Ancient DNA from Neolithic Sweden (Skoglund et al. 2012)

A new paper in Science solidifies the case for migration as the cause for the diffusion of agriculture in Europe. Discontinuity between early Neolithic farmers and Mesolithic foragers in Central Europe had provided strong hints about this discontinuity, and these were confirmed by other ancient European DNA, e.g., from Treilles, or the Tyrolean Iceman. The case now appears irrefutable, that people not ideas were involved in the spread farming to the northern fringes of Europe.

If we were to ever find signs of acculturation, the north-eastern corner of Europe may be best place to look for it. Agriculture arrived late to Scandinavia and the Baltic, so there was maximum opportunity for Neolithic groups in the area to acquire pre-Neolithic genes from acculturated farmers during their ~2ky long journey from the Aegean. Conversely, forager populations persisted here longer than elsewhere in Europe, both due to the remoteness of the area and the relative unsuitability of the Neolithic package brought from more southern latitudes.

During the Neolithic period there still existed foragers in Scandinavia who belonged to the Pitted Ware (PWC) culture. These have been the object of a previous mtDNA study, which found them to be strongly differentiated from contemporaneous Funnel Beaker or Trichterbecherkultur (TRB) farmers. The latter were farmers who were also associated with Megalithic monuments in northern Europe.

A recent article by Rowley-Conwy (2011), from which the figure on the left is taken, gives some archaeological perspective on the Neolithic of southern Scandinavia:

This farming spread must have been by boat. There were no native aurochs on Zealand (Aaris-Sorensen 1980), so the early cattle at Akonge were definitely imported. Farther north, agriculture was probably carried by boat up the coasts, an easier method of travel than overland (see above). Baltic crossings would require longer open-water voyages than in the Cardial or LBK. Irish curraghs can, however, make substantial voyages and weather considerable seas (Hornell 1938, sec. 5:17–21), and a large one has even crossed the Atlantic (Severin 1978).

...

The agricultural arrival in southern Scandinavia thus appears sharp. Gradualist views of Late Mesolithic developments can be discounted despite the spread of shoe-last axes beyond the farming frontier. Western Norway presents a similar pattern: axes and ceramics were in circulation for over a millennium beyond the farming boundary.

This was the dusk of the European foragers: whatever their contribution to subsequent European populations, their way of life would soon give way to that of the farmer and shepherd. The Pitted Ware culture can indeed be seen as their "last stand", the last time in prehistory when they could co-exist on fairly equal terms with their farmer neighbors.

Hence, it is very exciting to be able to study DNA from this place and time directly, as Skoglund et al. do in a new paper which reports the successful extraction and analysis of ancient DNA from 3 PWC hunter-gathers and one TRB farmer of about ~5,000 years ago:

The Neolithic farmer sample ('Gok4') was excavated from a megalithic burial structure in Gokhem parish, Sweden, and has been directly 14C-dated to 4,921 ± 50 calibrated years BP (calBP), similar to the age (5,100-4,900 calBP) of the majority of other finds in the area (15). There were no indications from the burial context suggesting that Gok4 was different from other TRB individuals (15, 16), and strontium isotope analyses indicate that Gok4 was born less than 100 km from the megalithic structure, similar to all other analyzed TRB individuals from the area (17). The three Neolithic hunter-gatherer samples were excavated from burial grounds with single inhumation graves on the island of Gotland, Sweden, for which associated remains have been dated to 5300-4400 calBP (16).

We must keep in mind that a limited amount of DNA sequence was extracted, which corresponds to a few tens of thousands of SNPs in common with the best modern SNP set used; this corresponds to ~5% of the genome, with different success rates for the four sampled individuals. We must also not forget that these are farmers and foragers from a single point in space-time, and from the periphery of Europe, so we should be cautious in generalizing about the Neolithic transition in other parts of Europe.

Nonetheless, the new study reveals two important pieces of information:

First, the 3 PWC individuals are strongly differentiated from the single TRB one:

Regardless of the underlying model, our study provides direct genomic evidence of stratification between Neolithic cultural groups separated by less than 400 km, differentiation which encapsulates the extremes of modern-day Europe, and appears to have been largely intact for ~1,000 years after the arrival of agriculture.

So, it appears that these individuals lived at roughly the same time and within a small area of Europe, and yet they are as different from each other as the most distant current European populations are. These were not simply drawn from the same or similar populations, some of them deciding to take up farming while others to practice fishing and hunting. These were different populations who maintained their distinctiveness long after "first contact".

