Who were the originating source populations of Bronze Age Eurasians?

Migration movements of Bronze Age populations across Eurasia

Migration movements of Bronze Age populations across Eurasia

A study on autosomal DNA was published based on 101 ancient human samples from different periods of times and cultures from across Eurasia, including two samples from Sintashta culture were used. Leaving aside the question of linguistics, we focus on the migration patterns touched upon in the research paper by Morten E. Allentoft et al., Population genomics of Bronze Age Eurasia (full pdf text hereNature 2015 Jun;522(7555):167-72:

The Bronze Age of Eurasia (around 3000–1000 BC) was a period of major cultural changes. However, there is debate about whether these changes resulted from the circulation of ideas or from human migrations, potentially also facilitating the spread of languages and certain phenotypic traits. We investigated this by using new, improved methods to sequence low-coverage genomes from 101 ancient humans from across Eurasia. We show that the Bronze Age was a highly dynamic period involving large-scale population migrations and replacements, responsible for shaping major parts of present-day demographic structure in both Europe and Asia. Our findings are consistent with the hypothesized spread of Indo-European languages during the Early Bronze Age. We also demonstrate that light skin pigmentation in Europeans was already present at high frequency in the Bronze Age, but not lactose tolerance, indicating a more recent onset of positive selection on lactose tolerance than previously thought….

Bronze Age Europe

Populations in northern and central Europe were composed of a mixture of the earlier hunter-gatherer and Neolithic farmer10 groups, but received ‘Caucasian’ genetic input at the onset of the Bronze Age (Fig. 2). This coincides with the archaeologically well-defined expansion of the Yamnaya culture from the Pontic-Caspian steppe into Europe (Figs 1 and 2). This admixture event resulted in the formation of peoples of the Corded Ware and related cultures, as supported by negative ‘admixture’ f3 statistics when using Yamnaya as a source population (Extended Data Table 2, Supplementary Table 12). Although European Late Neolithic and Bronze Age cultures such as Corded Ware, Bell Beakers, Unetice, and the Scandinavian cultures are genetically very similar to each other (Fig. 2), 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 (Fig. 2b and Extended Data Table 1). Using D-statistics, we find that Corded Ware and Yamnaya individuals form a clade to the exclusion of Bronze Age Armenians (Extended Data Table 1) showing that the genetic ‘Caucasus component’ present in Bronze Age Europe has a steppe origin rather than a southern Caucasus origin….”

“… The ‘Caucasian’ component is clearly present during Late Bronze Age in Montenegro (Fig. 2b). The close affinity we observe between peoples of Corded Ware and Sintashta cultures (Extended Data Fig. 2a) suggests similar genetic sources of the two, which contrasts with previous hypotheses placing the origin of Sintastha in Asia or the Middle East28. 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 (Fig. 2b and Extended Data Table 1).

Bronze Age Asia

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 (Figs 1 and 3b; Extended Data Fig. 2b and Extended Data Table 1), 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 (Fig. 1). The Andronovo culture, which arose in Central Asia during the later Bronze Age (Fig. 1), is genetically closely related to the Sintashta peoples (Extended Data Fig. 2c), and clearly distinct from both Yamnaya and Afanasievo (Fig. 3b and Extended Data Table 1). 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 multiethnic and show gradual admixture with East Asians (Fig. 3b and Extended Data Table 2), corresponding with anthropological and biological research29. However, Iron Age individuals from Central Asia still show higher levels of West Eurasian ancestry than contemporary populations from the same region (Fig. 3b). Intriguingly, individuals of the Bronze Age Okunevo culture from the Sayano-Altai region (Fig. 1) are related to present-day Native Americans (Extended Data Fig. 2d), which confirms previous craniometric studies30. 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 Americans4 .

…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 BC15,18,31. 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 (Fig. 1) corresponds well with the hypothesized expansion of the Indo-European languages. In contrast to recent genetic findings32, 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 (Z 5 22.39; Supplementary Table 12). This could be due to the absence of eastern hunter-gatherers as potential source population for admixture in our data set. Modern Europeans show some genetic links to Mal’ta4 that has been suggested to form a third European ancestral component (Ancestral North Eurasians (ANE))10. 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 (Figs 2b and 3b and Extended Data Fig. 3).

