Saturday, June 7, 2014

A new allele for blond hair


 
Geographic prevalence of the new allele for blond hair (Guenther et al., 2014). Just one of many alleles that create the European palette of hair and eye colors.
 

There is a widespread belief that whatever made Europeans fair-skinned also gave them their unique palette of hair and eye colors. In reality, fair skin has only a weak genetic linkage with either non-black hair or non-brown eyes:


If we were to take all the human beings in the world who have dark brown eyes and black or dark brown hair, we would not only have the vast majority of the human species, but would have a group which shows virtually the complete range of human skin color, from black to almost completely depigmented. (Brues, 1975)


Hair color and eye color are largely uncoupled from skin color in our species—or rather in Europeans, to be more precise. It looks as if the pressure of selection has moved European color traits in different directions, on the one hand making the skin progressively lighter, and on the other making the hair and the eyes more and more diversely hued.

There have thus been different changes at different genes. 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.

In a recent study, Guenther et al. (2014) have shown that new alleles for European hair color proliferated not only at MC1R but also at other genes. In particular, blond hair seems to be due to an allele near KITLG, although other loci in this region seem involved as well. Thus, the diverse palette of European hair colors is not a side effect of a single genetic change. It is due to a proliferation of new alleles at many different places on the human genome. The only common element seems to be a selection pressure for more hair colors.

Guenther et al. (2014) likewise note that changes to hair color and eye color became uncoupled from changes to skin color in ancestral Europeans:
 

Some human pigmentation variants alter general aspects of pigment biosynthesis, producing changes in all melanocytes, and therefore have pleiotropic effects on hair, skin and eye color. However, it is well known that hair and eye color can also vary independently, producing common human phenotypes such as light-haired individuals with brown eyes or brown-haired individuals with blue eyes. The rs12821256 variant alters an enhancer that is active specifically in the hair follicle environment, providing a simple genetic explanation for previous observations that this SNP is associated with changes in hair pigmentation but not eye pigmentation in northern Europeans.


Why this uncoupling of European hair, eye, and skin color? These three color traits have probably undergone divergent selection pressures. Moreover, in all three cases the selection pressure seems to have acted primarily on women and only secondarily on men—an indication of some form of sexual selection where women were the sex in excess supply on the mate market (Frost, 2014). Because skin color is sexually dimorphic in all humans, with women being the "fair sex," this dimorphism may have biased sexual selection in the direction of increasingly lighter skin.  

Hair and eye color, however, had no preexistent sexual dimorphism. So sexual selection was driven simply by a desire for bright or novel colors. In other words, whenever a new color arose through mutation, it would have initially benefited from sexual selection. As it became more and more common in the population, this selection pressure would have gradually diminished until the new color had become as prevalent as other existing hues. As a result, the palette of hair and eye colors would have steadily grown larger and larger (Frost, 2006; Frost, 2014).
 

References

Brues, A.M. (1975). Rethinking human pigmentation, American Journal of Physical Anthropology, 43, 387-391.

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

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  

Guenther, C.A., B. Tasic, L. Luo, M.A. Bedell, and D.M. Kingsley. (2014). A molecular basis for classic blond hair color in Europeans, Nature Genetics, advance online
http://www.nature.com/ng/journal/vaop/ncurrent/full/ng.2991.html  

27 comments:

Anonymous said...

Moreover, in all three cases the selection pressure seems to have acted primarily on women and only secondarily on men—an indication of some form of sexual selection where women were the sex in short supply (Frost, 2014)

Haven't you argued previously that sexual selection on women implies that men were the sex in short supply?

Anonymous said...

Finally a reason for white folks to celebrate diversity /sarcasm>

Sean said...

Uniquely dark skinned and light eyed indigenous population mixes with light skinned and dark eyed haired farmers, and the resultant people are conquered by Kurgans with blonde hair. Hence the people of southern Sweden are mainly descended from an invasion of a few thousand years ago that populated the rest of northern Europe.

The above is more like butterfly collecting that an attempt to provide a scientific explanation for current European hair and eye colour traits that are mainly independent of each other and white skin. No one can come up with a credible alternative to the sexual selection explanation for the light eyes of north Europeans. So why all the doubts about variable light hair and white skin colour coming from the same place?

