Genomic analysis of Swakara sheep sub-populations.

Abstract

The Swakara, originally derived from the Karakul breed of Uzbekistan, is a fat-tailed sheep breed first imported into Namibia in the 1900’s and then later spread throughout Southern Africa. With the aim of producing superior pelts, the breed was subjected to intense crossbreeding and selection with the white wooled indigenous Namaqua Afrikaner and Blackhead Persian breeds, with the aim of producing superior pelts possessing wavy hair with short, lustrous fibres and clear patterns. Swakara sheep can be found in four different coat colours (black, grey, brown, and white), with only the black being inherent to the original Karakul with the presence of coat colour variation thought to be the basis of some of the inbreeding and selection imposed on the breed. The sheep are prone to genetic disorders such as the subvital factor that causes the animals to die within 48 hours of birth and is prevalent in grey and white-wooled sheep. It is suggested that these genetic disorders are due to intensive selection imposed on a breed of limited population size. Little is known about the genomic architecture of the Swakara sheep and its divergence between the sub-populations and from the founding breeds. Such lack of information makes it difficult to understand the factors contributing to the appearance of genetic disorders. Furthermore, it imposes a challenge in the implementation of future breeding programs, trying to select for new traits as well as in the conservation of genetic resources. In this study, 244 sheep from 8 sub-populations representative of Swakara Sheep from Namibia (n = 171), and South Africa (n = 44) and founding Karakul sheep from Germany (n = 5) were sampled and genotyped using the OvineSNP50 beadchip. These sheep were of Brown (n = 25), Black (n = 51), Grey (n = 42), White Vital (n = 34), and White Subvital (n = 63) sheep. In addition, ancestral breeds of Namaqua Afrikaner (n = 10) and Blackhead Persian (n = 14) were obtained from previously published data. The first set of analysis investigated the genetic diversity and structure of Swakara sub-populations and its presumed founding breeds. Genetic diversity ranged from HO = 0.29±0.15 for the White Subvital to HO = 0.41±0.22 for the Karakul. The first principal component analysis (PCA) produced five clusters with PC1 explaining 27.35% of the total variation whilst PC2 accounted for 19.25% of the total variation. Cluster A consisted of only the Brown Swakara, Cluster B consisted of the Black, Grey, and White Swakara. Some of the White Vital and Black Vital also clustered together with the Karakul in Cluster C. The Namaqua Afrikaner and Blackhead Persian clustered separately in Clusters D and E, respectively. Per marker FST showed differentiated SNPs within QTLs associated with milk production, wool quality traits, and coat colour. Signatures of selection were identified utilising three methods of within population (iHS), between population (XP-EHH) and across the global population (HapFLK). A total of 73, 619 and 1931 selective sweeps were detected from each of the analysis, respectively. A large number of significant selective sweeps (|iHS|>3.0) were identified within the ancestral populations across 16 different chromosomes (OAR1, OAR2, OAR3, OAR4, OAR5, OAR6, OAR7, OAR8, OAR12, OAR15, OAR17, OAR18, OAR20, OAR21, OAR22, OAR23) and 28 of the signals were detected within the coat colour groups and ancestral groups. Overlapping genes were associated with QTLS of body weight (FBN2, CNTNAP5) and milk fat percentage (TMEM163, NDUFB3). The strongest signals were observed between the coat colour sub-populations with XP-EHH values ranging from 3.93 to 5.27. Further analysis detected signatures of selection related to 56 candidate genes, including PTGER3, ADAMTS3, TROAP, NEIL2, FBXO8, BTBD10, KLF13, and CCNT1 that are associated with hot carcass weight, testes weight and milk yield. HapFLK revealed strong selection signals on chromosome 2 and 3. Genes related to gastrointestinal parasites such as GPC6, KAZN, MCTP1, and HS3ST3A1 were detected. Runs of homozygosity (ROH) analysis revealed the Brown Vital and Blackhead Persian to have ROHs of the longest mean lengths. Furthermore, FROH based inbreeding estimates were low across populations with the highest inbreeding (FROH = 0.26) identified in the Namaqua Afrikaner. This study sought to provide insight into the genomic architecture of Swakara sheep and the presumed ancestors to understand the prevalence of genetic disorders, guide future breeding programs and facilitate preservation of genetics.