Past human expansions shaped the spatial pattern of Neanderthal ancestry

Abstract

The worldwide expansion of modern humans (Homo sapiens) started before the extinction of Neanderthals (Homo neanderthalensis). Both species coexisted and interbred, leading to slightly higher introgression in East Asians than in Europeans. This distinct ancestry level has been argued to result from selection, but range expansions of modern humans could provide an alternative explanation. This hypothesis would lead to spatial introgression gradients, increasing with distance from the expansion source. We investigate the presence of Neanderthal introgression gradients after past human expansions by analyzing Eurasian paleogenomes. We show that the out-of-Africa expansion resulted in spatial gradients of Neanderthal ancestry that persisted through time. While keeping the same gradient orientation, the expansion of early Neolithic farmers contributed decisively to reducing the Neanderthal introgression in European populations compared to Asian populations. This is because Neolithic farmers carried less Neanderthal DNA than preceding Paleolithic hunter-gatherers. This study shows that inferences about past human population dynamics can be made from the spatiotemporal variation in archaic introgression.

Fig. 1.. Expected ancestry after range expansion and paleogenomic dataset.

(A) Schematic representation of the expected spatial gradient of introgression from the local taxon into an invasive taxon after a biological invasion with hybridization in the case of a uniform environment where both taxa occur everywhere. (B) Distribution of samples in Eurasia used for elucidating spatial gradients of Neanderthal ancestry in MHs. The colored dots represent paleogenomic samples of hunter-gatherers (HGs; ~40,000 to 6000 years BP, n = 129), early farmers (FAs; ~10,000 to 2000 years BP, n = 679), other ancient (OTs; ~6400 to 300 years BP, n = 1726), and modern (MDs; current time, n = 91). The dotted ellipse represents the presumed geographic source of the Paleolithic OOA expansion into Eurasia (~50,000 years BP), and the dotted circle represents the source of the Neolithic expansion of agricultural populations from the Fertile Crescent (~11,000 years BP). The red triangle represents the longitudinal limit (34°) that, in our study, separates European (n = 1517) from Asian (n = 1108) population samples.

Fig. 2.. Effects of latitude and longitude on the level of Neanderthal ancestry in both Europe and Asia.

(A) Effect of latitude and (B) effect of longitude. The solid and dotted lines represent the estimated values and 95% confidence intervals, respectively. The colored dots represent the distribution of the full dataset of ancient and modern DNA samples used in the Full Eurasia analysis (n = 2625).

Fig. 3.. Influence of latitude and time on the level of Neanderthal ancestry.

(A) Ancestry level in Europe and (B) ancestry level in Asia. The analysis considers the full dataset of ancient and modern DNA samples (Full Eurasia, n = 2625). The y axis corresponds to the range where both regions (Asia and Europe) have the most data.

Fig. 4.. Temporal variation in the level of Neanderthal ancestry in different cultural populations.

HG, hunter-gatherers; FA, Neolithic farmers; OT, other ancient samples. (A) Ancestry level in Europe and (B) ancestry level in Asia. The solid and dotted lines represent the estimated values and 95% confidence intervals, respectively. The colored dots represent the distribution of ancient DNA samples used in the best Ancient Eurasia analysis (n = 2534).

Fig. 5.. Spatial variation on the level of Neanderthal ancestry.

The ancestry levels in European hunter-gatherers and farmers were projected using the best Europe model (n = 1517). The gray dots represent the distribution of DNA samples.