Tales from old bones

Around three thousand years ago Bantu began to spread east and south from the Nigeria/Cameroun border, eventually replacing the original inhabitants of eastern and southern Africa. Those people no longer exist. Only the DNA in their skeletal remains are left to speak for them.

When scientists began to retrieve ancient DNA from human remains, they succeeded only at sites in the temperate and arctic zones. It seemed impossible to retrieve any at tropical sites, apparently because warm year-round temperatures soon reduce DNA to a meaningless molecular jumble.

This problem seems to be solved. Two years ago, DNA was successfully retrieved from 4,500 year old remains in Ethiopia. Now, we have ancient DNA from several sites across eastern and southern Africa over a range of dates from 10,000 to 400 years ago (Skoglund et al. 2017).

Vanished peoples

This new study shows that eastern and southern Africans have changed a lot since the time of the ancient Greeks. As far north as Tanzania, the continent was once home to peoples related to the Hottentots (now called Khoisans, Khoe-Sans, or simply San)—short in stature, gracile in body build, and light yellowish brown in color. From Zanzibar north, people were of mixed Middle Eastern and Cushitic origin—sort of like present-day Ethiopians but with more Arab ancestry.

What happened to these peoples? They were either replaced or absorbed by Bantus moving in from the west, although it now looks like they were replaced a lot more than they were absorbed. No trace of them remains in Malawi's gene pool:

Population replacement by incoming food producers appears to have been nearly complete in Malawi, where we detect little if any ancestry from the ancient individuals who lived ~8,100-2,500 BP. Instead, present-day Malawian individuals are consistent with deriving all their ancestry from the Bantu expansion of ultimate western African origin. (Skoglund et al. 2017)

The original inhabitants were related to present-day Khoisans but had significantly diverged from them:

Notably, the Khoe-San-related ancestry in ancient individuals from Malawi and Tanzania is symmetrically related to the two previously identified lineages present in the San [...], estimated to have diverged at least 20,000 years ago [...], implying that this was an ancient divergent branch of this group that lived in eastern Africa at least until 1,400 BP. (Skoglund et al. 2017)

This is in line with previous DNA findings from the Fwe (a Bantu group of southwestern Zambia), particularly the presence of Khoisan admixture that resembles nothing in present-day Khoisans:

[It is possible] that the Fwe intermarried with a Khoisan group whose genetic composition differed from that of the populations included in molecular anthropological investigations to date. [...] it is plausible that the Fwe ancestors interacted with a Khoisan community that differed genetically from those still settled in southern Africa today, which was ultimately replaced by the newcomers. (Barbieri et al. 2013)

Aside from these scattered fragments of DNA, we also have the testimony of ancient observers. Two tenth-century Arab geographers state that "in the outer reaches of the land of the Zanj there are cool highlands in which live white Zanj" (Lewis 1990, p. 121, n. 3). The Zanj are the dark-skinned peoples of east Africa and the term 'white' is better translated by 'lighter-skinned.' (The words 'black' and 'white' are often used in a relative sense in Arabic). The highlands might be the Drakensberg Escarpment of South Africa. 

Encounters with the archaic Other

Modern humans arose some 80,000 years ago in eastern Africa through a series of population expansions that culminated twenty thousand years later in a big bang that spread outward in Africa and then into the Middle East, Europe, and Asia (Watson et al. 1997). There, they encountered more archaic hominins: Neanderthals and, farther east, Denisovans. There was some intermixture. How much? Some have argued that modern Europeans and Asians are 3.4 to 7.9 percent admixed (Lohse and Frantz 2013). Most still opt for a lower figure of 1.5 to 2.1 percent (Prüfer et al. 2014).

But it wasn't only in Eurasia that modern humans encountered Neanderthal-like groups. Archaic hominins were present in Africa itself, some being relatively close to modern humans, and some more distantly related.

