Genetic evidence for archaic admixture in Africa

Abstract

A long-debated question concerns the fate of archaic forms of the genus Homo: did they go extinct without interbreeding with anatomically modern humans, or are their genes present in contemporary populations? This question is typically focused on the genetic contribution of archaic forms outside of Africa. Here we use DNA sequence data gathered from 61 noncoding autosomal regions in a sample of three sub-Saharan African populations (Mandenka, Biaka, and San) to test models of African archaic admixture. We use two complementary approximate-likelihood approaches and a model of human evolution that involves recent population structure, with and without gene flow from an archaic population. Extensive simulation results reject the null model of no admixture and allow us to infer that contemporary African populations contain a small proportion of genetic material (≈ 2%) that introgressed ≈ 35 kya from an archaic population that split from the ancestors of anatomically modern humans ≈ 700 kya. Three candidate regions showing deep haplotype divergence, unusual patterns of linkage disequilibrium, and small basal clade size are identified and the distributions of introgressive haplotypes surveyed in a sample of populations from across sub-Saharan Africa. One candidate locus with an unusual segment of DNA that extends for >31 kb on chromosome 4 seems to have introgressed into modern Africans from a now-extinct taxon that may have lived in central Africa. Taken together our results suggest that polymorphisms present in extant populations introgressed via relatively recent interbreeding with hominin forms that diverged from the ancestors of modern humans in the Lower-Middle Pleistocene.

Fig. 1.

Schematic of the (A) two-population model and the (B) three-population model. Both demographic models test the fit of admixture with an archaic group (dotted lines) who split from the ancestors of modern humans at time T₀ and a (%) of alleles introgressed into the modern gene pool at time T_a. The dashed lines represent all possible locations where admixture could occur. Both models begin with a single population of size N_a, followed by a population split at time T₁, with population growth beginning at times g₁ and g₂, and a constant symmetric migration rate M. For B, an additional population split at time T₂ also occurs. This model also assumes that the ancestors of the San split first from those of the Mandenka and Biaka (22).

Fig. 2.

Approximate likelihood profile based on 60 loci for time of introgression and archaic split time. A log-likelihood difference of 3.92 defines the 95% confidence region (using the χ² approximation). Likelihood estimates at each locus have at least 10 ARGs for both ψ_old and ψ_recent.

Fig. 3.

(A) Schematic of the original (filled bars) and extended sequence data (open bars) for the 4qMB179 locus. The unusual Biaka haplotype extends for ≈31.4 kb between the vertical dotted lines. (B) Recombinational landscape as inferred from HapMap Phase I data.

Fig. 4.

Frequency of introgressive variants within three sequenced regions in an expanded sample of ≈500 sub-Saharan Africans (SI Materials and Methods). The filled bar represents the frequency of a variant marking the divergent haplotype at 4qMB179 (Left), 18qMB60 (Center), and 13qMB179 (Right) in each of 14 population samples. Each horizontal line on the bar charts represents a frequency of 5%.