A hair-color allele of Neanderthal origin?

 

Taiwanese aboriginal children, Bunun village (source: Jeremy Kemp). 60-70% of Taiwanese aborigines have a loss-of-function allele at the main hair color gene, MC1R, yet their hair is as black as humans with the original “African” allele. This seems to be a general pattern in Asians. They have fewer MC1R alleles than do Europeans, and the ones they have produce the same hair color.

 

When I first wrote about the puzzle of European hair and eye color, a common explanation was Neanderthal admixture. Modern humans intermixed with Neanderthals in Europe, and one legacy of this intermixture is the high prevalence of non-black hair and non-brown eyes we see in present-day Europeans.

I was skeptical. Scientists had already retrieved mtDNA from the remains of Neanderthals and early modern humans, and there was no discernible genetic continuity between the two. Neanderthal admixture seemed minor and could hardly account for the high proportion of Europeans who deviate from the species norm of black hair and brown eyes (Frost, 2006).

With the sequencing of the Neanderthal genome, it became apparent that some admixture had taken place, but only on the order of 1 to 4% in modern Eurasians. Neanderthals did resemble modern humans in having the same main gene for hair color, i.e., MC1R, but the Neanderthal allele at that gene was unlike any allele in modern humans (Lalueza-Fox et al., 2007). Moreover, there was no evidence of the polymorphism that exists for European hair color. The same allele was present in the two Neanderthal individuals that had been sampled.

That seemed to be the end of the story. A new twist, however, has been added by a recent paper. Ding et al. (2014) have found that one of the MC1R alleles in modern humans (Val92Met) appears to be of Neanderthal origin:

In this paper, we present evidences of Neanderthal introgression encompassing the MSH receptor gene MC1R. Furthermore, our evidences support that the derived allele at the functional variant Val92Met of MC1R (i.e., rs2228479*A) is likely of two origins: the vast majority of haplotypes carrying this allele in the human gene pool is resulted from Neanderthal introgression, while one haplotype (NA19084_a) carrying this allele may be from a recurrent mutation in the AMH linage, double recombination, or biased gene conversion.

This finding is consistent with the theory, first advanced by Gregory Cochran, that archaic admixture made it easier for modern humans to adapt to new environments. To be sure, Val92Met is only one of eleven derived MCIR alleles that exist in modern humans. But Ding et al. (2014) also believe that some of these other MC1R alleles are mosaics of Neanderthal and non-Neanderthal segments. So Neanderthal admixture may have helped European hair color to diversify by providing raw material for selection to act on.
 

A silent allele or a silenced allele?

By itself, Neanderthal admixture cannot explain the unusual diversity of hair color in present-day Europeans. It simply provided some of the raw material for this evolutionary development, and in most cases this raw material had to undergo further changes, through mutation and recombination, before it could become useful.

Indeed, despite being a loss-of-function allele, Val92Met seems to produce the same black hair as the original "African" allele. This may be seen in its geographic distribution: ~5% in Europeans, ~30% in continental East Asians, and 60-70% in Taiwanese aborigines (Ding et al., 2014). It has also been reported in South Asians, Papua-New Guineans, Japanese, and Inuit (Harding et al., 2000). Ding et al. (2014) state that this allele is associated with red hair, but the study they cite found only one individual with Val92Met among the 21 redheads examined (Valverde et al., 1995). This proportion is almost identical to the allele's incidence among Europeans in general. More likely than not, that single individual owed her red hair to an allele somewhere else on her genome.

Hair color is much less diverse in Asians, and this is reflected in lower MC1R diversity. Whereas Europeans have eleven MC1R alleles, Asians have only five, and all five produce the same black hair color (Harding et al., 2000). In short, Asians have fewer alleles and proportionately fewer of these differ phenotypically from the ancestral African allele. It looks as if something downstream prevents these alleles from affecting hair color.