Formation of Eurasian genetic structure

It is clear from our autosomal, mitochondrial DNA and Y chromosome data (Extended Data Fig. 6) 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 (Figs 2 and 3; Extended Data Fig. 1 and Supplementary Fig. 6). 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 (Extended Data Figs 4 and 5). 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 5 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 (Extended Data Fig. 5). These results are 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 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; Fig. 4), indicating a more recent onset of positive selection than previously estimated34. 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 described12. 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) (Fig. 4b). Among Bronze Age Europeans, the highest tolerance frequency was found in Corded Ware and the closely-related Scandinavian Bronze Age cultures (Extended Data Fig. 7). Interestingly, the Bronze Age steppe cultures showed the highest derived allele frequency among ancient groups, in particular the Yamnaya (Extended Data Fig. 7), indicating a possible steppe origin of lactase tolerance.

Implications 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 agriculture13,15,35,36. 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 (Fig. 1), 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 data15,31. In the light of our results, the existence of the Afanasievo culture near Altai around 3000 BC could also provide an explanation for the mysterious presence of one of the oldest Indo-European languages, Tocharian in the Tarim basin in China37. It seems plausible that Afanasievo, with their genetic western (Yamnaya) origin, spoke an Indo-European language and could have introduced this southward to Xinjiang and Tarim38. 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.”

Lactase persistence allelic incidence mirrors Bronze Age migrations

From Archaeology: The milk revolution:

Existence of milk-drinking lactase persistence gene means some ancestry in a nomadic herding population at some point of time. …

Most people who retain the ability to digest milk can trace their ancestry to Europe, where the trait seems to be linked to a single nucleotide in which the DNA base cytosine changed to thymine in a genomic region not far from the lactase gene. …

During the most recent ice age, milk was essentially a toxin to adults because — unlike children — they could not produce the lactase enzyme required to break down lactose, the main sugar in milk. But as farming started to replace hunting and gathering in the Middle East around 11,000 years ago, cattle herders learned how to reduce lactose in dairy products to tolerable levels by fermenting milk to make cheese or yogurt. Several thousand years later, a genetic mutation spread through Europe that gave people the ability to produce lactase — and drink milk — throughout their lives. That adaptation opened up a rich new source of nutrition that could have sustained communities when harvests failed.

This two-step milk revolution may have been a prime factor in allowing bands of farmers and herders from the south to sweep through Europe and displace the hunter-gatherer cultures that had lived there for millennia. “They spread really rapidly into northern Europe from an archaeological point of view,” says Mark Thomas, a population geneticist at University College London. That wave of emigration left an enduring imprint on Europe, where, unlike in many regions of the world, most people can now tolerate milk. “It could be that a large proportion of Europeans are descended from the first lactase-persistent dairy farmers in Europe,” says Thomas.

By the late Neolithic and early Bronze Age, around 5,000 years ago, the LP allele was prevalent across most of northern and central Europe, and cattle herding had become a dominant part of the culture. “They discover this way of life, and once they can really get the nutritional benefits they increase or intensify herding as well,” says Burger. Cattle bones represent more than two-thirds of the animal bones in many late Neolithic and early Bronze Age archaeological sites in central and northern Europe.

The LeCHE researchers are still puzzling out exactly why the ability to consume milk offered such an advantage in these regions. Thomas suggests that, as people moved north, milk would have been a hedge against famine. Dairy products — which could be stored for longer in colder climes — provided rich sources of calories that were independent of growing seasons or bad harvests.”

Yuval Itanet al., A worldwide correlation of lactase persistence phenotype and genotypes BMC Evolutionary Biology, 201010:36 DOI: 10.1186/1471-2148-10-36 http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-36

The recent identification of independent nucleotide changes that are strongly associated with lactase persistence in different populations worldwide has led to the possibility of genetic tests for the trait. However, it is highly unlikely that all lactase persistence-associated variants are known. Using an extensive database of lactase persistence phenotype frequencies, together with information on how those data were collected and data on the frequencies of lactase persistence variants, we present a global summary of the extent to which current genetic knowledge can explain lactase persistence phenotype frequency.

In this study we have demonstrated that lactase persistence genotype data is currently insufficient to explain lactase persistence phenotype frequency in western and eastern Africa and several other Old World regions. The identification of additional LP-associated or LP-causative alleles, especially in these regions, will help not only in developing a better understanding of the evolution of LP but also in elucidating the physiological mechanisms that underlie the trait. The interpolation and mapping approach that we have applied in this study may also be of value in studying the underlying genetic basis and evolution of other phenotypic variation that impacts on human health, such as the distribution of functional variation in drug metabolising enzymes [42].

