Genome flux and stasis in a five millennium transect of European prehistory

The affinity to Southern Mediterranean individuals persists through nine successive time points in the data, including a diversity of Neolithic cultures.

“This affinity persists through nine successive time points in our data, including a diversity of Neolithic cultures.”

The oldest sample, Körös Neolithic KO1, falls towards the hunter-gatherer vicinity of the PCA plot despite its early Neolithic farming context.

“Despite its early Neolithic farming context, this genome falls towards the hunter-gatherer vicinity of the PCA plot (Fig. 2).”

Neolithic genomes all cluster with affinity to Southern Mediterranean individuals, particularly Sardinians.

“Our Neolithic genomes all cluster with affinity to Southern Mediterranean individuals, particularly Sardinians, echoing the results of previous direct analyses of European Neolithic and post-Neolithic genomes268.”

• cites [268]Not checked yet

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The two Bronze Age samples BR1 and BR2 fall among modern Central European genotypes.

“Our two Bronze Age samples, BR1 (1,980–2,190 cal BC) and BR2 (1,110–1,270 cal BC) fall among modern Central European genotypes.”

The single Iron Age genome IR1 shows a distinct shift towards Eastern Eurasian genotypes, specifically in the direction of several Caucasus population samples.

“The single Iron Age genome, sampled from the pre-Scythian Mezőcsát Culture (Iron Age (IR1), 830–980 cal BC), shows a distinct shift towards Eastern Eurasian genotypes, specifically in the direction of several Caucasus population samples within the reference data set.”

Endogenous DNA yields from a further seven petrous bones from Hungary remained exceptionally and consistently high.

“We extended this sampling to a further seven petrous bones from Hungary and yields of endogenous DNA remained exceptionally and consistently high (Supplementary Table 3).”

Sample KO2, contemporaneous to KO1 and from a Neolithic Körös Culture site only ~70 km distant, clusters with later Neolithic individuals.

“In contrast, sample KO2, which is contemporaneous to KO1 (5,570–5,710 cal BC) and also from a Neolithic Körös Culture site only ~70 km distant, clusters with later Neolithic individuals (Fig. 2 and Supplementary Fig. 1).”

No ancient genome in the analysis showed a clear excess of long runs of homozygosity (>1.6 Mb).

“Unlike a small subset of modern genomes, no ancient genome in our analysis showed a clear excess of long runs of homozygosity (ROH) (>1.6 Mb), suggesting each to have been outbred.”

PCA shows clear shifts in the genomic affinities of the ancient genotypes coinciding with cultural shifts and bracketing a 2,800-year period of Neolithic stasis.

“This analysis shows clear shifts (including two within multi-phased archaeological sites) in the genomic affinities of the ancient genotypes coinciding with cultural shifts and bracketing a 2,800 year period of Neolithic stasis.”

KO1 was a blue-eyed male.

“The outlying Neolithic individual, KO1, was a blue-eyed male (Fig. 3)”

At least for Europeans, imputation of 1× genome coverage sequences can give genome-wide diploid calls for ~80% of genome-wide SNPs at ~99% accuracy.

“We also show that, at least for Europeans, imputation of 1 × genome coverage sequences can give genome-wide diploid calls for ~80% of genome-wide SNPs, at ~99% accuracy, greatly leveraging their information content.”

ADMIXTURE analysis reaffirmed the clustering and temporal shifts in affinity observed in the PCA visualization.

“These data were used in an ADMIXTURE analysis29, which reaffirmed the clustering and temporal shifts in affinity observed in the PCA visualization (Fig. 4).”

• cites [29] Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009). sourceNot checked yet

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KO1's Y-chromosome lineage I2a matches the only haplogroup reported to date in Mesolithic Central and Northern Europeans (n=6).

“his Y-chromosome lineage, I2a, matches the only haplogroup reported to date in Mesolithic Central and Northern Europeans58 (n=6).”

• cites [58]Not checked yet

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High mtDNA diversity was observed during the Neolithic period.

“In contrast, we observe high mtDNA diversity during this period, as previously observed in Central Europe23.”

• cites [23] Brandt, G. et al. Ancient DNA reveals key stages in the formation of central european mitochondrial genetic diversity. Science 342, 257–261 (2013). sourceNot checked yet

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The selected variant at TYRP1 shows some tendency to higher prevalence in later samples.

