Model-based analyses of whole-genome data reveal a complex evolutionary history involving archaic introgression in Central African Pygmies

Abstract

Comparisons of whole-genome sequences from ancient and contemporary samples have pointed to several instances of archaic admixture through interbreeding between the ancestors of modern non-Africans and now extinct hominids such as Neanderthals and Denisovans. One implication of these findings is that some adaptive features in contemporary humans may have entered the population via gene flow with archaic forms in Eurasia. Within Africa, fossil evidence suggests that anatomically modern humans (AMH) and various archaic forms coexisted for much of the last 200,000 yr; however, the absence of ancient DNA in Africa has limited our ability to make a direct comparison between archaic and modern human genomes. Here, we use statistical inference based on high coverage whole-genome data (greater than 60×) from contemporary African Pygmy hunter-gatherers as an alternative means to study the evolutionary history of the genus Homo. Using whole-genome simulations that consider demographic histories that include both isolation and gene flow with neighboring farming populations, our inference method rejects the hypothesis that the ancestors of AMH were genetically isolated in Africa, thus providing model-based whole genome-level evidence of African archaic admixture. Our inferences also suggest a complex human evolutionary history in Africa, which involves at least a single admixture event from an unknown archaic population into the ancestors of AMH, likely within the last 30,000 yr.

The origin and evolution ofHomo sapiens

“…H. heidelbergensis or H. rhodesiensis) into at least the later middle Pleistocene of Europe and Africa [8,25]. In addition, recent evidence of late Pleistocene episodes of introgression between different human lineages in Eurasia [30] and perhaps also in Africa [31] shows us that comparable genetic exchanges could also have been occurring in the middle Pleistocene.…”

Evolutionary and Medical Consequences of Archaic Introgression into Modern Human Genomes

“…Furthermore, there is growing evidence that archaic introgression occurred also within Africa (Labuda et al, 2000;Hammer et al, 2011;Lachance et al, 2012;Hsieh et al, 2016;Xu et al, 2017;Zanolli et al, 2017), raising the exciting possibility that other unknown archaic groups may have contributed to human genetic diversity. Therefore, recent work suggests that apparently distinct species can exchange the genetic material along their evolutionary history (Mallet et al, 2016).…”

“…Figure 1. Family tree of the four groups of early humans living in Eurasia 50,000 years ago and the inferred gene flow between the groups due to interbreeding (based on Prüfer et al, 2014;Mondal et al, 2016;Hsieh et al, 2016; Medina-Gomez et al, 2017). The direction and estimated magnitude of inferred gene flow events are shown.…”

Something old, something borrowed: Admixture and adaptation in human evolution

“…The increasing availability of ancient and present-day human genomes from Africa will also make it easier to study admixture patterns between modern African populations [71] , or between present-day and archaic human groups in Africa [72][73][74] (Figure 1). As the bulk of human evolution happened in this continent, it will not be surprising to find cases of introgression -and adaptive introgression -between different African human groups, once ancient DNA from Africa becomes more readily available.…”

“…For example, there is some evidence to suggest that the lactase persistence allele located in a regulatory region of the LCT gene -one of the best-known examples of positive selection in humans [68,69] -was perhaps introduced into Western Eurasia via eastward migrations by steppe hereder populations [65,70] . However, the evidence for this hypothesis is still scant, and more ancient sequences will be needed to determine with certainty exactly how this occurred, if it occurred at all [68] .The increasing availability of ancient and present-day human genomes from Africa will also make it easier to study admixture patterns between modern African populations [71] , or between present-day and archaic human groups in Africa [72][73][74] (Figure 1). As the bulk of human evolution happened in this continent, it will not be surprising to find cases of introgression -and adaptive introgression -between different African human groups, once ancient DNA from Africa becomes more readily available.…”