Monday, January 14, 2019

Unusually diverse

Portrait “Mijke” – Frans Koppelaar (1943 - ). Europeans are unusually diverse for hair color. Over 200 alleles have been identified in British subjects.

Europeans are unusually diverse for hair color. When this diversity was being studied two decades ago, 11 nonsynonymous alleles for hair color had been identified in Europeans, versus 5 in Asians and 1 in Africans (Harding et al. 2000; Rana et al. 1999). The disparity is even greater because the Asian alleles produce pretty much the same hair color.

European hair color is unusual in another way. “Nonsynonymous alleles” make a visible difference and are usually outnumbered by those that don’t. The reverse is true, however, at the main gene for hair color, MC1R, where nonsynonymous alleles outnumber synonymous alleles by a ratio of two to one. 

Rana et al. (1999) concluded that some kind of selection had caused hair color to diversify outside Africa. Harding et al. (2000) disagreed, attributing this diversification to relaxation of selection: as humans spread out of Africa, selection for black hair grew weaker and new hair colors gradually accumulated. Of course, this scenario would require a long span of time: close to a million years to produce the current variability of hair color, including approximately 80,000 years for today's prevalence of red hair alone (Harding et al. 2000; Templeton 2002). 

That is a long time. Given that modern humans left Africa some 60,000 years ago and arrived in Europe only 45,000 years ago, some academics began to argue that Europeans must have inherited their diverse hair colors from the Neanderthals. 

A Neanderthal origin is nonetheless problematic, if only because ancestral Neanderthals and Denisovans separated from ancestral modern humans an estimated three quarters of a million years ago (Rogers et al. 2017). Well, perhaps that's close enough to the above estimate of one million years ago. Another problem: when Ding et al. (2017) examined alleles for red hair, they identified only one as being of Neanderthal origin; the others apparently arose among modern humans. Finally, even if the different alleles for hair color had been introduced through Neanderthal admixture, some kind of selection would have still been needed to increase their frequency in the European gene pool, which is only 1 to 4% of Neanderthal origin.

With enough hand-waving, one can explain the many hair colors of Europeans in terms of relaxation of selection and Neanderthal admixture... as long as there are only a dozen alleles to explain away. A recent study, however, has found a lot more:

We report here the analysis of the majority of UK Biobank, a total of almost 350,000 subjects. By performing genome-wide analyses across hair colours, we have discovered novel variation in and around MC1R that contributes to red hair. [...] Furthermore, we identify more than 200 genetic variants independently associated with multiple hair colours on the spectrum of blond to black. (Morgan et al. 2018)

More than two hundred! If these alleles were due to relaxation of selection we would have to assume they had slowly accumulated over tens of millions of years—a time span longer than the existence of all hominids. Clearly, the facts call for another explanation: some kind of selection created these numerous hair colors, and very strong selection at that. 

This selection operated relatively fast and over a relatively small geographic area, while also causing eye color to diversify at the same time. Ancient DNA shows that most Europeans had only black hair and brown eyes until seven thousand years ago, and perhaps later still. Previously, the other hair and eye colors existed only in humans from Scandinavia, the East Baltic and, apparently, areas farther east (Günther et al. 2018; Mittnik et al. 2018). 

In fact, the oldest genetic evidence of blond hair, dated to 18,000 years ago, comes from the site of Afontova Gora in central Siberia (Mathieson et al. 2018, p. 52). At sites in south-central Siberia dating from the third millennium B.C. to the fourth century A.D. we find that most individuals had blue or green eyes and blond, red, or brown hair (Bouakaze et al. 2009). This finding is consistent with old Chinese records, which mention south Siberian peoples with "green eyes" and "red hair" (Keane 1886, p. 703).

The evidence thus suggests that the current European phenotype came into being during the last ice age 10,000 to 20,000 years ago on the plains stretching from the Baltic to central Siberia. But why would a cold, open environment select for a diverse palette of hair and eye colors? Apparently, this was not natural selection by the steppe-tundra environment; it was sexual selection by the accompanying social environment, specifically a mate market where too many women had to compete for too few men. Polygyny was not an option for most men. Almost all of the food was obtained through hunting of big game (reindeer, bison, etc.), and this high meat diet made it too costly for all but the ablest hunters to support a second wife and her offspring. High male mortality further reduced the number of men available for mating. Game animals had to be pursued over long distances and unstable terrain with no alternative food sources (Frost 2006; Frost 2014; Frost, Kleisner, and Flegr 2017).

This new phenotype eventually died out in its eastern range and became confined to the northeast of Europe. From there it spread to the rest of the continent on the eve of recorded history. Only then, not long before the beginnings of ancient Greece, did most Europeans come to look European ... as if they were a cast of actors who had been made up and rushed onto the stage just moments before curtain time.


Bouakaze, C., C. Keyser, E. Crubézy, and D. Montagnon, and B. Ludes. (2009). Pigment phenotype and biogeographical ancestry from ancient skeletal remains: inferences from multiplexed autosomal SNP analysis. International Journal of Legal Medicine 123(4): 315-325.

Ding, Q., Y. Hu, S. Xu, C.C. Wang, H. Li, R. Zhang, et al. (2014). Neanderthal origin of the haplotypes carrying the functional variant Val92Met in the MC1R in modern humans. Molecular Biology and Evolution 31(8): 1994-2003

Frost, P. (2006). European hair and eye color - A case of frequency-dependent sexual selection? Evolution and Human Behavior 27(2): 85-103.

