The mysterious Ainu

Ainu men and Ainu woman, 18th century painting by Kodama Sadayoshi (source)

The Ainu of northern Japan have long been a puzzle. With their bushy beards, profuse body hair, large sunken eyes, and robust facial features, they look more European than East Asian. Yet genetic studies have shown no particular link to Europeans, at least no more than for East Asians in general: 

Omoto (1972, 1972) computed genetic distances among various populations of the world, and by constructing a phylogenetic tree he concluded that the Ainu population may have originated in East Asia, in spite of their unique morphological characters somewhat resembling West Eurasians. (Jinam et al., 2012)

This conclusion has been confirmed by a new study using close to a million single nucleotide polymorphisms. Genetically, the Ainu are closest to the Ryukyans, the inhabitants of Japan’s southernmost islands, and then to the Japanese themselves (Jinam et al., 2012).

So is the physical similarity to Europeans just a matter of chance? Convergent evolution? No, it may be that the Ainu have just not changed as much physically as other East Asians. They may thus preserve more of the original appearance that ancestral Eurasians once had before the last ice age split them into East and West Eurasians some 20,000 years ago (Rogers, 1986). This may also be why Kennewick Man (an ancient skeleton found in Kennewick, Washington and dated to 8410 BP) looks more like a European than a present-day Amerindian. Kennewick Man might have been closer to that proto-Eurasian population.

This point is sometimes hard to grasp. Real evolutionary change—the kind that shapes physical appearance—involves only a tiny fraction of the genome. The rest of the genome will change little in a new environment with a new set of selection pressures, either because it has little or no adaptive value (i.e., junk DNA) or because it has the same adaptive value in a wide range of environments.

So the evolutionary changes that made other East Asians look different from the Ainu involve relatively few genes. At other genes, the two groups are genetically indistinguishable. We likewise see genetic overlap between many sibling species that are nonetheless anatomically distinct. The same disconnect exists between genetic and anatomical data when we look at dog breeds … or human populations.

But why have the Ainu been so evolutionarily conservative? Why has time stood still for them? They probably didn’t undergo the severe selection pressures that shaped the appearance of other East Asians, notably selection for Arctic adaptations like the epicanthic eye-fold. Keep in mind that the Japanese archipelago enjoyed a relatively mild climate during the last ice age. As a “refugium” it did not impose the harsh selection pressures that mainland Asia imposed on its human populations. 

References

Jinam, T., N. Nishida, M. Hirai, S. Kawamura, H. Oota, K. Umetsu, R. Kimura, J. Ohashi, A. Tajima, T. Yamamoto, H. Tanabe, S. Mano, Y. Suto, T. Kaname, K. Naritomi, K. Yanagi, N. Niikawa, K. Omoto, K. Tokunaga, & N. Saitou. (2012). The history of human populations in the Japanese Archipelago inferred from genome-wide SNP data with a special reference to the Ainu and the Ryukyuan populations, Journal of Human Genetics advance online publication 8 November 2012; doi: 10.1038/jhg.2012.114

Omoto, K. (1972). Polymorphisms and genetic affinities of the Ainu of Hokkaido. Hum. Biol. Oceania, 1, 278–288.

Omoto, K. (1973). The Ainu: a racial isolate? Israel J. Med. Sci., 9, 1195–1215.

Rogers, R.A. (1986). Language, human subspeciation, and Ice Age barriers in Northern Siberia. Canadian Journal of Anthropology, 5, 11‑22.

Are women changing color?

Tanned arm (source). Underarm skin color used to be a reliable measure of constitutive pigmentation (skin color before tanning). Is it still?

After puberty, girls become lighter-skinned than boys. This sexual differentiation has been shown to be hormonal in origin by a digit ratio study (Manning, Bundred, and Mather, 2004), by studies on normal, castrated, and ovariectomized individuals (Edwards & Duntley, 1939, Edwards & Duntley, 1949; Edwards et al., 1941), and by a twin study of boys and girls at different stages of puberty (Omoto, 1965). In addition, women are lighter-skinned than men in a wide range of human populations, although the sex difference is smaller in very light-skinned and very dark-skinned populations (Frost, 2007; Madrigal & Kelly, 2006).

