Saturday, May 24, 2014

The puzzle of European hair, eye, and skin color


 
Taylor Swift (photo by David Shankbone). The physical appearance of Europeans seems to result from a selection pressure that acted primarily on women and only secondarily on men. This is especially true for highly visible traits on or near the face—the focus of visual attention.

 

I have just published a paper on "The puzzle of European hair, eye, and skin color." The introduction is reproduced below (reference citations have been removed for ease of reading). The full text is available here.
 

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Most humans have black hair, brown eyes, and brown skin. Europeans have a different color scheme, their hair being also brown, flaxen, golden, or red, and their eyes also blue, gray, hazel, or green. Finally, their skin is pale, almost like an albino's.

How did this unusual color scheme come about? Perhaps the genetic change that lightened the skin also affected the hair and the eyes. Yet the genes are different in each case. European skin lightened mainly through the appearance of new alleles at three genes: SLC45A2, SLC24A5, and TYRP1. European hair color diversified through a proliferation of new alleles at MC1R. European eye color diversified through a proliferation of new alleles in the HERC2-OCA2 region and elsewhere.

Light skin is associated with a few of the new hair and eye color alleles, particularly the ones for red hair or blue eyes. Conceivably, these alleles may be a side effect of selection for lighter skin. But why would such selection increase the total number of alleles for hair and eye color, especially when so many of them have little or no effect on skin color? And why have neither red hair nor blue eyes reached fixation in any human population, even those with milk-white complexions?

The European color scheme has another puzzling aspect. It seems to result from a selection pressure that acted primarily on women and only secondarily on men:

- Hair color varies more in women than in men. Redheads are especially more frequent among women.

- Eye color varies more in women than in men when both copies of the so-called blue-eye allele are present, the result being a greater diversity of female eye colors wherever blue eyes are the single most common phenotype, i.e., in northern and eastern Europe.

- Blue eyes are associated in men with a more feminine face shape.

- In all human populations, women are paler than men after puberty. This post-pubescent lightening is due to sexual maturation and not to differences in sun exposure. In women, lightness of skin correlates with thickness of subcutaneous fat and with 2nd to 4th digit ratio—a marker of prenatal estrogenization. Admittedly, this sex difference is not greater in Europeans than in other populations, although it could not easily be otherwise, since Europeans are so close to the physiological limit of depigmentation.

While women are more diverse than men both in hair and eye color, this greater diversity came about differently in each case. With hair color, women have more of the intermediate hues because the darkest hue (black) is less easily expressed. With eye color, women have more of the intermediate hues because the lightest hue (blue) is less easily expressed. 

In sum, European hair and eye color diversified through a selection pressure that acted on different genes via different pigmentary changes. The common denominator seems to be the creation of new visual stimuli on or near the face—the focus of visual attention.


Reference 

Frost, P. (2014). The puzzle of European hair, eye, and skin color, Advances in Anthropology, 4, 78-88.
http://www.scirp.org/journal/PaperInformation.aspx?PaperID=46104

15 comments:

Anonymous said...

Very interesting.

It seems quite plausible that the EDAR370A gene that Nicholas Wade mentions played a parallel role in the evolution of modern East Asian phenotypes during the same time period.

Both Europeans and East Asians as we know them seem to be quite recent evolutionary phenomena - so recent that, to some degree, they have co-evolved with the rise of modern civilization since the Neolithic.

Prior to the appearance and fixation of this particular suite of genes, it's conceivable that Eurasian populations were very hard to distinguish from one another, and, as a rule, may have looked something like the Murrayian type of Australian Aborigine that Joseph Birdsell described - stocky, brown-skinned, and probably quite hirsute.

barakobama said...

Geneticker is going to search for pigmentation-related SNPs in the samples from Skoglund 2014 today. He already discovered alot by looking at their Y SNPs(Gok4 had hg I2, Ajv52 had hg I2a2a1, Ajv70 did not have hg I, etc.), so we might learn more about the pigmentation of European's two ancestral populations; Hunter gatherers(WHG+ANE) and farmers(EEF, and or other middle eastern ancestors).

I have some ideas and arguments to give to Peter, but I will wait till Geneticker's results and after i do more research.

Sean said...

The world sees no puzzle, it's all so obviously down to UVB vitamin D synthesis at high latitude being blocked by melanin. Wade says that "the pale skin necessary for living at high latitudes".

