The Evolution of Human Skin and Skin Color

▪ Abstract Humans skin is the most visible aspect of the human phenotype. It is distinguished mainly by its naked appearance, greatly enhanced abilities to dissipate body heat through sweating, and the great range of genetically determined skin colors present within a single species. Many aspects of the evolution of human skin and skin color can be reconstructed using comparative anatomy, physiology, and genomics. Enhancement of thermal sweating was a key innovation in human evolution that allowed maintenance of homeostasis (including constant brain temperature) during sustained physical activity in hot environments. Dark skin evolved pari passu with the loss of body hair and was the original state for the genus Homo. Melanin pigmentation is adaptive and has been maintained by natural selection. Because of its evolutionary lability, skin color phenotype is useless as a unique marker of genetic identity. In recent prehistory, humans became adept at protecting themselves from the environment through clothin...

[1]  Gf Odland,et al.  The structure of the skin , 1991 .

[2]  D. F. Roberts,et al.  Environmental correlations of skin colour. , 1976, Annals of human biology.

[3]  John Tomes,et al.  The Structure and Development of Bone , 1853, The American journal of dental science.

[4]  A. Young,et al.  UV-induced pigmentation in human skin. , 2001 .

[5]  J. Relethford Hemispheric difference in human skin color. , 1998, American journal of physical anthropology.

[6]  P. E. Wheeler The evolution of bipedality and loss of functional body hair in hominids , 1984 .

[7]  M. Cabanac,et al.  Natural selective cooling of the human brain: evidence of its occurrence and magnitude. , 1979, The Journal of physiology.

[8]  H. Walter Remarks on the environmental adaptation of man , 2004, Humangenetik.

[9]  G. Wassermann On the Nature of the Theory of Evolution , 1981, Philosophy of Science.

[10]  P. V. D. Berghe,et al.  Skin color preference, sexual dimorphism and sexual selection: A case of gene culture co‐evolution?* , 1986 .

[11]  A M Kligman,et al.  Photoprotection by melanin--a comparison of black and Caucasian skin. , 1979, Journal of the American Academy of Dermatology.

[12]  L. Rosenblum,et al.  Allometry of primate hair density and the evolution of human hairlessness. , 1981, American journal of physical anthropology.

[13]  W. Montagna The consequences of having a naked skin. , 1981, Birth defects original article series.

[14]  D. F. Roberts Human pigmentation: its geographical and racial distribution and biological significance , 1977 .

[15]  A. Robins Biological Perspectives on Human Pigmentation , 1991 .

[16]  Wassermann Hp The circulation of melanin--its clinical and physiological significance. Review of literature on leucocytic melanin transport. , 1965 .

[17]  R. Lewontin The Apportionment of Human Diversity , 1972 .

[18]  J. Cleaver,et al.  UV damage, DNA repair and skin carcinogenesis. , 2002, Frontiers in bioscience : a journal and virtual library.

[19]  F. Parker The biology of pigmentation. , 1981, Birth defects original article series.

[20]  D. Falk Brain evolution in Homo: The “radiator” theory , 1990, Behavioral and Brain Sciences.

[21]  G. Prota CHAPTER 10 – PHOTOBIOLOGY AND PHOTOCHEMISTRY OF MELANOGENESIS , 1992 .

[22]  Wassermann Hp Human Pigmentation and Environmental Adaptation , 1965 .

[23]  D. Nelson,et al.  Brain temperature and limits on transcranial cooling in humans: quantitative modeling results , 1998, European Journal of Applied Physiology and Occupational Physiology.

[24]  P. Giacomoni Sun Protection in Man , 2001 .

[25]  L. Jin,et al.  Microsatellite data support an early population expansion in Africa. , 1997, Genome research.

[26]  F. Murray PIGMENTATION, SUNLIGHT, AND NUTRITIONAL DISEASE , 1934 .

