Just for show?

European woman in Mughal costume and jewelry, 19th century (Wikicommons)

People of European origin have an unusually diverse palette of hair and eye colors. This diversity is commonly ascribed to their unusually white skin. Ancestral Europeans became lighter-skinned, and this genetic change therefore caused other changes to hair and eye pigmentation.

Actually, the genetic changes are different in each case. European skin turned white through a replacement of alleles, primarily at TYRP1, SLC24A5, and SLC45A2. European hair and eyes diversified in color through a proliferation of new alleles, primarily at MC1R for hair color and in the HERC2-OCA2 region for eye color.

It now appears that this diversification has occurred at other gene loci as well. Zhang et al. (2013) report that a region downstream from EDNRB is associated with differences in hair color and that two other loci, VASH2 and POLS, are associated with differences in eye color. Sulem et al. (2008) report that TPCN2 is associated with differences in hair color and that ASIP is associated with red hair.

A common selection pressure, not a common gene

This is further proof that a selection pressure created the visual effect of color diversity by acting on whatever genes it could. In short, this diverse palette of hues seems to exist “just for show.”

The evolutionary problem is spelled out by Walsh et al. (2012):

People of European descent display the widest variation in pigmentation traits, such as iris (eye) and hair colouration, in the world. In particular, eye colour variation is nearly restricted to people of (at least partial) European descent. Eye colour categories here often concern blue, brown and intermediate (green, etc.). In the rest of the world, people tend to have brown eye colour, which is considered to be the ancestral human trait in agreement with the Out-of-Africa hypothesis of modern humans. The current variation in eye colour is thought to have originated via a genetic founder event involving non-brown irises in early European history. It is furthermore assumed that eye colour variation in Europe has been shaped by positive selection via sexual selection i.e., mate choice preference. Alternatively it has been proposed that eye colour variation evolved via a correlation with skin colour and its environmental adaptation e.g. maximizing vitamin D conversion in low levels of UV radiation, or as a combination of both. One suggested geographic region for the origin of blue eye colour in Europe is the southern Baltic, as indicated by concentric rings of decreasing frequency of the blue eye colour trait spreading from the southern Baltic region, resulting in a strong north–south gradient in blue eye colour frequency across Europe.

It is doubtful whether a lack of vitamin D at northern latitudes played a role in the whitening of European skin, let alone in the diversifying of European hair and eye color. As Elias and Williams (2012) note, certain northern populations whitened much more than others:

An obvious feature of the northward dispersal of humans is a quasi-geographic reduction in pigmentation (Murray, 1934; Loomis, 1967; Chaplin and Jablonski, 2009). Coloration varies greatly among northerners. Native Inuit display medium-to-dark (type III/IV), rather than light pigmentation, and both northern and central-dwelling Asians display medium (type III) pigmentation. Recent population genetic data show that the reduction in skin pigmentation occurred sporadically and incompletely in northern and Asian populations (Sturm, 2009). Moreover, while modern humans reached Central Europe ≈40 ka (thousands of years ago), they reached northern Europe only after the last ice sheets receded less than 11 ka. It is only these humans that display light pigmentation, and recent molecular genetic studies suggest that the very light pigmentation of northern Europeans did not develop until 5-6 ka (Norton et al., 2007; Norton and Hammer, 2008).

Heather Norton’s estimate for European skin whitening (which she set within a broader range of 3,000 to 12,000 years ago) has been revised upward by Sandra Beleza to a range of 11,000 to 19,000 years ago, the second estimate being now accepted as the better one by Norton (Beleza et al., 2013; Norton and Hammer, 2007; Norton, 2012). This time period still began long after the entry of modern humans into Europe, the implication being that ancestral Europeans were brown-skinned for tens of thousands of years.

Elias and Williams (2012) also note that the vitamin-D hypothesis cannot explain the changes to European hair color, since hair is not involved in vitamin-D synthesis. Their alternate hypothesis is that European skin became white as a way to cut back on unnecessary energy expenditure:

[…] a declining need to heavily pigment the epidermis favored the retention of mutations in genes that reduced pigment synthesis, thereby diverting energy toward the production of more urgently-needed proteins.

But why, then, did ancestral Europeans wait over twenty thousand years before cutting back on this unnecessary expenditure? And why would this expenditure be less unnecessary at northern latitudes in Asia and North America? Moreover, in the case of hair color, what has happened is not a loss of pigment but rather a shift from production of one kind of pigment, i.e., eumelanin (black-brown hues), to production of another, i.e., pheomelanin (yellow-red hues).

Sexual selection?