In view of the fact that bio active vitamin D corrolates with bone density , blacks in Europe and North America must really have sub clinical rickets, not denser bones.

And this recent research must be all wrong.

ben10 said...

Any possible effects of the introgression of Neanderthal genes in Europeans?

Neanderthal genes could have trigger these phenotypic variations before they almost disappeared to the current level.
The early modern/Neanderthal hybrids could have experienced a short period of genetic and/or transcriptomic instability during their entrance in Europe.

Perhaps you could reverse engineer that, and find out If the genes containing the hair and eyes alleles you mentioned have been unstable during and after the Neanderthal gene introgression.
There may have been more allelic variants for hair, skin, eyes, in the Cro-Magnon populations, which I assume had more than the current 4% level of Neanderthal dna, of which only survived the few alleles you mentioned.

barakobama said...

Very interesting paper Peter.

I think you wrongly called many lighting mutations European. Namely the skin lighting ones, in genes SLC24A5 and SLC24A5, which are just about as popular in middle easterns and many south Asians.

(1)http://mbe.oxfordjournals.org/content/24/3/710.full

(2)http://dienekes.blogspot.com/2013/11/europeans-and-south-asians-share-by.html

(3)http://www.academicjournals.org/article/article1379514057_Lucotte%20and%20Yuasa%20pdf.pdf

(4)http://www.theapricity.com/forum/showthread.php?35882-New-Hair-and-Eye-color-statistics-(2011)

The Ala111 mutation is nearly fixated in Europeans and most middle easterns(1)(2). African, south Asian, and east Asian admixture can probably explain the few populations in Europe and the middle east who are not fixated for it. The 374F mutation is around 95% in northern Europe, anywhere from 70-90% in southern Europe, and around 40-50% in the middle east(1)(3). This mutation is associated with light skin and hair, so the higher percentages in northern Europe than in southern Europe and in Europe than in the middle east, is probably because of hair color difference.

rs1042602 A/A or A/C, is around 40-50% in Europe and the middle east(1). I can't find percentages for other light skin mutations, but I do remember all were at the same rate in Europe and the middle east.

My point is that these are not exclusively European mutations, and there are unknown factors giving Europeans uniform light skin.

Blonde and red hair, and light colored eyes are also not exclusively European, and certainly did not originate in Europe. Even though WHG(what makes Europeans distinct genetically from middle easterns) ancestry is pretty much exclusive to Europe, light eyes range from 15-20% in the near east, and even exist in Arabia and north Africa at around 5%(4).

Blonde and red hair are very very very rare in the middle east but they does exist.

barakobama said...

What we have learned about the pigmentation of European's two stone age ancestral populations; farmers and hunter gatherers.

Pigmentation of stone age Swedish hunter gatherers and farmers.

http://genetiker.wordpress.com/2014/05/25/pigmentation-snp-genotypes-for-prehistoric-swedes/

Spreadsheet of stone age European hunter gatherer's and farmer's genotypes in pigmentation SNPs of the 8-plex and Hirisplex system, and SNPs of blue eye haplotypes.

https://docs.google.com/spreadsheets/d/1I8NhFE8j8TrmNm_fW9QN66TwIiyXE3ZuBZoDolVkPpw/edit?usp=sharing

Map of Mesolithic-Neolithic European hunter gatherer DNA

https://mapsengine.google.com/map/edit?mid=zpAcd_2YNln8.kYMnaPX2WqH0

>The hunter gatherers were primarily light eyed. While the farmers were almost entirely dark eyed.

>Both European's stone age farmer and hunter gatherer ancestors were fixated for dark hair.

>Most European hunter gatherers did not have light skin mutations which are fixated in modern Europeans, while the farmers had them at around the same rate as modern Europeans.

>Most European hunter gatherers had rs12203592(in gene IRF4 T/T or C/T(so far 4/4 samples). It has to mean something.

Conclusions

Obviously known light skin mutations were selected for in European's hunter-farmer mixed ancestors. Blonde hair went from close to nothing in stone age Europe, to being the main hair color in many northern Europeans probably within a few thousand years at the most. Northern European's ancestors must have really loved blonde hair, because sexual selection and other forms of non-survival selection is the only explanation for such a quick rise in percentages.