[27]  T. Mhlanga,et al.  An investigation into a possible relationship between vitamin D, parathyroid hormone, calcium and magnesium in a normally pigmented and an albino rural black population in the Northern Province of South Africa. , 2000, BioFactors.

[28]  D. A. Brown,et al.  Skin pigmentation enhancers. , 2001, Journal of photochemistry and photobiology. B, Biology.

[29]  R. Binford,et al.  Cold injury and the evolution of "white" skin. , 1975, Human biology.

[30]  M. Xiong,et al.  Interaction between the melanocortin-1 receptor andP genes contributes to inter-individual variation in skin pigmentation phenotypes in a Tibetan population , 2001, Human Genetics.

[31]  R. Dmi’el,et al.  Is a black coat in the desert a means of saving metabolic energy? , 1980, Nature.

[32]  P. E. Wheeler The environmental context of functional body hair loss in hominids (a reply to Amaral, 1996) , 1996 .

[33]  L. Björn,et al.  Effects of increased solar ultraviolet radiation on terrestrial ecosystems , 1998 .

[34]  Jean-Paul Ortonne,et al.  Photoprotective properties of skin melanin , 2002, The British journal of dermatology.

[35]  C. Ruff,et al.  Postcranial robusticity in Homo. I: Temporal trends and mechanical interpretation. , 1993, American journal of physical anthropology.

[36]  J. Relethford,et al.  Human skin color diversity is highest in sub-Saharan African populations. , 2000, Human biology.

[37]  G. Chaplin Geographic distribution of environmental factors influencing human skin coloration. , 2004, American journal of physical anthropology.

[38]  M. Ramsay,et al.  Human DNA sequence variation in a 6.6-kb region containing the melanocortin 1 receptor promoter. , 2001, Genetics.

[39]  O. Hoevels [Vitamin D deficiency rickets]. , 1962, Der Internist.

[40]  Environmental Light: Effects on Vitamin D Synthesis and Calcium Metabolism in Humans a , 1985, Annals of the New York Academy of Sciences.

[41]  R. Pakyz,et al.  Pyrimethamine: an approach to the development of a male contraceptive. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Barrett T. Kitch,et al.  Hypovitaminosis D in medical inpatients. , 1998, The New England journal of medicine.

[43]  J P Ortonne,et al.  Pigmentary changes of the ageing skin , 1990, The British journal of dermatology.

[44]  A. Thody,et al.  HORMONES AND SKIN PIGMENTATION IN THE MAMMAL , 1977, International journal of dermatology.

[45]  Shosuke Ito,et al.  A Chemist's View of Melanogenesis , 2003 .

[46]  R. Neer The evolutionary significance of vitamin D, skin pigment, and ultraviolet light. , 1975, American journal of physical anthropology.

[47]  D. Barker,et al.  Comparison of the responses of human melanocytes with different melanin contents to ultraviolet B irradiation. , 1995, Cancer research.

[48]  H. Blum Does the Melanin Pigment of Human Skin Have Adaptive Value?: An Essay in Human Ecology and the Evolution of Race , 1961, The Quarterly Review of Biology.

[49]  Lasker Gw,et al.  The sun-tanning potential of human skin. , 1959 .

[50]  M. Holick A perspective on the beneficial effects of moderate exposure to sunlight: bone health, cancer prevention, mental health and well being , 2001 .

[51]  P. Ehrlich,et al.  The race bomb: Skin color, prejudice, and intelligence , 1977 .

[52]  R. Luboshitzky,et al.  High prevalence of vitamin D deficiency among Ethiopian women immigrants to Israel: exacerbation during pregnancy and lactation. , 1995, Israel journal of medical sciences.

[53]  H. DeLuca,et al.  Current understanding of the molecular actions of vitamin D. , 1998, Physiological reviews.

[54]  C. Brace Structural Reduction in Evolution , 1963, The American Naturalist.

[55]  M. Holick,et al.  Influence of season and latitude on the cutaneous synthesis of vitamin D3: exposure to winter sunlight in Boston and Edmonton will not promote vitamin D3 synthesis in human skin. , 1988, The Journal of clinical endocrinology and metabolism.

