Pigmentation, phylogeny, history, and adaptation

By Razib Khan | August 7, 2013 2:45 am

SLC45A2 rs16891982 frequency, Norton, Heather L., et al. “Genetic evidence for the convergent evolution of light skin in Europeans and East Asians.” Molecular biology and evolution 24.3 (2007): 710-722.


The above figure is from Norton et al.’s Genetic Evidence for the Convergent Evolution of Light Skin in Europeans and East Asians. It shows that rs16891982 on the SLC45A2 locus exhibits strong differentiation between Europe and the rest of the world. This is in contrast to SLC24A5, where the well known allele which differentiates Africans/East Asians from Europeans is found at very high frequencies across Western Eurasia (both my parents are homozygotes for the “European” variant; in fact SLC24A5’s derived variant is found at fractions on the order of ~50% in eastern and southern India). The ancestral allele on SLC24A5 is very difficult to find in Europeans, it is so close to fixation for the derived variant. In contrast SLC45A2‘s minor allele is segregating at appreciable frequencies in places like southern Spain, and the derived allele is not fixed even in Northern Europe.

I won’t review the literature on the genomics and evolution of human pigmentation at this point. Rather, I’ll just note that it seems most of the inter-population variation is controlled by a handful of genes. It’s a polygenic trait, but just. Second, a fair amount of evidence has emerged that some of the lightening derived variants have increased in frequency only very recently (e.g., on the order of ~10,000 years). Pigmentation is then a peculiar trait where the genetic underpinnings can give historical phylogenetic information because of the varied dates of differentiation and selective sweeps.

Below I’ve collated results from several studies on frequencies of SLC45A2. I invite readers to persue them. I will say two things. First, the frequency of the “European” variant in ~140 northern Ethiopians is 0%. This is peculiar for a population which may be on the order of ~50% West Eurasian. Second, the fraction of SLC45A2 derived variant in South Asians coincidentally tracks the “NE Euro” percentage in Zack Ajmal’s results.


Country/Region Group/Place N Frequency light allele

A Decreasing Gradient of 374F Allele Frequencies in the Skin Pigmentation GeneSLC45A2, from the North of West Europe to North Africa
Denmark Copenhagen 51 0.98

England London 56 0.955

Belgium Brussels 53 0.934

France Lille 64 0.945

  Rheims 98 0.893

  Rennes 52 0.971

  Marseilles 312 0.888

  Perpignan 101 0.827

  Corsica 328 0.878

Germany Mulheim 59 0.975

Switzerland Basel 51 0.96

Italy Genoa 97 0.85

  Roma 64 0.898

  Napoli 128 0.859

  Sicily 39 0.833

  Sardinia 100 0.805

Spain Barcelona 59 0.856

  Sevilla 71 0.725

Portugal North 79 0.829

  South 59 0.78

Near Fixation of 374l Allele Frequencies of the Skin Pigmentation Gene SLC45A2 in Africa
Algeria Algiers 141 0.7

Morocco Tangier 123 0.69

Rabat 102 0.68

Berbers from Morocco 75 0.57

Libya Tripoli 38 0.58

Egypt Alexandria 162 0.65

Assouan 66 0.14

South 46 0.2

Mauritania Moors 65 0.41

Senegal Wolof 209 0

Serrere 92 0

Mandingue 51 0

Diola 42 0

Balant 21 0

Peuls 71 0.1

Toucouleur 70 0.03

Soninké 69 0.03

Ethiopia Addis Ababa 104 0

Falashas 38 0

Democratic Republic of Congo
188 0
Distribution of the F374 Allele of the SLC45A2 (MATP) Gene and Founder-Haplotype Analysis
Munich German 93 0.962

