Population Genomics of Bronze Age Eurasia

The archaeological record testifies to major cultural changes in Europe and Asia after the Neolithic period. By 3000 BC, the Neolithic farming cultures in temperate Eastern Europe appear to have been largely replaced by the Early Bronze Age Yamnaya culture, which rapidly stretched from Hungary to the Urals, and is associated with a completely new perception of family, property and personhood. By 2800 BC a new social and economic formation, variously named Corded Ware, Single Grave or Battle Axe cultures developed in temperate Europe, possibly deriving from a Yamnaya background, and culturally replacing the remaining Neolithic farmers. In Western and Central Asia, hunter-gatherers still dominated in the Early Bronze Age, except in the Altai Mountains and Minusinsk Basin where the Afanasievo culture existed with a close cultural affinity to Yamnaya. From the beginning of 2000 BC, a new class of master artisans, known as the Sintashta culture, emerged in the Urals, building chariots, breeding and training horses, and producing sophisticated new weapons. These innovations quickly spread across Europe and into Asia where they appeared to give rise to the Andronovo culture. In the Late Bronze Age around 1500 BC, the Andronovo culture was gradually replaced by the Mezhovskaya, Karasuk, and Koryakova cultures. It remains debated if these major cultural shifts during the Bronze Age in Europe and Asia resulted from the migration of people or through cultural diffusion among settled groups, and if the spread of the Indo-European languages was linked to these events or predates them.


Genomes obtained from ancient biological remains can provide information on past population histories that is not retrievable from contemporary individuals. However, ancient genomic studies have so far been restricted to single or a few individuals because of the degraded nature of ancient DNA, making sequencing costly and time consuming. To overcome this, we increased the average output of authentic endogenous DNA fourfold by: (1) targeting the outer cementum layer in teeth rather than the inner dentine layer, (2) adding a ‘pre-digestion’ step to remove surface contaminants, and (3) developing a new binding buffer for ancient DNA extraction. This allowed us to obtain low-coverage genome sequences (0.01–7.4× average depth, overall average equal to 0.7×) of 101 Eurasian individuals spanning the entire Bronze Age, including some Late Neolithic and Iron Age individuals. Our data set includes 19 genomes, between 1.1–7.4× average depth, thereby doubling the number of existing Eurasian ancient genomes above 1× coverage.

By analysing our genomic data in relation to previously published ancient and modern data, we find evidence for a genetically structured Europe during the Bronze Age. Populations in northern and central Europe were composed of a mixture of the earlier huntergatherer and Neolithic farmer groups, but received ‘Caucasian’ genetic input at the onset of the Bronze Age. This coincides with the archaeologically well-defined expansion of the Yamnaya culture from the Pontic-Caspian steppe into Europe. This admixture event resulted in the formation of peoples of the Corded Ware and related cultures. Although European Late Neolithic and Bronze Age culturessuch as Corded Ware, Bell Beakers, Unetice, and the Scandinavian cultures are genetically very similar to each other, they still display a cline of genetic affinity with Yamnaya, with highest levels in Corded Ware, lowest in Hungary, and central European Bell Beakers being intermediate. We find that Corded Ware and Yamnaya individuals form a clade to the exclusion of Bronze Age Armenians showing that the genetic ‘Caucasus component’ present in Bronze Age Europe has a steppe origin rather than a southern Caucasus origin. Earlier studies have shown that southern Europeans received substantial gene flow from Neolithic farmers during the Neolithic. Despite being slightly later, we find that the Copper Age Remedello culture in Italy does not have the ‘Caucasian’ genetic component and is still clustering genetically with Neolithic. Hence this region was either unaffected by the Yamnaya expansion, or the Remedello pre-dates such an expansion into southern Europe. The ‘Caucasian’ component is clearly present during the Late Bronze Age in Montenegro. The close affinity we observe between peoples of Corded Ware and Sintashta cultures suggests similar genetic sources of the two, which contrasts with previous hypotheses placing the origin of Sintashta in Asia or the Middle East. Although we cannot formally test whether the Sintashta derives directly from an eastward migration of Corded Ware peoples or if they share common ancestry with an earlier steppe population, the presence of European Neolithic farmer ancestry in both the Corded Ware and the Sintashta, combined with the absence of Neolithic farmer ancestry in the earlier Yamnaya, would suggest the former being more probable.

