stone age eurasia
STONE AGE EURASIA
https://www.biorxiv.org/content/10.1101/2022.05.04.490594v1
Allenthoft & Willerslev et. al. 2022, Biorxiv.
Abstract:
The transitions from foraging to farming and later to pastoralism in Stone Age Eurasia (c. 11-3 thousand years before present, BP) represent some of the most dramatic lifestyle changes in human evolution. We sequenced 317 genomes of primarily Mesolithic and Neolithic individuals from across Eurasia combined with radiocarbon dates, stable isotope data, and pollen records. Genome imputation and co-analysis with previously published shotgun sequencing data resulted in >1600 complete ancient genome sequences offering fine-grained resolution into the Stone Age populations. We observe that: 1) Hunter-gatherer groups were more genetically diverse than previously known, and deeply divergent between western and eastern Eurasia. 2) We identify hitherto genetically undescribed hunter-gatherers from the Middle Don region that contributed ancestry to the later Yamnaya steppe pastoralists; 3) The genetic impact of the Neolithic transition was highly distinct, east and west of a boundary zone extending from the Black Sea to the Baltic. Large-scale shifts in genetic ancestry occurred to the west of this "Great Divide", including an almost complete replacement of hunter-gatherers in Denmark, while no substantial ancestry shifts took place during the same period to the east. This difference is also reflected in genetic relatedness within the populations, decreasing substantially in the west but not in the east where it remained high until c. 4,000 BP; 4) The second major genetic transformation around 5,000 BP happened at a much faster pace with Steppe-related ancestry reaching most parts of Europe within 1,000-years. Local Neolithic farmers admixed with incoming pastoralists in eastern, western, and southern Europe whereas Scandinavia experienced another near-complete population replacement. Similar dramatic turnover-patterns are evident in western Siberia; 5) Extensive regional differences in the ancestry components involved in these early events remain visible to this day, even within countries. 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 (this research has been conducted using the UK Biobank resource); 6) Shifts in diet, lifestyle and environment introduced new selection pressures involving at least 21 genomic regions. Most such variants were not universally selected across populations but were only advantageous in particular ancestral backgrounds. Contrary to previous claims, we find that selection on the FADS regions, associated with fatty acid metabolism, began before the Neolithisation of Europe. Similarly, the lactase persistence allele started increasing in frequency before the expansion of Steppe-related groups into Europe and has continued to increase up to the present. Along the genetic cline separating Mesolithic hunter-gatherers from Neolithic farmers, we find significant correlations with trait associations related to skin disorders, diet and lifestyle and mental health status, suggesting marked phenotypic differences between these groups with very different lifestyles. This work provides new insights into major transformations in recent human evolution, elucidating the complex interplay between selection and admixture that shaped patterns of genetic variation in modern populations.
Our study comprises the largest genomic dataset on European hunter-gatherers to date, including
329 113 imputed hunter-gatherer genomes of which 79 were sequenced in this study. Among them, we
330 report a 0.83X genome of an Upper Palaeolithic (UP) skeleton from Kotias Klde Cave in Georgia,
331 Caucasus (NEO283), directly dated to 26,052 - 25,323 cal BP (95%). In the PCA of all non-African
332 individuals, it occupies a position distinct from other previously sequenced UP individuals, shifted
333 towards west Eurasians along PC1 (Supplementary Note 3d). Using admixture graph modelling, we
334 find that this Caucasus UP lineage derives from a mixture of predominantly West Eurasian UP
335 hunter-gatherer ancestry (76%) with ~24% contribution from a “basal Eurasian” ghost population,
first observed in West Asian Neolithic individuals29 336 (Extended Data Fig. 5A). Models attempting to
337 reconstruct major post-LGM clusters such as European hunter-gatherers and Anatolian farmers
338 without contributions from this Caucasus UP lineage provided poor admixture graph fits or were
339 rejected in qpAdm analyses (Extended Data Fig. 5B,C). These results thus suggest a central role of
340 the descendants related to this Caucasus UP lineage in the formation of later West Eurasian
341 populations, consistent with recent genetic data from the nearby Dzudzuana Cave, also in
Georgia30 342 .
