Puzzle of European hair and eye color

Hair and eye color diversity is unusual in two ways. It’s confined to Europeans. And it seems to be linked to prenatal feminization.
Europeans are distinguished from other humans by a diverse palette of eye and hair colors. I’ve argued that these color traits arose from intense sexual selection of women in ancestral European environments (Frost, 1994, 2006, 2008). Until 10,000 years ago, Europe had vast expanses of continental tundra—an environment where male hunters provided almost all the food and where long-distance hunting caused more deaths among young men than among young women. With fewer men overall, and fewer who could shoulder the costs of polygyny, the mate market had a surplus of unmated women. The pressure of sexual selection was therefore on the female sex. They were the ones who had to compete for mates.

East of Europe, the tundra zone swung north into colder and more arid territory. Humans were present there too, but in fewer numbers and less continuously. Only in Europe did this zone have a continuous human presence throughout the last ice age, and only in Europe could humans pass on and steadily accumulate the genetic legacy of intense female-directed sexual selection.

But if sexual selection had created European hair and eye colors, wouldn’t we see some sex linkage? Wouldn’t these color traits be expressed more in women than in men?

When I initially wrote on this subject, I had some evidence of sex linkage. Blond hair darkens with age more slowly in women than in men (Olivier, 1960, p. 74). I had also read an unpublished study that found higher digit ratios, and thus higher prenatal exposure to estrogen, in individuals with blond hair or non-brown eyes (Mather et al., unpublished).

But that was it. So I fell back on the explanation that sex linkage would have taken too long to evolve, especially because men incurred little cost in having unnecessarily showy eye and hair colors.

I’ve since come across more evidence of sex linkage. First, a twin study has shown that hair is, on average, lighter-colored in women than in men, with red hair being especially more frequent in females. Women also show greater variation in hair color (Shekar et al., 2008).

Second, blue-eyed men seem to have a more feminine face shape. This was the unintended finding of a rating study of male facial photos, which initially found that brown-eyed men were perceived to be more dominant than blue-eyed men. As a control, the authors repeated the experiment after altering the photos to give the brown-eyed men blue eyes. The altered photos were still rated as more dominant. Careful study revealed that the brown-eyed men had more masculine faces with broader and more massive chins, broader mouths, larger noses, larger eyebrows, and closer-set eyes. The blue-eyed men had smaller and sharper chins, narrower mouths, smaller noses, and a greater span between the eyes. It was thus face shape and not eye color that made the brown-eyed men seem more dominant. The authors denied the possibility of ethnic differences between the two groups, stating that the photos depicted only university students of Czech origin (Kleisner et al., 2010).

Finally, a study of preschool children suggests that blue eyes are sex-linked to shyness:

In the present study, 152 Caucasian preschool-aged (Mage=54.09 months, SD=5.84) children (77 males) with either blue (n=84) or brown (n=68) eyes, were compared in terms of parental and teacher ratings of social wariness, social play, and aggression. A significant Eye Color×Gender Interaction was found in terms of indices of social wariness; blue-eyed males were rated as more socially wary than brown-eyed males, while blue- and brown-eyed females did not differ in this regard. (Coplan et al., 1997)

This finding seems robust in the sense that other authors (cited by Coplan et al.) have found similar results. Although shyness in itself is not more common in girls than in boys, girls show a stronger interaction between loneliness and aggression (Coplan et al., 2007). In a male brain, this interaction might lead to a higher likelihood of social withdrawal, given the generally higher level of aggression in boys than in girls.

But how does this sex linkage operate? It may be mediated by prenatal exposure to estrogen, as Mather et al found in their unpublished study. This pre-natal estrogenization would be over-determined in women, i.e., almost all women are fully exposed to estrogen before birth regardless of their eye color. In men, however, it would be limited to blue-eyed individuals. Thus, blue-eyed men may be partially feminized not only in their face shape but also in their behavior.

Could other behaviors be partially feminized in blue-eyed or fair-haired men? Sexual orientation comes to mind, but that’s one thing that natural selection should have quickly rectified (as Greg Cochran has often pointed out). Indeed, Ellis et al. (2008) failed to find any significant relationship between sexual orientation and eye color or hair color.

Alternate explanations

- Neanderthal admixture?

Not many alternate explanations are still in the running. For a while, a plausible one was Neanderthal admixture. We’ve since managed to retrieve the Neanderthal MC1R allele and it doesn’t match any existing allele in modern humans. In any case, the estimated Neanderthal admixture of 1 to 4% in modern Europeans is well below the frequency of non-black hair and non-brown eyes.

- Genetic linkage to lighter skin?

Perhaps eye and hair color diversity is genetically linked to lighter skin. Eyes and hair have diversified in color in the same part of the world where skin color has lightened the most. Perhaps this lightening involved genes that also affect hair and eye color.

Yet the genes are different in each case. European skin has lightened mainly through replacement of alleles at two genes: SLC45A2 (AIM1) and SLC24A5. European hair color has diversified through a proliferation of new alleles at the MC1R gene. European eye color has diversified through a proliferation of new alleles in the HERC2-OCA2 region and elsewhere.

Lighter skin is associated with a few of the new alleles, namely the ones for red hair or blue eyes. Conceivably, these two color variants are a side effect of selection for lighter skin. But why would such selection increase the total number of alleles for hair and eye color? This is especially strange because many of the alleles have little or no effect on skin pigmentation. And why have neither red hair nor blue eyes reached fixation in any population, even those with milk-white complexions?