Frost, P. (2014). The puzzle of European hair, eye, and skin color. Advances in Anthropology 4(2): 78-88. 

Frost, P., K. Kleisner, and J. Flegr. (2017). Health status by gender, hair color, and eye color: Red-haired women are the most divergent. PLoS One 12(12): e0190238. 

Günther, T., H. Malmström, E.M. Svensson, A. Omrak, F. Sánchez-Quinto, G.M. Kilinç, et al. (2018). Population genomics of Mesolithic Scandinavia: Investigating early postglacial migration routes and high-latitude adaptation. PLoS Biol 16(1): e2003703. 

Harding, R.M., E. Healy, A.J. Ray, N.S. Ellis, N. Flanagan, C. Todd, et al. (2000). Evidence for variable selective pressures at MC1R. American Journal of Human Genetics 66(4): 1351-1361.

Keane, A.H. (1886). Asia with Ethnological Appendix. London: Edward Stanford.

Mathieson, I., S.A. Roodenberg, C. Posth, A. Szécsényi-Nagy, N. Rohland, S. Mallick, et al. (2018). The Genomic History of Southeastern Europe, Supplementary Information, p. 52. Nature 555: 197-203

Mittnik, A., C-C. Wang, S. Pfrengle, M. Daubaras, G. Zarina, F. Hallgren, et al. (2018). The genetic prehistory of the Baltic Sea region. Nature Communications 9(442)

Morgan, M.D., E. Pairo-Castineira, K. Rawlik, O. Canela-Xandri, J. Rees, D. Sims, A. Tenesa, and I.J. Jackson. (2018). Genome-wide study of hair colour in UK Biobank explains most of the SNP heritability. Nature Communications 9: 5271

Rana, B.K., D. Hewett-Emmett, L. Jin, B.H.J. Chang, N. Sambuughin, M. Lin, et al. (1999). High polymorphism at the human melanocortin 1 receptor locus. Genetics 151(4): 1547-1557.

Rogers, A.R., R.J. Bohlender, C.D. Huff. (2017). Early history of Neanderthals and Denisovans. Proceedings of the National Academy of Sciences 114 (37): 9859-9863, 

Templeton, A.R. (2002). Out of Africa again and again. Nature 416(6876): 45-51.


Marvro said...

Excellent and well researched blog.Would you agree there's strong link between R1a and blond hair origins.In Germany for example Northern/Eastern parts (~20/25% R1a) are visibly more blondish than the Western parts.

Sean said...

If I recall rightly, early on your in your writings on this subject you did place a lot of emphasis on the Baltic as the westermost extent of the original steppe tundra phenotype, did your time in Russia influence that I wonder?

The explanation in this post is the only one that has made sense since John Snow and Charles Darwin. Always a good idea to go back and see what great minds of the past have thought, but science is not about the opposite of Eureka!

Peter Frost said...


It's been proposed that R1a has its origins in an expansion that followed the last glacial maximum, i.e., 15,000 years ago and later. By that time blond hair was already present. It is attested at Afontova Gora in central Siberia (18,000 years ago). Although that's only one data point, and I would like to see more,the current evidence suggests that the modern European phenotype began to develop before the last glacial maximum. Again, I would like to see analysis of more aDNA from that timeframe and earlier.


No, I don't think so. I originally thought that the modern European phenotype could not have developed east of the Urals because the steppe-tundra was colder and drier there (and hence supported a smaller population). It looks like I was wrong on that point. There used to be a variety of hair and eye colors in central Siberia, and then it disappeared less than two thousand years ago (see the paper by Bouakaze et al. 2009). This was incidentally a frequent counter-argument I ran into: if steppe-tundra was key to intense sexual selection of women, why was the evolution of this phenotype limited to Europe?

Clipping Path said...

I m so glad to visit this blog.This blog is really so amazing

Sean said...

Taymyr origin?.

Off topic and millions of years ago, but it concerns Siberia: UV-B–induced forest sterility: Implications of ozone shield failure in Earth’s largest extinction.

Truth Seeker said...

Was there ever blond hair in the Middle East? I've read studies that the ancient Hebrews may have had blond or red hair. But other sources say that European Jews only got it due to European intermixing. The Middle East is brown, so I don't see a reason why the Jewish region (which is even more to the South than Turkey or Syria) would have ever had blondes. Was there something special about Jews that distinguished them from other Middle-Easterners?

Sean said...

Peter, Regarding the NYT piece on Reich. Frederique Valentin's argument was that though they look like Papuans, Vanuatus were descended from Asians not Papuans. Could this be an example of sexual selection?

Sean said...

"Ancient Fennoscandian genomes reveal origin and spread of Siberian ancestry in Europe Broadly, present-day Europeans have ancestors in three deeply diverged source populations: European hunter-gatherers who settled the continent in the Upper Paleolithic, Europe’s first farmers who expanded from Anatolia across Europe in the early Neolithic starting around 8000 years ago, and groups from the Pontic Steppe that arrived in Europe during the final Neolithic and early Bronze Age ~ 4500 years ago. As a consequence, most Europeans can be modelled as a mixture of these three ancestral populations3.

This model, however, does not fit well for present-day populations from north-eastern Europe such as Saami, Russians, Mordovians, Chuvash, Estonians, Hungarians, and Finns..."

de Ruyter said...

Mijke is spelled with only one I.

Nice article, though.

Anonymous said...

Why is the gene for eye and hair color recessive, those being loss of function, when the genes for light skin aren't recessive? Does the latter have some mechanism that isn't loss of function?