Could someone explain how the people of the west coast of Ireland look so different to Swedes?

Anonymous I said...

"Hair and eye color, however, had no preexistent sexual dimorphism. So sexual selection was driven simply by a desire for bright or novel colors."

This does not follow. Pigmentation in women is probably lighter than in men to begin with because children are fairer than adults; fairness is a signal of youth. Blonde hair, like white skin, would therefore be a supernormal stimulus that signaled neoteny.

Anonymous said...

"a supernormal stimulus that signaled neoteny. "

that's interesting because lactase retention is neotenous. Europeans are a bunch of cry babies!

Sean - I have this idea that bears no relation to genetics but it works. It's based on observation and reduction, of course. Suppose there were a line of continuum from Ireland to the Baltic that went from Black hair/blue eyes to White hair/grey eyes. And suppose there were another continuum from Bulgaria to Wales that went from Brown hair/yellow eyes to Red hair/green eyes. That would pretty much explain hair and eye colour distribution in Europe!

Sean said...

Red hair is nowhere the most common colour. Everywhere, it is more common in women. Europe is the ground zero of hair colour.

A scientific explanation would explain how and why the these hair colours conferred some fitness advantage in Europe. Merely suggesting they originated from an adjacent region explains nothing.

Anonymous said...

What's the estimated date for this blond mutation in Europeans?

The recent evidence from ancient DNA studies would seem to rule out anything much earlier than 7000BP, since all the Mesolithic and Neolithic individuals of which I've heard are judged to have been brunets.

I seem to recall reading that there is some artistic evidence of a few stray blonds being present in Crete and even Egypt by the early Bronze Age. Queen Hatep Heres of the 4th Dynasty, who lived around 2500BC, is claimed by some to have been depicted as a strawberry blonde with fair skin - though its possible this coloring was symbolic of some religious meme rather than her actual pigmentation.

jaakkeli said...

"And suppose there were another continuum from Bulgaria to Wales that went from Brown hair/yellow eyes to Red hair/green eyes. That would pretty much explain hair and eye colour distribution in Europe!"

Except for the high rates of red hair in the Urals region. The most red-headed people in the world are also part-Mongoloid, eg. Google up some Udmurts:

https://www.google.fi/search?q=udmurts

The connection of a single non-polygenic trait like red hair to an ethnicity or region is likely to be meaningless unless it approaches fixation as frequencies of such a trait can jump between a few % and 10 % and 20 % through simple founder effects and drift in an isolated population. You're bound to found these anomalies in fringe populations and trying hard to explain something that doesn't really need an explanation is likely to just create confused theories.

Light eyes are another thing as they seem to be driven to near fixation in some northern European populations which is too unlikely for founder effect or drift.

Blonde hair is very noticeably different from red hair as it is obviously polygenic: hair colour has an obviously Gaussian distribution in northern Europeans (and possibly in everyone else - it's just that in everyone else it's only different shades of really dark hair). This is much less susceptible to large fluctuations with founder effects and drift and begs for some evolutionary explanation.

Sean said...

Assume the variegated alleles for blonde hair originated outside Europe, that would not explain how they were able to supplant the supposedly dark hair ones as typical European hair colour alleles, except by population replacement.

Alleles for blonde hair lighten skin negligibly compared to alleles for red hair, so no reason for blonde hair to have been selected for skin lightening.

Variegated alleles converging on a certain hair colour appearance show there must have been a selection pressure for that appearance: blonde hair.

Anonymous I said...

"Europeans are a bunch of cry babies!"

Not just Europeans! We're all of us hairless, with big eyes and foreheads, flat faces, underdeveloped brow ridges, and cute little teeth.

Peter Fros_ said...

Anon,

Merde ! The mistake has been corrected.

Sean,

A lot of people, like Greg Cochran, are arguing that light skin originated with Neolithic farmers and not with Mesolithic hunter-fisher-gatherers. Yet the oldest example of the derived allele for SLC24A5 comes from a Mesolithic site (Motala, Sweden). How does Greg explain this?

Anon,

If the selection had merely been for lighter hair, there would not have been a diversification of hair color. There would simply have been a replacement of black hair by blond hair. Yet there is no population where blond hair has become the dominant hair color, let alone the only one. Also, how would you explain the evolution of red hair?