We find that the Bronze Age in Asia is equally dynamic and characterized by large-scale migrations and population replacements. The Early Bronze Age Afanasievo culture in the Altai-Sayan region is genetically indistinguishable from Yamnaya, confirming an eastward expansion across the steppe, in addition to the westward expansion into Europe. Thus, the Yamnaya migrations resulted in gene flow across vast distances, essentially connecting Altai in Siberia with Scandinavia in the Early Bronze Age. The Andronovo culture, which arose in Central Asia during the later Bronze Age, is genetically closely related to the Sintashta peoples, and clearly distinct from both Yamnaya and Afanasievo. Therefore, Andronovo represents a temporal and geographical extension of the Sintashta gene pool. Towards the end of the Bronze Age in Asia, Andronovo was replaced by the Karasuk, Mezhovskaya, and Iron Age cultures which appear multi-ethnic and show gradual admixture with East Asians, corresponding with anthropological and biological research. However, Iron Age individuals from Central Asia still show higher levels of West Eurasian ancestry than contemporary populations from the same region. Intriguingly, individuals of the Bronze Age Okunevo culture from the Sayano- Altai region are related to present-day Native Americans, which confirms previous craniometric studies. This finding implies that Okunevo could represent a remnant population related to the Upper Palaeolithic Mal’ta hunter-gatherer population from Lake Baikal that contributed genetic material to Native Americans.


Historical linguists have argued that the spread of the Indo- European languages must have required migration combined with social or demographic dominance, and this expansion has been supported by archaeologists pointing to striking similarities in the archaeological record across western Eurasia during the third millennium BC. Our genomic evidence for the spread of Yamnaya people from the Pontic-Caspian steppe to both northern Europe and Central Asia during the Early Bronze Age corresponds well with the hypothesized expansion of the Indo-European languages. In contrast to recent genetic findings, however, we only find weak evidence for admixture in Yamnaya, and only when using Bronze Age Armenians and the Upper Palaeolithic Mal’ta as potential source populations. This could be due to the absence of eastern hunter-gatherers as potential source populations for admixture in our data set. Modern Europeans show some genetic links to Mal’ta that has been suggested to form a third European ancestral component (Ancestral North Eurasians (ANE)). Rather than a hypothetical ancient northern Eurasian group, our results reveal that ANE ancestry in Europe probably derives from the spread of the Yamnaya culture that distantly shares ancestry with Mal’ta.

It is clear from our autosomal, mitochondrial DNA and Y chromosome data that the European and Central Asian gene pools towards the end of the Bronze Age mirror present-day Eurasian genetic structure to an extent not seen in the previous periods. Our results imply that much of the basis of the Eurasian genetic landscape of today was formed during the complex patterns of expansions, admixture and replacements during this period. We find that many contemporary Eurasians show lower genetic differentiation (FST ) with local Bronze Age groups than with earlier Mesolithic and Neolithic groups. Notable exceptions are contemporary populations from southern Europe such as Sardinians and Sicilians, which show the lowest FST with Neolithic farmers. In general, the levels of differentiation between ancient groups from different temporal and cultural contexts are greater than those between contemporary Europeans. For example, we find pairwise FST = 0.08 between Mesolithic hunter-gatherers and Bronze Age individuals from Corded Ware, which is nearly as high as FST between contemporary East Asians and Europeans. These resu described. Our results confirm a low frequency of rs4988235 in Europeans, with a derived allele frequency of 5% in the combined Bronze Age Europeans (genotype probability >0.85). Among Bronze Age Europeans, the highest tolerance frequency was found in Corded Ware and the closely-related Scandinavian Bronze Age cultures. Interestingly, the Bronze Age steppe cultures showed the highest derived allele frequency among ancient groups, in particular the Yamnaya, indicating a possible steppe origin of lactase tolerance.

