The genomic architecture of South African mutton, pelt, dual-purpose and nondescript sheep breeds relative to global sheep populations.

South Africa has a diverse array of phenotypically distinct and locally adapted sheep breeds that have been developed for different production systems ranging from mutton to wool and pelt, and some dual-purpose and nondescript breeds kept by smallholder farmers. This study investigated genetic diversity, population genetic structure and divergence between South African sheep breeds in order to gain an insight into breed history and genomic architecture aligned to breeding goals and production systems. The Illumina OvineSNP50 BeadChip was used to genotype 400 sheep belonging to 14 breeds representing mutton, pelt and mutton and wool dual-purpose breeds. Nguni sheep were included as a representative of indigenous nondescript breeds that are reared by smallholder farmers. Seeking a clearer understanding of the genetic diversity of South African breeds relative to global populations, 623 genotypes of sheep from worldwide populations were included in the analysis. These sheep breeds included six African, two Asian and eight European breeds. Across breeds, genetic diversity ranged from observed heterozygosity (H ) = 0.26 ± 0.02 in Namaqua Afrikaner to H  = 0.38 ± 0.01 in Dohne Merino. The overall mean H was 0.35 ± 0.04. The African and Asian populations were the most inbred populations with F ranging from 0.17 ± 0.05 in Grey Swakara and Ronderib Afrikaner sheep to 0.34 ± 0.07 in the Namaqua Afrikaner. The South African Dohne Merino (F  = 0.03 ± 0.01), SA Merino (F  = 0.05 ± 0.04) and Afrino (F  = 0.09 ± 0.02) and other global Merino-derived breeds were the least inbred. The first principal component explained 27.7% of the variation and separated the fat- and rump-tailed sheep (i.e. Swakara, Nguni, Blackhead Persian, Ethiopian Menzi, Meatmaster) from the Merino and Merino-derived breeds and the Dorset Horn. The second principal component separated the Merino and Merino-derived breeds from the English breed of Dorset Horn. Overall, South African indigenous breeds clustered together with indigenous breeds from other African and Asian countries. The optimal admixture cluster (K = 20) revealed various sources of within- and amongst-breed genomic variation associated with production purpose, adaptation and history of the breeds. The Blackhead Persian, Nguni and Namaqua Afrikaner breeds differed significantly from other breeds, particularly with the South African Mutton Merino and Dorset Horn. Breed-differentiating SNPs were observed within genomic regions associated with growth, adaptation and reproduction. Genes such as RAB44, associated with growth and meat/carcass traits, differentiated the Blackhead Persian from the Dorset Horn and South African Mutton Merino. The MAP2 and HRAS genes, which are associated with immune traits involving Toll-like receptors and Chemokine signalling pathways, differentiated the Nguni from the Dorset Horn. The current results give insight into the current status of the sheep genetic resources of South Africa relative to the global sheep population, highlighting both genetic similarities as well as divergence associated with production systems, geographical distribution and local adaptation.