Genetic and climatic factors in the dispersal of Anatomically Modern Humans Out of Africa

Abstract

The evolutionarily recent dispersal of Anatomically Modern Humans (AMH) out of Africa and across Eurasia provides an opportunity to study rapid genetic adaptation to multiple new environments. Genomic analyses of modern human populations have detected limited signals of strong selection such as hard sweeps1, but genetic admixture between populations2,3 is capable of obscuring these patterns and is well known in recent human history, such as during the Bronze Age 4. Here we show that ancient human genomic datasets contain multiple genetic signatures of strong selection including 57 hard sweeps, many with strong associations with cold adaptation. Similar genetic signatures of adaptation are also observed in adaptively-introgressed archaic hominin loci, as well as modern Arctic human groups. Consistent targets include the regulation of fat storage, skin physiology, cilia function and neural development; with multiple associations to modern western diseases. The spatiotemporal patterns of the hard sweeps allow reconstruction of early AMH population dispersals, and reveal a prolonged period of genetic adaptation (~80-50,000 years) following their initial out of Africa movement, before a rapid spread across Eurasia reaching as far as Australia. 2 When Anatomically Modern Human populations moved Out of Africa (OoA) they encountered a range of environments that were markedly different from their African past. Despite this, modern human populations show few classical genetic signatures of strong selection such as hard sweeps, where new or rare beneficial alleles have been driven to high-frequency by selection. This has led to the suggestion that most recent human genetic adaptation may have instead involved alternate modes of selection that leave less pronounced signatures in genomes5,6 (e.g. ‘soft’ sweeps and polygenic selection; Supplementary Information 1). To examine whether recent population admixture may have obscured signatures of past genetic adaptation we constructed a dataset containing genomic information and curated metadata from 1,162 ancient western Eurasian genome datasets including both low-coverage genomes and high-density Single Nucleotide Polymorphism (SNP) scans7, which are concentrated mostly in western Eurasia between the early Holocene (~12ka) and Bronze Age 8 (Fig. 1, Extended Data Figs. 1, 2, Extended Data Table 1). We were able to group 18 distinct ancient populations based on their archaeological and genetic relationships. …