We replicate previous results of broadscale genetic structure correlated to geography in European hunter-gatherers after the LGM17 347 , while
348 also revealing novel insights into their fine-scale structure. Ancestry related to southern European
349 hunter-gatherers (source: Italy_15000BP_9000 BP) predominates in western Europe. This includes
350 Denmark, where our 28 sequenced and imputed hunter-gatherer genomes derive almost exclusively
351 from this cluster, with remarkable homogeneity across a 5,000 year transect (Fig. 3A). In contrast,
352 hunter-gatherer individuals from the eastern and far northern reaches of Europe show the highest
353 proportions of Russian hunter-gatherer ancestry (source: RussiaNW_11000BP_8000BP; Fig. 2B,
354 D), with genetic continuity until ~5,000 BP in Russia. Ancestry related to Mesolithic hunter355 gatherer populations from Ukraine (source: Ukraine_10000BP_4000BP) is carried in highest
356 proportions in hunter-gatherers from a geographic corridor extending from south-eastern Europe
357 towards the Baltic and southern Scandinavia. Swedish Mesolithic individuals derive up to 60% of
358 their ancestry from that source (Fig. 2C). Our results thus indicate northwards migrations of at least
359 three distinct waves of hunter-gatherer ancestry into Scandinavia: a predominantly southern
360 European source into Denmark; a source related to Ukrainian and south-eastern European hunter361 gatherers into the Baltic and southern Sweden; and a northwest Russian source into the far north,
before venturing south along the Atlantic coast of Norway31 362 (Fig. 2). These movements are likely to
represent post glacial expansions from refugia areas shared with many plant and animal species32,33 363 .
Interestingly, two herein reported ~7,300-year-old imputed
383 genomes from the Middle Don River region in the Pontic-Caspian steppe (Golubaya Krinitsa,
384 NEO113 & NEO212) derive ~20-30% of their ancestry from a source cluster of hunter-gatherers
385 from the Caucasus (Caucasus_13000BP_10000BP) (Fig. 3). Additional lower coverage (non386 imputed) genomes from the same site project in the same PCA space (Fig. 1D), shifted away from
387 the European hunter-gatherer cline towards Iran and the Caucasus. Our results thus document
388 genetic contact between populations from the Caucasus and the Steppe region as early as 7,300
389 years ago...
From approximately 5,000 BP, an ancestry component appears on the eastern European plains in
425 Early Bronze Age Steppe pastoralists associated with the Yamnaya culture and it rapidly spreads
across Europe through the expansion of the Corded Ware complex (CWC) and related cultures20,21 426 .
427 We demonstrate that this “steppe” ancestry (Steppe_5000BP_4300BP) can be modelled as a
428 mixture of ~65% ancestry related to herein reported hunter-gatherer genomes from the Middle Don
429 River region (MiddleDon_7500BP) and ~35% ancestry related to hunter-gatherers from Caucasus
430 (Caucasus_13000BP_10000BP) (Extended Data Fig. 4). Thus, Middle Don hunter-gatherers, who
431 already carry ancestry related to Caucasus hunter-gatherers (Fig. 2), serve as a hitherto unknown
432 proximal source for the majority ancestry contribution into Yamnaya genomes. The individuals in
433 question derive from the burial ground Golubaya Krinitsa (Supplementary Note 3). Material culture
434 and burial practices at this site are similar to the Mariupol-type graves, which are widely found in
435 neighbouring regions of Ukraine, for instance along the Dnepr River. They belong to the group of
436 complex pottery-using hunter-gatherers mentioned above, but the genetic composition at Golubaya
437 Krinitsa is different from the remaining Ukrainian sites (Fig 2A, Extended Data Fig. 4).
Individuals associated with Neolithic
470 farming cultures from Denmark show some of the highest overall hunter-gatherer ancestry
471 proportions (up to ~25%), mostly derived from Western European-related hunter-gatherers
472 (EuropeW_13500BP_8000BP) supplemented with marginal contribution from local Danish groups
473 in some individuals (Extended Data Fig. 7D; Supplementary Note 3f). We estimated the timing of
the admixture using the linkage-disequilibrium-based method DATES48 474 at ~6,000 BP. Both lines of
475 evidence thus suggest that a significant part of the hunter-gatherer admixture observed in Danish
476 Neolithic individuals occurred already before the arrival of the incoming Neolithic people in the
477 region (Extended Data Fig. 7), and further imply Central Europe as a key region in the resurgence
478 of HG ancestry.
