Genetic diversity and differentiation of pelt, mutton and wool sheep breeds of South Africa using genome-wide single nucleotide polymorphisms.
Loading...
Date
2021
Authors
Journal Title
Journal ISSN
Volume Title
Publisher
Abstract
Sheep, Ovis aries, are a versatile species that has, over hundreds of years, been adapted to
South African environmental conditions resulting in more than 40 breeds that are raised for
various objectives and production systems and constituting a population of close to 30 million
animals. The South African sheep genetic resource presents unique and distinct phenotypes
and genotypes that, put together, contribute to the global biodiversity observed in sheep that
ought to be conserved and used for improved human livelihoods and economies. South Africa
shares its sheep genetics with the global world, through both exportation and importation of
germplasm. The broad objective of the study was to profile the genomic architecture of South
African sheep populations to provide information for optimal utilization, conservation and
improvement. Four hundred South African sheep belonging to 13 breeds of mutton, wool, dual
purpose (mutton and wool), pelt and uncharacterised non-descript indigenous sheep were
sampled and genotyped. In addition, 623 genotypes from the International Sheep Genomics
Consortium representing European, Asian, African sheep breeds were subsampled.
A series of statistical genomic analyses were pursued. In Chapter 3, genetic diversity,
population genetic structure and divergence between South African sheep breeds was
investigated using the OvineSNP50 Beadchip. A total of 400 sheep belonging to 13 breeds
representing mutton, pelt and mutton and wool dual-purpose breeds and Nguni sheep as a
representative of indigenous non-descript genotypes were genotyped. To gain a clearer
understanding of the genetic diversity of South African breeds relative to other breeds, 623
genotypes from six African, two Asian and eight European breeds were included in the
analyses. The study demonstrated low genetic diversity (HO ≤ 0.27) in small and geographically
restricted populations of Namaqua Afrikaner; Nguni, and Blackhead Persian relative to
moderate to high diversity (HO ≥ 0.38) in Merino and Merino-derived commercial breeds (i.e.
Dohne Merino, Australian Merino and Chinese Merino). Overall, the African and Asian
populations were the most inbred populations with FIS ranging from 0.17 ± 0.05 in Grey
Swakara and Ronderib Afrikaner sheep to 0.34 ± 0.07 in the Namaqua Afrikaner.
Principal component analysis separated the fat-tailed sheep (i.e. Swakaras, Nguni, Black Head
Persian, Ethiopian Menzi, Meatmaster) from the rump-tailed sheep of Merino and Dorset Horn
etc., as well as according to breed history and production systems. Similarly, ADMIXTUREbased
clustering revealed various sources of within- and amongst-breed genomic variation
associated with production purpose, adaptation and history of the breeds. An analysis of FSTv
based breed differentiating SNPs suggested selection and population divergence on genomic
regions associated with growth, adaptation and reproduction. Overall, the analysis gave 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 system and geographical distribution and local adaptation.
The second set of analyses (Chapter 4) focused on assessing the genetic diversity, population
structure and breed divergence in 279 animals including the three Merino-derived breeds and
five presumed ancestral populations of Merinos and non-Merino founding breeds of Damara,
Ronderib Afrikaner and Nguni. Highest genetic diversity values were observed in Dohne
Merino with Ho = 0.39 ± 0.01 followed by Meatmaster and South African Merino with Ho =
0.37 ± 0.03. The level of inbreeding ranged from 0.0 ± 0.02 (Dohne Merino) to 0.27 ± 0.05
(Nguni). Analysis of Molecular Variance (AMOVA) showed high within population variance
(>80 %) across all population categories. The first Principal Component (PC1) separated the
Merino, South African Mutton Merino (SAMM), Dohne Merino and Afrino from the
Meatmaster, Damara, Nguni and Ronderib Afrikaner. PC2 aligned each Merino derived breed
with its presumed ancestors and separated the SAMM from the Merino and SA Merino. Within
population selection based on |iHS| indices yielded selection sweeps across the AFR (12
sweeps), Meatmaster (4 sweeps) and Dohne Merino (29 sweeps). Genes associated with
hair/wool traits such as FGF12, metabolic genes of ICA1, NXPH1 and GPR171 and immune
response genes of IL22 IL26, IFNAR1 and IL10RB were reported. Other genes included HMGA
which was observed as a selection signature in other populations, WNT5A important in the
development of the skeleton and mammary glands, ANTXR2 associated with adaptation to
variation in climatic conditions and BMP2 which has been reported as strongly selected in both
fat-tailed and thin-tailed sheep. Using the Rsb analysis for selection sweeps, the Dohne Merino
vs SAMM shared all six sweeps regions on chromosomes 1, 10 and 11 with the comparison
for Afrino vs SAMM. Genes such as FGF12 on OAR 1:191,3-194,7Mb and MAP2K4 on
OAR11:28,6-31,3Mb were observed. The selection sweep on chromosome 10 region 28,6-30,3
Mb, harbouring the RXFP2 for polledness, was shared between Dohne Merino vs Merino,
Meatmaster vs Merino and Meatmaster vs Nguni. The Dohne Merino vs Merino and the
Meatmaster vs Merino also shared an Rsb-based selection sweep on chromosome 1 region
268,5 - 269,9 Mb associated with the Calpain gene, CAPN7. The study demonstrated some
genetic similarities between the Merino and Merino-derived breeds emanating from common
founding populations as well as some divergence driven by breed-specific selection goals.