The latest DNA study has confirmed that modern humans intermixed with at least one archaic group as they expanded into western Africa:

The possible basal western African population lineage would represent the earliest known divergence of a modern human lineage that contributed a major proportion of ancestry to present-day humans. Such a lineage must have separated before the divergence of San ancestors, which is estimated to have begun on the order of 200-300 thousand years ago. (Skoglund et al. 2017)

This archaic ancestry is visible in human remains found at the Iwo Eleru rock shelter, in southwestern Nigeria, and dated to approximately 16,300 BP:

Our analysis indicates that Iwo Eleru possesses neurocranial morphology intermediate in shape between archaic hominins (Neanderthals and Homo erectus) and modern humans. This morphology is outside the range of modern human variability in the PCA and CVA analyses, and is most similar to that shown by LPA individuals from Africa and the early anatomically modern specimens from Skhul and Qafzeh. (Harvati et al., 2011)

Archaic ancestry is also visible in present-day West Africans, particularly in their teeth: 

[...] compared to other world populations, Africans south of the Sahara Desert are distinct dentally — especially in their expression of nine high- and two low-frequency morphological features. [...] the same nine high-frequency traits are also ubiquitous in the dentitions of extinct hominids and many extinct and extant non-human primates.  

[...] The presence and, indeed, prevalence (see next section), of high-frequency Sub-Saharan dental traits in fossil and recent hominoids—some of which are probably direct ancestors of modern humans, suggests they have been around for a long time.  

[...] A final ancestral feature found with some regularity in Sub-Saharan Africans, relative to other modern groups, is polydontia. Numerous cases of extra incisors, third premolars, and fourth molars have been noted [...] In one study (Watters, 1962) the incidence reached 2.5-3% in several hundred west Africans; many of the extra teeth were fully formed and erupted. "Typical" mammals exhibit three incisors and four premolars (Jordan et al., 1992). Polydontia is also found in living non-human primates. (Irish, 1998)

How much archaic ancestry do sub-Saharan Africans have today? The latest DNA study is silent on this point. Any answer can only be approximate, there being no reconstructed genome of this Neanderthal-like population. Moreover, there was probably more than one such population within Africa. Watson et al. (1997) attribute 13% of the sub-Saharan gene pool to a population that expanded some 111,000 years ago—when Skhul-Qafzeh hominins entered the Middle East from Africa. Those hominins were anatomically modern, or almost so, but culturally Neanderthal. Hammer et al. (2011) estimate that about 2% of the sub-Saharan African genome comes from a much more divergent population that split off from the ancestors of modern humans some 700,000 years ago. That admixture entered the sub-Saharan gene pool about 35,000 years ago, perhaps in Central Africa, since pygmy groups from that region have the most.

It looks like the proportion of archaic ancestry is higher in sub-Saharan Africans than in other modern humans. This is to be expected because of the broader range of archaic populations in Africa, including some that were almost modern anatomically and behaviorally. Admixture with them would have been likelier.

Admixture: good, bad, or neither?

Some alleles have successfully introgressed from archaic hominins, thus helping our ancestors adapt to new climates and new diets (Racimo et al. 2015). In general, however, we should not expect such alleles to perform as well in the body of a modern human as they did in the body of an archaic hominin. It's like taking a part from a Chevy and installing it on a Subaru. It might work, but I wouldn't count on it. 

If we look at Neanderthal admixture in the Eurasian genome, we see that natural selection has tended to remove functional genes, while leaving the non-functioning ones alone. 

Neanderthal ancestry decreases in proximity to functional elements in all populations [...] as does Denisovan ancestry in Oceanians [...] most likely reflecting greater selection against Neanderthal ancestry in low B statistic regions. Power to detect archaic ancestry is elevated close to regions of linked selection due to a reduction in the rates of incomplete lineage sorting caused by the lower effective population size in these regions, so these results are not artifacts of reduced power. Thus, similar processes appear to have worked to remove Neanderthal and Denisovan ancestry near genes. (Sankararaman et al. 2016)

Archaic admixture is also associated with reduced male fertility:

Our study provides new evidence in support of the hypothesis that reduced male fertility may be a common feature of admixture between human populations diverged by at least a half million years, a hypothesis that was previously suggested based on genetic patterns associated with the hybridization between Neanderthals and modern humans.