Anon,

There has been no dating of the origin of non-black hair colors in Europe. I don't think we'll get any answers until we have more ancient DNA from the time frame of 20,000 BP to 10,000 BP. The Mesolithic individuals from Luxembourg and Spain are interesting but peripheral.

jaakkeli said...

"Alleles for blonde hair lighten skin negligibly compared to alleles for red hair, so no reason for blonde hair to have been selected for skin lightening."

...but there's little evidence that skin lightening from Mediterranean to northern European levels conveys any direct benefit at all so connecting hair color to it wouldn't actually explain anything anyway.

"that would not explain how they were able to supplant the supposedly dark hair ones as typical European hair colour alleles,"

Before we try to explain this we would need to have convincing evidence that dark hair was typical for northern Europeans. If anything it looks like the blondest Europeans like Swedes and Finns are the ones who have the least amounts of Kurgan invader ancestry and the least amount of early farmer ancestry, especially Finns who seem to be part really ancient East Asian ancestry and part old European ancestry with no Indo-European invader or Middle Eastern farmer ancestry.

If you really want to identify some population as the original source of blonde hair, I would suggest the common pre-Indo-European and pre-Finno-Ugric substrate that seems to exist in both Germanic speakers (especially Swedes) and western Finnic speakers (especially Finns).

BTW theories about Kurgan people are actually easy to put to the test since they're burial sites and there's DNA to test. The first Kurgan samples seem to have turned out the opposite of your expectations - those Kurgan people were swarthy Caucasoids with a bit of Mongoloid admixture, dark haired but commonly light eyed. But we'll have a lot more Kurgan samples soon so that will be settled.

Anonymous said...

"If the selection had merely been for lighter hair, there would not have been a diversification of hair color."

Two groups of people. One that looked like some people in Georgia or Tajikistan with black hair and pale skin, similar to the Celtic Fringe, migrated round the Atlantic and turned white like huskies. One group that migrated west from the Steppe, say they looked like alsatians, some variation, browns and tans. Then the two groups mixed.

"how do you explain the evolution of red hair?"

not be facetious but orangutans have red hair and there are pockets of human red haired people such as East Iran. The NE Atlantic Archipelago just happens to be the biggest pocket. So red 'looks' old; a spare allele that doesn't often get expressed. But I would bet that men will be growing red beards long after fair hair has disappeared.

Peter Fros_ said...

Anon,

Europeans have at least 11 nonsynonymous alleles at the main hair-color gene, MC1R (as compared to the original state of 1 in sub-Saharan Africans). This new finding shows that the same proliferation occurred at other gene loci.

You seem to be suggesting that each of these alleles reached fixation in different populations. Then, at some point, these different populations (more than 11 by my count) came together.

Interesting hypothesis, but not very likely.

spagetiMeatball said...

"A lot of people, like Greg Cochran, are arguing that light skin originated with Neolithic farmers and not with Mesolithic hunter-fisher-gatherers. Yet the oldest example of the derived allele for SLC24A5 comes from a Mesolithic site (Motala, Sweden). How does Greg explain this?"

Peter, SLC24A5 is at about 50% in the maasai and 45% in the sinhalese. Two places with proven pre-historical contact with the middle east.

According to your theory, european hunter-gatherers sailed all around africa skipping the bantu peoples and the san, to mix with the ancient african peoples in present ethiopia to make the present day mixed population. Could you believe such a thing?

spagetiMeatball said...

I'm sorry, I meant to say, SLC24A5 is found in about 50% of ethiopians, 27% of maasai, and 45% of sinhalese.

Anonymous said...

The original home of Nordic man is in the TROPICS:

https://i.imgur.com/PGzhdgF.jpg

dr.bill said...

Pardon the intrusion (poorly informed lurker here), but in these studies that you reference, how do you decide what to call someone's hair colour?

I have what is typically called medium brown hair (and grey-green eyes), but in fact, I have a whole bunch of different kinds/colours/shapes of individual hairs on my head and particularly in my beard (black, brown, red, blonde, straight, twisty, thick, thin, round, and flat). From even a short distance away, however, it does look brown.

Are such variations taken into account in the labelling system?

Anonymous I said...

