European hunter-gatherers were mostly replaced, but not totally. And they were neither black nor white

Peter Frost over at his blog has a long post on the transition to agriculture and pastoralism in Northern Europe.

He tagged me on Twitter, so presumably, he’s soliciting my opinion/response.

The post starts off with a quick reference to the attempt to leverage massive replacement in Northern Europe eight to four thousand years ago in the interests of contemporary politics. I’m not going to address that because I’m not very interested in how these topics relate, and I won’t post comments (or will delete) that engage with that. I will focus on the science.

First, I tried to leave a comment on his weblog and blogger ate it. So I’m just going to put a post here in the interests of open exchange. I also think many readers here have some of the same opinions as Peter, or suspicions, so it might be best to clear things up.

I don’t think his Peter’s argument can really be understood without reading his 2006 paper, European hair and eye color: A case of frequency-dependent sexual selection? My opinion in regards to this hypothesis is that I think it’s probably wrong and I’m skeptical. More skeptical than I was when I first read the paper because we have more understanding of the process of the settlement of Europe during the late Pleistocene and early Holocene. But, there is still a small window for it to be correct, as one can see in Peter’s post.

The argument hinges a lot on the pigmentation profiles of proto-European groups based on predictions from algorithms which use modern Europeans as a training set. These predictions are in the papers themselves, so Peter isn’t doing anything that the authors didn’t do. But, I have come to the conclusion that they’re probably not trustworthy. These ancient populations were very different from modern Europeans, and their genetic architecture for pigmentation may have been different (modern Europeans are a compound of several groups).

Though Mesolithic Western European hunter-gatherers were probably darker in complexion than modern Europeans, I believe it is likely that they were not nearly as dark as pigmentation prediction algorithms suggest. Second, it is true that alleles correlated with blonde hair in Europeans within the KITLG locus are found in Siberia nearly 20,000 years ago. But it is not true that “Ancient DNA from Afontova Gora has shown that people had blond hair in mid-Siberia as early as 18,000 years ago.”

What has been found is that Europeans who carry the derived variant at rs12821256 are more likely to have blonde hair. Those who are heterozygote are twice as likely, while homozygotes are four times as likely. At least against the population base rate. The frequency in Scandinavia of the derived variant is ~20%. Many blonde people don’t have the derived variant. And, not all people who have the derived variant have blonde hair.

Of my three children two are heterozygotes for the derived variant (they carry one copy). Probably not coincidently these two have lighter hair than the third. But neither are really blonde, though perhaps they are blond(ish) during certain times of the year. More accurately their hair is probably sandy brown. Why? I’m their father, and as a normally complected South Asia, I give them a host of alleles at other loci which make them different from the typical European genetic architecture of pigmentation.

As I said earlier Peter can’t really be blamed for making these inferences because they are in the scientific literature themselves. But just because they’re there doesn’t make them true (though I do think Peter should be careful about extrapolating from odds ratios against a particular base rate probability to some deterministic relationship).

A final issue is the idea that the alleles that define modern Northern European pigmentation were present in Scandinavian and Eastern European hunter-gatherers. This is correct. But again, modern prediction algorithms are trained groups with modern genetic backgrounds. In mixed populations, the largest effect QTLs explain only half the variance in pigmentation. The rest of it is accounted for by “genomic ancestry”, which basically means there are loci associated with ancestral groups that haven’t been discovered yet. But a second and more important issue is that the frequency of some the alleles in modern Northern European groups is different from what you find in the ancient ones. The ancestral variant on SLC24A5 is almost impossible to find in Northern Europe in indigenous people today (in Europeans the ancestral variant is most often found in Spain, due to admixture with Africa during the Moorish period). I don’t need to review the literature, but there is evidence for a fair amount of selection on these loci within the last 4,000 years. Even SHG and EHG still segregated ancestral variants at higher frequencies that modern Europeans.

The second major theme in the blog post has to do with hunter-gatherer ancestry. There’s a section on haplogroup U where Peter suggests that its disappearance is due to selection, not a replacement. U is associated with hunter-gatherer ancestry. This may be true, but mtDNA and Y need to be interpreted cautiously in any case (both R1b and R1a are far more common than one might predict from autosomal distributions of the ancestry of populations in which they were originally found).

Then there is the argument that bottlenecks/founder effects and natural selection might have skewed our estimates. I don’t really get the former argument at all:

Founder effects may be another causal factor. When bands of hunter-gatherers are given the opportunity to adopt farming, most of them turn up their noses and only a few will make the change. Because those few bands are not perfectly representative of the hunter-gatherer gene pool, and because their numbers may increase many times over (thanks to the increase in food supply) the resulting founder effects will be substantial.