With the recent discovery of nucleotide changes associated with LP comes the prospect of direct genetic tests for the trait [8,910]. However, it has become clear that there are multiple, independently derived LP-associated alleles with different geographical distributions [181112]. LP is particularly common in Europe and certain African and Middle Eastern groups. As a consequence these are the regions where most genetic studies have been focused and all currently known LP alleles have been identified [71112]. The first allelic variant that was shown to be strongly associated with increased lactase activity is a C>T change 13,910 bases upstream of the LCT gene in the 13th intron of the MCM6 gene [13]. Functional studies have indicated that this change may affect lactase gene promoter activity and increase the production of lactase-phlorizin hydrolase mRNA in the intestinal mucosa [14151617] but, as with all LP-associated variants, there remains the possibility that linkage to as yet unknown causative nucleotide changes may explain observed associations. Haplotype length conservation [8], linked microsatellite variation [19] and ancient DNA analysis from early European farmers [20] later confirmed that this allele has a recent evolutionary origin and had been the subject of strong positive natural selection. Furthermore, a simulation model of the origins and evolution of lactase persistence and dairying in Europe has inferred that natural selection started to act on an initially small number of lactase persistent dairyers around 7,500 BP in a region between Central Europe and the northern Balkans, possibly in association with the Linearbandkeramik culture [21]. Another simulation study has inferred that it is likely that lactase persistence selective advantage was not constant over Europe, and that demography was a significant element in the evolution and spread of European lactase persistence [22].

However, the presence of this allele could not explain the frequency of LP in most African populations [8]. Further studies identified three additional variants that are strongly associated with LP in some African and Middle Eastern populations and/or have evidence of function, all are upstream of the LCT gene in the 13thintron of the MCM6 gene: -13,907*G, -13,915*G and -14,010*C [11122324]. Where data were sufficient, some of these alleles also showed genetic signatures of a recent origin and strong positive natural selection [1223].

Lactase persistence among Japanese:

Some studies have found that most Japanese can consume 200 ml (8 fl oz) of milk without severe symptoms. Milk tolerance is about 81% in Japanese adults. The relatively low prevalence of lactose malabsorption among the Kazakhs suggests that lactose persistence may be frequent in herding pastoralist populations of southwest Asia.

The −13910*T allele, which is widespread in Europe, was found to be located on an extended haplotype of 500 kb or more.  In Central Asia, the causal polymorphism for LP is the same as in Europe (−13.910C > T, rs4988235; Heyeretal., 2011), suggesting genetic diffusion between the two geographical regions.

It is indicated that the allele responsible for lactose persistence (13.910*T) may have arisen in Central Asia, based on the higher frequency of lactase persistence among Kazakhs who have the lowest proportion of “western” gene pool inferred from admixture analysis from autosomal microsatellite data. This, in turn, could also be an indirect genetic proof of early domestication of horses for milk products as recently attested from archaeological remains. In Kazakhs, traditionally herders, lactose persistence frequency is estimated to 25–32%, of which only 40.2% have symptoms and 85–92% of the individuals are carriers of the −13.910*T allele.The allele frequencies associated with lactase persistence (T-13910) were 10.9% in ancient groups of Hungary, 35.9% in modern-day Hungarians and 40% in Hungarian Seklers of Transylvania, respectively.[70]At ages 2 – 3 yr, 6 yr, and 9 – 10 yr, the amount of lactose intolerance is, respectively: approximately 10%, 20%, and 25% in Chinese and Japanese. Source:  Lactase_persistence (Wikipedia)

 Lidan Xu et al., The -22018A allele matches the lactase persistence phenotype in northern Chinese populations Scandinavian Journal Of Gastroenterology Vol. 45 , Iss. 2,2010

“…found that -13910C/T is not a good predictor of lactase persistence in Chinese populations. To obtain a better understanding of the mechanism of lactase persistence, we examined the frequencies in Northern China of the four other alleles that are associated with lactase persistence. Material and methods. We evaluated the allele frequencies of -22018G/A, -13907C/G, -13915T/G, and -14010G/C in six northern Chinese populations (Manchu, Mongol, Hezhen, Oroqen, Kazak, and northern Han) using the methods of polymerase chain reaction–restriction fragment length polymorphism and resequencing. Results. By genotyping 1092 chromosomes, we found that the frequency of the -22018A allele was highest in the Kazak population and extremely low in the northern Han population. Although there are little available data about the frequency of lactase persistence in northern Chinese populations, we compared the allele frequencies with the phenotype frequencies that have been published previously. We found that the frequency of the -22018A allele was basically consistent with the reported frequencies of lactase persistence in Northern China. With respect to the -13907C/G, -13915T/G, and -14010G/C polymorphisms, we found no individuals with the derived allele. Conclusions. The frequency of the -22018A allele differed significantly among the six populations and the frequency reflected the frequency of lactase persistence. Taking into consideration the results of previous studies, we believe that the origins of lactase persistence-associated alleles are different in different pastoral populations.”