West Germany Turk 200 0.615

New Delhi Indian 51 0.147

Dhaka Bangladeshi 118 0.059

Ulaan Baator Khalha 173 0.113

Dashbalbar Buryat 143 0.115

Shenyang Han 89 0.028

Wuxi Han 119 0

Huizhou Han 111 0.005

Tottori Japanese 103 0

Okinawa Japanese 87 0

Surabaya Indonesian 105 0.005

  White S African 54 0.89

  Ghanaian 50 0

  New Guinean 52 0

  Japanese 49 0

Polymorphisms of four pigmentation genes (SLC45A2, SLC24A5, MC1R and TYRP1) among eleven endogamous populations of India
Jharkhand Munda 68 0.03

Madhya Pradesh Kanyabuja Brahmin 78 0.11

Madhya Pradesh Gond 75 0.02

Maharashtra Konkanastha Brahmin 71 0.06

Maharashtra Mahadev Koli 65 0.06

Tamil Nadu Iyengar Brahmin 66 0.07

Tamil Nadu Kurumans 67 0.07

Tripura Tripuri 65 0

Tripura Riang 67 0.01

  • Karl Zimmerman

    That pigmentation was under heavy selection in Ethiopia keeps with what you see looking at Horners, who often have “white” facial features and dark skin, which in extreme cases results in them looking like incredibly tanned Europeans.

    I was going to say I was a bit surprised that India doesn’t appear to have been placed under the same heavy selection regarding skin color as Ethiopia, as both areas developed from a similar mixture of lighter skinned West Eurasians and a dark-skinned indigenous population. However, looking at a world map the Ethiopian highlands tend to be significantly further south in latitude than the majority of the Indian subcontinent. Indeed, one could argue that the present-day distribution of skin color in India is probably more “natural” regarding solar radiation influx than the distribution in the Mesolithic.

    I do wonder if enough time has passed in the settlement of the New World that some selection for skin color has begun in Latin America. If we head for another “dark age” we might find that a thousand or two years hence everyone in Central America is black in terms of skin color, no matter what other traits they have regarding external phenotype.

    • razibkhan

      re: americans. gain of function is harder than loss. though they’ve gone the alleles now with african admixture….

    • Lank

      I was going to say I was a bit surprised that India doesn’t appear to have been placed under the same heavy selection regarding skin color as Ethiopia, as both areas developed from a similar mixture of lighter skinned West Eurasians and a dark-skinned indigenous population.

      The light-skinned variant of the SNP which was found to be most strongly associated with skin reflectance in South Asian populations (rs1834640), is also found at a high frequency (>50%) in many Ethiopian populations. This allele is located close to SLC24A5, which is very important in all West Eurasian populations. SLC45A2, on the other hand, is increasingly important the farther north you go, so the absence in the Ethiopian sample mentioned above probably says something about the different origins (to some degree) of the West Eurasian admixture in Ethiopia and South Asia.

      • razibkhan

        to be explicit, the *total lack* of the euro-SLC45A2 variant does i think speak to *recent* admixture from west asia/south europe into ethiopians…. (what it says is debatable, but it’s a prior)

        • Lank

          Speaks against it, you mean? And I would agree. This is also what we get from ADMIXTURE, mtDNA, Y-DNA; the West Eurasian admixture in Ethiopians seems very “southern”. Though this is in the context of modern populations, so it could still have entered Africa through the Levant, via the Nile Valley or Red Sea coast, at an early date.

          • razibkhan

            the frequency of the SLC45A2 variant is >50% in northern egypt. i’d be skeptical that it’s that much lower in arabia. either there’s selection in horn of africa against. the sweep was very late. or the sweep was older, and the admixture is older still.

            if you comb through the genome you’ll find plenty of weird allelic differences. but the pigmentation pathways are often strongly shaped by adaptation, so differences are not likely to be happenstance.

        • Lank

          Modern Egyptians have higher “West Asian” affinities than even Arabians, and
          probably even some “Euro-Mediterranean”, so the high frequency is not that surprising.

