Visualizing intra-European phylogenetic distances

Neighbor-joining tree of genetic distances between populations

 

In L. L. Cavalli-Sforza’s The History and Geography of Human Genes he used between population group genetic distances, as measured in FST values, to generate a series of visualizations, which then allowed him to infer historical processes. Basically the way it works is that you look at genetic variation, and see how much of it can be allocated to between groups. If none of it can be allocated to between groups, then in a population genetic sense it doesn’t make much sense to speak of distinctive groups, they’re basically one breeding population. The higher the FST statistic is, the more of the variation is partitioned between the groups.

Roughly this is used to correlate with genetic distance as well as evolutionary divergence. The longer two populations have been separated, the more and more genetic differences they’ll accumulate, inflating the FST value. There are a lot of subtleties that I’m eliding here (see Estimating and interpreting FST: the impact of rare variants for a survey of the recent literature on the topic and pathways forward), but for a long time, FST was the go-to statistic for making phylogenetic inferences on a within-species scale.

Today we have other techniques, Structure, Treemix, fineStructure, and various local ancestry packages.

But FST is still useful to give one a Gestalt sense of population genetic differences. Cavalli-Sforza admits in The History and Geography of Human Genes that European populations had very low pairwise FST, but because of the importance of Europe for sociocultural reasons a detailed analysis of the region was still provided in the text. Additionally, they had lots of European samples (non-European Caucasoids were thrown into one category for macro-group comparisons because there wasn’t that many samples).

Using results from the 2015 paper Massive migration from the steppe was a source for Indo-European languages in Europe, I visualized pairwise genetic distances for European populations, ancient and modern (Han Chinese as an outgroup), on a tree. What the results illustrate is that

  1. Ancient populations were very distinct in Europe from modern ones.
  2. Many modern groups are clustered close together.

The bulk of the population genetic structure in modern Europe seems to have been established in the period between 3000 BCE and 2000 BCE. This is not that much time for a lot of distinctiveness to develop, especially on the geographically open North European plain. I suspect with more and more Mesolithic and early to middle Neolithic DNA we’ll see that some of the modern population structure is a ghost of ancient substrate absorption.

Many of the ethno-national categories that are very significant in recent history, and impact the cultural memories of modern people and their genealogies, have very shallow roots. This does not mean they are not “real” (I don’t know what that’s supposed to mean at all), just that many of the identities which seem so salient to us today may be relatively recent in terms of their significance to large groups of humans….

Crescent over the North Sea

Pew has a nice new report up, Europe’s Growing Muslim Population. Though it is important to read the whole thing, including the methods.

I laugh when people take projections of the year 2100 seriously. That’s because we don’t have a good sense of what might occur over 70+ years (read social and demographic projections from the 1940s and you’ll understand what I mean). Thirty years though is different. In the year 2050 children born today, such as my youngest son, will be entering the peak of their powers.

First, one has to note that these statistics include a lot of people who are what some would term “Muslimish”. That is, they are not religious believers, but have some identification with Muslim culture. That’s explicitly noted in the methods.

The problem with this is that there is a wide range of religious commitment and identification across Europe’s Muslim communities. On the whole, they are more religiously observant than non-Muslims in their nations of residence,  but, for example, British Muslims are consistently more religious than French Muslims on surveys (or express views constant with greater religious conservatism).

Here are the results of a 2006 survey:

  France Britain Germany
Yes, Westerners are respectful of women 77 49 73
Yes, there is a conflict between being devout Muslim and living in modern society 28 47 36
Yes, sometimes violence against civilian targets in order to defend Islam can be justified 16 15 7
Did Arabs carry out 9/11? (yes) 48 17 35
People in Western countries are selfish (yes) 51 67 57
People in Western countries are arrogant (yes) 45 64 48
People in Western countries are violent (yes) 29 52 34
Do you consider yourself Muslim first? (yes) 46 81 66
In my country Muslims are perceived to adopt customs of nation 78 41 30
     

Numbers such as those above indicate even if France and the United Kingdom both have Muslim minorities on the order of 17% of the population, the nature of those populations differs to such an extent that that similarity in value may mislead.

In God’s Continent Philip Jenkins observes that public statistics of Christians often work to exclude cultural Christians, but those of Muslims include cultural Muslims. What many estimates of “Muslims” in the European context do is give a sense of the proportion of the population which is of Muslim background. This is especially true in a nation like France where religious survey data is not collected by government agencies.

Overall I think this data is important to consider, but there’s nothing really new in a qualitative sense. And, it is important to keep in mind the details. It is highly probable that the idea of a European superstate will have faltered by 2050, and each nation will its own Muslim minority, and engage with them differently depending on local values and context. Though Muslims, broadly construed, will form about the same proportion of the French and British general population, I suspect that in Britain the distinction between Muslim and non-Muslim will be much more obvious and strict than in France.

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 The Humans Who Went Extinct). 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 (War Before Civilization 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.