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. 2012;8(10):e1002947.
doi: 10.1371/journal.pgen.1002947. Epub 2012 Oct 4.

The date of interbreeding between Neandertals and modern humans

Sriram Sankararaman  1 , Nick Patterson, Heng Li, Svante Pääbo, David Reich
Affiliations

The date of interbreeding between Neandertals and modern humans

Sriram Sankararaman et al. PLoS Genet. 2012.

Abstract

Comparisons of DNA sequences between Neandertals and present-day humans have shown that Neandertals share more genetic variants with non-Africans than with Africans. This could be due to interbreeding between Neandertals and modern humans when the two groups met subsequent to the emergence of modern humans outside Africa. However, it could also be due to population structure that antedates the origin of Neandertal ancestors in Africa. We measure the extent of linkage disequilibrium (LD) in the genomes of present-day Europeans and find that the last gene flow from Neandertals (or their relatives) into Europeans likely occurred 37,000-86,000 years before the present (BP), and most likely 47,000-65,000 years ago. This supports the recent interbreeding hypothesis and suggests that interbreeding may have occurred when modern humans carrying Upper Paleolithic technologies encountered Neandertals as they expanded out of Africa.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Linkage disequilibrium patterns expected due to recent gene flow and ancient structure.
(A) In the case of recent gene flow from Neandertals (NEA) into the ancestors of non-Africans (CEU) but not into the ancestors of Africans (YRI), we expect long range LD at sites where Neandertal has the derived allele, and this expectation of admixture generated LD is verified by computer simulation as shown in the right of the panel along with a fitted exponential decay curve. (B) In the case of ancient structure, we expect short range LD, reflecting the time since Neandertals and non-Africans derived from a shared ancestral population, and this expectation is also verified by simulation.
Figure 2
Figure 2. Classes of demographic models relating Africans (Y), Europeans (E), and Neandertals (N).
a) Recent gene flow but no ancient structure. RGF I has no bottleneck in E. RGF II has a bottleneck in E after gene flow while RGF VI has a bottleneck in E before the gene flow. RGF IV and V have constant population sizes of Ne = 5000 and Ne = 50000 respectively. b) Ancient structure but no recent gene flow. AS I has a constant population size while AS II has a recent bottleneck in E. c) Neither ancient structure nor recent gene flow. NGF I has a constant population size while NGF II has a recent bottleneck in E. d),e) Ancient structure+Recent gene flow. HM IV consists of continuous migration in the Y-E ancestor and the Y-E-N ancestor while HM I consists of continuous migration only in the Y-E ancestor. HM II consist of a single admixture event in the ancestor of E while HM III also models a small population size in one of the admixing populations.
Figure 3
Figure 3. Decay of LD for SNPs with minor allele frequency <10%.
(A, B) Real data for European Americans and East Asians shows longer range LD when the Neandertal genome has the derived allele (left) than when it has the ancestral allele (right). This is as expected due to gene flow from Neandertal, but is not expected in the absence of gene flow. In other words, the fact that LD conditional on Neandertals having the derived allele is longer than LD when Neandertal does not strongly suggests that the pattern we are observing among ascertained SNPs is reflecting the complex historical relationship between non-African modern humans and Neandertals, the signal we care about here, and not demographic events that solely involve the ancestors of non-Africans. The scale of the LD decay (1/e drop of the fitted exponential curve) is shown in the top right of each panel based on the deCODE genetic distance. (In Figure S8 of Text S1, we show that this signal persists when stratified into narrow allele frequency bins.) (C) In West Africans the pattern is qualitatively different such that when Neandertal is derived at both SNPs, LD decays more quickly than when Neandertal is ancestral at both SNPs, as expected in the absence of gene flow (without gene flow, the derived allele is always expected to be older so LD is expected to have had more time to break down).
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