The second continental-wide and CWC-mediated transition from Neolithic farmer ancestry to
497 Steppe-related ancestry was found to differ markedly between geographic regions. The contribution
498 of local Neolithic farmer ancestry to the incoming groups was high in eastern, western and southern
Europe, reaching >50% on the Iberian Peninsula (“postNeol” set; Extended Data Fig. 4, 6B, C)34 499 .
500 Scandinavia, however, portrays a dramatically different picture, with a near-complete replacement
501 of the local Neolithic farmer population inferred across all sampled individuals (Extended Data Fig.
502 7B, C). Following the second transition, Neolithic Anatolian-related farmer ancestry remains in
503 Scandinavia, but the source is now different. It can be modelled as deriving almost exclusively from
504 a genetic cluster associated with the Late Neolithic Globular Amphora Culture (GAC)
505 (Poland_5000BP_4700BP; Extended Data Fig. 4). Strikingly, after the Steppe-related ancestry was
506 first introduced into Europe (Steppe_5000BP_4300BP), it expanded together with GAC-related
507 ancestry across all sampled European regions (Extended Data Fig. 7I). This suggests that the spread
508 of steppe-related ancestry throughout Europe was predominantly mediated through groups that were
509 already admixed with GAC-related farmer groups of the eastern European plains.
The Neolithic transition also
610 marks a considerable rise in frequency of major effect alleles associated with light hair
pigmentation79 611 , whereas polygenic score predictions for height are generally low throughout the
612 first millennium of the Neolithic (Funnel Beaker epoch), echoing previous findings based on a
smaller set of individuals45,80 613 .
. The most recent individual
618 in our Danish dataset with Mesolithic WHG ancestry is “Dragsholm Man” (NEO962), dated to
619 5,947-5,664 cal. BP (95%) and archaeologically assigned to the Neolithic Funnel Beaker farming
culture based on his grave goods81,82 620 . Our data confirms a typical Neolithic diet matching the
621 cultural affinity but contrasting his WHG ancestry. Thus, Dragsholm Man represents a local person
622 of Mesolithic ancestry who lived in the short Mesolithic-Neolithic transition period and adopted a
623 Neolithic culture and diet.
STONE AGE EURASIA
https://www.biorxiv.org/content/10.1101/2022.05.04.490594v1
Allenthoft & Willerslev et. al. 2022, Biorxiv.
Abstract:
The transitions from foraging to farming and later to pastoralism in Stone Age Eurasia (c. 11-3 thousand years before present, BP) represent some of the most dramatic lifestyle changes in human evolution. We sequenced 317 genomes of primarily Mesolithic and Neolithic individuals from across Eurasia combined with radiocarbon dates, stable isotope data, and pollen records. Genome imputation and co-analysis with previously published shotgun sequencing data resulted in >1600 complete ancient genome sequences offering fine-grained resolution into the Stone Age populations. We observe that: 1) Hunter-gatherer groups were more genetically diverse than previously known, and deeply divergent between western and eastern Eurasia. 2) We identify hitherto genetically undescribed hunter-gatherers from the Middle Don region that contributed ancestry to the later Yamnaya steppe pastoralists; 3) The genetic impact of the Neolithic transition was highly distinct, east and west of a boundary zone extending from the Black Sea to the Baltic. Large-scale shifts in genetic ancestry occurred to the west of this "Great Divide", including an almost complete replacement of hunter-gatherers in Denmark, while no substantial ancestry shifts took place during the same period to the east. This difference is also reflected in genetic relatedness within the populations, decreasing substantially in the west but not in the east where it remained high until c. 4,000 BP; 4) The second major genetic transformation around 5,000 BP happened at a much faster pace with Steppe-related ancestry reaching most parts of Europe within 1,000-years. Local Neolithic farmers admixed with incoming pastoralists in eastern, western, and southern Europe whereas Scandinavia experienced another near-complete population replacement. Similar dramatic turnover-patterns are evident in western Siberia; 5) Extensive regional differences in the ancestry components involved in these early events remain visible to this day, even within countries. 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 (this research has been conducted using the UK Biobank resource); 6) Shifts in diet, lifestyle and environment introduced new selection pressures involving at least 21 genomic regions. Most such variants were not universally selected across populations but were only advantageous in particular ancestral backgrounds. Contrary to previous claims, we find that selection on the FADS regions, associated with fatty acid metabolism, began before the Neolithisation of Europe. Similarly, the lactase persistence allele started increasing in frequency before the expansion of Steppe-related groups into Europe and has continued to increase up to the present. Along the genetic cline separating Mesolithic hunter-gatherers from Neolithic farmers, we find significant correlations with trait associations related to skin disorders, diet and lifestyle and mental health status, suggesting marked phenotypic differences between these groups with very different lifestyles. This work provides new insights into major transformations in recent human evolution, elucidating the complex interplay between selection and admixture that shaped patterns of genetic variation in modern populations.
