Not so fast

Theresa May (Wikicommons) – “Citizens of nowhere”

The overriding lesson ancient DNA teaches is that the population in any one place has changed dramatically many times since the great human post-ice age expansion, and that recognition of the essentially mongrel nature of humanity should override any notion of some mystical, longstanding connection between people and place. We are all, to use Theresa May's derisive label, "citizens of nowhere". (Forbes 2018)

It seems that some pundits are getting tingles from ancient DNA. Still, there is more to this than political spin. Greg Cochran is no fan of Theresa May, and yet he too agrees with the above narrative— as late as 10,000 years ago nobody in Europe looked like the modern Dutch (Cochran 2018). As he sees it, Europeans were transformed beyond recognition during the last ten millennia, specifically by two demographic events:

1. The native hunter-gatherers of Europe were largely replaced by farmers from Anatolia, i.e., from the Middle East.

2. There then came another wave of demographic replacement. Warriors from the Pontic steppe spread out over Europe, killing the men and taking their women.

What do I think? In my opinion, there were indeed migrations in European prehistory, and these migrations led to some populations replacing others to varying degrees. But the magnitude of replacement has been exaggerated. This is partly due to misreading of ancient DNA data and partly due to contrary data being ignored. Let me explain myself.

What did Europeans look like before farming?

First, the modern European phenotype—pale skin with various hair colors (red, blond, black) and eye colors (blue, green, brown)—was already in place 10,000 years ago, and probably several thousand years earlier.

It didn't exist throughout Europe. Western Europeans had a combination of dark skin, dark hair, and blue eyes until very late in time. This we know from DNA retrieved at hunter-gatherer sites in Western Europe: Cheddar Gorge in England (11,000 BP), Loschbour in Luxembourg (8000 BP), and La Braña in Spain (7000 BP) (Brace et al. 2018; Lazaridis et al. 2014; Olalde et al. 2014). Dark skin persisted even after hunting and gathering gave way to farming, as attested by a Neolithic individual from England, nicknamed 'Sven,' who lived 4,000 to 5,000 years ago: "Sven most likely had intermediate to dark skin pigmentation, brown eyes and black possibly dark brown hair" (Brace et al. 2018). Sven lived just before the dawn of European history, being almost a contemporary of Hammurabi.

We get a different picture, however, from the ancient DNA of hunter-gatherers in northern and eastern Europe. There, long before farming, the phenotype was already fully modern. This has been shown by ancient DNA from Scandinavian and Eastern hunter gatherers:

Norway/Sweden, 9500-6000 BP, 7 individuals: light skin, blue eyes, light brown eyes (Günther et al. 2018)

Sweden (Motala), 8000 BP, 7 individuals: light skin ("predominantly" derived alleles), red hair, blond hair, blue eyes (Anthrogenica 2015; Mathieson et al. 2015)

East Baltic, 7460-5360 BP, 12 individuals: light skin, blue eyes (Mittnik et al. 2018)

Russia (Karelia), 7500-7000 BP, 1 individual: light skin, dark hair, brown eyes (Eupedia 2015)

Russia (Samara), 7500-7000 BP, 1 individual: light skin, blond hair, blue eyes (Eupedia 2015).

The latest study from Scandinavia notes the contrast between Scandinavian hunter-gatherers (SHGs) and Western hunter-gatherers (WHGs):

The genomic data further allowed us to study the physical appearance of SHGs; for instance, they show a combination of eye color varying from blue to light brown and light skin pigmentation. This is strikingly different from the WHGs—who have been suggested to have the specific combination of blue eyes and dark skin and EHGs—who have been suggested to be brown-eyed and light-skinned. (Günther et al. 2018)

We have less data on physical appearance from earlier times. Ancient DNA from Afontova Gora has shown that people had blond hair in mid-Siberia as early as 18,000 years ago. Using inferential methods, one research team has estimated that light skin first appeared 19,000 to 11,000 years ago (Beleza et al., 2013) and another has estimated 19,200 to 7,600 years ago (Canfield et al., 2014). The modern European phenotype seems to have taken shape during the last ice age, probably 20,000 to 15,000 years ago within an area stretching from northeast Europe to mid-Siberia. This new phenotype died out in northern Asia, probably at the height of the last ice age, and became confined to northeast Europe. It later spread to the rest of the continent not long before historic times.