It has been debated for decades if the major cultural changes that occurred during the Bronze Age resulted from the circulation of people or ideas and whether the expansion of Indo-European languages was concomitant with these shifts or occurred with the earlier spread of agriculture. Our findings show that these transformations involved migrations, but of a different nature than previously suggested: the Yamnaya/Afanasievo movement was directional into Central Asia and the Altai-Sayan region and probably without much local infiltration, whereas the resulting Corded Ware culture in Europe was the result of admixture with the local Neolithic people. The enigmatic Sintashta culture near the Urals bears genetic resemblance to Corded Ware and was therefore likely to be an eastward migration into Asia. As this culture spread towards Altai it evolved into the Andronovo culture, which was then gradually admixed and replaced by East Asian peoples that appear in the later cultures (Mezhovskaya and Karasuk). Our analyses support that migrations during the Early Bronze Age is a probable scenario for the spread of Indo-European languages, in line with reconstructions based on some archaeological and historical linguistic data. In the light of our results, the existence of the Afanasievo culture near Altai around 3000 BC could also provide anare indicative of significant temporal shifts in the gene pools and also reveal that the ancient groups of Eurasia were genetically more structured than contemporary populations. The diverged ancestral genomic components must then have diffused further after the Bronze Age through population growth, combined with continuing gene flow between populations, to generate the low differentiation observed in contemporary west Eurasians.

The size of our data set allows us to investigate the temporal dynamics of 104 genetic variants associated with important phenotypic traits or putatively undergoing positive selection. Focusing on four well-studied polymorphisms, we find that two single nucleotide polymorphisms (SNPs) associated with light skin pigmentation in Europeans exhibit a rapid increase in allele frequency. For rs1426654, the frequency of the derived allele increases from very low to fixation within a period of approximately 3,000 years between the Mesolithic and Bronze Age in Europe. For rs12913832, a major determinant of blue versus brown eyes in humans, our results indicate the presence of blue eyes already in Mesolithic hunter-gatherers as previously described. We find it at intermediate frequency in Bronze Age Europeans, but it is notably absent from the Pontic-Caspian steppe populations, suggesting a high prevalence of brown eyes in these individuals. The results for rs4988235, which is associated with lactose tolerance, were surprising. Although tolerance is high in present-day northern Europeans, we find it at most at low frequency in the Bronze Age (10% in Bronze Age Europeans), indicating a more recent onset of positive selection than previously estimated. To further investigate its distribution, we imputed all SNPs in a 2 megabase (Mb) region around rs4988235 in all ancient individuals using the 1000 Genomes phase 3 data set as a reference panel, as previously explanation for the mysterious presence of one of the oldest Indo- European languages, Tocharian in the Tarim basin in China. It seems plausible that Afanasievo, with their genetic western (Yamnaya) origin, spoke an Indo-European language and could have introduced this southward to Xinjang and Tarim. Importantly, however, although our results support a correspondence between cultural changes, migrations, and linguistic patterns, we caution that such relationships cannot always be expected but must be demonstrated case by case.
 
Eske Willerslev

Eske Willerslev holds the Prince Philip Chair in Evolution and Ecology at the University of Cambridge. He is also the Lundbeck Foundation Professor at University of Copenhagen and director for the Centre of Excellence in GeoGenetics. Willerslev is an evolutionary geneticist recognized for his studies on human evolution and dispersal, megafaunal extinctions, and environmental DNA. He is particularly known for sequencing the first ancient human genome, conducting the first large-scale ancient population genomic study, and establishing the field of environmental DNA, where modern and ancient DNA from organisms such as higher plants and animals are obtained directly from environmental samples such as sediments, ice and water. After spending his youth as an explorer and fur trapper in Siberia, he established the first ancient DNA laboratory in Denmark and obtained his DSc at University of Copenhagen in 2004. At the age of 33, Willerslev became Full Professor at the University of Copenhagen - the youngest in Denmark at the time. In 2015 he took up the Prince Philip Chair at the University of Cambridge. Willerslev has more than 200 peer-reviewed papers, including 41 papers published in the journals Nature and Science (28 as first or last author). He has communicated his scientific work to the public through multiple films, popular books and interviews.

( Eske Willerslev     University of Copenhagen)