This sex differences is reversed, however, in a recent study of subjects from Ireland, Poland, Italy, and Portugal: 

Surprisingly, we find in our cohort that males have lighter skin pigmentation (lower M) than females in all four European countries. (Candille et al., 2012)

All of the subjects were post-puberty (largely in their early to mid-20s) and the measurements came from the upper inner arm, a site relatively unaffected by tanning. So what happened?

First, a different kind of instrument was used to measure skin color:

Our results in populations of European ancestry contradict earlier anthropological studies that have concluded females are more lightly pigmented than males in most populations (reviewed in [2]). One potential reason for the conflicting results is the different instruments used. In early studies, which used the Evans Electric Limited (EEL) and Photovolt broad-spectrum spectrophotometers, skin pigmentation estimates may be confounded by the hemoglobin level to a greater extent than for the DermaSpectrometer used in the present study (Candille etal., 2012)

The Candille et al. research team didn’t measure skin color at all wavelengths of visible light. They focused on those wavelengths that melanin absorbs. Previous researchers had studied the overall visual difference between male and female skin, which is due as much to differences in hemoglobin as to differences in melanin. In short, men are browner and ruddier than women.

It is misleading, then, to state that the male subjects had lighter skin pigmentation. Hemoglobin too is a skin pigment.

Nonetheless, it’s still surprising that the women had more melanin than did the men, and this was on the upper inner arm—a body site relatively unexposed to tanning. That finding does contradict earlier studies. According to the earliest major one on human skin color:

It is generally known that women are lighter colored than men. From our studies it is apparent that this is due to the female skin containing less blood and melanin (Edwards & Duntley, 1939)

The study also found that this sex difference was smaller over much of the body surface, apparently because women exposed more of it to the sun:

The skin of women is generally poorer in melanin than that of men (fig. 16). However, because of their manner of dress, women of the white races show a comparatively higher pigmentation of the shoulders, upper chest and upper extremities (Edwards & Duntley, 1930)

For this reason, most subsequent researchers have measured skin color at the upper inner arm, this site being relatively unexposed to the sun and thus providing a better measure of constitutive pigmentation.

The study’s authors, Edwards and Duntley, went on to study castrated and ovariectomized subjects to understand how the sex hormones affect skin color. Although testosterone had a stronger impact than did estrogen on skin pigments (both melanin and hemoglobin), the absence of these hormones did not eliminate all of the sex-specific characteristics of male and female skin. The two researchers concluded:

Our observations show that ovariectomy does not entirely change the basic peculiarities which distinguish the female from the male skin. Similarly, the male castrates previously studied had maintained to some extent, their differences from the female. In both sexes, therefore, we can assert that sex differences are basically due to genic influence. This base line of pigmentary characteristics is then modified by the presence of the sex hormones. Unlike the situation in many other animals, where reactivity to the hormones is localized in special areas, the human skin reacts probably in its entirety (Edwards & Duntley, 1949)

This “genic influence” is now known to be the prenatal hormonal surge that determines whether an individual will develop as a boy or a girl. “Presence of the sex hormones” would be better described as “circulating sex hormones”—the individual’s current hormonal status. This is the conclusion of Manning, Bundred, & Mather (2004) in their digit ratio study:

We find that 2D:4D and female ‘constitutive’ pigment scores are negatively related. Since women with light skin tend to have high ‘feminised’ digit ratios, and there is evidence that the 2D:4D ratio is positively related to prenatal oestrogen levels, it seems that oestrogen may have an early organisational effect on skin pigment in women. The absence of a relationship between 2D:4D and skin colour in men suggests that other factors, such as prenatal testosterone, may obscure the in utero effects of oestrogen.

Other studies have focused on the sexual differentiation of skin color at puberty. All of them conclude that female skin loses melanin at puberty:

Though both the boys and the girls of the two populations show a decline in the melanin content of the skin when passing through adolescence, yet the decline in the pigment is so much pronounced in the girls that it reverses the sex differences in skin pigmentation. The boys, who were lighter in skin colour than the girls at younger ages (i.e. below 13 years), become darker than the girls at advanced age (at least up to 16 years) (Kalla, 1973).