Chapter 5 tested the hypothesis that production systems geared towards specific traits of
importance or natural or artificial selection pressures influenced the occurrence and distribution
of runs of homozygosity (ROH) in the South African sheep population. The ROH were
screened and their distribution within chromosomes and between breeds were analysed to
assess breed history and associated selected pressures. ROH were computed at cut-offs of 1-6
Mb, 6-12 Mb, 12-24 Mb, 24-48 Mb and >48 Mb. Analysis of the distribution of ROH according
to their size showed that, for all breeds, the majority of the detected ROH were in the short (1-
6 Mb) category (88 %). Most animals had no ROH >48 Mb. Of the South African breeds, the
Nguni and the Blackhead Persian displayed high ROH based inbreeding (FROH) of 0.31 ±
0.05 and 0.31 ± 0.04, respectively. Highest incidence of common ROH per SNP across breeds
was observed on chromosome 10 with over 250 incidences of common ROHs. Mean
proportion of SNPs per breed per ROH islands ranged from 0.02 ± 0.15 (island ROH224 on
chromosome 23) to 0.13 ± 0.29 (island ROH175 on chromosome 15). Seventeen of the islands
had SNPs observed in single populations (unique ROH islands). The MacArthur Merino
population had five unique ROH islands followed by Blackhead Persian and Nguni with three
each whilst the South African Mutton Merino, SA Merino, White Vital Swakara, Karakul,
Dorset Horn and Chinese Merino each had one unique ROH island. Genes within ROH islands
were predominantly associated with metabolic and immune response traits and predomestic
selection for traits such as presence or absence of horns. In line with observations in Chapter
3, the frequency and patterns of distribution of ROH observed in this study corresponded to the
breed history and implied selection pressures exposed to the sheep populations under study.
Chapter 6 investigated (i) LD between adjacent SNPs, (ii) LD decay with increased marker
distance, (iii) trends in effective population size over time and (iv) consistency of gametic phase
in 13 South African sheep breeds South African Merino (n = 56), Merino (n =10); Mutton
Merino (n = 10), Dohne Merino (n = 50), Meatmaster (n = 48), Blackhead Persian (n =14) and
Namaqua Afrikaner (n = 12), the four pelt-colour based Swakara subpopulations of Grey (n =
22); Black (n = 16); White-vital (n = 41) and White-subvital (n =17) Dorper (n = 23); Afrino
(n = 51) and unimproved Nguni sheep (n = 30). Linkage disequilibrium (r2) averaged 0.16 ±
0.021and ranged from 0.09 ± 0.14 and 0.09 ± 0.13 observed in the SA Merino and Dohne
Merino respectively to 0.28 ± 0.29 observed in the Blackhead Persian sheep. Chromosome 10
had the highest LD with r2 values ranging from 0.10 ± 0.15 (SA Merino) and 0.12 ± 0.18
(Dohne Merino) to 0.28 ± 0.30 in Blackhead Persian and 0.29 ± 0.30 (SA Mutton Merino).
Across the 14 breeds, LD decayed from 0.27 ± 0.30 at 0-10Kb window to 0.02 ± 0.03 at 1000-
2000 Kb window. A progressive decrease in Ne across generations across all populations was
observed with effective population size of <500 for all the populations 66 generations ago
decreasing to <250, 23 generations ago and well below 100, 13 generations ago. Highest
correlations in gametic phase were observed within the 0-10kb window between pairs of
Merino and Merino-derived breeds. The highest correlation observed with Nguni sheep was
with Dorper sheep (0.33) within the 0-10kb window, which was similar to that observed with
Blackhead Persian sheep and Dorper (0.32) again within the same window. The study reported
considerable LD persistent over short distance in the South African sheep breeds. The
implications of the observed LD, LD decay and consistency in gamete phase on applications
such as GWAS, QTL mapping and GS were discussed.
It was concluded that the South African sheep population is highly diverse with that diversity
found both within and between populations. Genetic differences between fat tailed sheep
population, Merino type breeds and the English Dorset were demonstrated as well as low levels
of genetic diversity in small and indigenous breeds such as the Nguni, Namaqua Afrikaner and
Blackhead Persian. The frequency and patterns of distribution of ROH observed in this study
corresponded to the breed history and implied selection pressures exposed to the sheep
populations under study. The utility of the OvineSNP50 Beadchip as a genomic tool for the
South African Sheep population was also demonstrated.
Keywords: Ovis aries; SNP data; genomic structure; production system; selection signatures;
ROH
Description
Doctoral Degree. University of KwaZulu-Natal, Pietermaritzburg.