The Indian Ocean slave trade and colonial expansion resulted in strong sex-biased admixture in South Africa

The colonial-period arrival of Europeans in southern Africa is associated with strong sex-biased migration by which male settlers displaced Indigenous Khoekhoe and San men. Concurrently, the importation of enslaved individuals from South Asia, Indonesia, and eastern Africa likely contributed to female-biased migration. Using genetic data from over 1,400 individuals, we examine the spatial and temporal spread of sex-biased migration from the Cape to the northern edges of the historic colonial frontier. In all regions, admixture patterns were sex biased, with evidence of a greater male contribution of European ancestry and greater female contribution of Khoe-San ancestry. While admixture among Khoe-San, European, equatorial African, and Asian groups has likely been continuous from the founding of Cape Town to the present day, we find that Khoe-San groups further north experienced a single pulse of European admixture 6–8 generations ago. European admixture was followed by additional Khoe-San gene flow, potentially reflecting an aggregation of Indigenous groups due to disruption by colonial interlopers. Male migration into the northern frontier territories was not a homogenous group of expanding Afrikaners and slaves. The Nama exhibit distinct founder effects and derive 15% of their Y chromosome haplogroups from Asian lineages, a pattern absent in the ≠Khomani San. Khoe-San ancestry from the paternal line is greatly diminished in populations from Cape Town, the Cederberg Mountains, and Upington but remains more frequent in self-identified Indigenous ethnic groups. Strikingly, we estimate that Khoe-San Y chromosomes were experiencing unprecedented population growth at the time of European arrival. Our findings shed light on the patterns of admixture and population history of South Africa as the colonial frontier expanded.