In the above study, skin color was measured on the upper inner arm at a time of year (December-January) when tanning was minimal. Kalla (1973) concluded that the external environment could not have caused this sexual differentiation, the only possible explanation being “the puberty changes of the endocrine status.”

This was likewise the conclusion of Mesa (1983):

[…] the remarkable changes in pigmentation that occurred during the pubertal period (and which are related to hormonal changes) are a major factor in the differences (between the sexes and between the [upper inner] arm and the forehead) that were found at older ages and, also, in the differences observed in the adult population.

So how can we explain the recent findings by Candille et al. (2012)? Perhaps underarm skin color is no longer a reliable measure of constitutive pigmentation, i.e., color of untanned skin. Removal of underarm hair has become the norm in recent years, especially among European women. This has led to concern about tan lines in the underarm region and a consequent desire for “full body tanning,” as described below by one e-columnist:

How to Tan Underarms in a Tanning Bed

By Lauren Wise, eHow Contributor

A tanning bed provides a quick, easy, natural looking tan to a man or woman's body. The bed nearly triples your tanning time with the extra strong rays it provides. Unfortunately, since it is difficult to move around in a tanning bed, it is hard to tan every angle and crevice of the body, in particular the underarms. It is easy to change this by alternating your movements within the tanning bed throughout the session.

References

Candille, S.I., Absher, D.M., Beleza, S., Bauchet, M., McEvoy, B., et al. (2012). Genome-Wide Association Studies of Quantitatively Measured Skin, Hair, and Eye Pigmentation in Four European Populations. PLoS ONE 7(10): e48294. doi:10.1371/journal.pone.0048294

http://www.plosone.org/article/info:doi/10.1371/journal.pone.0048294

Edwards, E.A. & S.Q. Duntley. (1949). Cutaneous vascular changes in women in reference to the menstrual cycle and ovariectomy, American Journal of Obstetrics and Gynecology, 57, 501-509.

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

Edwards, E.A., J.B. Hamilton, S.Q. Duntley, & G. Hubert. (1941). Cutaneous vascular and pigmentary changes in castrate and eunuchoid men, Endocrinology, 28, 119-128.

File:Skin tanning.JPG

http://commons.wikimedia.org/wiki/File:Skin_tanning.JPG?uselang=fr

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.

Kalla, A.K. (1973). Ageing and sex differences in human pigmentation, Zeitschrift für Morphologie und Anthropologie, 65, 29-33.

Madrigal, L. & W. Kelly. (2006). Human skin-color sexual dimorphism: A test of the sexual selection hypothesis, American Journal of Physical Anthropology, 132, 470-482.

Manning, J.T., P.E. Bundred, & F.M. Mather. (2004). Second to fourth digit ratio, sexual selection, and skin colour, Evolution and Human Behavior, 25, 38-50.

Mesa, M.S. (1983). Analyse de la variabilité de la pigmentation de la peau durant la croissance, Bulletin et mémoires de la Société d'Anthropologie de Paris, t. 10 série 13, 49-60.

Omoto, K. (1965). Measurements of skin reflectance in a Japanese twin sample, Journal of the Anthropological Society of Nippon (Jinruigaku Zassi), 73, 115-122.

Wise, L. (2012). How to Tan Underarms in a Tanning Bed, eHow style

http://www.ehow.com/how_5034924_tan-underarms-tanning-bed.html

Are the cads outbreeding the dads?

Whom will she choose? (source)

 

There has been much talk about two findings from a recent study: (a) boys reach puberty at different ages in different ethnic groups and (b) boys are reaching puberty earlier now than in the recent past.

