Ancient Europeans: isolated, always on the edge of extinction

A few years ago I suggested to the paleoanthropologist Chris Stringer that the first modern humans who arrived in Europe did not contribute appreciable ancestry to modern populations in the continent (appreciable as in 1% or more of the genome).* It seems I may have been right according to results from a 2016 paper, The genetic history of Ice Age Europe. The very oldest European ancient genome samples “failed to contribute appreciably to the current European gene pool.”

Why did I make this claim? Two reasons:

1) 40,000 years is a long time, and there was already substantial evidence of major population turnovers across northern Eurasia by this point. You go far enough into the future and it’s not likely that a local population leaves any descendants. So just work that logic backward.

2) There was already evidence of low population sizes and high isolation levels between groups in Pleistocene and Mesolithic/Neolithic Europe. This would again argue in favor of a high likelihood of local extinctions give enough time.

This does not only apply to just modern humans, descendants of southern, likely African, populations. Neanderthals themselves show evidence of high homogeneity, and expansions through bottlenecks over the ~600,000 years of their flourishing.

The reason that these dynamics characterized modern humans and earlier hominins in northern Eurasia is what ecologists would term an abiotic factor: the Ice Age. Obviously humans could make a go of it on the margins of the tundra (the Neanderthals seem less adept at penetrating the very coldest of terrain in comparison to their modern human successors; they likely frequented the wooded fringes, see ). We have the evidence of several million years of continuous habitation by our lineage. But many of the ancient genomes from these areas, whether they be Denisovan, Neanderthal, or Mesolithic European hunter-gatherer, show indications of being characterized by very low effective population sizes. Things only change with the arrival of farming and agro-pastoralism.

For two obvious reasons we happen to have many ancient European genomes. First, many of the researchers are located in Europe, and the continent has a well developed archaeological profession which can provide well preserved samples with provenance and dates. And second, Europe is cool enough that degradation rates are going to be lower than if the climate was warmer. But if Europe, as part of northern Eurasia, is subject to peculiar exceptional demographic dynamics we need to be cautious about generalizing in terms of the inferences we make about human population genetic history. Remember that ancient Middle Eastern farmers already show evidence of having notably larger effective population sizes than European hunter-gatherers.

Two new preprints confirm the long term population dynamics typical of European hunter-gatherers, Assessing the relationship of ancient and modern populations and Genomics of Mesolithic Scandinavia reveal colonization routes and high-latitude adaptation. The first preprint is rather methods heavy, and seems more of a pathfinder toward new ways to extract more analytic juice from ancient DNA results. Those who have worked with population genomic data are probably not surprised at the emphasis on collecting numbers of individuals as opposed to single genome quality. That is, for the questions population geneticists are interested in “two samples sequenced to 0.5x coverage provide better resolution than a single sample sequenced to 2x coverage.”

I encourage readers (and “peer reviewers”) to dig into the appendix of Assessing the relationship of ancient and modern populations. I won’t pretend I have (yet). Rather, I want to highlight an interesting empirical finding when the method was applied to extant ancient genomic samples: “we found that no ancient samples represent direct ancestors of modern Europeans.”

This is not surprising. The ‘hunter-gatherer’ resurgence of the Middle Neolithic notwithstanding, Northern Europe was subject to two major population replacements, while Southern Europe was subject to one, but of a substantial nature. Recall that the Bell Beaker paper found that “spread of the Beaker Complex to Britain was mediated by migration from the continent that replaced >90% of Britain’s Neolithic gene pool within a few hundred years.” This means that less than 10% of modern Britons’ ancestry are a combination of hunter-gatherers and Neolithic farmers.

