The indigenous goat population represents the main links to the development of commercial meat-type breeds and may potentially be relevant as a future source of untapped adaptable genetic material [61]. Therefore, improving our understating of within-ecotype relationships among the major goat producing provinces in South Africa offers a rare opportunity enhancing efficient use of the breeds and implementing conservation programs. This study investigated the indications for population status on inbreeding and runs of homozygosity in the communal indigenous goat population. Data from a previous study [38] enabled a broad geographical coverage of South Africa and represents populations from the major goats producing provinces within the country.
Effective population size (Ne) is a crucial population genetic parameter because of its relationship to the loss of genetic variation, increases in inbreeding, the accumulation of mutations, and the determination of the accuracy of genomic selection [21, 5]. Gauteng had the smallest estimated Ne among the population and Limpopo had the highest. It was also observed in other studies that effective population size (Ne) showed a reduction to 132 in the Kingdom of Eswatini and highest in South Africa 12 generations ago [61]. It is recommended that to prevent a reduction of the adaptive value in populations, Ne values between 50 and 100 animals [40] are accepted to be within a factor of 2 from the true value to avoid inbreeding depression. A study by [10], reported a large Ne (140) in local goats breeds, such as those from Africa, Spain and Central-Southern Italy local goats breeds and a small Ne (42) in the Angora, Boer, Nubian, Cashmere, Saanen and Alpine populations. The introduction of records keeping as part of the conservation strategy for the communal indigenous goat populations and occasional DNA-based controls will help to design mating plans that enabled farmers to control inbreeding and maintain effective population size. This can be particularly the case for breeds with distinctive phenotypic traits, such as horn shape, and sizes and coat colours in the ecotypes.
The rapid increase pattern in Ne may also include bottlenecks associated with domestication, selection and breed formation, and the endangerment of the breed [56]. A study by [38] based on SNP data and using the same method reported large Ne for all investigated breeds (ranging from 140 to 348). Furthermore, a study by [39] revealed that the ecotype goat was slightly higher (145) in effective population sizes than the Tankwa and commercial breeds across generations. From a conservation standpoint, the indigenous goat population should top the priority in the population studied due to their diminishing effective population size and increased inbreeding coefficients.
Runs of Homozygosity (ROH) can disclose the genetic relationships among individuals, estimating with high accuracy the autozygosity at the individual and population levels and can elucidate about selection pressure events [54]. If long ROH accumulates in the genome of some individuals, they could seriously impact the overall biological fitness [29], therefore, it was an important objective to investigate and understand the level of homozygosity among the populations. In this study, only 1 animal was lacking ROH, whilst 206 (99.52%) had at least one ROH longer than 1 Mb. The genomic inbreeding coefficients (FROH) values found in the study for the Ethiopian goats were FROH > 1Mb values [44]. Similar results were found by [44] with more African goats (Cameroon, Ethiopia, Kenya, Madagascar, Malawi, Mali, Mozambique, Nigeria, Tanzania, Uganda, and Zimbabwe) using a clustering algorithm. In this study, differences in terms of total number and length of ROH were short (>5Mb) were more abundant (57.61%). [48] reported results that showed lower than the FROH > 2Mb for Kenya, Uganda, and Mozambique goat breeds when Goat 50K BeadChip was used. On the other hand, the Eastern Cape population showed very low amounts of ROH. This has been suggested to be consistent with recent admixture in the individuals in Chinese cattle [62]. Long segments were abundant in the North West population. [25] recent study revealed a high mean ROH in the long length category (>30 Mb), and their study suggested that inbreeding is more recent and is indicative of demographic decline. This is possible considering the extensive management systems of goats in the region, where goats are on free-range or are herded with other flocks for some part of the year, although some researchers have argued that such extensive systems may lead to inbreeding [58, 22]. [29] suggested that the lower inbreeding levels in African goats could be due to the openness of the breeding systems in most of Africa due to the loose definition of livestock breeds in the region.
One of the main advantages of genomic coefficients is the availability of chromosomal inbreeding coefficients [34]. ROH islands can be defined as genomic regions with reduced genetic diversity and, consequently, high homozygosity around the selected locus that might harbor targets of positive selection and are under strong selective pressure [51,50]. ROHs, representing the level of genomic autozygosity, are continuous homozygous segments at the individual and population levels that can be used as a measurement of inbreeding; more in-depth ROHs are the result of demography, natural and artificial selection, and inbreeding [55]. In this study, all the genomic regions associated with ROH were not discussed in details, but the focus was on some selected regions that show associations with several specific traits related to livestock breeding. Five genes were identified and reported to be associated with the important traits of goats (Figure. 5) identified by the selection signature. Overall, the highest coverage by ROH was observed on chromosome 1, 2, 6 respectively. Gene INHA, located on chromosome 2, was reported as a candidate gene for litter size in goats [24]. The PPP1R36 and Heat Shock Protein A2 (HSPA2) (CHI10, 26.402–26.719 Mb) identified in this communal indigenous goats are involved in heat stress response and in other studies, HSPA2, DNAJC24, and DNAJC13 are associated with the heat shock family of genes[55] . The presence of multiple genes associated with heat stress would seem to suggest that the trait is under intense selection pressure in tropically adapted breeds [48].
In accordance with [46], these regions in humans, when they are present in more than 50% of the individuals of a population, can indicate a strong selection occurrence. The occurrence of ROH hotspots in genomic regions that harbour candidate genes may be involved in selection pressure in response to production and environmental conditions. This study identified 58 ROH hotspots in Gauteng and Free State populations and revealed 871 genes and 292 KEGG pathways. This threshold did not yield any results and only in 20% ROH islands were detected in the communal indigenous oat population. The stringent criteria on the communal indigenous goats were used to minimize incorrect discovery of ROH (false positives) within regions of low marker density. The 20% threshold has been used in indigenous Chinese pigs, Jinhua [62]. The minimum expected length of homozygous DNA segments is based on the time frame of approximately 25 generations, over which goats are believed to have been characterized in separate breeds [48].
This study further explored the population genetic structure of all South African communal indigenous goat populations. In accordance with our earlier studies [37, 27], the principal component analysis (PCA), the ADMIXTURE analyses based on the SNP array and sequence data sets capitulated the major genetic division among the South African goat populations from two large geographic regions: Eastern Cape and Limpopo. The analysis of genotyping data for communal indigenous goat populations revealed a geographical pattern that underlies the distribution of genomic diversity, and a moderate and weak population structure in the Gauteng, Free State and North West provinces respectively. The genomes of KwaZulu-Natal and Limpopo shared an origin but have substantial admixture from the Eastern Cape and North West populations. Population admixture analysis generated some signals of admixture and underlying genetic relationships among the populations [24]. The observation supported a migration route of ancient goat from the northern part of South Africa to the eastern areas of the KwaZulu-Natal, during their migration periods of the Bantu nation. This results can also be influenced by communal-traditional indigenous goat farming system and adaptation to different climatic conditions. However, a more extensive sampling of communal indigenous goat populations that would cover more evenly the other South African provinces is necessary to assess the impact of these factors.