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Study Suggests African Khoisan Hunter-Gatherers Remained Isolated, Represented Largest Population

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NEW YORK (GenomeWeb) – An international research team led by Pennsylvania State University and Nanyang Technological University in Singapore has delved into the population history of Khoisan hunter-gatherers from Southern Africa, comparing the genomes of several Khoisan individuals with those of other ethnic groups.

Two of the Khoisan genomes, from the Ju/'hoansi group, appear to show no genetic contributions from other human populations, suggesting that members of the group may have remained genetically isolated for up to 150,000 years.

In addition, the Khoisan – a relatively small population today – may have been the largest human population throughout much of modern human history, maintaining large genetic diversity, while other groups inside and outside of Africa experienced dramatic declines in population size and diversity.

A possible reason for this, the researchers suggest, is a change in climate about 80,000 to 100,000 years ago that increased precipitation in southern Africa where the Khoisan lived, making it more hospitable, whereas west and central Africa became drier and more difficult to live in.

The researchers, led by Stephan Schuster, a professor at Nanyang Technological University, published their results online in Nature Communications today.

According to Schuster, who used to be a professor at Penn State, the study was an extension of his group's earlier work, published in 2010, in which they sequenced the genomes of a Khoisan from Namibia and Archbishop Desmond Tutu, a Bantu, as well as the exomes of three other Namibian Khoisans.

"Something we were still unsatisfied with after that publication is, we wanted to show it is indeed possible that a human lineage remained un-admixed for a very long time," Schuster told GenomeWeb.

For their latest study, which included the two original genomes, they sequenced the genomes of five Namibian Khoisan hunter-gatherers and Archbishop Tutu using the Illumina HiSeq platform. The four new Khoisan samples came from two married couples, both among the eldest members of their tribes. One couple belongs to a Tuu-speaking group of the southern Kalahari Desert, the other to the Ju/'hoansi group of the northern Kalahari region.

The scientists compared the genomes with eight publicly available genome sequences from African Yoruban, European, Southern Indian, Japanese, and Korean individuals and analyzed them against SNP genotyping data from 1,448 individuals from all over the world.

Their analysis, which employed four different methods, showed that the Ju/'hoansi couple had no evidence of admixture from non-Khoisan groups, whereas the other Khoisan genomes displayed a small percentage of western African ancestry, and Archbishop Tutu showed both western African and southern Khoisan ancestries.

According to Schuster, the lack of admixture in the Ju/'hoansi individuals runs counter to a "very large consensus in the field that admixture is so prevalent." The finding was possible, he said, because of the care taken by the researchers to obtain samples from very isolated Khoisan tribes that have had not only geographic but also cultural barriers to mixing with other populations. "We should not by definition rule out that people cannot remain non-admixed over long periods of time," he said, adding that "there might be other very interesting surprises out there."

However, the finding is not undisputed. "I am not convinced that the two individuals have exclusive Khoe-San ancestry," said Pontus Skoglund, a postdoctoral fellow in David Reich's group at the department of genetics at Harvard Medical School. Skoglund told GenomeWeb in an email that the result is based on a type of clustering analysis that "is not always able to detect such non-Khoe-San ancestry." Previous research by Reich's group has shown "that there is probably a small proportion of East African and Middle Eastern ancestry in all living Khoe-San, and I don't see how that is refuted by the analyses in this paper," he said.

In addition to determining the ancestry of the Khoisan genomes, Schuster and his colleagues applied a so-called Pairwise Sequentially Markovian Coalescent (PSMC) model to the 14 genome sequences in order to reconstruct changes in their effective population size over time.

Based on that analysis, they concluded that the Khoisan split from other African populations around 100,000 to 150,000 years ago and maintained high genetic diversity throughout, and the largest population. Non-Khoisans, on the other hand, saw a decline in their effective population size and lost more than half of their diversity over the last 30,000 to 120,000 years.

According to Skoglund, while the high genetic diversity of Khoisans was already known, "there are reservations for the claim that the Khoe-San was the largest population on earth at some point." Both genetic variation and PSMC inference is sensitive to population structure, he said, in addition to population size changes, and "if there is a lot of population structure, say, in the ancestors of the Khoe-San, that could give the same signal as a large population size." In addition, there might be other African populations with a larger population size, for example central African pygmies, that were not included in the study. "Finally, in general the population size estimated by these methods is a measure of genetic drift, and so not necessarily strongly related to actual census population size," he added.

To explain the decline in effective population size of non-Khoisan groups compared to the Khoisan, Schuster and his colleagues turned to paleoclimate models and records. After the Khoisan split from the other populations, the climate likely became hotter and drier in western in central Africa, but in southern Africa, where the Khoisan resided, it became wetter. This, the researchers hypothesized, might have led to the decline in western African populations, the ancestors of the current Bantu-speaking populations, but not the Khoisan.

This model holds true even if a lower mutation rate is used, which some researchers favor, the authors noted. This would put the split of the Khoisan about 100,000 years earlier, but a similar climate change likely happened close to that time.

About 40,000 to 60,000 years ago, humans then started to migrate out of Africa, which led to the split between African and non-African populations and a steep decline in genetic diversity in the latter. "You could speculate that the decline in population of the Yoruba and West African population might actually have triggered members of these groups to attempt to go out of Africa," Schuster said.

Given sufficient funding, he said he plans to further study the Khoisan hunter-gatherers. "The original interest in this people is that they are probably one of the few left in the world that have a hunter-gatherer lifestyle," he said. "I believe that it is absolutely essential that we do whatever we can to learn about this really archaic population within the modern human population, which allows you to get at least some insight of what life was like 8,000 years ago," prior to the agricultural revolution.