And yet if you look at various forms of model-based admixture analyses it seems as if modern Europeans have substantial dollops of hunter-gatherer ancestry (and hunter-gatherer U5 mtDNA and Y chromosomal lineage I1 and I2, associated with Pleistocene Europeans, is found at ~10% frequency in modern Europe in the aggregate; though I suspect this is a floor). What gives? Let’s look at the second preprint, which is more focused on new empirical results from ancient Scandinavian genomes, Genomics of Mesolithic Scandinavia reveal colonization routes and high-latitude adaptation. From early on in the preprint:

Based on SF12’s high-coverage and high-quality genome, we estimate the number of single nucleotide polymorphisms (SNPs) hitherto unknown (that are not recorded in dbSNP (v142)) to be c. 10,600. This is almost twice the number of unique variants (c. 6,000) per Finnish individual (Supplementary Information 3) and close to the median per European individual in the 1000 Genomes Project (23) (c. 11,400, Supplementary Information 3). At least 17% of these SNPs that are not found in modern-day individuals, were in fact common among the Mesolithic Scandinavians (seen in the low coverage data conditional on the observation in SF12), suggesting that a substantial fraction of human variation has been lost in the past 9,000 years (Supplementary Information 3). In other words, the SHGs (as well as WHGs and EHGs) have no direct descendants, or a population that show direct continuity with the Mesolithic populations (Supplementary Information 6) (13–17). Thus, many genetic variants found in Mesolithic individuals have not been carried over to modern-day groups.

The gist of the paper in terms of archaeology and demographic history is that Scandinavian hunter-gatherers were a compound population. One component of their ancestry is what we term “Western hunter-gatherers” (WHG), who descended from the late  Pleistocene Villabruna cluster (see paper mentioned earlier). Samples from Belgium, Switzerland, and Spain all belong to this cluster. The second element are “Eastern hunter-gatherers” (EHG). These samples derive from the Karelia region, to the east of modern Finland, bound by the White Sea to the north. EHG populations exhibit affinities to both WHG as well as Siberian populations who contributed ancestry to Amerindians, the “Ancestral North Eurasians” (ANE). There is a question at this point whether EHG are the product of a pulse admixture between an ANE and WHG population, or whether there was a long existent ANE-WHG east-west cline which the EHG were situated upon. That is neither here nor there (the Tartu group has a paper addressing this leaning toward isolation-by-distance from what I recall).

Explicitly testing models to the genetic data the authors conclude that there was a migration of EHG populations with a specific archaeological culture around the north fringe of Scandinavia, down the Norwegian coast. Conversely, a WHG population presumably migrated up from the south and somewhat to the east (from the Norwegian perspective).

And yet the distinctiveness of the very high quality genome as inferred from unique SNPs they have suggests to them that very little of the ancestry of modern Scandinavians (and Finns to be sure) derives from these ancient populations. Very little does not mean all. There is a lot of functional analysis in the paper and supplements which I will not discuss in this post, and one aspect is that it seems some adaptive alleles for high latitudes might persist down to the present in Nordic populations as a gift from these ancient forebears. This is no surprise, not all regions of the genome are created equal (a more extreme case is the Denisovan derived high altitude adaptation haplotype in modern Tibetans).

Nevertheless, there was a great disruption. First, the arrival of farmers whose ultimate origins were Anatolia ~6,000 years ago to the southern third of Scandinavia introduced a new element which came in force (agriculture spread over the south in a few centuries). A bit over a thousand years later the Corded Ware people, who were likely Indo-European speakers, arrived. These Indo-European speakers brought with them a substantial proportion of ancestry related to the hunter-gatherers because they descended in major fraction from the EHG (and later accrued more European hunter-gatherer ancestry from both the early farmers and likely some residual hunter-gatherer populations who switched to agro-pastoralism**).

For several years I’ve had discussions with researchers whose daily bread & butter are the ancient DNA data sets of Europe. I’ve gotten some impressions implicitly, and also from things they’ve said directly. It strikes me that the Bantu expansion may not be a bad analogy in regards to the expansion of farming in Europe (and later agro-pastoralism). Though the expanding farmers initial mixed with hunter-gatherers on the frontier, once they got a head of steam they likely replaced small hunter-gatherer groups in totality, except in areas like Scandinavia and along the maritime fringe where ecological conditions were such hunter-gatherers were at advantage ( seems to describe a massive farmer vs. coastal forager war on the North Sea).

But this is not the end of the story for Norden. At SMBE I saw some ancient genome analysis from Finland on a poster. Combined with ancient genomic analysis from the Baltic, along with deeper analysis of modern Finnish mtDNA, it seems likely that the expansion of Finno-Samic languages occurred on the order of ~2,000 years ago. After the initial expansion of Corded Ware agro-pastoralists.

