Evolution of Skin Pigmentation Differences in Humans

The distribution of human skin pigmentation variation is highly correlated with the intensity of ultraviolet radiation (UVR). Several hypotheses propose that this strong relationship between skin colour and UVR is best explained by natural selection. The identification of a large number of genes involved in the pigmentary system now enables researchers to test these hypotheses within an evolutionary genetics framework. Genetic data indicate that the light pigmentation that characterizes populations in Europe and East Asia has evolved independently through positive selection, and that functional variation in pigmentation genes in high UVR populations has likely been subject to purifying selection.

Keywords: skin pigmentation; natural selection; human evolution

Figure 1. Melanocyte and keratinocyte in (a) darkly pigmented skin. Note darker, ellipsoidal eumelanosomes distributed singly in keratinocytes versus (b) spherical, lighter pheomelanosomes grouped together as aggregates in lighter pigmented skin.
Figure 2. Diagram of melanocyte showing selected genes involved in pigmentary pathway. Enlarged regions show melanosome and melanosomal proteins and the transport of melanogenesis proteins from the trans-Golgi network to the melanosome by MATP.
close
 References
    Agar N and Young A (2005) Melanogenesis: a photoprotective response to DNA damage? Mutation Research 571: 121–132.
    Aoki K (2002) Sexual selection as a cause of human skin colour variation: Darwin's hypothesis revisited. Annals of Human Biology 29: 589–608.
    Barker D, Dixon K, Medrano EE et al. (1995) Comparison of the responses of human melanocytes with different melanin contents to ultraviolet B irradiation. Cancer Research 55: 4041–4046.
    Bennett D and Lamoreux M (2003) The color loci of mice – a genetic century. Pigment Cell Research 16: 334–344.
    Blum H (1961) Does the melanin pigment of human skin have adaptive value? Quarterly Review of Biology 36: 50–63.
    Bonilla C, Boxill LA, Donald SA et al. (2005) The 8818G allele of the agouti signaling protein (ASIP) gene is ancestral and is associated with darker skin color in African Americans. Human Genetics 116: 402–406.
    Bower C and Stanley F (1989) Dietary folate as a risk factor for neural tube defects: evidence froma case-control study in Western Australia. Medical Journal of Australia 150: 613–619.
    Branda RF and Eaton JW (1978) Skin color and nutrient photolysis: an evolutionary hypothesis. Science 201: 625–626.
    Chaplin G (2004) Geographic distribution of environmental factors influencing human skin coloration. American Journal of Physical Anthropology 125: 292–302.
    Cosentino MJ, Pakyz RE and Fried J (1990) Pyrimethamine: an approach to the development of a male contraceptive. Proceedings of the National Academy of Sciences of the USA 87: 1431–1435.
    book Darwin C (1871) The Descent of Man, and Selection in Relation to Sex. London: J. Murray.
    book Diamond J (1992) The Third Chimpanzee. 120. New York: Harper Collins Publishers.
    Duffy DL, Montgomery GW, Chen W et al. (2007) A three-single-nucleotide polymorphism haplotype in intron 1 of OCA2 explains most human eye-color variation. American Journal of Human Genetics 80: 241–252.
    Flemming A and Copp A (1998) Embryonic folate metabolism and mouse neural tube defects. Science 280: 2107–2109.
    Frudakis T, Thomas M, Gaskin Z et al. (2003) Sequences associated with human iris pigmentation. Genetics 165: 2071–2083.
    Fuller BB, Spaulding DT and Smith DR (2001) Regulation of the catalytic activity of preexisting tyrosinase in black and Caucasian human melanocyte cell cultures. Experimental Cell Research 262: 197–208.
    Graf J, Hodgson R and van Daal A (2005) Single nucleotide polymorphisms in the MATP gene are associated with normal human pigmentation variation. Human Mutation 25: 278–284.
    Graf J, Voisey J, Hughes I and van Daal A (2007) Promoter polymorphisms in the MATP (SLC45A2) gene are associated with normal human skin color variation. Human Mutation 28: 710–717.
    Harding RM, Healy E, Ray AJ et al. (2000) Evidence for variable selective pressures at MC1R. American Journal of Human Genetics 66: 1351–1361.
    Holick MF (2003) Vitamin D: a millenium perspective. Journal of Cellular Biochemistry 88: 296–307.
    Holick MF (2005) The vitamin D epidemic and its health consequences. The Journal of Nutrition 135: 2739S–2748S.
    Izagirre N, Garcia I, Junquera C, de la Rua C and Alonso S (2006) A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Molecular Biology and Evolution 23: 1697–1706.
    Jablonski N and Chaplin G (2000) The evolution of human skin coloration. Human Evolution 39: 57–106.
    Kaidbey K, Agin P, Sayre R and Kligman A (1979) Photoprotection by melanin: a comparison of black and Caucasian skin. American Academy of Dermatology 1: 249–260.
    Kollias N (1995) The physical basis of skin color and its evaluation. Clinics in Dermatology 13: 361–367.