Color polymorphisms are not limited to humans. They occur in many other species for reasons that Hofreiter and Schöneberg (2010) discuss in a recent review article. One reason is crypsis—the need to blend into a background that may vary from one place to another. Deer mice, for instance, have light fur where the ground is likewise light in color and dark fur where it is dark in color. Another reason is aposematism—individuals with a rare coloration have better chances of survival, since they are a poorer match for a predator’s search image.

Such a frequency dependent effect, favouring the rarer colour morphs, is also known from sexual selection, when females preferentially mate with rare colour morph males, a phenomenon also known from guppies. (Hofreiter and Schöneberg, 2010)

This kind of color polymorphism typically involves bright colors, since sexual selection is influenced by sensory biases that favor not only novel colors but also bright ones as well. In fish species, for instance, color morphs are often red because a sensory bias for this color has developed irrespective of mating contexts.

If we look at the polymorphisms for human hair and eye color, the recently evolved “European” hues tend to be brighter than the species norm of black hair and brown eyes. Eyes may be light blue, but not navy blue. Hair may be carrot red, but not beetroot red. Sexual selection is also indicated by a greater variability of hair color in women, with red hair being especially more frequent (Shekar et al., 2008).

But why?

Why would sexual selection have been more intense among ancestral Europeans? Such selection happens when too many of one sex are competing to mate with too few of the other. In most mammals, the males do the competing—because polygyny dries up the pool of available females. So the males are brilliantly colored, and the females duller in appearance.

But here we have the reverse. Hair color is brighter and more diverse in European women than in European men. We see a similar pattern with skin color. “European” physical traits seem to be female traits. It looks as though sexual selection primarily targeted women and then secondarily spilled over on to men.

This unusual color scheme seems to result from the unusual steppe-tundra that covered the plains of northern and eastern Europe during the last ice age 25,000 to 10,000 years ago. This environment offered ancestral Europeans a huge amount of edible biomass, but nearly all of it was locked up as meat in wandering herds of reindeer and other herbivores. Since male hunters provided almost all of the food for their wives and offspring, the cost of supporting a second wife and her children was prohibitive for them, being feasible for only the ablest hunters. At the same time, pursuit of migratory game greatly lengthened the mean hunting distance and boosted male death rates accordingly.

Thus, limited polygyny, combined with higher hunting-related mortality, skewed the mate market towards a shortage of available men. Women had to compete for men, unlike the situation among tropical humans and most other mammalian species. This intense mate competition in turn drove sexual selection for colorful features that could, by their brightness or their novelty, catch the attention of a prospective mate (Frost, 2006; Frost, 2008).

References

Beleza, S., A. Murias dos Santos, B. McEvoy, I. Alves, C. Martinho, E. Cameron, M.D. Shriver, E.J. Parra, and J. Rocha. (2013). The timing of pigmentation lightening in Europeans, Molecular Biology and Evolution, 30, 24-35.

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

Frost, P. (2008). Sexual selection and human geographic variation, Journal of Social, Evolutionary,and Cultural Psychology, 2(4), 169-191. http://137.140.1.71/jsec/articles/volume2/issue4/NEEPSfrost.pdf

Hofreiter, M., and T. Schöneberg. (2010). The genetic and evolutionary basis of colour variation in vertebrates, Cellular and Molecular Life Sciences, 67, 2591–2603.

Norton, H.L., and M.F. Hammer. (2007). Sequence variation in the pigmentation candidate gene SLC24A5 and evidence for independent evolution of light skin in European and East Asian populations. Program of the 77th Annual Meeting of the American Association of Physical Anthropologists, p. 179

Norton, H.L. (2012). Personal communication

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

Sulem, P., D.F Gudbjartsson, S.N. Stacey, A. Helgason, T. Rafnar, M. Jakobsdottir, S. Steinberg, S.A. Gudjonsson, A. Palsson, G. Thorleifsson, S. Palsson, B. Sigurgeirsson, K. Thorisdottir, R. Ragnarsson, K.R. Benediktsdottir, K.K. Aben, S.H. Vermeulen, A.M. Goldstein, M.A. Tucker, L.A. Kiemeney, J.H. Olafsson, J. Gulcher, A. Kong, U. Thorsteinsdottir, and K. Stefansson. (2008). Two newly identified genetic determinants of pigmentation in Europeans, Nature Genetics, 40, 835-837.

Walsh, S., A. Wollstein, F. Liu, U. Chakravarthy, M. Rahu, J.H. Seland, G. Soubrane, L. Tomazzoli, F. Topouzis, J.R. Vingerling, J. Vioque, A.E. Fletcher, K.N. Ballantyne, and M. Kayser. (2012). DNA-based eye colour prediction across Europe with the IrisPlex system, Forensic Science International: Genetics, 6, 330–340.