The Sami in particular seem to have followed the same path along the northern fringe of Scandinavia that the EHG blazed. Though they herd reindeer, they were also Europe’s last indigenous hunter-gatherers. Genetically they exhibit the same minority eastern affinities in their ancestry that the Finns do, though to a greater extent. But their mtDNA harbors some distinctive lineages, which might be evidence of absorption of ancient Scandinavian substate.

I’ll leave it to someone else to explain how and why the Finns and Sami came to occupy the areas where they currently dominate (note that historically Sami were present much further south in Norway and Sweden than they are today). But note that in Latvia and Lithuania the N1c Y chromosomal lineage is very common, despite no language shift, indicating that there was a great deal of reciprocal mixing on the Baltic.

Overall the story is of both population and cultural turnover. This should not surprise when one considers that northern Eurasia is on the frontier of the human range. And perhaps it should temper the inferences we make about other areas of the world.

* You may notice that this threshold is lower than the Neanderthal admixture proportions in the non-African genome. Why is this old admixture still detectable while modern human lineages go extinct? Because it seems to have occurred with non-African humans had a very small effective population, and was mixed thoroughly. Because of the even genomic distribution this ancestry has not been lost in any of the daughter populations.

** Haplogroup I1, which descends from European late Pleistocene populations, exhibits a star phylogeny of similar time depth as R1b and R1a.

7 thoughts on “Ancient Europeans: isolated, always on the edge of extinction

  1. Without the ice in northern Scandinavian inland enforcing the coastal route of EHG’s the proportions of WHG and EHG in western and eastern SHG’s would probably be even, or reversed.

    Finno-Samic is, as the wiki says, almost identical to proto-“Finno-Mordvinic” and even proto-Uralic. This means that like Proto-Uralic it wasn’t spoken anywhere near Finland or the Baltic, perhaps in the Volga region, and branches of Uralic languages probably had a star-like expansion during the Bronze Age, to all directions after which they developed independently for often long periods before splitting again. This has strong linguistic support.

    Only a part of the Finnic branch, the one ancestral to Finns, Karelians and Veps, came to Finland and indeed it looks like ~2000 years ago. These also have Saami admixture relative to the rest of Finnic branch – North Estonians and especially South Estonians and Livonians who had less recent contacts with Finland. It took some time after that to “Finnicize” the area based on those Saami-like Iron Age genomes. It follows that Saamis came to Finland earlier (but no earlier than 3000 years ago, according to recent papers on their prehistory), on a different route.

  2. * I tend to put more stock in archaeological dates than estimated genetic dates, and for the reasons articulated in a lengthy and heavily linked post on Finnish history in August of 2014, it appears to me that the beginning of the Finnish Bronze age (ca. 1500 BCE) is a more plausible date for the arrival of Uralic languages in the region than the other potentially plausible date, the beginning of the Finnish Iron Age (ca. 500 BCE), although the case that an Indo-European language probably most closely related to the modern Baltic languages arrived with the Corded Ware people (ca. 2500 BCE) is very solid.

    Both of these dates are quite a bit earlier than the 0 CE estimate for the arrival of the Uralic languages in Finland that your post suggests (and there is really nothing going on in Finland’s archaeological cultures at 0 CE to suggest a dramatic language shift causing cultural transition then in the 400 year period when there is increased trade with the Roman Empire midway through the Finnish Iron Age, until the Germanic migration period begins and starts to have an impact on Finland. Neither Roman trade nor Germanic invasion are likely sources of Uralic language shift).

    The Finnish Iron Age ca. 500 BCE (i.e. 2500 year ago) is a possible source of Uralic in Finland, but probably a less likely one than the Finnish Bronze Age (ca. 1500 BCE to 500 BCE) (which likely resulted in more demic turnover and cultural change), although both 500 BCE and 1500 BCE are dates with some arguable archaeological support.

    * The notion that distinctively Finnish mtDNA populations started to decline when the Corded Ware people arrived, while Corded Ware populations with broadly European mtDNA held steady or grew, told by mtDNA effective population sizes, until 1000 CE, is plausible.

    Notably, whichever date you pick for the arrival of the Uralic languages with a significant demic component, the Uralic immigrants left the distinctively Finnish mtDNA populations no better off than the Corded Ware people who came before them had, and arguably left them worse off, as the steepest decline in this population’s effective population size came between 2000 years ago and 1000 years ago, at a time when Finland was indisputably Uralic language speaking.