In my opinion eastern European groups like Indo Europeans probably spread blonde hair.

Interestingly bronze age Indo Iranians from south Siberia were pigmentated just like modern north Europeans. They had the combination of farmer light skin, hunter light eyes, and the newly selected light hair.

Light hair probably rose with old hunter gatherer light eyes, which is why the two are connected today. There is a light hair-eye-skin package in modern Europe, that closely correlates with post-Neolithic east European ancestry(primarily indo Europeans).

Red hair is probably a whole nother story. It is not pan-European, it only reaches 1% in west Europe and the Urals. It was probably selected for in some populations recently, like during the copper and bronze ages. Maybe for similar reasons as light hair was selected for, and that could maybe explain why redheads also have a high percentage of light eyes.

I think these pigmentation changes did occur in pre historic Europe, just I don't know why. Maybe sexual selection is why.

Sean said...

"A vitamin D-deficient diet rescued many aging-like phenotypes of Klotho-deficient mice and FGF23-deficient mice"

Vitamin D supplementation reduces soluble Klotho concentration in hemodialysis patients"

"Approximately 20% of the population carries one copy of the KL-VS variant of KLOTHO, which results in an increased level of klotho protein in the blood of carriers"

BLOOD tests showed that subjects who had one copy of the KL-VS variant also had higher levels of circulating klotho protein. The levels decreased with age as others have observed. The researchers speculate that the age-related decrease in circulating levels of klotho protein may have caused some of the decline in performance on the cognitive tests. [...]
“Overall our results suggest that klotho may increase cognitive reserve or the brain’s capacity to perform everyday intellectual tasks,” said senior author Lennart Mucke, M.D."

Sean said...

Genes and intelligence: A potent source of genetic variation in cognitive ability has just been discovered

"What they found was startling. KL-VS did not curb decline, but it did boost cognitive faculties regardless of a person’s age by the equivalent of about six IQ points. If this result, just published in Cell Reports, is confirmed, KL-VS will be the most important genetic agent of non-pathological variation in intelligence yet discovered.."

Peter Fros_ said...

Anon,

The Ainu may best preserve this original Eurasian phenotype, which was predominant across northern Eurasia until the last glacial maximum (20,000 to 15,000 years ago). It was probably only then that west Eurasians and east Eurasians began to pursue different evolutionary trajectories. This may be why early Amerindians looked more European. They were closer in time to the west Eurasian/east Eurasian split.

Barak,

My position is that present-day Middle Easterners are largely the product of a demographic expansion that pushed out of Europe around the Holocene/Upper Paleolithic time boundary.

I’m wary of mtDNA data, especially for the transition from hunting/fishing/gathering to farming. Many of these haplogroups are sensitive to natural selection, especially with regard to the pattern of energy use. Farming tends to rely on a steady expenditure of energy, whereas hunting requires short bursts of energy.

“Blonde and red hair, and light colored eyes are also not exclusively European, and certainly did not originate in Europe.”

Non sequitur

Sean,

If skin color varies among human populations, why can’t vitamin-D metabolism? This is something that many doctors have trouble understanding. Unfortunately, there’s a lot of support within the medical community for large-scale administration of vitamin D supplements to African Americans. Their attitude seems to be: “What could go wrong? Vitamin-D supplementation is harmless!” Yeah, people said the same about thalidomide. If this goes through, a lot of African Americans are going to experience premature aging, just like Michael Jackson. They’ll look like withered old men and women by the time they reach their 40s.

I wonder how the KL-VS allele varies among human populations.

Ben10,

This has been investigated. The alleles for European hair, eye, and skin color seem to be of modern human origin. They don’t appear in the reconstructed Neanderthal genome.

barakobama said...

Pigmentation SNPs of MA1 and AG2.

http://genetiker.wordpress.com/2014/05/28/pigmentation-snp-genotypes-for-malta-1-and-afontova-gora-2/

The results confirm that MA1 had dark eyes unlike Mesolithic and Neolithic European hunter gatherers. The results are constant with MA1 and AG2 having dark hair, but there are not enough SNPs to be for sure.

