Complex Patterns of Genomic Admixture within Southern Africa

Within-population genetic diversity is greatest within Africa, while between-population genetic diversity is directly proportional to geographic distance. The most divergent contemporary human populations include the click-speaking forager peoples of southern Africa, broadly defined as Khoesan. Both intra- (Bantu expansion) and inter-continental migration (European-driven colonization) have resulted in complex patterns of admixture between ancient geographically isolated Khoesan and more recently diverged populations. Using gender-specific analysis and almost 1 million autosomal markers, we determine the significance of estimated ancestral contributions that have shaped five contemporary southern African populations in a cohort of 103 individuals. Limited by lack of available data for homogenous Khoesan representation, we identify the Ju/'hoan (n = 19) as a distinct early diverging human lineage with little to no significant non-Khoesan contribution. In contrast to the Ju/'hoan, we identify ancient signatures of Khoesan and Bantu unions resulting in significant Khoesan- and Bantu-derived contributions to the Southern Bantu amaXhosa (n = 15) and Khoesan !Xun (n = 14), respectively. Our data further suggests that contemporary !Xun represent distinct Khoesan prehistories. Khoesan assimilation with European settlement at the most southern tip of Africa resulted in significant ancestral Khoesan contributions to the Coloured (n = 25) and Baster (n = 30) populations. The latter populations were further impacted by 170 years of East Indian slave trade and intra-continental migrations resulting in a complex pattern of genetic variation (admixture). The populations of southern Africa provide a unique opportunity to investigate the genomic variability from some of the oldest human lineages to the implications of complex admixture patterns including ancient and recently diverged human lineages. Author Summary: The Khoesan have received recent attention, as they are the most genetically diverse contemporary human populations. However, Khoesan populations are poorly defined, while archeological evidence suggests a once broader dispersal of click-speaking southern African foragers. Migrations into the regions populated by contemporary Khoesan involved agro-pastoral Bantu around 1,500 years ago, followed over a millennium later by the arrival of European colonists establishing a halfway station for a maritime route between Europe and the East, which led to unions between diverse global populations. Using almost a million genetic markers for 103 individuals, we confirmed a significant Khoesan contribution to five southern African populations. The Ju/'hoan show genetic isolation (early divergence from all other modern humans), carry no significant non-Khoesan contributions, and unlike most global populations lack signatures of gene-based adaption to agriculture. The !Xun show two distinct Khoesan prehistories; while comparable to the female-derived Khoesan contribution to the amaXhosa Bantu, the male-derived Bantu contribution to the !Xun most likely represents cultural-driven gender-biased gene-flow. Emanating largely from male-derived European ancestral contributions, the Basters showed the highest maternal Khoesan contribution, while the Coloured showed the largest within population and regional-associated variability. The unique admixture fractions of the two latter populations reflect both early diverged and recently diverged human lineages.