Zhang, M., F. Song, L. Liang, H. Nan, J. Zhang, H. Liu, L.-E. Wang, Q. Wei, J.E. Lee, C.I. Amos, P. Kraft, A.A. Qureshi, and J. Han. (2013). Genome-wide association studies identify several new loci associated with pigmentation traits and skin cancer risk in European Americans, Human Molecular Genetics, advance access 1–12 

When Europeans turned white

No, that’s not a climatic adaptation

(actress Lily Cole - source)


“European skin turned pale only recently”—such was the headline in Science five years ago. 

[…] a new report on the evolution of a gene for skin color suggests that Europeans lightened up quite recently […]  the implication is that our European ancestors were brown-skinned for tens of thousands of years (Gibbons, 2007)

The report had been presented by a postdoc, Heather Norton, at the annual meeting of the American Association of Physical Anthropologists (Norton & Hammer, 2007). Over the following years, I e-mailed periodically to ask her when the study would be published. To make a long story short, she landed a faculty position and found herself overwhelmed by new responsibilities. There were still problems with the dating of this genetic change, and time couldn’t be found to work them out. So the study stayed “on the back burner.”

Five years later, the study has finally been published … by another research team. Beleza et al. (2012) generally confirmed Norton’s preliminary finding but found evidence that Europeans had lightened through a 2-stage process. Around 30,000 years ago, not long after entering Europe, the ancestors of today’s Europeans and East Asians lightened in skin color through a new allele at the KITLG gene. But the real whitening came much later, between 19,000 and 11,000 years ago among ancestral Europeans only, through new alleles at TYRP1, SLC24A5, and SLC45A2. This finding strikes down the two leading explanations for the whiteness of European skin:

1.     As modern humans spread north from Africa and into higher latitudes with less solar UV, their skin had to lose pigmentation to maintain the same level of vitamin-D synthesis. Europeans therefore began to turn white once their ancestors entered European latitudes some 40,000 years ago (Loomis, 1970; Murray, 1934).

This explanation might account for the initial loss of pigmentation circa 30,000 BP, when ancestral Europeans probably became as light-skinned as Amerindians. But it cannot explain the much greater loss of pigmentation more than twenty thousand years later.

2.     Some writers, like Sweet (2002), have suggested that the transition from hunting and gathering to farming increased the body’s need for vitamin D (because cereals contain phytic acids that immobilize calcium and phosphorus within the body and because a high-meat diet seems to reduce vitamin-D requirements). In Europe, however, this transition began only 8,000 years ago and did not reach northern Europe until 7,000-3,000 BP.

Beleza et al. (2012) suggest that a colder climate forced Ice Age Europeans to wear more clothing and spend more time in shelters, thus reducing their exposure to solar UV. It was thus at that time, and not when modern humans first entered Europe, that European skin turned white in order to maintain the same level of vitamin-D synthesis.

But then why didn’t Europeans revert after the Ice Age to their original brown color? And why do we see brown skin in humans who have long lived with weaker solar UV and even colder weather in northern Asia and North America? This is notably the case with Amerindian groups in Canada and Alaska who derive very little vitamin D from either the sun or their diet (Frost, 2012a, 2012b).

In any case, it is only during the summer that solar UV is intense enough for the skin to synthesize vitamin D. Yet European summers were not much cooler during the last ice age than they are today. The Central Russian Plain, for instance, had a July mean temperature of 16° back then, versus 18° now (Hoffecker, 2002, p. 23). So Ice Age Europeans had little reason to be less exposed to solar UV. Indeed, the open steppe-tundra was much more exposed to the sun than the forested environments before and after the Ice Age.

Sexual selection?

There remains of course my explanation (Frost, 2006; Frost, 2008). White skin was not climatically advantageous. It was visually advantageous, as were two other unique color traits. Within this same geographic area, centered on northern and eastern Europe, hair is not only black but also brown, flaxen, golden, or red. Eyes are not only brown but also blue, gray, hazel, or green.

Yet, in each case, the genes are different. European skin lightened mainly through replacement of alleles at three genes: SLC45A2, SLC24A5, and TYRP1. European hair color diversified through a proliferation of new alleles at the MC1R gene. European eye color diversified through a proliferation of new alleles in the HERC2-OCA2 region and elsewhere.

These European color traits have evolved along separate trajectories, yet the goal seems similar—a shift toward brighter and more visible colors. But visible to whom?