    There is a common tendency to assume that Finland was indigenously Uralic, viewing it as a relict outpost of pre-Indo-European languages in Europe (the way the Basque are often viewed), but this is almost certainly not the case.

    Both distinctively Finnish mtDNA populations and Finns with not distinctively Finnish mtDNA saw incredible surges in effective population size starting ca. 1000 CE (60 fold for people with distinctively Finnish mtDNA bringing their effective population size to two-thirds that of people without distinctively Finnish mtDNA in Finland, after having plunged precipitously). This is a time frame that corresponds to Viking colonization (ca. 800 CE to 1025 CE) (many of whom were from Sweden), Christianization (attested from 1150 CE), and expressly Swedish colonization (particularly in the “Northern Crusade” starting in the early 1200s CE).

    Swedes were clearly good for the economy, and perhaps Christianization led to a transition from genocide (on a War Before Civilization model) to assimilation as a policy for the latest wave of migrants to Finland.

    There is also some evidence that terrestrial food production (i.e. farming and herding) had become less important in Scandinavia at some point after its late arrival in the region, only to experience a resurgence ca. 1000 CE. Some of this may have been climate driven, but whatever the reason, it could explain the rapid expansion of effective population sizes for all populations in Finland after 1000 CE.

    * Distinctively Finnish mtDNA which show expansions around the time of the arrival of the Corded Ware people included mtDNA haplogroups traditionally associated with Mesolithic hunter gathers (Finland was completely depopulated and buried under glaciers during the LGM with the earliest Mesolithic humans only returning sometime in the range of 9000 BCE to 7300 BCE) defined as mtDNA U and V, and mtDNA haplogroups traditionally associated with Neolithic farmers (e.g. mtDNA H, J and T — the authors of the study did not suggest an affiliation for the WIX mtDNA haplogroups).

    The authors suggest that it is possible the distinctive farmer mtDNA may have arrived with women who were part of the Corded Ware population, while the Mesolithic hunter-gather mtDNA types may have been present in Finland already when the Corded Ware people arrived, but that non-founder mtDNA types may have been lost due to drift prior to their arrival, while the founder mtDNA types of mtDNA U and V may show an expansion coincident with the arrival of the Corded Ware people because the indigenous population may have expanded at the same time due to cultural interchange with the Corded Ware people and the integration of indigenous women into Corded Ware society.

    If this is the case, then the Mesolithic component of modern Finnish genomes may be higher than one would infer from the inference that the expansion dates of distinctively Finnish mtDNA U and V clades correspond to new migrants to Finland.

    Certainly, lots of indigenous Finnish people who were present when the Corded Ware folk who had genetic diversity not represented in any modern population died off. Lots of ancient Finns have no ancestors today. But, it doesn’t follow from this fact that it isn’t possible that a significant proportion of Finnish ancestry doesn’t derive from some small subset of that ancient Mesolithic Finnish population represented in a significant share of the one-third of Finns who have distinctively Finnish mtDNA (20% by a more strict definition), that did survive.

    The other possibility, of course, is that Mesolithic mtDNA in Finland is derived not from Mesolithic Finns but from Eastern Hunter Gatherer people incorporated into Corded Ware populations. But, in that scenario it is hard to account, for example, for the high levels of mtDNA V in Finnish (and especially Saami) populations in Scandinavia which seems to fit an Atlantic coastal migration pattern extending from a Franco-Cantabrian refugium to all Atlantic Coastal points north and also south into North Africa where it enters the Berber gene pool. Some distinctive mtDNA U clades also seem to follow this pattern.

    Given this analysis, and the points you mention in your posts about Y-DNA I and Mesolithic mtDNA frequencies in Europe, I think that a 1% pre-Neolithic ancestry component for modern Europeans is too low, although your estimate of 10% as a ceiling is probably on target. Don’t forget that initial Neolithic replacement retreated with significant new hunter-gatherer admixture after the collapse of the first farmer Neolithic farming economy at various times around Europe. My guess for pre-Neolithic ancestry in modern Europeans is that it is probably in the mid- to high single digit percentages.