The first finding is in line with previous studies:

[…] we found significant differences in the age of onset of stage 2 genital and pubic hair growth between African American boys as compared with white and Hispanic boys and transition to testicular volumes ≥4 mL (but not 3 mL). The meaning of this finding is unclear, as no existing studies inform differences in mean testicular size at given ages, by race/ethnicity, and sexual maturity stage; or in racial/ethnic differences in the rate of advancement through the Tanner stages over time. (Herman-Giddens, 2012)

The second finding is new:

We observed that onset of secondary sexual characteristics in US boys as seen in office practice appears to occur earlier than in previous US studies and the 1969 British study commonly used for pubertal norms. […] White boys in our study entered stage 2 genital growth 1.5 years earlier than the British boys (10.14 vs 11.60 years of age).

 

[…] These data are consistent with recent trends from other countries, such as Denmark, Sweden, Great Britain, Italy, and China. For example, urban Han Chinese boys achieve a testicular volume of ≥4 mL (13% by age 9) and spermarche earlier than studies conducted several decades ago; Danish boys achieve a testicular volume  ≥3 mL more than 3 months earlier now than 15 years ago. (Herman-Giddens, 2012)

The authors put the cause down to “exposure to chemicals, changes in diet, less physical activity, and other modern lifestyle changes and exposures.” In an article for CNN, the lead author elaborated:

 

"The changes are too fast," Herman-Giddes said. "Genetics take maybe hundreds, thousands of years. You have to look at something in the environment. That would include everything from (a lack of) exercise to junk food to TV to chemicals." (Wilson, 2012)

Yes, new genetic variants take time to appear through mutation. But variants for early puberty already exist in the population. Natural selection has only one thing to do: increase the proportion of people with those variants. And that can happen with each passing generation.

In any given population, almost all variability in male pubertal timing is genetic. This was the conclusion of a Swedish twin study: 

The heritability was 0.91 for age at onset of growth spurt and 0.93 for age at peak height velocity in this Swedish cohort of male twin pairs. Of interest is that these heritability estimates are almost the same as those reported from a Belgian twin study; that is, 0.93 and 0.92, respectively. Lower heritability estimates, 0.49 and 0.74, respectively, were found in a Polish twin study. (Silventoinen et al., 2008)

There is thus plenty of genetic variation for selection to act on. No need to wait for new mutations. But why would there be natural selection for earlier male puberty?

One reason is that early puberty is genetically linked to other sexual characteristics. In particular, a class of X-linked androgen receptor alleles is linked in males to aggression, impulsivity, sexual compulsivity, and lifetime number of sex partners and in females to paternal divorce, father absence, and early menarche (Comings et al., 2002). It is likely that these alleles also influence male pubertal timing, but research on this point is lacking—apparently because it is difficult to find a marker for pubertal maturation among boys that is as salient as age at menarche among girls (Ge et al., 2007). Early male puberty thus seems to be part of a “package,” or more precisely a reproductive strategy, that affects the way men go about finding a mate. Natural selection may favor one strategy or another, depending on the current cultural environment.

Is natural selection now favoring the “cads” over the “dads”? That might be what’s happening. As sexual relationships become less stable and shorter-term, women will ignore men who are oriented towards stable, long-term relationships.  This was the conclusion of a study directed by Kruger et al. (2003) at the University of Michigan's Institute for Social Research:

In the study, 257 women in college were asked to read passages from Scott's novels. Each read a paragraph describing a dark hero and one describing a proper hero. Then the women were asked which type of man they would prefer for a relationship.

 

As predicted by the cad-dad theory of human mating strategies, the women preferred the proper heroes for long-term unions. When asked which character they would like to see their future daughters choose, they also selected proper heroes. But when asked who appealed to them most for short-term affairs, the women turned to the dark heroes: the handsome, passionate and daring cads (Duenwald, 2003).

References

Comings, D.E., D. Muhleman, J.P. Johnson, & J.P. MacMurray. (2002). Parent-daughter transmission of the androgen receptor gene as an explanation of the effect of father absence on age of menarche. Child Development, 73, 1046-1051.

Duenwald, M. (2003). For a good time, well, don’t call dad, University of Nebraska-Lincoln, Anthropology, Raymond Hames

http://www.unl.edu/rhames/courses/current/dad-cad.htm

Ge, X., M.N. Natsuaki, J.M. Neiderhiser, & D. Reiss. (2007). Genetic and Environmental Influences on Pubertal Timing: Results From Two National Sibling Studies, Journal of Research on Adolescence, 17, 767–788.