          The “West Asian” element may not have been present in Northeast Africans until some time after the Southwest Asian element. Y-DNA and mtDNA seem to indicate some common ancestry between Cushites and Egyptians, despite the significant WA in the latter. Linguists have also suggested that Cushitic spread south from Northeast Africa, which would fit with the north-south cline of more and less divergent branches of Cushitic (ranging from Beja in the north to South Cushitic in Kenya/Tanzania). Interestingly, the top match for the West Eurasian component in Ethiopians from Pagani et al. were Behar’s Egyptians.

          If non-African SLC45A2 went through significant, negative selection among the ancestors of Ethiopians, shouldn’t this also apply to non-African SLC24A5 to some degree? Instead SLC24A5 shows signs of positive selection in Semitic/Cushitic groups according to Pagani et al.

          • razibkhan

            If non-African SLC45A2 went through significant, negative selection among the ancestors of Ethiopians, shouldn’t this also apply to non-African SLC24A5 to some degree?

            i’m not convinced that slc24a5 is under that much constraint in the tropics. it’s at high frequencies in sri lanka and tamil nadu (25-50% derived).

        • Karl Zimmerman

          I cannot recall if I read it in the comments here or elsewhere, but I know I have read that while the European mutation for lighter skin causes a significant increase in skin cancer rates, the East Asian variant does not.

          If the *proto-Ethiopians faced significant risk of melanoma, particularly before their reproductive years were over, that would place heavy selection on the darker-skinned intermixed individuals. In contrast, India was mostly far enough north (and also mainly in the lowlands) so natural selection wasn’t strong enough to overcome sexual selection.

          • Tobus

            While it’s true that the European mutations cause a 10 to 20-fold increase in skin cancer, it’s not really considered a factor in the selection of dark skin pigmentation as it rarely manifests before reproductive age. The main theory is that selection for dark skin is driven by protection against folate depletion – folate deficiency is known to cause embryonic neural tube defects (see Jablonski/Chaplin 2000). India is mostly in the tropics and from the UV maps I’ve seen, would have similar pressuse for dark skin as Africa, Australia and Melanesia (more so in the south than the north of course).

    • razibkhan

      also, the % of SLC45A2 in mongolians fits VERY close with presumed west eurasian admixture via autosomal. same among uygurs.

    • Jacob M

      “…we might find that a thousand or two years hence everyone in Central America is black in terms of skin color…”

      I have certainly always noticed that in New York, Guatemalens are often much darker than Mexicans, even ones whose facial structures appear equally indigenous. I am unsure if perhaps indigenous groups from different areas of the New World had significantly different skin tone to begin with.

      Could the Aztecs and Mexicas (who lived in the central plain of Mexico which are usually warm but not awfully hot) be lighter skinned than people who lived in the jungles of nearby areas?

      • razibkhan

        there’s variation. some of it is simple north-south. some of it is elevation (peruvian highlanders somewhat darker than amazonian lowlanders who live in shade).

      • Karl Zimmerman

        I was also thinking about how much darker Central Americans tend to be than Mexicans. The admixture components of Central Americans don’t seem too different from Mexicans in the few studies that I’ve seen (similarly low levels of SSA ancestry, and not notably different levels of white ancestry).

        Unadmixed Central American tribes are slightly darker than Mexican tribes however, at least according to skin tone maps online, which may account for the entire difference.

        On the other hand, West Africans were brought into Central America by the Spaniards very early. When Balboa discovered the Pacific Ocean, his men were astonished to find a Maroon village right nearby. This was only twenty years after Columbus discovered the New World. Put another way, it was 500 years ago. Even given the comparably long human generation lengths, that should be enough to start showing notable evidence of selection.

  • http://blogs.discovermagazine.com Apple Pie

    The “Paleo Northern European” theory of white skin color and blond/blue pigmentation is IMO dubious at best. Anyone who is paying attention to the newer genetic research should already be questioning the assumption that human depigmentation as it exists today is solely the product of natural selection in exclusively northern environments.

    The best case for natural selection presented so far is the notion that skin depigmentation evolved as an adaptation to Vitamin D deficient diets in a cloudy environment. This could only have happened in certain places in farming cultures living in cloudy areas. It might not have affected hunters as much, even hunters living further north.

