (Capra aegagrus). After quality control, 27,728,288 biallelic single nucleotide variants (SNVs) were used for the identification of runs of homozygosity (ROH) and the detection of ROH islands.

Results: Across the 226 caprine genomes from 11 populations, we detected 344 ROH islands that harbor 1220 annotated genes. We compared the ROH islands between the modern breeds and the Bezoar goats. As a proof of principle, we confirmed a signature of selection, which contains the ASIP gene that controls several breed-specific coat color patterns. In two other ROH islands, we identified two missense variants, STC1:p.Lys139Arg and TSHR:p.Ala239Thr, which might represent causative functional variants for domestication signatures.

Conclusions: We have shown that the information from ROH islands using WGS data is suitable for the analysis of signatures of selection and allowed the detection of protein coding variants that may have conferred beneficial phenotypes during goat domestication. We hypothesize that the TSHR:p.Ala239Thr variant may have played a role in changing the seasonality of reproduction in modern domesticated goats. The exact functional significance of the STC1:p.Lys139Arg variant remains unclear and requires further investigation. Nonetheless, STC1 might represent a new domestication gene affecting relevant traits such as body size and/or milk yield in goats.

Fig. 1

Population structure of the 11 caprine populations analysed. Multidimensional scaling plot representing population structure based on the first (C1) and second (C2) components (left) and on the first (C1) and third (C3) components (right). Both plots are based on pruned genotypes at 4,831,063 SNVs from 226 sequenced caprine genomes

Fig. 2

Genomic inbreeding (F_ROH) in 11 caprine populations. Average F_ROH per breed and relative contribution of the five length classes (0.1 to 0.3 Mb, 0.3 to 0.5 Mb, 0.5 to 1.0 Mb, 1.0 to 5.0 Mb and > 5.0 Mb)

Fig. 3

Genome-wide detection of 15 ROH islands. Manhattan plot representing the average fraction of the 217 individuals of the modern goat breeds having a given SNV in a ROH. The threshold (red dashed line) was set to 80% and SNVs defining the ROH islands are visualized in green color. Autosomal regions harboring two ROH islands are indicated with an asterisk

Fig. 4

Details of the STC1: p.Lys139Arg variant. a Fraction of individuals having the tested SNV in a ROH is given for Bezoars and three modern goat breeds (SAN, CAG, PFA). b Allele frequencies of the STC1:p.Lys139Arg variant in domesticated goats (CH) and in Bezoars in (BEZ). c Allele frequencies for each of the 10 modern goat breeds

Fig. 5

Details of the TSHR:p.Ala239Thr variant. a Fraction of individuals having the tested SNV in an ROH is given for Bezoar goats and three modern goat breeds (SAN, CAG, PFA). b Allele frequencies of the TSHR:p.Ala239Thr variant in domesticated goats (CH) and in Bezoar goats (BEZ). c Allele frequencies for each of the 10 modern goat breeds