Herman-Giddens, M.E., J. Steffes, D. Harris, E. Slora, M. Hussey, S.A. Dowshen, R. Wasserman, J.R. Serwint, L. Smitherman, & E.O. Reiter. (2012). Secondary sexual characteristics in boys: Data from the Pediatric Research in Office Settings Network, Pediatrics, 130, e1058-e1068.

http://pediatrics.aappublications.org/content/130/5/e1058.full.pdf+html

Kruger, D.J., M. Fisher, & I. Jobling. (2003). Proper and dark heroes as DADS and CADS. Alternative mating strategies in British Romantic literature, Human Nature, 14, 305-317.

Silventoinen, K., J. Haukka, L. Dunkel, P. Tynelius, & F. Rasmussen. (2008). Genetics of pubertal timing and its associations with relative weight in childhood and adult height: The Swedish Young Male Twins Study, Pediatrics, 121, e885-891

http://pediatrics.aappublications.org/content/121/4/e885.full.pdf+html

Wilson, J. (2012). Boys – like girls – hitting puberty earlier, October 23, CNN

http://edition.cnn.com/2012/10/20/health/boys-early-puberty/index.html

A detour through Europe?

The lithic technology of southwestern France (c. 22,000-17,000 BP) strangely resembles that of the first paleo-Amerindians (c. 12,000). Some people speculate that early Europeans reached North America by crossing the Atlantic. The truth is even more incredible. Early Europeans spread eastward and became the ancestors not only of the Amerindians but also of East Asians. (source)

The recent study by Beleza et al. (2012) has elicited comment on two findings:
 

1. European skin turned white long after modern humans had entered Europe (c. 40,000 BP). Moreover, it whitened relatively fast—between 19,000 and 11,000 years ago. Such a narrow timeframe implies some form of selection, and not just relaxation of selection for darker skin. 

2. The new skin-color alleles did not come from the Neanderthals. This point may have broader repercussions because some have argued that the rapidity of evolution among modern humans required “cherry picking” of useful alleles from Neanderthals and other archaic hominins.

But another finding deserves comment. This is the discovery that an earlier (though minor) lightening of skin color had occurred shortly after the entry of modern humans into Europe:

[…] the initial stages of European skin lightening occurred in a proto-Eurasian population, about 30,000 years ago, after the out-of-Africa migration ~60,000-70,000 years ago […] and slightly more recently than the earliest archaeological evidences for the dispersal of anatomically modern humans in Europe, around 40,000 years ago (Beleza et al., 2012).

It’s widely accepted that the ancestors of Europeans and East Asians parted company long after modern humans had begun spreading out of Africa. It’s usually assumed, however, that this splitting took place somewhere in the Middle East or Central Asia. If we are to believe Beleza et al (2012), it must have happened after the entry of modern humans into Europe.

So the first Europeans were also the first East Asians. Cro-Magnon Man wasn’t just a proto-European. He was also a proto-Eurasian.

From Africa to East Asia … by way of Europe?

A straight line isn’t always the easiest route from point A to point B. In any case, modern humans weren’t going anywhere in particular when they began spreading out of Africa. They were seeking new lands and following the path of least resistance.

Let’s suppose you’re a band of hunter-gatherers in the Levant circa 50,000 BP. What new territories would tempt you? The Iranian Plateau and, beyond it, the arid steppes of Central Asia? No, that doesn’t seem very tempting.

You would look to lands farther north and west along the Mediterranean. Those lands are similar in climate, vegetation, and wildlife. You can continue using the same life skills, since the means of subsistence are almost the same.

As your descendants grow in numbers and spread farther out, they will eventually bump up against an ecological zone that differs in climate, vegetation, and wildlife. At that point, they’ll have to stop their advance and begin a slow process of adaptation within transitional environments on the edge of this zone. Once they’ve sufficiently adapted, they will break out from this “beachhead.” And begin a new wave of advance.