    Sexual selection could then have acted on this. Humans, as primates, are highly visual and react strongly to color. Depigmentation would have been hard to ignore and could have been selected for or against in terms of “social fitness” (sexual selection) from then on (possibly in multiple separate sweeps).

    The million dollar question here is: when *exactly* did these selective sweeps take place. What if it happened really recently? Just as a thought experiment, what if it happened after 1,000 BC for instance (thus after the southern pulse into the Horn of Africa)?

    Not to get sidetracked, but reflectivity might be a different matter. That could be a benefit in sunny areas (unlike extreme depigmentation).

    • razibkhan

      The million dollar question here is: when *exactly* did these selective sweeps take place. What if it happened really recently? Just as a thought experiment, what if it happened after 1,000 BC for instance (thus after the southern pulse into the Horn of Africa)?

      why is this a thought experiment? there’s a lot of research on this area over the past 10 years. >3000 BC is likely too recent. 10000-5000 BC perhaps for the recent stuff. but some of it is older. though weak-to-moderate confidence on specific assertions.

    • Karl Zimmerman

      The example of Tasmanians clearly shows that hunter-gatherers don’t just lighten on their own due to living in high latitudes. Of course, in that case one could argue their effective population size was too small to get the pool needed to assure light-skinned people would survive to adulthood. Still, much of Australia had similar issues (based on solar radiation, Aboriginals in Victoria should have been as light as modern Italians) and didn’t show much color drift despite a larger population.

  • Balaji

    Ethiopians are not only in the tropics, they also live in the highlands and are therefore exposed to even more ultraviolet radiation. This would account for their quite dark pigmentation.
    In India there is a cultural preference for light pigmentation and natural selection for dark pigmentation. The balance of these opposing forces results in a variety of shades of color even within members of the same caste which has been practicing endogamy for many centuries, even millenia. Often even siblings have very different complexions.

    • Karl Zimmerman

      In all fairness, Ethiopian highlanders are significantly lighter than neighboring groups. Some East Africans (particularly in South Sudan) are among the darkest people on Earth. In contrast, the range of skin tones in Ethiopia seems pretty similar to African-Americans (who of course are around 80% or so SSA). Regardless, the issue isn’t that there has been no skin lightening, only that there is less than you would have expected given the starting populations.

      • razibkhan

        to be clear, the phenotypic values of ethiopians don’t surprise me too much. it is that they, in a sample of 140, had no copies of the ‘european’ variant of SLC45A2. it is found in the fulani sample, which seems to have admixture with west eurasians, but to a far lower level.

  • razibkhan

    Razib, what is your reference that excludes a late date >3,000 KYA?

    the haplotype blocks seen around these loci are big, but not THAT big. selection coefficients not realistic if sweeps were so late and they fixed. this is a big literature, familiarize yourself with it before you talk to people like they don’t know what they’re talking about. recent paper with all requisite references going back to mid-2000s


    since you are a reference demander, the follow up comments had better be higher quality. i don’t really care about your opinion about various things.

  • Onur

    Razib, what is the source of the allele frequency data above?

    • razibkhan

      google the titles at the top of the sections. those are papers, and those papers have the allele frequency data.

      • Onur


  • http://skadhiblog.wordpress.com/ skadhithjassisdottir

    Mmm… this reminds me of Gayre who described East Africans to have an undertone similar to that of Congoid x Khoesanoid crosses, West Africans to have a reddish undertone and Horners to be greyish (turning dark skinned later on).

    Plus very dark skinned people cannot blush, yet all human races possess the physiology that exists only for blushing. logically the modern human MRCA must’ve been relatively pale skinned and the extremes of light and dark coloration must be apomorphic.


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About Razib Khan

I have degrees in biology and biochemistry, a passion for genetics, history, and philosophy, and shrimp is my favorite food. In relation to nationality I'm a American Northwesterner, in politics I'm a reactionary, and as for religion I have none (I'm an atheist). If you want to know more, see the links at http://www.razib.com


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