Fine-Scale Human Population Structure in Southern Africa Reflects Ecogeographic Boundaries

Abstract

Recent genetic studies have established that the KhoeSan populations of southern Africa are distinct from all other African populations and have remained largely isolated during human prehistory until 2000 years ago. Dozens of different KhoeSan groups exist, belonging to three different language families, but very little is known about their population history. We examine new genomewide polymorphism data and whole mitochondrial genomes for .100 South Africans from the 6 ¼Khomani San and Nama populations of the Northern Cape, analyzed in conjunction with 19 additional southern African populations. Our analyses reveal fine-scale population structure in and around the Kalahari Desert. Surprisingly, this structure does not always correspond to linguistic or subsistence categories as previously suggested, but rather reflects the role of geographic barriers and the ecology of the greater Kalahari Basin. Regardless of subsistence strategy, the indigenous Khoe-speaking Nama pastoralists and the N|u-speaking 6 ¼Khomani (formerly hunter-gatherers) share ancestry with other Khoe-speaking forager populations that form a rim around the Kalahari Desert. We reconstruct earlier migration patterns and estimate that the southern Kalahari populations were among the last to experience gene flow from Bantu speakers, 14 generations ago. We conclude that local adoption of pastoralism, at least by the Nama, appears to have been primarily a cultural process with limited genetic impact from eastern Africa.

An Unexpectedly Complex Architecture for Skin Pigmentation in Africans

“…The ‡Khomani San and the Nama have both experienced admixture with neighboring darker-skinned Bantu-speaking groups beginning ~450 years ago, as well as with lighter-skinned European settlers who first arrived in the Northern Cape during the late 18 th century (Uren et al, 2016a). We assessed these ancestry proportions using unsupervised allele frequency clustering with ADMIXTURE as well as principal components analysis (PCA, STAR Methods ).…”

“…The Nama differ from the ‡Khomani in their proportion of northern versus southern Kalahari ancestry; they have 17% northern Kalahari ancestry, 62% southern Kalahari ancestry, 9% European ancestry, 10% western African ancestry, and 1% attributable to other African populations on average. The western African fraction in the Nama is significantly more variable among individuals (p=1.08e-5), resulting from recent Damara gene flow (Uren et al, 2016a). The partition of ancestry components occurs in the same order and is correlated between ADMIXTURE and PCA (Figure 2, Figure S2A,D–F).…”

“…Three possible evolutionary scenarios that may explain these elevated frequencies are: 1) these variants arose in southern Africa more than 100,000 years ago and were later selected for in Europeans after the out-of-Africa migration in response to northern UVR environments. Alternatively, 2) these variants arose in Europe/Near East, were introduced into KhoeSan populations via “back to Africa” migration into southern Africa predating 17 th century European colonialism (Pickrell et al, 2014; Uren et al, 2016a), and have since been positively selected in the KhoeSan. Lastly, 3) a recurrent mutation (G to A transition at the CpG ancestral dinucleotide, a class of mutations shown to have elevated mutation rates) occurred.…”

“…As described previously (Henn et al, 2011; Uren et al, 2016b), sampling of the ‡Khomani San took place in the Northern Cape of South Africa in the southern Kalahari Desert region (near Upington and neighboring villages) in 2006, 2010, 2011, 2013, and 2015. Sampling of the Nama took place in the Richtersveld in 2014 and 2015.…”

“…35 ‡Khomani, 21 Hadza, and 35 Sandawe individuals were previously genotyped on the Illumina Beadchip 550K custom v2 chip (Henn et al, 2011). 86 ‡Khomani and 13 Nama were genotyped on the Illumina OmniExpress and OmniExpressPlus arrays (same base content, additional exome content in the Plus version of the array) (Uren et al, 2016b). 105 Nama individuals were genotyped on the Illumina Omni2.5 array as part of the African Genome Diversity Project.…”