AG2 had skin lighting mutation rs1426654 A/A, like Motala12, Stuttgart, Otzi, Gok2, and bronze-iron age Siberian Indo Iranians, proving this mutation is very ancient in west Eurasians. AG2 having this mutation is constant study which estimated this mutation to be 22,000-28,000 years old. I think it is older though because it existed in WHG, ANE, and middle easterns(brother to WHG+basal Eurasian), who are the three main ancestral groups of modern west Eurasians.

MA1 had rs1426654 G/G, like most European hunter gatherer samples, and is evidence the majority of WHG-ANE hunter gatherers did.

barakobama said...

Peter,

"My position is that present-day Middle Easterners are largely the product of a demographic expansion that pushed out of Europe around the Holocene/Upper Paleolithic time boundary.

I’m wary of mtDNA data, especially for the transition from hunting/fishing/gathering to farming. Many of these haplogroups are sensitive to natural selection, especially with regard to the pattern of energy use. Farming tends to rely on a steady expenditure of energy, whereas hunting requires short bursts of energy.
"

There is no evidence in modern mtDNA and Y DNA variation that modern middle easterns primarily descend from a migration from Upper Palaeolithic Europe. Everything points to a middle eastern origin of every major west Eurasian mtDNA haplogroup, RO, ROa, HV, HV1, maybe Europe for HVO, H, R2'JT, JT, J, T, etc. etc. They all point to origins in the middle east not Europe.

Upper Palaeolithic Europeans were ancestors of Mesolithic ones. U5 already been found in the Gravettian(two over 30,000 year old samples), Solutrean, and magdalenian cultures, proving its existence in Upper Palaeolithic Europe. Upper Palaeolithic European mtDNA shows no evidence of being ancestral for clades that appear to have originated in the middle east during the Upper Palaeolithic age like H, J, and T.

In a way your theory has already been proven incorrect with ancient DNA.

"I’m wary of mtDNA data, especially for the transition from hunting/fishing/gathering to farming. Many of these haplogroups are sensitive to natural selection, especially with regard to the pattern of energy use. Farming tends to rely on a steady expenditure of energy, whereas hunting requires short bursts of energy."

Even so, that doesn't take away the fact that modern Europeans largely descend from the near easterns who gave Europe farming.

This theory contridicts your other theory because in this theory you are trying to prove Upper Palaeolithic maternal continuum in europe, and in the other one you are trying to prove middle easterns(like early European farmers) descend from Upper Palaeolithic Europeans.

The evidence says that there are unknown factors giving Europeans light skin and there is no way to predict the skin color of pre historic populations, like ANE and WHG, by finding whether they had known light skin mutations or not. I don't understand why you and others stubbornly refuse to believe these facts.

Sean said...

The UV theory explanation for light skinned agriculturalists is the removal of meat from the diet makes creates a need for white skin because an agricultural diet causes nutritional rickets, which vitamin D can help. But nutritional rickets is common in Africa. And I would point out that the hunter gatherers of Africa are far more light skinned that African agriculturalists.

Anyway, it is most unlikely that European hunter gatherers had dark skin long after they had been selected for light eyes; no current population shows that evolutionary combination. There is no credible explanation for the evolution of light eyes but sexual selection, and males are lighter skinned than females to the extent that is is used as a sex recognition cue.

Gottlieb said...

I think if the modern indian obsession with light skin will can increase the number of lighter indians and if it happen with europeans when the majority them was 'brown skinned''??

Anonymous said...

I kind of agree with the general, but not specific ideas of this article. evo-psy studies and even global data from dating sites clearly suggest that asian women are more a product of runaway male sexual selection than caucasian women, with black women and asian men faring the worst in "the global gene pool," while caucasians show signs of having the closest thing to "balancing selection". If recorded Ainu traditions are indicative of their "recent" evolutionary past, they were highly monogamous and the young men and women had equal say in who they would marry.

Anonymous said...

"The common denominator seems to be the creation of new visual stimuli on or near the face—the focus of visual attention."

Taking that back a step could the first stage in this process have been slightly lightening the skin while reddening the lips (which I assume is possible with MC1R) requiring another step - a mutation of a mutation - to lead to red hair?

.

"And why have neither red hair nor blue eyes reached fixation in any human population, even those with milk-white complexions?"

I know there's no evidence yet - apart from fragmentary written records - but I still think the red hair phenotype was much more common and widespread than it is now but has been gradually replaced by the farmer phenotype over time.