If sexual selection of women diversified the eye color of early Europeans, the new colors should tend to be sex-linked, since the selection targeted women more than men. There is now evidence that blue eyes are linked to feminization of face shape.
Throughout most of the world, humans have brown eyes, black hair, and varying shades of dark skin. An exception is Europe, especially its northern and eastern portions. Here, eyes are not only brown but also blue, gray, hazel, or green. Hair is not only black but also brown, flaxen, golden, or red. Finally, skin has been whitened to the end point of depigmentation.
How can we explain this unusual color pattern? Is it simply due to lightening of skin color? In other words, did reduction of skin pigmentation incidentally reduce eye and hair pigmentation? The diverse palette of eye and hair colors would thus be a side effect of selection for lighter skin.
This explanation is dubious. For one thing, the gene loci are not the same. European skin has whitened mainly through allelic change at SLC45A2 (AIM1) and SLC24A5 (Soejima et al., 2005; Voight et al., 2006). European hair has diversified in color through a proliferation of new alleles at MC1R (Makova & Norton, 2005; Rana et al., 1999). European eyes have diversified in color mainly through a proliferation of new alleles at the OCA2-HERC2 gene complex (Duffy et al., 2007; Kayser et al., 2008; Sturm & Frudakis, 2004; Sturm et al., 2008).
Some of these novel hair and eye colors are also associated with lighter skin, notably the red hair and blue eye phenotypes. But why would selection for lighter skin lead to a proliferation of new alleles for hair and eye color—most of which have little or no influence on skin color? Why is it that red hair and blue eyes have not reached fixation in any human population, even those with milk-white skin?
I have argued that the cause was an intensification of sexual selection among early Europeans, specifically sexual selection of women (Frost, 2006; Frost, 2008). When too many women have to compete for too few men, there is selection for visible female traits that hyperstimulate certain algorithms in the male brain, particularly those for gender recognition or fertility assessment.
Among hunter-gatherers—and all humans were hunter-gatherers until 10,000 years ago, sexual selection of women tends to intensify farther away from the equator. On the one hand, hunting distances lengthen, thus increasing male mortality. On the other, polygyny becomes less common because women are less able to provide for themselves and their children in winter, thus making it costlier for a man to provide for a second wife. Result: a growing imbalance between the numbers of women and men on the mate market.
Among early modern humans, these two equator-to-arctic trends reached a common end-point in the steppe-tundra of northern Eurasia, such as existed during the last ice age (25,000 – 10,000 years ago). Hunting distances were very long because almost all food came from highly mobile herds of mammals, notably reindeer. Male provisioning was similarly at a maximum, women having little or no food autonomy.
The Eurasian steppe-tundra was continuously inhabited only in portions of its European end, where it ran farther south because of the large icecap over Scandinavia and where the moderating influence of the Atlantic Ocean and the Gulf Stream made the climate moister and milder. Here, the effects of intense sexual selection could accumulate and be passed on from generation to generation. Conversely, northern Asia appears to have suffered episodes of complete depopulation, particularly at the height of the last ice age.
Sexual selection: color novelty and color diversification
When sexual selection is weak, the adaptive equilibrium is dominated by selection for a dull, cryptic appearance that reduces detection by predators (Kirkpatrick, 1987). As sexual selection grows stronger, the equilibrium shifts toward a more noticeable appearance that retains the attention of potential mates, typically by means of vivid and/or novel colors.
One outcome may be a polymorphism of brightly colored phenotypes, due to selection shifting to scarcer and more novel hues whenever a color variant becomes too common (Endler, 1980; Frost, 2006; Hughes et al., 1999; Hughes et al., 2005; Olendorf et al., 2006). This frequency dependence has been shown in humans. Thelen (1983) presented male participants with slides showing attractive brunettes and blondes and asked them to choose, for each series, the woman they would most like to marry. One series had equal numbers of brunettes and blondes, a second 1 brunette for every 5 blondes, and a third 1 brunette for every 11 blondes. Result: the rarer the brunettes were in a series, the likelier any one of them would be chosen.
But why would this stronger selection diversify hair and eye color while simply whitening skin color? The answer seems to be that sexual selection acts on skin color not only through rare-color preference but also by hyperstimulating a gender-recognition algorithm, i.e., by accentuating a visible female-specific trait. In our species, female skin has less melanin and hemoglobin than does male skin, i.e., women look paler, men browner and ruddier (Edwards & Duntley, 1939; Hulse, 1967; Jablonski & Chaplin, 2000).