"If the selection had merely been for lighter hair, there would not have been a diversification of hair color. There would simply have been a replacement of black hair by blond hair."

And if selection had merely been for higher intelligence, there would not have been a diversification of IQ scores? Or if selection had merely been for less body hair, there would not have been a diversification of hirsuteness?


"Also, how would you explain the evolution of red hair?"

Remember, I'm not really opposed to your general position; red hair may indeed be evidence for females under heavy selection to look different one to the next.

On the other hand, genes for red hair are associated with extremely light skin, so it isn't clear that rufism is evidence for a preference for novelty and variety, either. Pale skin, like pale hair, is a neotenous trait. Men are attracted to women signalling youth and fertility signals, and paleness in both skin and hair signals youth. Yes, men do like variety, and I wouldn't be surprised to know that you were right about this being a major factor in the evolution of hair and eye color among European women. But neither the spread blondism or rufism provide clear evidence for this.

Generally, I would say that men only like variety in traits that are unrelated to attractiveness; they can be quite merciless when it comes to a woman being too fat, too thin, too tall, too flat, too deep-voiced, and so on. When I look at Playboy models or miss America contestants, they don't seem like caricatures or political cartoons with exaggerated physical differences. Rather, they all look very similar variations on a theme. And as we have seen from other studies, it is often averageness rather than distinctness which is seen as desirable.

Anonymous said...

"Interesting hypothesis, but not very likely."

I'm sure you're right.

Some random thoughts:

There is a male irish/scot phenotype with coarse black hair that goes silver early; before the ageing processes that are normally associated with greying in brown hair, wrinkles and such, almost as a late secondary sex charac.

Supposing people with fine white hair had proliferated to the sort of population size of the Chinese.

I have mixed colouring too. I have what I call horse hairs, really tough brown, not many. Underneath is fine white and the rest is a variation of shades of yellow and brown.

MRC1 codes for triggering phenol...brown pigment, which we know is protective. All the other 11 alleles fail to trigger phenol... Is it possible that having lost the trigger, the other 11 alleles are attempts to recreate it?

Peter Fros_ said...

Spageti,

We have historical and linguistic evidence for a migration from the Arabian Peninsula to the highlands of Ethiopia, probably two thousand years ago. We have weaker evidence, based on linguistic data, for earlier migrations from the Middle East into the Horn of Africa.

I was simply asking a question that no one seems to want to answer. The oldest ancient DNA with that skin-lightening allele comes from a hunter/fisher/gatherer people in Sweden.

Dr. Bill,

There have been attempts to standardize classification of hair color. These attempts run into two problems: hair color varies along a continuum; and hair color changes with age (see Steggerda, M. (1941)Change in hair color with age,Journal of Heredity, 32, 402-404). In the future, it will probably be better to identify hair color by its underlying alleles. Unfortunately, we're still discovering new ones.

Anon,

We don't see a diversification of IQ scores in any human population that I know of. Please enlighten me if I'm wrong. The typical pattern is something like a bell curve, i.e., most people clump around the median with fewer people as one goes out to the left-hand or right-hand tail.

The same goes for hirsuteness and most body characteristics.

Keep in mind that with hair color we're looking at a large number of alleles for a single trait. This is not the usual pattern.

I'm not arguing that sexual selection favors diversity for all visible traits. It seems to favor diversity for color traits, particularly brightly colored ones. Sexual selection also has to reach a high enough intensity for this kind of diversifying effect to take off.

Anon,

As I understand it, the different hair-color alleles produce different proportions of eumelanin (black-brown) and pheomelanin red-brown).

Sean said...

"Polymorphisms in the MC1R gene are a major source of normal variation of human hair color and skin pigmentation, response to ultraviolet radiation (UVR), and skin cancer susceptibility. The identification of a surprisingly high number of MC1R natural variants strongly associated with pigmentary phenotypes and increased skin cancer risk has prompted research on the functional properties of the wild-type receptor and frequent mutant alleles" Here

Stephen said...