Two models have dominated European prehistory in recent decades: acculturationists claimed that the Neolithic package of domesticated plants and animals was transmitted across the continent while the people largely stayed put, while demic diffusionists claimed that people did move, but -at least in the most popular version of the model- that they gradually intermarried with local hunter-gatherers, forming a genetic cline of ancestry, at the far end of which the farmers were mostly derived from local foragers.

One could very well say that the acculturationist model views prehistoric people as smart folk with no legs, apparently ready to take up a good new idea, but reluctant to leave their birthplace. The demic diffusionist model, on the other hand, viewed them as mindless automata, moving across the landscape with little purpose, marrying who they met, and filling a continent in much the same way that gas molecules end up filling a room into which they are introduced.

Both these models are now revealed to be wrong: rather, it seems that "leapfrog" colonization may be responsible for the spread of agriculture and its associated technologies (such as Megalithism) across Europe. In this model, farmers lept from place to place across the landscape intentionally, preserving their gene pool and largely ignoring the pre-existing foragers of the landscape.

Of course, farmer and hunter eventually did mix, and hunting cultures became extinct. But, this was a process that seems to have been complete after 4,000 years BP. Acculturation did eventually happen, and agriculturalists did eventually diffuse to every corner of Europe. But, these are events that happened after the initial group(s) of pioneers had opened the frontier. In this respect, the colonization of Europe bears some resemblance to the settlement of the Americas by Europeans: it happened by leaps and bounds, and the early waves of explorers and pioneers may have opened the landscape but did not immediately fill it: this happened later as a result of demographic growth and new waves of migration, with the extant populations being differentially descended -in different proportions- from migrants and natives.

The second important point of the new study is the revelation that the single Neolithic individual from northernmost Europe was similar to extant southern Europeans:

To more closely investigate the genetic similarity of extant European populations (22, 24) to Neolithic humans, we determined for each SNP and each extant population the average frequency of the particular allele found in either the Neolithic hunter-gatherers or the Neolithic farmer (16). The Neolithic hunter-gatherers shared most alleles with Northern Europeans, and the lowest allele sharing was with populations from Southeastern Europe (Fig. 3A). In contrast, the Neolithic farmer shared the greatest fraction of alleles with Southeastern European populations (Cypriots and Greeks), and showed a pattern of decreasing genetic similarity for populations from the Northwest and Northeast extremes of Europe (Fig. 3B). Individuals from Turkey stand out by low levels of allele sharing with both Neolithic groups, possibly due to gene flow from outside of Europe, but all other European populations can roughly be represented as a cline where allele sharing with Neolithic hunter-gatherers is negatively correlated with allele sharing with Neolithic farmers (Fig. 3C). 

Panel C from the allele sharing figure (left) suggests why we should be cautious about trying to reconstruct European prehistory on the basis of a simple 2-way model of admixture between farmers and hunters.

It is true that extant European populations do fall on a clear cline between them that is strongly significant (R=-0.58, p=0.0029). This means is that they are different to each other in the same ways that farmers/hunters were different from each other. But, this still leaves about 2/3 of the variance unexplained: this may be partly due to the "noise" added by the small number of SNPs, and partly by the contribution of other ancestral groups to extant variation. One of these groups may be the east Eurasian element which must contribute to the differentiation of Turks from Europeans. But, there were probably other West Eurasian elements not represented by the two Neolithic groups: the Mesolithic Pitted Ware individuals have been previously assigned predominantly to mtDNA haplogroup U, which forms a minority in extant Europeans; and a handful of Neolithic samples (LBK, Oetzi, Treilles) have failed to turn up any signs of the dominant R1 Y-haplogroup of extant Northern Europeans. There must be other actors to be revealed in the unfolding story of European origins.

A strong hint for this can also be found in the quite unexpectedly low "TRB" allele sharing of groups from the Northwestern Balkans. This is quite unexpected, as the area is widely believed to be a conduit through which agriculture spread into Central Europe. It is also an area with world maxima of Y-haplogroup I, a lineage which may be a remnant of Paleolithic Europeans, and correspondingly low levels of haplogroups that appear to have arrived later into Europe.

Another important point is that levels of allele sharing between these Neolithic individuals and modern Europeans is generally lower than between most pairs of modern European populations. This is, in part, expected, since the Neolithic specimens are separated by modern populations by ~5ky of evolution, but may also be due to the contribution of unsampled groups to the ancestry of the latter.