    Kollias N, Sayer R, Zeise L and Chedekel M (1991) Photoprotection by melanin. Journal of Photochemistry and Photobiology. B, Biology 9: 135–160.
    Lamason RL, Mohideen MA, Mest JR et al. (2005) SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310: 1782–1786.
    Lao O, de Gruijter JM, van Duijn K, Navarro A and Kayser M (2007) Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Annals of Human Genetics 71: 354–369.
    Loomis W (1967) Skin pigment regulation of vitamin-D biosynthesis in man. Science 157: 501–506.
    Makova K and Norton H (2005) Worldwide polymorphism at the MC1R locus and normal pigmentation variation in humans. Peptides 26: 1901–1908.
    Mathur U, Datta S and Mathur B (1977) The effect of aminopterin-induced folic acid deficiency on spermatogenesis. Fertility and Sterility 28: 1356–1360.
    Myles S, Somel M, Tang K, Kelso J and Stoneking M (2007) Identifying genes underlying skin pigmentation differences among human populations. Human Genetics 120: 613–621.
    Nakayama K, Fukamachi S, Kimura H et al. (2002) Distinctive distribution of AIM1 polymorphism among major human populations with different skin color. Journal of Human Genetics 47: 92–94.
    Norton HL, Kittles RA, Parra E et al. (2007) Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Molecular Biology and Evolution 24: 710–722.
    Oetting W and King R (1993) Molecular basis of type I (tyrosinase-related) oculocutaneous albinism: mutations and polymorphisms of the human tyrosinase gene. Human Mutation 2: 1–6.
    Ortonne JP (2002) Photoprotective properties of skin melanin. The British Journal of Dermatology 146(suppl. 61): 7–10.
    Puri N, Gardner J and Brilliant M (2000) Aberrant pH of melanosomes in pink-eyed dilution (p) mutant melanocytes. Journal of Investigative Dermatology 115: 607–613.
    Rana BK, Hewett-Emmett D, Jin L et al. (1999) High polymorphism at the human melanocortin 1 receptor locus. Genetics 151: 1547–1557.
    Relethford JH (2002) Apportionment of global human genetic diversity based on craniometrics and skin color. American Journal of Physical Anthropology 118: 393–398.
    book Robins A (1991) Biological Perspectives on Human Pigmentation. New York: Cambridge University Press.
    Shriver M, Parra E, Dios S et al. (2003) Skin pigmentation, biogeographical ancestry and admixture mapping. Human Genetics 112: 387–399.
    Soejima M, Tachida H, Ishida T, Sano A and Koda Y (2006) Evidence for recent positive selection at the human AIM1 locus in a European population. Molecular Biology and Evolution 23: 179–188.
    book Stern C (1949) Polygenic Inheritance. San Francisco: W.H. Freeman and Company.
    Stokowski RP, Kirshna Pant PV et al. (2007) A genome-wide association study of skin pigmentation in a South Asian population. American Journal of Human Genetics 15: 1511–1518.
    Szabo G, Gerald AB, Pathak MA and Fitzpatrick TB (1969) Racial differences in the fate of melanosomes in human epidermis. Nature 222: 1081–1082.
    Thody AJ, Higgins EM, Wakamatsu K et al. (1991) Pheomelanin as well as eumelanin is present in human epidermis. The Journal of Investigative Dermatology 97: 340–344.
    Voight BF, Kudaravalli S, Wen X and Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biology 4: e72.
    Voisey J, Box NF and van Daal A (2001) A polymorphism study of the human Agouti gene and its association with MC1R. Pigment Cell Research 14: 264–267.
    Walter H (1971) Remarks on the environmental adaptation of man. Humangenetik 13: 85–97.
    Wong WY, Merkus HM, Thomas CM et al. (2002) Effects of folic acid and zinc sulfate on male factor subfertility: a double-blind, randomized, placebo-controlled trial. Fertility and Sterility 77: 491–498.
    Ye T, Hong L, Garguilo J et al. (2006) Photoionization thresholds of melanins obtained from free electron laser-photoelectron emission microscopy, femtosecond transient absorption spectroscopy and electron paramagnetic resonance measurements of oxygen photoconsumption. Photochemistry and Photobiology 82: 733–737.
 Further Reading
    Jablonski N (2004) The evolution of human skin and skin color. Annual Reviews in Anthropology 33: 585–623.
    McEvoy B, Beleza S and Shriver MD (2006) The genetic architecture of normal variation in human pigmentation: an evolutionary perspective and model. Human Molecular Genetics 15(Spec. No. 2): R176–R181.
    Parra E (2007) Human pigmentation variation: evolution, genetic basis, and implications for public health. Yearbook of Physical Anthropology 45(suppl.): 85–105.
    Rees JL (2003) Genetics of hair and skin color. Annual Review of Genetics 37: 67–90.
    Sturm R, Teasdale R and Box N (2001) Human pigmentation genes: identification, structure, and consequences of polymorphic variation. Gene 277: 49–62.
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Norton, Heather L(Jul 2008) Evolution of Skin Pigmentation Differences in Humans. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021001]