This is what happened when modern humans spread north from the Mediterranean and into more boreal environments with wider seasonal variations. Finally, they encountered the Eurasian steppe-tundra—a vast open plain of grassland stretching from southwestern France to Manchuria. Living in that environment would require a whole suite of new adaptations. The men would have to become much more mobile in order to hunt the herds of wandering herbivores. The women would have to abandon food gathering and take on new tasks like shelter building and garment making. So where do you think those adaptations were developed?

In southwestern France. This “beachhead” was the most southerly and resource-rich portion of the Eurasian steppe-tundra (Mellars, 1985). Sheltered valleys dissected the steppe and offered trees and other non-arctic vegetation, particularly on south-facing slopes (Blades, 1999b). In this protected environment, hunter-gatherers could live off salmon, local game, wild fruits, grains, and tubers while hunting reindeer herds that passed through in the fall and winter (Blades, 1999a; Blades, 1999b; Mellars, 1985). As the climate improved from 30,000 to 27,000 BP, closed forests became established, the herds moved further afield, and reindeer hunting was all but abandoned at valley sites (Blades, 1999b). The men had to move out of the valleys and onto the surrounding tundra tablelands. They now had to make further adaptations: more efficient use of raw materials (wood for fire and shelter, lithic materials); long-distance travel to procure them; and development of extensive social networks (Goebel, 1999; Hahn, 1987).

Sometime after 28,000 BP, they broke out from the beachhead and colonized the tundra plains in their entirety. This breakout may correspond to a demographic expansion (23,000-21,000 BP) of a genetic lineage that occurs most often among the Basques of northern Spain and southwestern France (Richards et al., 1996; Richards et al., 2000). Relatively few people were involved, as indicated by the very low variability of the northern European gene pool (Reich et al., 2001). Presumably, there were many semi-isolated groups, each one tinkering with its own mix of cultural adaptations until one of them got it right and colonized the Eurasian steppe-tundra.

After the breakout, nothing could stop them from spreading east throughout the Eurasian steppe-tundra … all the way to the Pacific Ocean, and from there to Beringia and North America. They would in time become the ancestors of most people living today, not only Europeans but also East Asians and Amerindians.

For this, we have several lines of evidence:

- a Y-chromosome study has found that all North Eurasian peoples descend from a common ancestral population dated to about 15,000 BP (Stepanov & Puzyrev, 2000; see also Armour et al., 1996; Santos et al., 1999; Zerjal et al., 1997).

- the language families of northern Eurasia, particularly Uralic and Yukaghir and more generally Uralic-Yukaghir, Eskimo-Aleut, Chukotko-Kamchatkan and Altaic, share deep structural affinities that point to a common origin and not simply to word borrowing (Cavalli-Sforza, 1994, pp. 97-99; Fortescue, 1998; Rogers, 1986).

- archeological evidence (characteristic lithic technology, grave goods with red ocher, and sites with small shallow basins) also suggests a common cultural tradition throughout Europe and Siberia 20,000 to 15,000 years ago (Goebel, 1999; Haynes, 1980; Haynes, 1982).

- dental and cranial remains from Mal’ta (23,000-20,000 BP) in southern Siberia indicate strong affinities with Upper Paleolithic Europeans (Alexeyev & Gokhman, 1994; Goebel, 1999).

Finally, the lithic technology of southwestern France (c. 22,000-17,000 BP), referred to as “Solutrean”, strangely resembles that of the first paleo-Amerindians (c. 15,000-12,000). Solutrean and Clovis points share common characteristics. Both are thin and bifacial, and both share the intentional use of the outre passé, or overshot flaking technique, which quickly reduces the thickness of a biface without reducing the width.

This similarity has led to the “Solutrean hypothesis”— the idea that early Europeans reached North America by crossing the Atlantic. Again, the easiest route between two points isn’t always a straight line. For the proto-Eurasians of southwestern France, the road to North America ran east ... over the unbroken grasslands of the Eurasian steppe-tundra.

References

Alexeyev, V.P., & Gokhman, I.I. (1994). Skeletal remains of infants from a burial on the Mal'ta Upper Paleolithic site. Homo, 45, 119‑126.