[...] One line of evidence for reduced fertility in male hybrids is that the proportion of archaic ancestry in modern humans is significantly reduced on chromosome X compared to the autosomes. This is suggestive of reduced male fertility as loci contributing to this phenotype are concentrated on chromosome X in hybrids of other species. We confirm an extreme reduction of Neanderthal ancestry on chromosome X (16%-34% of the autosomes depending on the population) and find a quantitatively similar reduction of Denisovan ancestry (21% of the autosomes in Oceanians).

The second line of evidence in support of the hypothesis of reduced fertility in hybrids is that there is a reduction of archaic ancestry in genes that are disproportionately expressed in testes, a known characteristic of male hybrid fertility (Sankararaman et al. 2016)

In sum, archaic admixture did provide modern humans with some ready-made alleles that have helped them adapt to new climates and new diets, but this advantage hardly applies to Africa. There, modern humans were already adapted to the local climate and diet. Archaic admixture couldn't have done much to help them adapt, since the new environments they faced were cultural ones of their own making.

References

Barbieri, C., A. Butthof, K. Bostoen, and B. Pakendorf. (2013). Genetic perspectives on the origin of clicks in Bantu languages from southwestern Zambia, European Journal of Human Genetics, 21(4), 430-436.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3598317/  

Hammer, M.F., A.E. Woerner, F.L. Mendez, J.C. Watkins, and J.D. Wall. (2011). Genetic evidence for archaic admixture in Africa, Proceedings of the National Academy of Science (USA), 108(37), 15123-15128, www.pnas.org/cgi/doi/10.1073/pnas.1109300108

Harvati, K., C. Stringer, R. Grün, M. Aubert, P. Allsworth-Jones, C.A. Folorunso. (2011). The Later Stone Age Calvaria from Iwo Eleru, Nigeria: Morphology and Chronology. PLoS ONE 6(9): e24024. doi:10.1371/journal.pone.0024024

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0024024  

Irish, J.D. (1998). Ancestral dental traits in recent Sub-Saharan Africans and the origins of modern humans, Journal of Human Evolution, 34, 81-98.

http://www.sciencedirect.com/science/article/pii/S0047248497901913  

Lohse, K., and L.A.F. Frantz. (2013). Maximum likelihood evidence for Neandertal admixture in Eurasian populations from three genomes, Populations and Evolution, 1307, 8263

http://www.integratedbiology.com/uploads/2/5/6/9/25695765/_1307.8263.pdf  

Prüfer, K., F. Racimo, N. Patterson, F. Jay; et.al. (2014). The complete genome sequence of a Neandertal from the Altai Mountains, Nature, 505(7481), 43-49.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4031459/

Racimo, F., S. Sankararaman, R. Nielsen, and E. Huerta-Sanchez. (2015). Evidence for archaic adaptive introgression in humans, Nature Reviews Genetics, 16(6), 359-371.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4478293/  

Sankararaman, S., S. Mallick, N. Patterson, D, Reich; et al. (2016). The combined landscape of Denisovan and Neanderthal ancestry in present-day humans, Current Biology, 26(9), 1241-1247.

http://www.sciencedirect.com/science/article/pii/S0960982216302470  

Skoglund, P., J.C. Thompson, M.E. Prendergast, A. Mittnik; et al. (2017). Reconstructing prehistoric African population structure, Cell, 171(1), 59-71

http://www.cell.com/cell/fulltext/S0092-8674(17)31008-5  

Watson, E., P. Forster, M. Richards, and H-J. Bandelt. (1997). Mitochondrial footprints of human expansions in Africa, American Journal of Human Genetics, 61, 691-704.

https://ac.els-cdn.com/S000292970764333X/1-s2.0-S000292970764333X-main.pdf?_tid=9bebd320-a127-11e7-9e7c-00000aacb360&acdnat=1506257895_6658dfe089335953bd04987696fa7444