We should remember that for a gene to be selected for it first has to appear in someone who survives to reproduce. A selection pressure may exist for a long time before the right mutation that will be spread by it appears. A new gene may first appear somewhere it is poorly adapted before spreading to somewhere it is advantageous and becomes more numerous. Testosterone seems to increase pigmentation in all humans so even if the selection for pale skin was primarily in males I would still expect European males to be slightly more tanned because that is what testosterone does in most humans. You would have to wait allot longer for a mutation which specifically reverses the the signal testosterone has on pigment production than a simpler mutation that suppresses pigment in general.

I eagerly await the sequencing of more ancient skeletons. But from what we have perhaps it seems that the Neolithic expansion brought together depigmentation genes from Eastern Europe and Western Europe to create a new hybrid ultra depigmented race. We could imagine a scenario where where people with rare combinations of recesive genes giving them eyes the color of the sky, hair the color of copper or golden sun, and skin the color of the clouds and the moon become the top priests and shamans in bronze age sun cults with access to many concubines from there devoted worshipers spreading there genes until they become to common to be a marker of elite status.

Peter Fros_ said...

Stephen,

The MC1R gene alone has 11 nonsynonymous alleles in Europeans (compared to a base value of 1 in Africans). Let's suppose that modern humans are the result of hybridization between three different groups (the model being advanced by David Reich). Each of these three groups has a different MC1R allele. You still haven't accounted for the proliferation of MC1R alleles over a relatively short time span. Moreover, as this latest paper has shown, this proliferation has occurred at other gene loci.

Boys and girls diverge in skin pigmentation during adolescence, but this divergence isn't due to rising testosterone levels in boys. It's due to girls becoming lighter-skinned and boys less so, i.e., the girls are the ones who change.

In any case, your basic point escapes me. If sexual selection acted primarily on men, it would tend to favor men with exaggerated male traits. Among other things, it would favor men with a darker and ruddier skin. Since most genes for skin color are not sex-linked, the entire population -- both men and women -- would darken in skin color. This is the reverse of what happened in Europeans.

Anonymous I said...

"We don't see a diversification of IQ scores in any human population that I know of. Please enlighten me if I'm wrong. The typical pattern is something like a bell curve, i.e., most people clump around the median with fewer people as one goes out to the left-hand or right-hand tail."

The shape of the distribution is irrelevant - the bell curve for IQ is broad enough that distinct social classes appeared across the world and throughout history, as you yourself have pointed out on this blog.

Of course, we also see non-bell-curve distributions in traits like baldness. And in fact, male pattern baldness is found to be somewhat higher in European males, as per

Axel M. Hillmer et al (2009). "Recent positive selection of a human androgen receptor/ectodysplasin A2 receptor haplotype and its relationship to male pattern baldness," Human Genetics.

So, was this caused by selection or varied male appearance?


"Keep in mind that with hair color we're looking at a large number of alleles for a single trait. This is not the usual pattern."

And? The number of alleles affecting IQ is so numerous that scientists are having trouble isolating any that have a meaningful effect.

Peter Fros said...

Anon I,

"The shape of the distribution is irrelevant"

The shape is relevant, at least to our discussion. A unimodal distribution does not indicate a balanced polymorphism. A multimodal distribution does.

All traits have some degree of variability because random mutations are always arising and because the force of stabilizing selection is not sufficient to elminate all variability.


"Keep in mind that with hair color we're looking at a large number of alleles for a single trait. This is not the usual pattern."

And? The number of alleles affecting IQ is so numerous that ..."

I'm sorry. Maybe I didn't express myself clearly. I'm talking about multiple alleles that seem to exist in a balanced polymorphism at a single genetic loci. That sort of pattern is not usual.

Peter Fros_ said...

"the bell curve for IQ is broad enough that distinct social classes appeared across the world and throughout history, as you yourself have pointed out on this blog."

Not really. I've referred to Gregory Clark's argument that the relative reproductive success of the middle class gradually altered the English gene pool. But that's hardly a case of a balanced polymorphism for IQ or any other trait. That is simply one set of heritable traits gradually displacing another set.

I've also referred to other cases, like the Cagots in France and the Burakumin in Japan where this kind of demographic turnover cannot proceed to completion because a caste has become reproductively isolated. I suppose you can call that diversification, but the diversification is not taking place within a single population, as is the case with hair color.

In all this, we shouldn't lose sight of the main point. Selection usually reduces genetic varability within a population. If it doesn't, something unusual is going on.