Did farmers replace native Europeans?

Doesn't ancient DNA show that European hunter-gatherers were largely replaced by Middle-Eastern farmers from Anatolia? That seems to be the accepted wisdom. Ancient DNA shows a lack of genetic continuity between late hunter-gatherers and early farmers in central and western Europe. Using mtDNA, Skoglund et al. (2012) estimated Anatolian admixture at 95% in Sardinians, 52% in northwest Europeans, 31-41% in Swedes, and 11% in Russians. Not surprisingly, this finding has been cited to show that Europeans are not even native to their own continent. "We're all citizens of nowhere."

More surprisingly, this finding also suggests a strange path of phenotypic evolution: northern Europeans evolved their current phenotype before the farmers came, then lost it to some extent, and then regained what they had lost in a short span of time. When Anatolian farmers moved into that region some 6,000 years ago, the resulting admixture (30 to 50%) would have greatly reduced the population frequencies of blue eyes, blond hair, and red hair in the native population. Only 3,000 years remained between that time and the earliest historical records to allow these population frequencies to bounce back to their former values. Possible? Only if you assume very strong selection for all of these traits.

Let’s take a closer look.

The case of haplogroup U

If we compare late hunter-gatherers with present-day Europeans, we see that the main change to mtDNA has been the loss of haplogroup U. Today, this haplogroup reaches high levels only among the Saami of Finland and the Mansi of northwestern Siberia, both of whom were hunter-gatherers until recently (Derbeneva et al 2002).

Most studies show a sharp break in the frequency of haplogroup U at the time boundary between late hunter-gatherers and early farmers. Yet, in a study of 92 Danish human remains from the Mesolithic to the Middle Ages, Melchior et al (2010) found high levels of haplogroup U as late as the Early Iron Age—long after the advent of farming. Instead of a sharp break, there was a gradual decline. When Jones et al. (2017) examined ancient DNA from Latvia and Ukraine, they found a similar persistence of haplogroup U across the time boundary between hunting-gathering and farming.

The sharp genetic break of previous studies seems to apply only to central and western Europe, where incoming farmers advanced rapidly through territory sparsely inhabited by hunter-gatherers. This wave of advance then stalled, however, from 7500 to 6000 BP, along a line running from the Low Countries in the West to the Black Sea in the East. North of that line, hunter-gatherers were harder to displace because they had achieved high population densities through an economy based on exploitation of marine resources (Price 1991).

In that part of Europe the loss of haplogroup U is more consistent with slow genetic change through natural selection.  In short, this haplogroup had given hunter-gatherers some kind of benefit, and they lost that benefit when they became farmers. Selection then gradually removed the obsolete haplogroup from the gene pool.

What was the benefit? Different haplogroups provide different trade-offs between thermogenesis and ATP synthesis (Balloux et al. 2009). Haplogroup U is associated with reduced sperm motility, an indication of a shift in energy balance from ATP production to heat production (Montiel-Sosa et al. 2006). Being nomadic, hunter-gatherers spend more time in the cold, especially when sleeping in temporary shelters. In contrast, farmers are more sedentary, sleep in a warmer environment, and have less need to raise body temperature at the expense of ATP production.

Although the decline in haplogroup U explains most of the mtDNA gap between hunter-gatherers and farmers, the two groups still differ genetically in other ways. Are these other differences a sign of Anatolian admixture? Perhaps. Or perhaps these differences, too, are caused by adaptation to a new regime of natural selection. No one really knows, and we should not assume that natural selection cannot be a causal factor when it clearly can.

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.

For all these reasons, population replacement is inevitably overestimated if it becomes the only explanation for genetic differences in early Europe between hunter-gatherers and farmers.

Transition from hunting and gathering to farming in the East Baltic

Lazaridis et al. (2014) estimated Anatolian farmer admixture in East Baltic peoples at 30%. This is less than the figure of 52% claimed for northwest Europeans, but it is still substantial. So a measurable signal of admixture should appear when late hunter-gatherers are compared with early farmers in the East Baltic. This comparison has been done by two research teams, and both failed to find any signal of Anatolian admixture. Jones et al. (2017) noted this absence in their study of ancient DNA from Latvia:

It is striking that we did not find evidence for early European or Anatolian farmer admixture in any of our Latvian Neolithic samples [...]. This lack of admixture is also supported by the mitochondrial haplogroup of the Latvian Neolithic samples (all belong to U; Figure 1), which is prevalent in European hunter-gatherers, including our Latvian Mesolithic samples, but not in early farmers.