See also Ancient DNA solves milk mystery http://www.nature.com/news/2007/070226/full/news070226-4.html

Breath hydrogen test for detecting lactose malabsorption in infants and children. Prevalence of lactose malabsorption in Japanese children and adults

In Brazil, the lactase persistence allele, LCT‐13910T, was found in approximately 43% of both white (European descent) and brown (European and African descent), and 20% of black (African descent) Brazilians, but was absent in all Japanese‐Brazilians studied.4 Recent epidemiological data regarding lactose intolerance/hypolactasia are lacking in Japan. This lack of information may be because of the relative rarity of symptoms; it has been shown that, although 92% of tested subjects were lactase deficient, only 2% were milk intolerant and 13% were lactose intolerant. (Source: LCT‐22018G>A single nucleotide polymorphism is a better predictor of adult‐type hypolactasia/lactase persistence in Japanese‐Brazilians than LCT‐13910C>T,  Clinics (Sao Paulo). 2010 Dec; 65(12): 1399–1400. doi:  10.1590/S1807-59322010001200030

“The incidence of lactose malabsorption was 30% in 3-year, 36% in 4-year, 58% in 5-year, and 86% in 6-year-old children, 85% in schoolchildren, and 89% in adults. Thus the incidence of lactase deficiency gradually increases with age from 3 years, and about 90% of all normal Japanese adults are lactase-deficient.”

Japanese variants 2 and 4 of lactase showed high frequencies of polymorphisms along with the highest frequencies with north Europeans Source:EJ Hollox et al., Highly variable region upstream of lactase:

The region –974 bp to –852 bp of human lactase is an unusually variable stretch of DNA sequence with marked allele frequency differences in different populations. The previously described variant 4 is found at polymorphic levels in southern Europeans, Japanese, and New Guineas, but rare in the black British cohort, San, and northern Europeans, and absent in Bantuspeaking South Africans.

O Nose et al., Breath hydrogen test for detecting lactose malabsorption in infants and children. Prevalence of lactose malabsorption in Japanese children and adults.  Arch Dis Child. 1979 Jun; 54(6): 436–440.

Y Itan et al., A worldwide correlation of lactase persistence phenotype and genotypes

Han-Jun Jin et al., The Peopling of Korea Revealed by Analyses of Mitochondrial DNA and Y-Chromosomal Markers

The Koreans are generally considered a northeast Asian group because of their geographical location. However, recent findings from Y chromosome studies showed that the Korean population contains lineages from both southern and northern parts of East Asia….

In general, the Korean mtDNA profiles revealed similarities to other northeastern Asian populations through analysis of individual haplogroup distributions, genetic distances between populations or an analysis of molecular variance, although a minor southern contribution was also suggested. Reanalysis of Y-chromosomal data confirmed both the overall similarity to other northeastern populations, and also a larger paternal contribution from southeastern populations.

This study concluded:

“The present work provides evidence that peopling of Korea can be seen as a complex process, interpreted as an early northern Asian settlement with at least one subsequent male-biased southern-to-northern migration, possibly associated with the spread of rice agriculture.”

“Our study documents the genetic relationships of the Koreans with their neighboring populations in unprecedented detail. Two major findings emerge. First, the Koreans are overall more similar to northeast Asians than to southeast Asians …”

Also from the paper:

The predominant genetic relationship with northern East Asians is consistent with other lines of evidence. Xue et al. [31] reported that the northern East Asian populations started to expand in number before the last glacial maximum at 21-18 KYA, while the southern populations all started to expand after it, but then grew faster, and they suggested that the northern populations expanded earlier because they could exploit the abundant megafauna of the “Mammoth Steppe,” while the southern populations could increase in number only when a warmer and more stable climate led to more plentiful plant resources such as tubers. By this criterion, the Koreans, expanding at about 30 KYA [31] also resemble other northern populations. (Historical evidence suggests that the Ancient Chosun, the first state-level society, was established in the region of southern Manchuria and later moved into the Pyongyang area of the northwestern Korean Peninsula). Based on archeological and anthropological data, the early Korean population possibly had an origin in the northern regions of the Altai-Sayan and Baikal regions of Southeast Siberia