Past human expansions shaped the spatial pattern of Neanderthal ancestry

Abstract

The worldwide expansion of modern humans (Homo sapiens) from Africa started before the extinction of Neanderthals (Homo neanderthalensis). Both species coexisted and interbred, as revealed by the sequencing of Neanderthal genomes, leading to ~2% Neanderthal DNA in modern Eurasians, with slightly higher introgression in East Asians than in Europeans. These distinct levels of ancestry have been argued to result from selection processes. However, recent theoretical simulations have shown that range expansions could be another explanation. This hypothesis would lead to the generation of spatial gradients of introgression, increasing with the distance from the source of the expansion, i.e., Africa for modern humans. Here, we investigate the presence of Neanderthal introgression gradients after past human expansions by analysing an extended palaeogenomic dataset of Eurasian populations. Our results show that the Out-of-Africa expansion of modern humans into Eurasia resulted in spatial gradients of Neanderthal ancestry that persisted through time. Moreover, while keeping the same gradient orientation, the expansion of early Neolithic farmers into western Eurasia contributed decisively to reducing the average level of Neandertal genomic introgression in European compared to Asian populations. This is because Neolithic farmers carried less Neanderthal DNA than preceding Palaeolithic hunter-gatherers. This study shows that inferences about past population dynamics within our species can be made from the spatiotemporal variation in archaic introgression.

Temporal variation in introgressed segments’ length statistics sheds light on past admixture pulses

“…It is only during the inter-pulse period that SP and MP model could be differentiated from one another, suggesting that any temporal sampling failing to capture genomes from within this period would miss the signature of multiple admixture events. While PI is a widely used summary statistics in hybridization studies 12,32,[38][39][40] , this finding highlights the challenges associated with using PI to differentiate admixture pulses and supports the use of alternative statistics when trying to reconstruct inter-lineage hybridization history. For instance, many studies have investigated the admixture history between Homo sapiens and archaic hominins 19,22,35,41 , yet summary statistics like FFS (Fragment Frequency Spectrum), SFS (Site Frequency Spectrum), D-statistic, or segments of archaic origin inferred using a HMM (Hidden Markov Model) have been preferred over PI (but see 37 ).…”

“…Future work incorporating natural selection into the simulation framework may be performed to evaluate its impact on temporal patterns of length summary statistics. In addition, we did not incorporate gene flow with other populations into our simulations, which could impact the proportion of introgressed segments in the sink population 40,55 . Finally, while introgression and admixed segments' lengths vary temporally, they also vary spatially 38,56,57 .…”