If European skin had whitened through selection for lighter-skinned women, it should have whitened more in women than in men, thus becoming more sexually dimorphic. Yet skin color actually seems to be less dimorphic in Europeans than in other humans (Madrigal & Kelly, 2006). This finding does not necessarily invalidate the sexual selection hypothesis. It may be that the pigmentary sex difference cannot fully express itself in light-skinned populations. Skin color is dimorphic because girls progressively lighten in color during adolescence, and such lightening may be less easily expressed if melanin production is already low. Indeed, this dimorphism seems to be almost absent in people whose skin starts off with very little pigment, such as Dutch and Belgian subjects (Frost, 2007).
And hair and eye color? Sexual selection of women should favor novel hair and eye colors more so in women than in men. Granted, both polymorphisms arose over a short and relatively recent span of time, so sexual selection would have worked with those alleles that were initially available and, for the most part, not sex-linked. But surely a few of these mutant alleles would have been sex-linked and, as such, favored over non-sex-linked ones.
This does seem to be the case with hair color. Blond hair darkens with age more slowly in women than in men (Olivier, 1960, p. 74). A ‘digit ratio’ study indicates that prenatal exposure to estrogen is higher in individuals with blond hair or non-brown eyes (Mather et al., unpublished). The same study, however, found no evidence of sexual dimorphism. Women and men had roughly the same proportions of hair and eye colors among the 18-to-38 year olds under study. Such a dimorphism, if it does exist, may be a transient one limited to younger age groups.
Moreover, Kleisner et al. (2010) have found an apparent sex linkage between blue eyes and feminization of face shape. They initially wished to determine whether eye color influences perception of male dominance, using facial pictures of Czech men. The results showed that brown-eyed men were rated as more dominant than blue-eyed men. As a control, the authors repeated the experiment after altering the facial photos of the brown-eyed men to make them blue-eyed. These altered photos were still rated as more dominant.
Careful study of the photos revealed that the brown-eyed men had more masculine facial features:
In contrast with blue-eyed males, brown-eyed males have statistically broader and rather massive chins, broader (laterally prolonged) mouths, larger noses, and eyes that are closer together with larger eyebrows. In contrast, blue-eyed males show smaller and sharper chins, mouths that are laterally narrower, noses smaller, and a greater span between the eyes.
The perception of brown-eyed men as more dominant is thus due to their more masculine facial appearance—and not to their brown eyes. The authors suggest that some kind of sex linkage may be responsible, while adding: “Repeating this study in other populations with polymorphism in eye color can test this hypothesis.”
If true, this finding would be consistent with Liberton et al. (2009) who found that European face shape has differentiated from West African face shape through a selective force that has acted primarily on women. Both findings, in turn, would support my argument that many of the differences we see among human populations are not due to differences in natural selection, and hence differing natural environments. Instead, the cause lies in differing intensities of sexual selection, and whether this selection has primarily targeted men or women (Frost, 2008).
When men are the prime targets of sexual selection, as in tropical ‘female farming’ societies, the result is accentuation of certain male features. Meanwhile, there is a slackening of female-targeted sexual selection, which leads to women having a more functional and less ornamental appearance. This pattern is reversed when women are the prime targets of sexual selection (Frost, 2008).
There is admittedly an alternate explanation for the above finding: ethnic substructure among the Czech subjects. The Czech Republic has historically been home to ethnic minorities who statistically differ from ethnic Czechs in facial appearance, i.e., Jews, Germans, and Roma. Jews and Roma, like other populations of Mediterranean or southwest Asian origin, tend to have brown eyes and a more robust face shape. Conversely, Germans are likelier to have blue eyes and more gracile faces. Although the Jewish and German communities were severely decimated during World War II and its aftermath, with many survivors later emigrating, there still remain significant numbers of Czech citizens who are wholly or partly of Jewish or German origin. Since WWII, there has also been an influx of Roma into the Czech Republic.
It would be difficult to rule out this kind of explanation, even if one questioned the subjects of the study. After the last war, many Czech citizens of Jewish or German origin felt it best to conceal their ancestry, for fear of discrimination or even expulsion from the country. Today, their grandchildren may be completely unaware of their origins.
This is all the more reason to replicate the results with subjects from another population, preferably one with as little ethnic substructure as possible.
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