Africa's Neanderthals

Skull from Zambia, dated to 110,000 years ago. Modern humans co-existed with archaic groups in Africa, particularly in the south and west.

When and where did modern humans emerge? Anatomical evidence points to somewhere in eastern Africa some 300,000 years ago. The time of origin is different if we look at behavioral and genetic evidence. Sophisticated tool-making, detailed artwork, and other signs of “behavioral modernity” appeared only 70,000 years ago (Brown et al., 2012). Genetic evidence points to a series of demographic expansions between 80,000 and 60,000 years ago in eastern Africa, with the last one spreading throughout Africa and into Eurasia (Watson et al. 1997). At that moment, an innovation in thinking seems to have given these truly modern humans an edge over everyone else.

As these humans spread throughout the world, to what extent did they intermix with the more archaic groups they replaced? We can answer this question for Eurasia by comparing the modern human genome with reconstructed genomes of the now-extinct Neanderthals (Europe, Middle East, and Central Asia) and Denisovans (East Asia, Southeast Asia). Present-day Eurasians have relatively low levels of archaic admixture: about 2% from Neanderthals and up to 5% from Denisovans (Sankararaman et al. 2016).

What about Africa? Unfortunately, we have not yet reconstructed the genome of any archaic population from that continent. We probably never will, given that DNA tends to degrade quickly in tropical climates. In theory, there should be more admixture in Africa than in Eurasia, since many archaic Africans would have been "near-modern," i.e., much more similar in appearance, behavior, and genetic makeup to modern humans than either Neanderthals or Denisovans. Greater genetic similarity would have also made hybrid infertility less likely. Indeed, it looks like male fertility suffered from hybridization with Neanderthals or Denisovans, given that present-day humans have a lower proportion of archaic ancestry on the X chromosome and in genes disproportionately expressed in the testes (Sankararaman et al. 2016). In these parts of the genome, natural selection has stepped in to remove archaic admixture.

The above speculations seem borne out by a recent and still unpublished paper. Its authors, Sriram Sankararaman and Arun Durvasula, came up with a novel way to measure admixture from an unknown archaic group, essentially by using a machine learning algorithm (which they validated with data on Neanderthal introgression in present-day Europeans). When they applied this method to Yoruba from Nigeria, they found a level of archaic admixture higher than in any other human population known to date:

Our results suggest that Yoruban individuals trace about 7.9% of their genomes to an as yet unidentified archaic population. This is in agreement with some results from previous papers in other African populations such as the Biaka and the Baka, suggesting that there was a rich diversity of hominin species within Africa and that introgression was commonplace. (Sankararaman and Durvasula 2018)

This finding is consistent with previous archaeological and genetic evidence, particularly from western and southern Africa. Both regions seem to have had archaic populations until recent times:

- A skull from a Nigerian site (Iwo Eleru) is only about 16,300 years old and yet looks intermediate in shape between modern humans on the one hand and Neanderthals and Homo erectus on the other. It resembles the skull of a near-modern human, like the Skhul-Qafzeh hominins who lived in the Middle East some 80,000 to 100,000 years ago (Harvati et al., 2011; Stojanowski, 2014).

- Genomic analysis of 16 prehistoric Africans suggests that modern humans spread out of eastern Africa and into western Africa, where they mixed with an archaic population as divergent from modern humans as Neanderthals were, the time of separation from modern humans being 200,000 to 300,000 years ago. This archaic admixture is estimated at 9% in Yoruba and 13% in Mende (Skoglund et al. 2017)

- Genomic analysis shows an apparently higher level of Neanderthal ancestry in the Yoruba of Nigeria than in the Luhya of Kenya. This admixture seems to come from a Neanderthal-like population that formerly lived in West Africa (Hawks 2012)

- A skull from Zambia has been dated to 110,000 years ago and yet looks very much like a Homo erectus (Bada et al., 1974; Stringer, 2011). 

