The Genetic Legacy of Introgression from Two Deeply Divergent Lineages in the Genus Homo

Ancient DNA has shown that a distantly-related “superarchaic” population interbred first with the ancestors of Neanderthals and Denisovans and later with Denisovans themselves. Other work has shown that a superarchaic population interbred with the African ancestors of all modern humans. But it is not yet clear whether these events involved the same superarchaic population. Here, we use the distribution of derived alleles among populations to evaluate hypotheses about superarchaics and their relationship to other hominins of the Pleistocene and Holocene. We find evidence for at least two distinct superarchaic populations. The one contributing to archaic Eurasian populations (Denisovans and Neanderthal-Denisovan ancestors) diverged earlier from the human lineage than did the one contributing to early moderns in Africa. This latter superarchaic contributed a large fraction—about 20%—to the ancestry of modern humans. These findings reveal previously unrecognized structure among hominin populations in the Pleistocene. Significance statement Genetic data have shown that all human populations are mixtures. Since the last ice age, the populations mixing have been relatively close relatives—separated by a few tens of thousands of years or less. Earlier in the Pleistocene, there was mixing between more distantly-related populations, with separation times in excess of a million years. Here, we document admixture events involving two distinct populations, each of which had separated from the human lineage well over a million years ago. One of these was apparently Eurasian, because it mixed with archaic Eurasian populations. The other was apparently African, because it mixed with the African ancestors of modern humans. This latter event was remarkable, because the distant relative contributed such a large fraction—about 20%—to the ancestry of modern humans. These results show that during the Pleistocene, the earth was home to hominin populations far more distantly related than any pair of modern human populations, with separation times similar to that of bonobos and chimpanzees. These distantly-related pairs existed not only on separate continents, but also within the African continent. And in spite of the large differences between them, these populations were able to interbreed.