Our study comprises the largest genomic dataset on European hunter-gatherers to date, including
329 113 imputed hunter-gatherer genomes of which 79 were sequenced in this study. Among them, we
330 report a 0.83X genome of an Upper Palaeolithic (UP) skeleton from Kotias Klde Cave in Georgia,
331 Caucasus (NEO283), directly dated to 26,052 - 25,323 cal BP (95%). In the PCA of all non-African
332 individuals, it occupies a position distinct from other previously sequenced UP individuals, shifted
333 towards west Eurasians along PC1 (Supplementary Note 3d). Using admixture graph modelling, we
334 find that this Caucasus UP lineage derives from a mixture of predominantly West Eurasian UP
335 hunter-gatherer ancestry (76%) with ~24% contribution from a “basal Eurasian” ghost population,
first observed in West Asian Neolithic individuals29 336 (Extended Data Fig. 5A). Models attempting to
337 reconstruct major post-LGM clusters such as European hunter-gatherers and Anatolian farmers
338 without contributions from this Caucasus UP lineage provided poor admixture graph fits or were
339 rejected in qpAdm analyses (Extended Data Fig. 5B,C). These results thus suggest a central role of
340 the descendants related to this Caucasus UP lineage in the formation of later West Eurasian
341 populations, consistent with recent genetic data from the nearby Dzudzuana Cave, also in
Georgia30 342 .
We replicate previous results of broadscale genetic structure correlated to geography in European hunter-gatherers after the LGM17 347 , while
348 also revealing novel insights into their fine-scale structure. Ancestry related to southern European
349 hunter-gatherers (source: Italy_15000BP_9000 BP) predominates in western Europe. This includes
350 Denmark, where our 28 sequenced and imputed hunter-gatherer genomes derive almost exclusively
351 from this cluster, with remarkable homogeneity across a 5,000 year transect (Fig. 3A). In contrast,
352 hunter-gatherer individuals from the eastern and far northern reaches of Europe show the highest
353 proportions of Russian hunter-gatherer ancestry (source: RussiaNW_11000BP_8000BP; Fig. 2B,
354 D), with genetic continuity until ~5,000 BP in Russia. Ancestry related to Mesolithic hunter355 gatherer populations from Ukraine (source: Ukraine_10000BP_4000BP) is carried in highest
356 proportions in hunter-gatherers from a geographic corridor extending from south-eastern Europe
357 towards the Baltic and southern Scandinavia. Swedish Mesolithic individuals derive up to 60% of
358 their ancestry from that source (Fig. 2C). Our results thus indicate northwards migrations of at least
359 three distinct waves of hunter-gatherer ancestry into Scandinavia: a predominantly southern
360 European source into Denmark; a source related to Ukrainian and south-eastern European hunter361 gatherers into the Baltic and southern Sweden; and a northwest Russian source into the far north,
before venturing south along the Atlantic coast of Norway31 362 (Fig. 2). These movements are likely to
represent post glacial expansions from refugia areas shared with many plant and animal species32,33 363 .
Interestingly, two herein reported ~7,300-year-old imputed
383 genomes from the Middle Don River region in the Pontic-Caspian steppe (Golubaya Krinitsa,
384 NEO113 & NEO212) derive ~20-30% of their ancestry from a source cluster of hunter-gatherers
385 from the Caucasus (Caucasus_13000BP_10000BP) (Fig. 3). Additional lower coverage (non386 imputed) genomes from the same site project in the same PCA space (Fig. 1D), shifted away from
387 the European hunter-gatherer cline towards Iran and the Caucasus. Our results thus document
388 genetic contact between populations from the Caucasus and the Steppe region as early as 7,300
389 years ago...