These are verbal models, and unpersuasive to anyone who has looked at the data and generated results. Mesolithic hunter-gatherers were a genetically homogeneous lot to begin with. They didn’t have all this variance to sample from. There was later increase in hunter-gatherer ancestry into European farmers from demographic reservoirs, but the argument about founder effect doesn’t work because the two groups are so different that playing around with biasing the sample from which one mixes does not change the overall result. Replace hunter-gatherer and farmer with “Ashkenazi Jew” and “Chinese.” The latter two groups have some variance, but a bottleneck on one isn’t going to change one’s estimate of admixture in a daughter population.

The issue about selection suffers from the problem that the magnitude would have to be too large and extensive across the whole genome to reshape hunter-gatherers in this manner to be plausible. One might imagine a case where gene flow and selection on parts of the genome from the donor group inflates the donor group proportion…but I don’t think that’s Peter’s point? Theoretically, a model of admixture followed by sweeps around one population’s ancestry component is possible, but I don’t think we see evidence of that in the ancient DNA.

In any case, though the verbal argument seems reasonable on first blush, the models and dynamics don’t work out.

Peter ends:

Some of the confusion in this debate may arise from the assumption that “late hunter-gatherers” formed a single group in Europe. In fact, there were at least three such groups (WHGs, SHGs, EHGs), whose genetic profiles significantly differed from each other and whose fates were likewise different. WHGs were an evolutionary dead end. They were replaced. The same cannot be said for the hunter-fisher-gatherers of Scandinavia and the Baltic, who were able to achieve high population densities by exploiting marine resources (Price 1991). With them we see more genetic continuity than rupture, and it is possible that some genetic characteristics formerly ascribed solely to “Anatolian” farmers were in fact of SHG origin.

The people who are making the assertions that Peter is rebutting are not confused as to the nature of the populations which they named and which they modeled. Peter can download the data and replicate the analyses himself. WHG, SHG and EHG seem to exist on some sort of continuum, with post-“Villabruna cluster” ancestry at one end of the spectrum and post-Ancestral North Eurasian (ANE) ancestry at the other. WHG is mostly descended from ancestors of the Villabruna cluster, who share a common ancestry derived from late Pleistocene West Eurasians with Anatolian farmers (the latter of whom admixed with Basal Eurasians). EHG is a mix of the same Villabruna people (or at least their eastern fringe), but with a preponderance of ANE-like ancestry. SHG is between these two groups.

It also seems that European hunter-gatherers sometime in the late Pleistocene and or early Holocene recieved a small but detectable pulse of East Asian ancestry. Also, commonly shared haplotypes with West Asians on SLC24A5 (SHG and EHG) and EDAR with East Asians (SHG) indicates some gene flow with other places (though I believe SHG has no detectable East Asian ancestry).

Finally, there is much discussion of a late occupation of Northeast Europe by farmers. Since I predicted this 10 years ago I don’t have much objection to this section…except I don’t think that it supports his other points at all. That is, the persistence of hunter-gatherer populations around the Baltic does not mean that hunter-gatherers were more similar to farmers than we might think, nor does it reject the likelihood of total replacement in many areas of Europe to the south.

The overall conclusion here is two-fold:

  1. The assertions about pigmentation are not necessarily wrong, but they are far weaker based on the data that might be inferred from the post. Additionally, modern Europeans have lots of evidence of recent selection and allele frequency change at several of these loci.
  2. The assertions about very large misestimations of inferred mixing proportions are probably wrong.

9 thoughts on “European hunter-gatherers were mostly replaced, but not totally. And they were neither black nor white

  1. Nobody can scientifically deny that Europe is a melting pot since LGM with two important invasions: neolithic farmers from Anatolia (and the Southern Levant?) and pastoralists from the Pontic steppe. The faces in contemporary Europe are faces shaped by these developments.

    I don’t see Peter Frost denying what can’t be denied.

    What impresses me mostly is his insistence on the importance of fishing. Where hunter-gatherers were primarily fisher-gatherers reluctance against the Early farmer package was strongest – for good reasons I learnt from Broodbank. Insofar I follow Peters deduction farther than you, Razib. He may, in sum, be proven quite right about north-eastern Europe. We shall see.

  2. I feel like he’s clutching at straws, and not being exactly truthful either.

    eg He says “..long before farming, the phenotype was already fully modern. This has been shown by ancient DNA from Scandinavian and Eastern hunter gatherers“… but:

    The Gunther et. al. paper found SLC45A2 at ~22%, and SCL24A5 at 50% in the new SHG samples. The original Motala were about 70% and 80%, but combined with the new samples they report overall SHG frequencies of 55% SLC45A2 and 62% SLC24A5.

