Population Genomics of Stone Age Eurasia

Abstract

SummarySeveral major migrations and population turnover events during the later Stone Age (after c. 11,000 cal. BP) are believed to have shaped the contemporary population genetic diversity in Eurasia. While the genetic impacts of these migrations have been investigated on regional scales, a detailed understanding of their spatiotemporal dynamics both within and between major geographic regions across Northern Eurasia remains largely elusive. Here, we present the largest shotgun-sequenced genomic dataset from the Stone Age to date, representing 317 primarily Mesolithic and Neolithic individuals from across Eurasia, with associated radiocarbon dates, stable isotope data, and pollen records. Using recent advances, we imputed >1,600 ancient genomes to obtain accurate diploid genotypes, enabling previously unachievable fine-grained population structure inferences. We show that 1) Eurasian Mesolitic hunter-gatherers were more genetically diverse than previously known, and deeply divergent between the west and the east; 2) Hitherto genetically undescribed hunter-gatherers from the Middle Don region contributed significant ancestry to the later Yamnaya steppe pastoralists; 3) The genetic impact of the transition from Mesolithic hunter-gatherers to Neolithic farmers was highly distinct, east and west of a “Great Divide” boundary zone extending from the Black Sea to the Baltic, with large-scale shifts in genetic ancestry to the west. This include an almost complete replacement of hunter-gatherers in Denmark, but no substantial shifts during the same period further to the east; 4) Within-group relatedness changes substantially during the Neolithic transition in the west, where clusters of Neolithic farmer-associated individuals show overall reduced relatedness, while genetic relatedness remains high until ~4,000 BP in the east, consistent with a much longer persistence of smaller localised hunter-gatherer groups; 5) A fast-paced second major genetic transformation beginning around 5,000 BP, with Steppe-related ancestry reaching most parts of Europe within a 1,000 years span. Local Neolithic farmers admixed with incoming pastoralists in most parts of Europe, whereas Scandinavia experienced another near-complete population replacement, with similar dramatic turnover-patterns also evident in western Siberia; 6) Extensive regional differences in the ancestry components related to these early events remain visible to this day, even within countries (research conducted using the UK Biobank resource). Neolithic farmer ancestry is highest in southern and eastern England while Steppe-related ancestry is highest in the Celtic populations of Scotland, Wales, and Cornwall. Overall, our findings show that although the Stone-Age migrations have been important in shaping contemporary genetic diversity in Eurasia, their dynamics and impact were geographically highly heterogeneous.