From approximately 5,000 BP, an ancestry component appears on the eastern European plains in
425 Early Bronze Age Steppe pastoralists associated with the Yamnaya culture and it rapidly spreads
across Europe through the expansion of the Corded Ware complex (CWC) and related cultures20,21 426 .
427 We demonstrate that this “steppe” ancestry (Steppe_5000BP_4300BP) can be modelled as a
428 mixture of ~65% ancestry related to herein reported hunter-gatherer genomes from the Middle Don
429 River region (MiddleDon_7500BP) and ~35% ancestry related to hunter-gatherers from Caucasus
430 (Caucasus_13000BP_10000BP) (Extended Data Fig. 4). Thus, Middle Don hunter-gatherers, who
431 already carry ancestry related to Caucasus hunter-gatherers (Fig. 2), serve as a hitherto unknown
432 proximal source for the majority ancestry contribution into Yamnaya genomes. The individuals in
433 question derive from the burial ground Golubaya Krinitsa (Supplementary Note 3). Material culture
434 and burial practices at this site are similar to the Mariupol-type graves, which are widely found in
435 neighbouring regions of Ukraine, for instance along the Dnepr River. They belong to the group of
436 complex pottery-using hunter-gatherers mentioned above, but the genetic composition at Golubaya
437 Krinitsa is different from the remaining Ukrainian sites (Fig 2A, Extended Data Fig. 4).
Individuals associated with Neolithic
470 farming cultures from Denmark show some of the highest overall hunter-gatherer ancestry
471 proportions (up to ~25%), mostly derived from Western European-related hunter-gatherers
472 (EuropeW_13500BP_8000BP) supplemented with marginal contribution from local Danish groups
473 in some individuals (Extended Data Fig. 7D; Supplementary Note 3f). We estimated the timing of
the admixture using the linkage-disequilibrium-based method DATES48 474 at ~6,000 BP. Both lines of
475 evidence thus suggest that a significant part of the hunter-gatherer admixture observed in Danish
476 Neolithic individuals occurred already before the arrival of the incoming Neolithic people in the
477 region (Extended Data Fig. 7), and further imply Central Europe as a key region in the resurgence
478 of HG ancestry.
The second continental-wide and CWC-mediated transition from Neolithic farmer ancestry to
497 Steppe-related ancestry was found to differ markedly between geographic regions. The contribution
498 of local Neolithic farmer ancestry to the incoming groups was high in eastern, western and southern
Europe, reaching >50% on the Iberian Peninsula (“postNeol” set; Extended Data Fig. 4, 6B, C)34 499 .
500 Scandinavia, however, portrays a dramatically different picture, with a near-complete replacement
501 of the local Neolithic farmer population inferred across all sampled individuals (Extended Data Fig.
502 7B, C). Following the second transition, Neolithic Anatolian-related farmer ancestry remains in
503 Scandinavia, but the source is now different. It can be modelled as deriving almost exclusively from
504 a genetic cluster associated with the Late Neolithic Globular Amphora Culture (GAC)
505 (Poland_5000BP_4700BP; Extended Data Fig. 4). Strikingly, after the Steppe-related ancestry was
506 first introduced into Europe (Steppe_5000BP_4300BP), it expanded together with GAC-related
507 ancestry across all sampled European regions (Extended Data Fig. 7I). This suggests that the spread
508 of steppe-related ancestry throughout Europe was predominantly mediated through groups that were
509 already admixed with GAC-related farmer groups of the eastern European plains.
The Neolithic transition also
610 marks a considerable rise in frequency of major effect alleles associated with light hair
pigmentation79 611 , whereas polygenic score predictions for height are generally low throughout the
612 first millennium of the Neolithic (Funnel Beaker epoch), echoing previous findings based on a
smaller set of individuals45,80 613 .
. The most recent individual
618 in our Danish dataset with Mesolithic WHG ancestry is “Dragsholm Man” (NEO962), dated to
619 5,947-5,664 cal. BP (95%) and archaeologically assigned to the Neolithic Funnel Beaker farming
culture based on his grave goods81,82 620 . Our data confirms a typical Neolithic diet matching the
621 cultural affinity but contrasting his WHG ancestry. Thus, Dragsholm Man represents a local person
622 of Mesolithic ancestry who lived in the short Mesolithic-Neolithic transition period and adopted a
623 Neolithic culture and diet.