    The Mittnik et al. East Baltic samples show about 30% SLC45A2 and 75% SLC24A5 for the 12 individuals he refers to.

    … “fully modern” would be more like 80%/100% – like we see in the Baltic Bronze Age.

  3. He may, in sum, be proven quite right about north-eastern Europe.

    as i said in the post, i said the same stuff about northeast europe 10 years ago. so why is he right and i’m wrong? also, i’ve talked extensively about the importance of fishing.

    again, none of that really speaks to his argument (which is somewhat vague on the numbers anyway).

  4. … “fully modern” would be more like 80%/100% – like we see in the Baltic Bronze Age.

    a dumb proto-frog-nazi used to leave comments where he just didn’t bother to read the paper and would say qualitative stuff like peter (‘all the alleles were there’!).

    the distinguishing thing about modern europeans is the high frequency at these loci. even west asians have higher freq. than the ancient hunter-gatherers at these positions.

  5. Frost seems to be repeating a theory that he’s been working on for a while now, only the recent genetic findings have basically made him move his “homeland” more to the east and north, from what I can understand, but he’s a bit vague and playing a bit loose with the specifics – geographic and otherwise.

    As for SHG-specific ancestry, no modern population seems to have that much of it, certainly less than EEF ancestry whether the latter was carried there in the Neolithic or via roundabout ways in the Chalcolithic which archaeologists already knew in a sense for the Baltic, aDNA just confirmed it. The SHGs right now seem to be even more of a “dead-end” than the WHGs.

    Since Peter mentions politics prominently in the intro, we could say he does similar stuff with his rather tenuous conclusions, a bias towards having the “Northern European” phenotypic-genotypic package as early and as close as possible in specifically his “Northwest” Europe. I don’t think he’s fully assimilated the aDNA results since much of what he writes seems a bit confused.

    Even if he’s somehow right, he will likely be for reasons he hasn’t come up with as far as I can tell and more in line with what you wrote. That being said, I’m receptive to his idea that population replacement might be bit exaggerated, at least in the more popular disseminations of these findings. We generally see a resurfacing of what seems like local ancestry in later samples to a degree, which quite possibly means that some of the earlier samples covering transitional periods have a potential bias to newcomers and the full variation isn’t always captured that well in the average (especially with how sparse the sampling for most areas and periods still is). But at least ongoing admixture seems the rule, even in what some might perceive as the most remote and pristine places, not the exception.

  6. which quite possibly means that some of the earlier samples covering transitional periods have a potential bias to newcomers

    sample bias due to how archaeologists engage in site discovery is a fascinating point.

    it could just be that sedentary farmers are easier to find in the physical record, and this is where ancient DNA is sampled….

  7. the ppl at the reich lab pretty much told me a few years back that SHG is a dead-end. modern HG ancestry being mixed in earlier into expanding pops. but one of my twitter followers told me that one of the baltic sites might indicate 10% admixture of SHG into local pops.

  8. I’m guessing your interlocutor had in mind those in-between HG populations of the Baltic and that’s why he referred to them as SHG?

    From what I recall, the older ones were much closer to the WHG side of the cline compared to Motala and they also seemed to follow the western pattern of pigmentation (light eyes and darker hair and skin) overall so that wouldn’t help the specifically Frost type of argument too much i.e. the modern phenotype potentially evolving in situ in any area west of Russia, outside of Scandinavia (with those populations apparently contributing small amounts overall). There was an increase in EHG type of ancestry in the later Neolithic, likely due to migrations from the eastern forest zone and well, we know the later massive changes that followed Corded Ware. Of interest is that higher HG-type of ancestry continued well into the Late Bronze Age in that area (see sites like Kivutkalns) and has been reduced down to modern times.

    It’s interesting to see this parallel to e.g. the recent South Asia paper playing out with northern Europeans too, with some liking the discovery that the plurality of their autosome is likely due to steppe Indo-Europeans and others trying to downplay it in the interest of deep autochthony (I’ve seen some even more “interesting” stuff floating around). There’s just not as much of a controversy there since those ancient steppe populations carrying a majority of their ancestry from the WHG – ANE cline were overall more similar to modern-day Northern Europeans than e.g. South Asians so they can be easily claimed as “European” if one wants to do so. I’m guessing a Russian, genetically and geographically more similar to the Yamnayans than the rest of us though the result of similarly complex procedures, could just as well claim that his distant ancestors conquered all of us anyway.

  9. Even though I am a natural blonde, and it’s lasted into adulthood, I have the standard variant of rs12821256. Though in what I have, the standard variant is T/T, while the less common variant is C/C.

    So I have the much more common one.

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