“The selected variant at a third pigmentary locus with a proposed adaptive history in Europe, TYRP1, also shows some tendency to higher prevalence in later samples.”

The Neolithic genomes reported here show an immigrant signature of Southern Mediterranean affinity, consistent with prior German, Scandinavian and Alpine early farmer genomes.

“The Neolithic genomes reported here accord with prior German, Scandinavian and Alpine early farmer genomes in showing an immigrant signature of Southern Mediterranean affinity2568.”

• cites [2568]Not checked yet

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A single individual within the Körös culture, part of the earliest Neolithic of Southern Europe, has a strongly Mesolithic genomic signature.

“However, an intriguing finding is that of a single individual with a strongly Mesolithic genomic signature within the context of the Körös culture, part of the earliest Neolithic of Southern Europe.”

The high percentages of human DNA indicate very good preservation in all samples.

“The high percentages of human DNA point to very good preservation in all samples.”

The lactase persistence allele remains absent throughout the 10 Neolithic/Copper Age stages of the transect.

“this variant remains absent throughout the 10 Neolithic/Copper Age stages of our transect.”

In the Middle and Late Hungarian Neolithic, local Mesolithic influence is discernible through the appearance of mtDNA and Y-chromosome haplogroups typical of European hunter-gatherer populations.

“In the Middle and Late Hungarian Neolithic local Mesolithic influence is further discernible through the appearance of mtDNA and Y-chromosome haplogroups typical of European hunter-gatherer populations”

A temporal transition towards lighter pigmentation is also seen with hair, with colours and shades estimated from SNPs grading from black/dark brown in earlier samples to light brown and dark blonde in later individuals.

“This temporal transition towards lighter pigmentation is also seen with hair where colours and shades estimated from SNPs used in the forensic Hirisplex system grade from black/dark brown in earlier samples to light brown and dark blonde in later individuals (Fig. 3).”

The single pre-Scythian IR1 genome shows a shift.

“The single pre-Scythian IR1 genome shows another shift”

The samples show a tendency towards lighter pigmentation through and after the Neolithic.

“Our samples show a tendency towards lighter pigmentation through and after the Neolithic.”

The high-coverage ancient Neolithic genome NE1 falls outside PCA clusters of the 1,000 Genomes reference individuals, along with KO1 and IR1.

“our high-coverage ancient Neolithic genome, NE1, falls outside PCA clusters of the 1,000 Genomes reference individuals, along with our KO1 and IR1 samples (Supplementary Fig. 8).”

The lactase persistence allele's appearance is delayed until the more recent Bronze Age individual, who lived only ~1,000 years BC.

“Here in our temporal sequence, its appearance is delayed until the more recent of our Bronze Age individuals, who lived only ~1,000 years BC.”

The Bronze Age genomes shift towards an affinity to Central Europe.

“In contrast, the Bronze Age genomes shift towards an affinity to Central Europe”

The archaeological record indicates increased technological and typological affinities with Steppe cultures at this time, including the importation of horse riding, carts, chariots and metallurgical techniques.

“This is supported by the archaeological record which indicates increased technological and typological affinities with Steppe cultures at this time, including the importation of horse riding, carts, chariots and metallurgical techniques26.”

• cites [26] Cunliffe, B. Europe Between the Oceans: 9000 Bc-Ad 1000 Yale University Press (2011).Not checked yet

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These two Bronze Age genomes represent the oldest genomic data sampled to date with clear Central European affinities.

“These two Bronze Age genomes represent the oldest genomic data sampled to date with clear Central European affinities.”

The IR1 result, supported by mtDNA and Y-chromosome haplogroups N and G2a1 with Asian affinities, suggests genomic influences from the East.

“This result, supported by mtDNA and Y-chromosome haplogroups (N and G2a1, respectively, both with Asian affinities) suggests genomic influences from the East.”

The marked genomic dichotomy between KO1 and KO2 suggests direct contact between indigenous hunter-gatherers and Neolithic communities.

“This marked genomic dichotomy between KO1 and KO2 suggests direct contact between indigenous hunter-gatherers and Neolithic communities as suggested previously2822.”

• cites [2822]Not checked yet

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Each ancient genome in the analysis was outbred.

“Unlike a small subset of modern genomes, no ancient genome in our analysis showed a clear excess of long runs of homozygosity (ROH) (>1.6 Mb), suggesting each to have been outbred.”