-  About 2% of the current African gene pool comes from a population that split from ancestral modern humans some 700,000 years ago. This archaic DNA was then picked up by modern African humans about 35,000 years ago, probably in central Africa because this admixture is highest in pygmy groups from that region (Hammer et al. 2011).

- Genomic analysis of western African pygmies (Biaka and Baka) indicates frequent, low-level interbreeding between archaic and modern humans, including an admixture event within the last 30,000 years (Hsieh et al. 2016). 

- Jawbone fragments from South Africa exhibits significant size and morphological variability, indicating admixture with an archaic population. The fragments fall within the range of 110,000 to 60,000 years ago (Malekfar, 2012)

- Sub-Saharan Africans exhibit dental traits that distinguish them from other modern humans (Sub-Saharan African Dental Complex). These traits are shared with extinct hominids and many extinct and extant nonhuman primates (Irish 1998). When dentitions are compared from western, central, eastern, and southern Africans, these ancestral traits appear to be least present in Kenyans and Tanzanians (Irish 1998). The SSADC thus seems least present in the "homeland" of modern humans (eastern Africa) and more present farther west and south.

Is the estimate of 7.9% archaic admixture a lower bound?

While the new finding of 7.9% archaic admixture is higher than what we see in other modern humans, the actual figure may be higher still. Sankararaman and Durvasula attribute this 7.9% admixture to "a deeply-diverged archaic population," while nonetheless acknowledging the "rich diversity of hominin species within Africa." Dienekes (2018) likewise notes that multiple admixture events had occurred between modern African humans and a range of "Palaeoafrican" groups.

Thus, Sankararaman and Durvasula are measuring admixture only from a highly divergent archaic group, apparently the same one that Skoglund et al. (2017) found in their study of the Yoruba. Indeed, the two studies found almost the same level of archaic admixture in the Yoruba: 7.9% versus 9%. Although Sankararaman and Durvasula validated their methodology with data on Neanderthal admixture in Europe, the two situations are not really comparable. In Europe, modern humans encountered only one archaic group over a relatively short time span, intermixture taking place essentially between 60,000 and 50,000 years ago with a second event more than 37,000 years ago (Yang and Fu 2018).  In Africa, modern humans likely encountered a range of archaic groups over a longer time, including "near-moderns" whose ancestors diverged from those of modern humans less than 200,000 years ago.

If we include introgression from these “near-moderns,” the total for archaic admixture in present-day sub-Saharan Africans should be much higher.  Indeed, 13% of the sub-Saharan gene pool seems to come from a demographic expansion that took place some 111,000 years ago and which probably brought the Skhul-Qafzeh hominins to the Middle East (Watson et al. 1997). Those hominins were anatomically modern, or almost so, but culturally Neanderthal.

Did archaic admixture help or hinder?

Mainstream evolutionary theorists have argued that admixture does more harm than good. As Ernst Mayr (1970, p. 80) wrote:

The claim has been made that species owe much of their genetic variability to introgressive hybridization. However, all the evidence contradicts this conclusion so far as animals is concerned. Not only are F1 hybrids between good species very rare, but where they occur the hybrids (even when not sterile) are demonstrably of inferior viability. The few genes that occasionally introgress into the parental species are not coadapted [...] and are selected against. Introgressive hybridization seems to be a negligible source of genetic variation in animals.

This view has been challenged by Hawks et al. (2007), who argue that gene introgression helped modern humans adapt to new environments. Instead of starting from scratch, they could cherry-pick genes that had already been tried and proven by the populations they were replacing: 

Compared with novel mutations, archaic genetic variants would have had several qualities that, in some cases, may have enhanced their selective value. Because they had long existed within human populations, these alleles had a much lower chance of being strongly deleterious. [...] Alleles with local advantages might never have been selected within the expanding modern population until it reached new climatic regimens. The spread of modern humans may have attained a burst of evolutionary change by drawing on the fruits of the existing adaptations of archaic humans. (Hawks et al. 2007)

The latest findings seem to lie between the above two views. Introgression can in some cases provide useful genes. Usually, however, it’s maladaptive.