    Also, there are a wide variety of genetic indications that Finns have more Mesolithic ancestry than any other major European population, whatever the Europe-wide average may be.

    Of course, if you go back far enough, and that is only 10,000 years, everyone is a hunter-gatherer, and by the time that the Neolithic revolution started to expand into Europe ca. 6,000 years ago from Anatolia, the Anatolian Neolithic had already incorporated a significant proportion of people who were almost genetically indistinguishable from the European hunter-gatherers whom they would encounter in the course of their expansion. Whether European hunter-gather ancestry genetically indistinguishable from the European hunter gatherers who were mostly replaced in the first wave Neolithic that was incorporated into the melting pot of the first wave of European Neolithic farmers counts as farmer ancestry or Mesolithic hunter-gatherer ancestry is a key definitional question that would dramatically swing the percentage one way or the other depending upon which definition you use.

  3. so re: arrival of finns. it is possible to argue for 1500 BCE, but page down here:

    the latvians <1000 BCE don't have N1c. even though that's as common as r1a among them today. from the preprint: "The spread of N into north-eastern
    Europe was proposed to have happened with speakers of Uralic languages from the
    east who contributed to the male gene pool of eastern Baltic populations and left
    linguistic descendants in the Finno-Ugric languages Finnish and Estonian37,38. As we
    do not see Y-haplogroup N in any of the male samples from Lithuania and Latvia
    dated as late as 230 calBCE we propose that this element was brought into the gene
    pool of the more southern region of the Baltic coast after the Late Bronze Age."

    you have a better grasp of dates and archaeology than i, ~0 is just a rough guess.

    i saw a poster from SMBE with ancient finnish stuff. i don't recall the exact date, but i thought it was from 1000 BCE. it was like corded ware. by 800 AD though there was siberian ancestry. though i'm vague on the dates here, and they are obv. very important.

    a major issue here is local heterogeneity in distribution. wouldn't be surprised if finnic n1c expanded to the indo-european pops relatively late.

  4. ohwilleke, Finnish Bronze Age could fit for the arrival of Saamic in Finland but not Finnic. Too early linguistically (Finnic languages like Finnish, Veps, Livonian and Estonian are so similar that they must have split recently, like Slavic) and the major I1 and N1c clades in Finland (in Finns specifically, Saami Y-DNA hasn’t been sequenced extensively) also expanded around 0 AD. More recently than the N1c found in Balts (closer to 1000 BCE).

  5. Modern DNA may not produce exact dates for expansions, but Yfull seems relatively accurate with their mutation rate. Major R1a clades, the major N1c1 clades found in Europe and I1 all have expansions 2500-3000 BC in their tree. In case of R1a there is ancient DNA to support the dates. The Russian members of the “Rurikid branch” of N1c have their sequences in the tree too, they have shared ancestor around 1000 AD and their next closest relatives are in Sweden, Finland and Estonia.

    The abstract of the Iron Age Finland ancient DNA study in SMBE was public, according to that all the samples were from around 500 AD:

    “Lamnidis, Majander, Salmela et al.
    Abstract: The population history of Finland is subject of an ongoing debate, in particular with respect to the relationship and origins of modern Finnish and Saami people. Here we analyse genome-wide data, extracted from three teeth found in the archaeological site of Levänluhta, in southern Ostrobothnia.
    The site dates back to the Iron Age between 550-800 AD, according to the artefacts recovered, while radiocarbon dating on scattered femurs from the site span 350-730 AD.

    When analysed together with previously published ancient European samples and with modern European populations, the ancient Finnish samples lack a genetic component found in early Neolithic Farmers and all modern European populations today. Instead, we find that they are more closely related to modern Siberian and East Asian populations than modern Finnish are, a pattern also observed in genetic data from modern Saami.

    Our results suggest that the ancestral Saami population 1500 years ago, inhabited a larger region than today, extending as far south as Levänluhta. Such a scenario is also supported by linguistic evidence suggesting most of Finland to have been speaking Saami languages before 1000 AD. We also observe genetic differences between modern Saami and our ancient samples, which are likely to have arisen due to admixture with Finnish people during the last 1500 years.”

  6. thanks for finding that! i definitely garbled it. no ancient samples. so we’re narrowing the window.

    interesting about the Y stuff. i’ve heard good things about Yfull.

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