[...] The emergence of Neolithic features in the absence of immigration by Anatolian farmers highlights the roles of horizontal cultural transmission and potentially independent innovation during the Neolithic transition. (Jones et al. 2017)

The first evidence of Anatolian admixture in the East Baltic appears much later, in the Bronze Age (Jones et al. 2017).

Mittnik et al. (2018) similarly found no evidence of such admixture during the transition to farming in the East Baltic. They ascribed the Anatolian admixture in present-day DNA to limited gene flow after the Bronze Age. They also found, however, that some of this “admixture” was already present in the earlier hunter-gatherers:

One Narva individual, Spiginas1, dated to ca. 4440-4240 calBCE, belongs to a mitochondrial haplogroup of the H branch, normally associated with the Neolithic expansion into Europe, but shows no evidence of Neolithic farmer ancestry on the nuclear level suggesting that this haplogroup might have been present already in foraging groups. (Mittnik et al. 2018)

It seems that some aspects of the Anatolian genetic profile were already shared with Scandinavian/Baltic hunter-gatherers. How did this come about? Perhaps there was trade between farmers and SHGs, including human merchandise—much like the later trade in Slavic women with the Middle East. Or perhaps the Anatolian farmers shared common ancestry with some hunter-gatherer groups (SHGs and EHGs) but not with others (WHGs). Perhaps these farmers had originated in an earlier southward expansion of the same hunter-gatherer groups toward the Black Sea and into Anatolia.

What about the Indo-European expansion?

In northern Europe, ancient DNA does show a demographic expansion by a Pontic steppe people called the Yamna culture (commonly identified with proto-Indo-Europeans). This expansion should have strongly impacted the people of Latvia and Ukraine, who indeed show signs of Yamna admixture. Even there, however, there is more continuity than rupture between hunter-gatherer and farmer samples (Jones et al. 2017).

Again, the same objection applies here as it does to Anatolian farmer admixture. Any estimate of Yamna admixture will tend to be an over-estimate because it is difficult if not impossible to exclude genetic differences due to other causes, notably adaptation to a new regime of natural selection, as well as founder effects. 

Whenever I raise this objection, the usual reply is that the length of time between late hunter-gatherers and early farmers is too short for significant change by any causal factor except admixture from an outside source. This is untrue in the case of founder effects. It is also untrue in the case of a change in natural selection, which can produce significant effects over any time interval longer than ten generations.

One might object that founder effects can be ignored because they are random, i.e., they cannot produce the sort of directional genetic change that is caused by admixture from an outside source. Unfortunately, some of this random change will point in the "right" direction and be thus misattributed to admixture. The likelihood of this error increases if one is looking for admixture from two possible sources, i.e., Anatolian farmers and Yamna pastoralists.

Conclusion

Farming began some 10,000 years ago in the Middle East and entered Europe from the southeast. As farming advanced farther and farther into Europe, the farmers at the "front" became less and less Anatolian through intermixture with native hunter-gatherers. This was especially so during the long period (7500-6000 BP) when the wave of advance stalled along a line running from the Low Countries to the Black Sea. The last push, particularly into the East Baltic and Ukraine, was much more a cultural change than a genetic one.

Indeed, estimates of Anatolian admixture seem to be inflated across all of northern Europe. It is often stated that population replacement must have happened because we see a sharp genetic break at the time boundary between late hunter-gatherers and early farmers. Yet the break seems to apply only to central and western Europe, where there was indeed a fairly rapid replacement of hunter-gatherers by incoming farmers. Ancient DNA from Denmark and the East Baltic shows no sharp break (Jones et al. 2017; Melchior et al. 2010; Mittnik et al. 2018).

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.

As for the Yamna expansion, it does seem to be a real genetic event, although even here we find more continuity than rupture. Again, estimates of admixture will tend to be overestimates because of concurrent genetic change due to natural selection and founder effects.

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