We observe a decrease in the frequency of archaic ancestry in the Yoruban populations in more constrained regions of the genome, suggesting that these archaic alleles have been subject to the effects of purifying selection similar to the deleterious consequences of Neanderthal and Denisovan alleles in the modern human genetic background. On the other hand, we find several loci that harbor archaic haplotypes at elevated frequencies (>60%). (Sankararaman and Durvasula 2018)

Similarly, Yang and Fu (2018) note that a "gradual decline in archaic ancestry in Europeans dating from ~37 to 14 ka suggests that purifying selection lowered the amount of Neanderthal ancestry first introduced into ancient modern humans."

This pattern is consistent with findings from nonhuman species. A study of admixture in trout found sharp declines in fitness even with 20% admixture. The decline has two causes:

Hybridization can reduce fitness by either introducing alleles to a population that are not suited to the local environment (extrinsic outbreeding depression) or disrupting co-adapted gene complexes (intrinsic outbreeding depression) (Templeton 1986). These mechanisms are not mutually exclusive, and identifying the contribution of each effect is difficult. However, the high reproductive success of F1 hybrids relative to post-F1 hybrids with similar amounts of admixture suggests that some of the outbreeding depression is intrinsic. (Muhlfeld et al. 2009)

By disrupting co-adapted gene complexes, introgression causes individual genes to lose their adaptive value. Selection will thus eliminate either the introgressed alleles or the previously existing ones. In the second scenario, the complex of co-adapted genes is replaced with a simpler version.

Conclusion

Something “clicked” in eastern Africa 80,000 to 60,000 years ago. A relatively small group of humans acquired a new way of imagining themselves, each other, and the world around them, and this innovation gave them an edge over everyone else. The result: a “big bang” of population growth. They began to spread outward, first within Africa and then into Eurasia.

Their expansion within Africa seems to have proceeded more slowly than in Eurasia. Initially, these modern humans were replacing “near-moderns”—people fairly similar in appearance and genetic makeup. As they pushed farther east and south, however, they encountered populations that were much less similar. West Africa seems to have been home to a people who were as different from modern humans as Neanderthals were, perhaps being related to them. In southern Africa, modern humans encountered people even more divergent: a relic Homo erectus population. Even these highly divergent archaic groups were not rapidly replaced; they may have persisted as late as 15,000 years ago in West Africa and 30,000 years ago in central Africa. Thus, modern and archaic groups seem to have long coexisted in parts of Africa.

In general, archaic admixture reduced fitness: “archaic alleles that introgressed into the Yoruban population were deleterious on average”; neutral alleles were more likely to be retained than those that had functional impacts (Sankararaman and Durvasula 2018). A few, however, seem to have been favored by selection. This is the case with alleles located at a tumor suppressor gene, a gene involved with hormone regulation, and a gene involved with potassium channels. These are individual genes, however, and it is hard to know the impact on co-adapted gene complexes. In theory, archaic admixture should have had a disruptive effect.

Present-day Africans thus have admixture from a range of archaic groups, some being similar to modern humans and others more like Neanderthals or even Homo erectus. This admixture is highest in western and southern Africa and lowest in eastern Africa. In West Africa, admixture from a Neanderthal-like group is estimated at 7.9% by Sankararaman and Durvasula (2018) and at 9 to 13% by Skoglund et al. (2017). Admixture from “near-moderns” is harder to measure. There seems to be a 13% pan-African admixture from a population that had expanded across much of the continent some 111,000 years ago and which perhaps spilled into the Middle East, giving rise to the Skhul-Qafzeh hominins, i.e., early modern humans with Neanderthal culture (Watson et al. 1997, see L1i in Table 2).

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