- Cochran’s theory

Greg Cochran has argued that European hair and eye color diversity reflects an underlying behavioral polymorphism, which in turn is due to a process of self-domestication that resulted from the advent of agriculture. As Europeans formed larger and more sedentary communities, they had to become more obedient to authority. An extra dose of prenatal estrogen might have been the necessary quick fix to tame European males.

Greg’s theory is a mirror image of my own. I argue that sexual selection of women was driving the evolutionary change. The effects on male behavior are thus merely collateral damage. Greg argues that the evolutionary change was driven by natural selection for male submissiveness. The new hair and eye colors are thus merely a cute side effect.

To my knowledge, Greg has presented this theory at length only in the book he published with Henry Harpending The 10,000 Year Explosion. Even there, the presentation is a bit hazy. The two authors start off well enough:

[…] selection on genes affecting skin color, eye color, and hair color somehow created lots of variety in Europeans: redheads and blondes, blue eyes and green eyes. Nowhere else in the world is that sort of variety common. In most parts of the world, even in temperate regions, everyone has dark eyes and dark hair. (Cochran & Harpending, 2009, p. 94)

This pattern points to “something fundamentally different in the selective forces.” The next few pages suggest that this “something” is selection for submission to authority, which in turn is incidentally linked to eye and hair color. But Cochran and Harpending never spell out the link. The closest they come is a paragraph eighteen pages onward:

Selection for submission to authority sounds unnervingly like domestication. In fact, there are parallels between the domestication in animals and the changes that have occurred in humans during the Holocene period. In both humans and domesticated animals, we see a reduction in brain size, broader skulls, changes in hair color or coat color, and smaller teeth. (Cochran & Harpending, 2009, p. 112)

That’s it. There are no references to the literature linking eye color to behavior. Why? Maybe it’s bad karma to imply that blue-eyed men are more civilized. That sounds a bit …. well, you know.

Personally, I don’t care whether or not a theory is socially acceptable. Only one question concerns me. Does it make sense?

Let’s walk through it step by step. Agriculture created a selection pressure for more obedient men. This selection in turn led to blue eyes and fair hair as a side effect. We know that agriculture spread through Europe in stages. For a long time, the wave of advance stalled along a line stretching from the Low Countries to the Black Sea. Then, around 7,500 years ago, agriculture resumed its northward spread. The last refuge of European hunter/fisher/gatherers seems to have been in the East Baltic, where farming became dominant only 3,000 years ago.

These last holdouts were presumably less affected by the process of self-domestication via agriculture. They should therefore have lower incidences of blue eyes and fair hair. Is that what we see?

Nope.

Greg’s theory has other weaknesses. Are farmers really more submissive than hunter-gatherers? Not necessarily. It isn’t so much farming that makes men less unruly as State formation, specifically the State’s monopoly on the use of violence. That’s a later historical development (Frost, 2010).

And blue eyes are linked not so much to male submissiveness as to male shyness. The two aren’t really the same thing. Can one confidently argue that male shyness is more adaptive among farmers? Aren’t social relations more extensive and intensive in farming communities than in small bands of hunter-gatherers?

References

Cochran, G.M. & H. Harpending. (2009). The 10,000 Year Explosion, Basic Books.

Coplan, R.J., L.M. Closson, & K.A. Arbeau. (2007). Gender differences in the behavioral association of loneliness and social dissatisfaction in kindergarten, Journal of Child Psychology and Psychiatry, 48, 988-995.

Coplan, R., B. Coleman, & K. Rubin. (1998). Shyness and little boy blue: Iris pigmentation, gender, and social wariness in preschoolers. Developmental Psychobiology, 32, 37–44.

Ellis, L., C. Ficek, D. Burke, & S. Das. (2008). Eye color, hair color, blood type, and the Rhesus factor: Exploring possible genetic links to sexual orientation, Archives of Sexual Behavior, 37, 145-149.

Frost, P. (2010). The Roman State and genetic pacification, Evolutionary Psychology, 8(3), 376-389. http://www.epjournal.net/filestore/EP08376389.pdf

Frost, P. (2008). Sexual selection and human geographic variation, Special Issue: Proceedings of the 2nd Annual Meeting of the NorthEastern Evolutionary Psychology Society. Journal of Social, Evolutionary, and Cultural Psychology, 2(4),169-191. http://137.140.1.71/jsec/articles/volume2/issue4/NEEPSfrost.pdf

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

Frost, P. (1994). Geographic distribution of human skin colour: A selective compromise between natural selection and sexual selection? Human Evolution, 9, 141-153.

Kleisner, K., T. Kočnar, A. Rubešova, & J. Flegr. (2010). Eye color predicts but does not directly influence perceived dominance in men. Personality and Individual Differences, 49, 59–64.

Mather, F., Manning, J.T., & Bundred, P.E. (unpublished). 2nd to 4th digit ratio, hair and eye colour in Caucasians: Evidence for blond hair as a correlate of high prenatal oestrogen.

Olivier, G. (1960). Pratique anthropologique. Paris: Vigot Frères.

Shekar, S.N., D.L. Duffy, T. Frudakis, G.W. Montgomery, M.R. James, R.A. Sturm, & N.G. Martin. (2008). Spectrophotometric methods for quantifying pigmentation in human hair—Influence of MC1R genotype and environment. Photochemistry and Photobiology, 84, 719–726.