From the paper:

We found that compared to a worldwide set of 1,638 individuals (21-23), all four Neolithic individuals clustered within European variation (Fig. S5). However, when focusing the analysis on 505 individuals of European and Levantine descent, the three Neolithic hunterg atherers appeared largely outside the distribution of the modern sample, but in the vicinity of Finnish and northern European individuals (Fig. 1A). In contrast, the Neolithic farmer clustered with southern Europeans, but was differentiated from Levantine individuals. This general pattern persisted for a geographically broader reference data set of 1,466 extant individuals of European ancestry (22, 24) (Fig. 1B), for a much larger number of markers from 241 individuals in the 1000 genomes project (25) (Fig. 1C), and using model-based clustering (26, 27) (Fig. 1D). Although all Neolithic individuals were excavated in Sweden, neither the Neolithic farmer nor the Neolithic hunter-gatherers appeared to cluster specifically within Swedish variation, a pattern that remained also for a larger sample of 1,525 individuals from across Sweden (28) (Fig. S9, Fig.S21-22).

I will try to perform an analysis of these 4 Neolithic Europeans, as I did with the Iceman, and see how they relate to a larger number of populations: for example, the Mesolithic hunter-gatherers have the highest allele sharing with Poles: do they share even more with Lithuanians and other Baltic peoples? The Neolithic farmer is by far closer to Cypriots: are there any populations of the Near East that are close to it as well?

Hopefully, in the near future we may get our first glimpses of genuine Mesolithic Europeans:

In our genomic analyses, the Scandinavian Neolithic hunter-gatherers (PWC) have a genetic profile that is not fully represented by any sampled contemporary population (Fig. 1), and may thus constitute a gene pool that is no longer intact or that no longer exists. While the origin of the Neolithic hunter-gatherers is contentious, the similar mtDNA haplogroup composition of PWC individuals (8) (Table 1) and Mesolithic- and Paleolithic individuals (7, 29) indicate some continuity with earlier European populations, but resolving this hypothesis will require pre-Neolithic genomic data.

The continuity between Mesolithic and Neolithic hunter-gatherer populations in the Baltic is supported by craniometric analysis from a recent paper (left), but it is definitely worth investigating whether -despite their strong differentiation- the Neolithic farmers and foragers of Sweden may not have already started -at least partially- the process of amalgamation.

Hopefully we can soon extract more DNA from other Neolithic Europeans, as well as pre-contact European foragers. It is probably in the Copper and Bronze Ages that we are to encounter some the remaining players that formed the European genetic landscape and witness how they all combined to form the proto-historical and recent Europeans.

A Postscript:

Until recently, it had become commonplace in archaeology to seek local origins for most archaeological phenomena. Three years ago, I pointed out that new evidence was pointing towards a major migrationism comeback in our understanding of European prehistory. So, it is worth reviewing what was once thought about the people buried in Swedish megalithic monuments. From Carleton Coon's The Races of Europe, (1936) Chapter IV):

In Sweden, out of twenty-four male crania found in passage graves, only one was brachycephalic; for the most part a pure Long Barrow type is represented. (Section 12) 

The Megalithic Long Barrow people must have come by sea, and they probably came from somewhere in the Mediterranean. (Section 10)

The paper is also discussed in the weekly Science podcast. The supplementary materials are freely available.


Science 27 April 2012: Vol. 336 no. 6080 pp. 466-469 DOI: 10.1126/science.1216304

Origins and Genetic Legacy of Neolithic Farmers and Hunter-Gatherers in Europe

Pontus Skoglund1,*, Helena Malmström1, Maanasa Raghavan2, Jan Storå3, Per Hall4, Eske Willerslev2, M. Thomas P. Gilbert2, Anders Götherström1,5,*,†, Mattias Jakobsson

The farming way of life originated in the Near East some 11,000 years ago and had reached most of the European continent 5000 years later. However, the impact of the agricultural revolution on demography and patterns of genomic variation in Europe remains unknown. We obtained 249 million base pairs of genomic DNA from ~5000-year-old remains of three hunter-gatherers and one farmer excavated in Scandinavia and find that the farmer is genetically most similar to extant southern Europeans, contrasting sharply to the hunter-gatherers, whose distinct genetic signature is most similar to that of extant northern Europeans. Our results suggest that migration from southern Europe catalyzed the spread of agriculture and that admixture in the wake of this expansion eventually shaped the genomic landscape of modern-day Europe.

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