To the opposite sex? Sexual selection favors visual qualities that catch the attention of potential mates. In the case of skin color, a pre-existing sexual dimorphism has made lighter skin a visible female characteristic. Women are the “fair sex.” They’re paler than men from puberty onward (Edwards & Duntley, 1939).

Skin color is, in fact, a key visual cue for sex recognition, being even more crucial than face shape (Bruce & Langton, 1994; Hill, Bruce, & Akamatsu, 1995; Russell & Sinha, 2007; Russell et al., 2006; Tarr et al., 2001; Tarr, Rossion, & Doerschner, 2002). When shown a human face, subjects can recognize its sex even if the image is blurred and differs only in color (Tarr et al., 2001).

The specific cues are hue and luminosity. A man is browner and ruddier in hue than a woman because melanin and blood are more present in his skin’s outer tissues (Edwards & Duntley, 1939). A woman has higher luminous contrast between her facial skin and her lips or eyes (Dupuis-Roy et al., 2009; Russell, 2003). These cues may explain the similar evolution of cosmetics in a wide range of culture areas, i.e., women generally seek to lighten their facial color and to increase its contrast with their lip and eye color (Russell, 2003; Russell, 2009; Russell, 2010).

Thus, the more a woman is lighter-skinned, the more she is recognizably female. This is not just a matter of conscious sex recognition. It’s also a matter of men acting on half-conscious feelings. Even when a woman is recognized as such, her mating success may be influenced by subtle differences in the way men perceive her femininity.

Extreme sexual selection on the European steppe-tundra

But if sexual selection were the cause, why did it occur only 19,000 to 11,000 years ago and only in Europe? What was so special about that time and place?

That time frame coincides with the last ice age (25,000-10,000 BP), particularly the glacial maximum (20,000-15,000 BP). In Europe, especially on the northern and eastern plains, there were now vast expanses of steppe-tundra that supported herds of wandering reindeer and other herbivores, which in turn supported a large human population. Bioproductivity was in fact much higher there than on today’s arctic barrens. Steppe-tundra also existed in Asia, but it was colder and drier, being farther north and farther from the moderating influence of the Atlantic Ocean. Its human population was not only smaller but also more vulnerable to periodic extinctions, particularly at the height of the last ice age.

Europe’s steppe-tundra was a singularity among the many environments that modern humans encountered as they spread out from Africa during the Paleolithic. It offered an abundance of food, but almost all of the food was in the form of meat. Since hunting was primarily a male activity, men had to bear almost the entire burden of food provisioning. Women either processed the food that men supplied or did activities unrelated to food, such as garment making or shelter building.

There were also demographic consequences. First, polygyny became less common, being limited to those able hunters who could support more than one family. Second, the death rate among young males increased. In hunter-gatherer societies, the male death rate increases with hunting distance, reaching a maximum in environments where hunters pursue migratory herds over long distances. As a result, women greatly outnumbered men on the mate market. Women had to compete for the attention of potential mates, and sexual selection favored the mating success of those who could.

In other species, sexual selection changes physical appearance from a dull, cryptic coloration to a brighter, more eye-catching one. This is especially true for traits on or near the face—the focus of visual attention. Since most genes for human skin, hair, and eye color are not sex-linked, any selection for new color traits in one sex would spill over onto the other sex. As European women whitened, so did Europeans of both sexes.

In time, sexual selection also leads to sexual dimorphism. Sex-linked alleles would appear through random mutation and gradually replace similar alleles that are not sex-linked. Some sexual dimorphism is indeed evident in European color traits. A twin study has shown that hair is lighter-colored in women than in men, with red hair being especially more frequent, and that women show greater variation in hair color (Shekar et al., 2008). Skin color, however, is actually less dimorphic in light-skinned humans than in those of medium skin color, probably because of a “ceiling effect,” i.e., girls cannot become much lighter-skinned after puberty if the population is already close to the limit of maximum paleness (Frost, 2007).

 

Conclusion

White European skin evolved relatively fast during the last ice age, specifically from 19,000 to 11,000 years ago. This was also probably the same time frame for the evolution of European hair and eye colors. Anyway, that’s my bet.

These color traits—white skin and a diverse palette of hair and eye colors— are not adaptations to a cooler, less sunny climate. They are adaptations by early European women to intense mate competition, specifically a shortage of potential mates due to a low polygyny rate and a high death rate among young men.

This situation was created by the steppe-tundra that covered most of Europe as late as 10,000 years ago. Early Europeans were able to colonize this environment but only at the price of a severe imbalance between men and women on the mate market.

