Genome-wide assessments of the genetic landscape of Farm Animal Genetic Resources (FAnGR) are key to developing sustainable breed improvements. Understanding the FAnGR adaptation to different environments and supporting their conservation programs from community initiative to national policymakers is very important. The objective of the study was to investigate the genetic diversity and population structure of communal indigenous goat populations from four provinces of South Africa. Communal indigenous goat populations from the Free State (FS) (n = 24), Gauteng (GP) (n = 28), Limpopo (LP) (n = 30), and North West (NW) (n = 35) provinces were genotyped using the Illumina Goats SNP50 BeadChip. An Illumina Goats SNP50 BeadChip data from commercial meat-type breeds: Boer (n = 33), Kalahari Red (n = 40), and Savanna (n = 31) was used in this study as reference populations. The H_o revealed that the genetic diversity of a population ranged between 0.39 ± 0.11 H_o in LP to 0.42 ± 0.09 H_o in NW. Analysis of molecular variance revealed variations of 3.39% (p < 0.0001) and 90.64% among and within populations, respectively. The first two Principal Component Analyses (PCAs) revealed a unique Limpopo population separated from GP, FS, and NW communal indigenous goat populations with high levels of admixture with commercial goat populations. There were unique populations of Kalahari and Savanna that were observed and admixed individuals. Marker F_ST (Limpopo versus commercial goat populations) revealed 442 outlier single nucleotide polymorphisms (SNPs) across all chromosomes, and the SNP with the highest F_ST value (F_ST = 0.72; chromosome 8) was located on the UHRF2 gene. Population differentiation tests (PCAdapt) revealed PC2 as optimal and five outlier SNPs were detected on chromosomes 10, 15, 20, and 21. The study revealed that the SNPs identified by the first two principal components show high F_ST values in LP communal goat populations and allowed us to identify candidate genes which can be used in the development of breed selection programs to improve this unique LP population and other communal goat population of FS, GP, and NW, and find genetic factors contributing to the adaptation to harsh environments. Effective management and utilization of South African communal indigenous goat populations is important, and effort should be made to maintain unique genetic resources for conservation.

Background: Indigenous goats forms the majority of populations in smallholder; low input, low output production systems and are considered an important genetic resource due to their adaptability to different production environments and support communal farming. Effective population size (N_e), inbreeding levels, and the runs of homozygosity (ROHs) are effective tools for exploring the genetic diversity and understanding the demographic history in efforts to support breeding strategies to use and conserve genetic resources. Results: Across populations, the current N_e of Gauteng was the lowest at 371 animals, while the historical N_e across populations suggests that the ancestor N_e has decreased by 53.86%, 44.58%, 42.16% and 41.16% in Free State (FS), North West (NW), Limpopo (LP) and Gauteng (GP), respectively, over the last 971 generations. Genomic inbreeding levels related to ancient kinship (F_ROH >5Mb) was highest in FS (0.08±0.09) and lowest for Eastern Cape (EC) (0.02±0.02). A total of 871 ROH island regions which include important environmental adaptation and hermo-tolerance genes such as IL10RB, IL23A, FGF9, IGF1, EGR1, MTOR and MAPK3 were identified (occurring in over 20% of the samples) in FS (n = 37), GP (n = 42), NW (n = 2) populations only. The mean length of ROH across populations was 7.76Mb and ranged from 1.61Mb KwaZulu-Natal (KZN) to 98.05Mb (GP and NW). Distribution of ROH according to their size showed that the majority (n = 1949) of the detected ROH were >5Mb in length than the other categories. Assuming two hypothetical ancestral populations, the population from KZN and LP are revealed, supporting PC 1. The genomes of KZN and LP shared an origin but have substantial admixture from the EC and NW populations.Conclusions: These findings indicated a greater negative impact of inbreeding in recent times which is important for planning conservation strategies. It was revealed that the occurrence of high N_e and autozygosity varied largely across breeds in communal indigenous goat populations at different recent and ancient events when a genome-wide SNP marker was used.