Armour, J.A.L., Anttinen, T., May, C.A., Vega, E.E., Sajantila, A., Kidd, J.R., Kidd, K.K., Bertranpetit, J., Paabo, S., & Jeffreys, A.J. (1996). Minisatellite diversity supports a recent African origin for modern humans. Nature Genetics, 13, 154‑160.

Beleza, S., A. Múrias 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

Blades, B.S. (1999a). Aurignacian settlement patterns in the Vézère valley, Current Anthopology, 40, 712-719.

Blades, B.S. (1999b). Aurignacian lithic economy and early modern human mobility: new perspectives from classic sites in the Vézère valley of France, Journal of Human Evolution, 37, 91-120.

Cavalli-Sforza, L.L., Menozzi, P. & Piazza, A. (1994). The History and Geography of Human Genes. Princeton: Princeton University Press.

Fortescue, M.D. (1998). Language Relations across Bering Strait. Reappraising the Archaeological and Linguistic Evidence. Cassell: London.

Goebel, T. (1999). Pleistocene human colonization of Siberia and peopling of the Americas: An ecological approach. Evolutionary Anthropology, 8, 208‑227.

Hahn, J. (1987). Aurignacian and Gravettian settlement patterns in Central Europe. In The Pleistocene Old World, O. Soffer (Ed.). New York: Plenum Press, pp. 251‑261.

Haynes, C.V. (1982).Were Clovis progenitors in Beringia? In Paleoecology of Beringia, D.M. Hopkins (Ed.). New York: Academic Press, pp. 383‑398.

Haynes, C.V. (1980). The Clovis culture. Canadian Journal of Anthropology, 1, 115‑121.

Mellars, P.A. (1985). The ecological basis of social complexity in the Upper Paleolithic of Southwestern France. In Prehistoric Hunter‑Gatherers. The Emergence of Cultural Complexity, T.D. Price & J.A. Brown (Eds.). Orlando: Academic Press, pp. 271‑297.

Reich, D.E., M. Cargill, S. Bolk, J. Ireland, P.C. Sabeti, D.J. Richter, T. Lavery, R. Kouyoumjian, S.F. Farhadian, R. Ward, and E.S. Lander. (2001). Linkage disequilibrium in the human genome, Nature, 411, 1999-2001.

Richards, M., H. Côrte-Real, P. Forster, V. Macaulay, H. Wilkinson-Herbots, A. Demaine, S. Papiha, R. Hedges, H.-J. Bandelt, & B. Sykes. (1996). Paleolithic and Neolithic lineages in the European mitochondrial gene pool, American Journal of Human Genetics, 59, 185-203.

Richards, M., V. Macaulay, E. Hickey, E. Vega, B. Sykes, et al. (2000). Tracing European founder lineages in the Near Eastern mtDNA pool, American Journal of Human Genetics, 67, 1251-1276.

Rogers, R.A. (1986). Language, human subspeciation, and Ice Age barriers in Northern Siberia. Canadian Journal of Anthropology, 5, 11‑22.

Santos, F.R., Pandya, A., Tyler‑Smith, C., Pena, S.D.J., Schanfield, M., Leonard, W.R., Osipova, L., Crawford, M.H., & Mitchell, R.J. (1999). The Central Siberian origin for Native American Y chromosomes. American Journal of Human Genetics, 64, 619‑628.

Stepanov, V.A., & Puzyrev, V.P. (2000). Evolution of Y‑chromosome haplotypes in populations of North Eurasia. American Journal of Human Genetics, 67, 220.

Zerjal, T., Dashnyam, B., Pandya, A., Kayser, M., Roewer, L., Santos, F.R., Scheifenhövel, W., Fretwell, N., Jobling, M.A., Harihara, S., Shimizu, K., Semjidmaa, D., Sajantila, A., Salo, P., Crawford, M.H., Ginter, E.K., Evgrafov, O.V., & Tyler‑Smith, C. (1997). Genetic relationships of Asians and Northern Europeans, revealed by Y‑chromosomal DNA analysis. American Journal of Human Genetics, 60, 1174‑1183. 

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

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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

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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.

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