The temporal transect suggests separate selective sweeps at SLC24A5 and SLC45A2, acting over a millennium apart.

“Our temporal transect suggests separate selective sweeps at these two pigmentary loci, acting over a millennium apart.”

The high density of the petrous bone results in reduced bacterial and chemical-mediated post-mortem DNA decay.

“We suggest that the high density17 of the petrous bone results in reduced bacterial and chemical-mediated post-mortem DNA decay.”

• cites [17] Lam, Y. M., Chen, X. & Pearson, O. M. Intertaxonomic Variability in patterns of bone density and the differential representation of Bovid, Cervid, and Equid Elements in the Archaeological record. Am. Antiq. 64, 343–362 (1999). sourceNot checked yet

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The appearance of hunter-gatherer haplogroups in the Middle and Late Hungarian Neolithic concurs with other evidence for admixture in the ancestry of European farmers.

“concurring with other evidence for admixture in the ancestry of European farmers582223.”

• cites 582223Not checked yet

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Selection on the lactase persistence variant was driven by dairying.

“Selection on this variant was undoubtedly driven by dairying, but despite evidence for milk residues in ceramic vessels from a Körös context in the 6th millenium BC (ref. 36) this variant remains absent throughout the 10 Neolithic/Copper Age stages of our transect.”

• cites [35] Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913–918 (2007). sourceNot checked yet

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• cites [36] Craig, O. E. et al. Did the first farmers of central and eastern Europe produce dairy foods? Antiquity 79, 882–894 (2005). sourceNot checked yet

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The IR1 shift indicates migration from the East.

“towards migration from the East.”

• AssumptionRests on an assumption: Shifts in genome affinity between archaeological periods reflect substantial migrations.

In PCA and ROH plots of imputed genotypes from 0.5×, 1× and 2.5× coverage samples of NE1 and BR2, the positions from each replicate were highly similar to those generated from high-coverage SNP calls.

“In both PCA and ROH plots of genotypes from these, the positions from each replicate were highly similar to those generated from high-coverage SNP calls (Supplementary Figs 6 and 7).”

The Bronze Age shift towards Central European affinity suggests migratory influence from the North.

“suggesting migratory influence from the North.”

• AssumptionRests on an assumption: Shifts in genome affinity between archaeological periods reflect substantial migrations.

The similarity of the Copper Age sample to Neolithic genomes is in accordance with archaeological continuity in the region.

“in accordance with archaeological continuity in the region.”

There is evidence for milk residues in ceramic vessels from a Körös context in the 6th millennium BC.

“despite evidence for milk residues in ceramic vessels from a Körös context in the 6th millenium BC (ref. 36)”

• cites [36] Craig, O. E. et al. Did the first farmers of central and eastern Europe produce dairy foods? Antiquity 79, 882–894 (2005). sourceNot checked yet

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Wilde et al. found intermediate frequencies for SLC45A2 in ancient Ukrainian Eneolithic and Early Bronze Age samples.

“Wilde et al.32 also found intermediate frequencies for SLC45A2 in ancient Ukranian Eneolithic and Early Bronze Age samples.”

• cites [32] Wilde, S. et al. Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y. Proc. Natl Acad. Sci. USA 111, 4832–4837 (2014). sourceNot checked yet

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Altogether, the results accord with archaeological perspectives that link these major transitions in European material culture to population movements rather than cultural diffusion alone.

“Altogether, our results accord with archaeological perspectives that link these major transitions in European material culture to population movements rather than cultural diffusion alone.”

• AssumptionRests on an assumption: Archaeological perspectives that link major transitions in European material culture to population movements rather than cultural diffusion alone are correct.
• AssumptionRests on an assumption: Shifts in genome affinity between archaeological periods reflect substantial migrations.

These changes in material culture were accompanied by substantial migrations.

“strongly implying that these changes in material culture were accompanied by substantial migrations.”

• AssumptionRests on an assumption: Shifts in genome affinity between archaeological periods reflect substantial migrations.

This individual is the earliest genetic indication of contact between Mesolithic and Neolithic subsistence strategies.

“This is the earliest genetic indication of contact between these two subsistence strategies.”

The absence of the lactase persistence allele until the late Bronze Age, ~1,000 years BC, suggests a more recent dating of this episode in European genome history.

“Its absence here until the late Bronze Age, ~1,000 years BC, suggests a more recent dating of this extremely interesting episode in the dynamic history of European genomes.”