As I've argued elsewhere, Europe's diverse palette of hair and eye colors is due to unusual evolutionary circumstances, i.e., intense sexual selection of women within an ecozone (continental steppe-tundra of the last ice age) where almost all food was obtained through long-distance hunting. The consequently higher death rate and lower polygyny rate among hunters dried up the pool of men available for mating and increased competition by women for mates. Women were more strongly selected for eye-catching traits, particularly bright or novel hues, thus creating an increasingly diverse palette of hair and eye colors (Frost, 2006; Frost, 2014).

This ecozone was more suitable for continuous human settlement in Europe than in northern Asia, where it was farther north and farther removed from the moderating influence of the Atlantic. A site in central Siberia from the last ice age has yielded human DNA that shows strong affinities with present-day Europeans and Amerindians, but much less affinity with present-day northern Asians, who seem to be largely the product of repeopling from the south near the end of the last ice age (Maanasa et al., 2014). Europeans have thus better preserved the legacy of this episode of intense sexual selection.

Perhaps the story ends there. Present-day Asians have preserved less of that MC1R diversity and what they have preserved has less functional significance. Or perhaps that diversity was initially functional and then gradually ceased to be functional … because of some other selection pressure? Perhaps, at the end of the last ice age, there was some non-black hair among northern Asians, though much less than among Europeans. Being less common and thus less normal, and no longer favored by intense sexual selection, there may have been stronger social selection to eliminate deviant hair colors.

A similar kind of social selection might explain why red hair is less common than blond hair among Europeans, i.e., stigmatization of redheads that was ultimately due to a mental association between red hair and menstrual blood (Frost, 2012).

There may be a story behind these "silent alleles." 

 

References 

Ding, Q., Y. Hu, S. Xu, C. Wang, H. Li, R. Zhang, S. Yan, J. Wang, and L. Jin (2014). Neanderthal origin of the haplotypes carrying the functional variant Val92Met in the MC1R in modern humans, Molecular Biology and Evolution, published online June 10, 2014

http://mbe.oxfordjournals.org/content/early/2014/06/02/molbev.msu180.abstract

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

Frost, P. (2012). Why are redheads less common than blondes? Evo and Proud, March 10

http://evoandproud.blogspot.ca/2012/03/why-are-redheads-less-common-than.html  

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

http://www.scirp.org/journal/PaperInformation.aspx?PaperID=46104

Harding, R.M., Healy, E., Ray, A.J., Ellis, N.S., Flanagan, N., Todd, C., Dixon, C., Sajantila, A., Jackson, I.J., Birch-Machin, M.A., and Rees, J.L. (2000). Evidence for variable selective pressures at MC1R. American Journal of Human Genetics, 66, 1351-1361. 

Lalueza-Fox, C., H. Römpler, D. Caramelli, C. Stäubert, G. Catalano, D. Hughes, N. Rohland, E. Pilli, L. Longo, S. Condemi, M. de la Rasilla, J. Fortea, A. Rosas, M. Stoneking, T. Schöneberg, J. Bertranpetit,  and M. Hofreiter. (2007). A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals, Science, 318 (5855), 1453-1455.

http://www.bio.davidson.edu/courses/genomics/Exams/2009/Neaderthal_pigment.pdf  

Maanasa, R., Skoglund, P., Graf, K.E., Metspalu, M., Albrechtsen, A., Moltke, I., Rasmussen, S., Stafford Jr, T.W., Orlando, L., Metspalu, E., Karmin, M., Tambets, K., Roots, S., Mägi, R., Campos, P.F., Balanovska, E., Balanovsky, O., Khusnutdinova, E., Litvinov, S., Osipova, L.P., Fedorova, S.A., Voevoda, M.I., DeGiorgio, M., Sicheritz-Ponten, T., Brunak, S., Demeshchenko, S., Kivisild, T., Villems, R., Nielsen, R., Jakobsson, M., and Willerslev, E. (2014). Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature, 505, 87-91.

http://cteg.berkeley.edu/~nielsen/wordpress/wp-content/uploads/2013/12/Raghavan-M.-et-al.-2013..pdf  

Valverde, P., E. Healy, I. Jackson, J.L. Rees, and J. Thody. (2005). Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans, Nature Genetics, 11, 328-330.

http://www.nature.com/ng/journal/v11/n3/abs/ng1195-328.html