References

Beleza, S., A. Murias dos Santos, B. McEvoy, I. Alves, C. Martinho, E. Cameron, M.D. Shriver, E.J. Parra & J. Rocha.(2012).The timing of pigmentation lightening in Europeans, Molecular Biology and Evolution, 20, online

Bruce,V., & S. Langton. (1994). The use of pigmentation and shading information in recognising the sex and identities of faces, Perception, 23(7), 803–822.

Dupuis-Roy, N., I. Fortin, D. Fiset, & F. Gosselin. (2009). Uncovering gender discrimination cues in a realistic setting, Journal of Vision, 9(2), 10, 1–8. http://journalofvision.org/9/2/10/, doi:10.1167/9.2.10.

Edwards, E.A. & S.Q. Duntley. (1939). The pigments and color of living human skin, American Journal of Anatomy, 65, 1-33.

Frost, P. (2012a). Vitamin D deficiency among northern Native Peoples: a real or apparent problem? International Journal of Circumpolar Health, 71, 18001 - DOI: 10.3402/IJCH.v71i0. http://www.circumpolarhealthjournal.net/index.php/ijch/article/view/18001

Frost, P. (2012b). Reply to W.B. Grant ‘Re: Vitamin D deficiency among northern Native Peoples’ International Journal of Circumpolar Health, 71, 18435 - DOI: 10.3402/ijch.v71i0.18435 http://www.circumpolarhealthjournal.net/index.php/ijch/article/view/18435/pdf_1

Frost, P. (2008). Sexual selection and human geographic variation, Special Issue: Proceedings of the 2^nd 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. (2007). Comment on Human skin-color sexual dimorphism: A test of the sexual selection hypothesis, American Journal of Physical Anthropology,133, 779-781.
http://onlinelibrary.wiley.com/doi/10.1002/ajpa.20555/abstract

Frost, P. (2006). European hair and eye color - A case of frequency-dependent sexual selection? Evolution and Human Behavior, 27, 85-103 http://www.sciencedirect.com/science/journal/10905138

Gibbons, A. (2007). American Association Of Physical Anthropologists Meeting: European Skin Turned Pale Only Recently, Gene Suggests. Science 20 April 2007:Vol. 316. no. 5823, p. 364 DOI: 10.1126/science.316.5823.364a
http://www.sciencemag.org/cgi/content/summary/316/5823/364a

Hill, H., V. Bruce, & S. Akamatsu. (1995). Perceiving the sex and race of faces: The role of shape and colour, Proceedings of the Royal Society B: Biological Sciences, 261, 367–373.

Hoffecker, J.F. (2002). Desolate Landscapes. Ice-Age Settlement in Eastern Europe, Rutgers University Press.

Loomis, W.F. (1970). Rickets. Scientific American, 223, 77-91.

Murray, F.G. (1934). Pigmentation, sunlight, and nutritional disease. American Anthropologist, 36, 438-445.

Norton, H.L. & M.F. Hammer (2007). Sequence variation in the pigmentation candidate gene SLC24A5 and evidence for independent evolution of light skin in European and East Asian populations, Program of the 77th Annual Meeting of the American Association of Physical Anthropologists, p. 179.

Russell, R. (2010). Why cosmetics work. In Adams, R., Ambady, N., Nakayama, K., & Shimojo, S. (eds.) The Science of Social Vision. New York: Oxford.

Russell, R. (2009). A sex difference in facial pigmentation and its exaggeration by cosmetics. Perception, 38, 1211-1219.

Russell, R. (2003). Sex, beauty, and the relative luminance of facial features, Perception, 32, 1093-1107.

Russell, R. & P. Sinha. (2007). Real-world face recognition: The importance of surface reflectance properties, Perception, 36, 1368-1374.

Russell, R., P. Sinha, I. Biederman, & M. Nederhouser. (2006). Is pigmentation important for face recognition? Evidence from contrast negation, Perception, 35, 749-759.

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.

Sweet, F.W. (2002). The paleo-etiology of human skin tone. http://backintyme.com/essays/?p=4

Tarr, M.J., D. Kersten, Y. Cheng, & B. Rossion. (2001). It’s Pat! Sexing faces using only red and green, Journal of Vision, 1(3), 337, 337a, http://journalofvision.org/1/3/337/, doi:10.1167/1.3.337.

Tarr, M.J., B. Rossion, & K. Doerschner. (2002). Men are from Mars, women are from Venus: Behavioral and neural correlates of face sexing using color, Journal of Vision, 2(7), 598, 598a, http://journalofvision.org/2/7/598/, doi:10.1167/2.7.598.