[56]  Devashish Mitra,et al.  Racial, geographic, genetic, and body habitus effects on vitamin D metabolism. , 1997 .

[57]  W. B. Watt,et al.  Adaptation at specific loci. VII. Natural selection, dispersal and the diversity of molecular–functional variation patterns among butterfly species complexes (Colias: Lepidoptera, Pieridae) , 2003, Molecular ecology.

[58]  L. Björn,et al.  Vitamin D in an ecological context. , 2000, International journal of circumpolar health.

[59]  K. Wakamatsu,et al.  Pheomelanin as well as eumelanin is present in human epidermis. , 1991, The Journal of investigative dermatology.

[60]  M. Moffatt Current status of nutritional deficiencies in Canadian aboriginal people. , 1995, Canadian journal of physiology and pharmacology.

[61]  T. Fitzpatrick,et al.  Role of light in human skin color viariation. , 1975, American journal of physical anthropology.

[62]  J. Adams,et al.  INCREASED SKIN PIGMENT REDUCES THE CAPACITY OF SKIN TO SYNTHESISE VITAMIN D3 , 1982, The Lancet.

[63]  W. Loomis Skin-Pigment Regulation of Vitamin-D Biosynthesis in Man , 1967, Science.

[64]  V. Batra,et al.  Increased Folate Catabolism Following Total Body γ-Irradiation in Mice , 2003 .

[65]  W. Montagna Comparative anatomy and physiology of the skin. , 1967, Archives of dermatology.

[66]  G. Lasker Seasonal changes in skin color. , 1954, American journal of physical anthropology.

[67]  M. Lucock,et al.  A critical role for B-vitamin nutrition in human developmental and evolutionary biology , 2003 .

[68]  David A. Brown Chapter 33 - Skin pigmentation enhancers , 2001 .

[69]  G. Barsh,et al.  The genetics of pigmentation: from fancy genes to complex traits. , 1996, Trends in genetics : TIG.

[70]  F. S. Johnson,et al.  AVERAGE LATITUDINAL VARIATION IN ULTRAVIOLET RADIATION AT THE EARTH'S SURFACE , 1976, Photochemistry and photobiology.

[71]  A. Herbig,et al.  New perspectives on folate catabolism. , 2003, Annual review of nutrition.

[72]  T. Gambichler,et al.  Serum folate levels after UVA exposure: a two-group parallel randomised controlled trial , 2001, BMC dermatology.

[73]  S. Wooding,et al.  Genetic Variation at the MC1R Locus and the Time since Loss of Human Body Hair1 , 2004 .

[74]  J. Marks What it Means to be 98% Chimpanzee: Apes, People, and their Genes , 2002 .

[75]  P. E. Wheeler The influence of bipedalism on the energy and water budgets of early hominids , 1991 .

[76]  E. A. Edwards,et al.  The pigments and color of living human skin , 1939 .

[77]  W. Montagna Cutaneous comparative biology. , 1971, Archives of dermatology.

[78]  N F Box,et al.  Human pigmentation genes: identification, structure and consequences of polymorphic variation. , 2001, Gene.

[79]  P. E. Wheeler The thermoregulatory advantages of large body size for hominids foraging in savannah environments , 1992 .

[80]  E. Mawer,et al.  The distribution and storage of vitamin D and its metabolites in human tissues. , 1972, Clinical science.

[81]  M. Holick,et al.  Environmental factors that influence the cutaneous production of vitamin D 13 , 1995 .

[82]  M. Shriver,et al.  Skin responses to ultraviolet radiation: effects of constitutive pigmentation, sex, and ancestry. , 2002, Pigment cell research.

[83]  A. Copp,et al.  Embryonic folate metabolism and mouse neural tube defects. , 1998, Science.

[84]  J. Haworth,et al.  Vitamin-D-deficient rickets in Manitoba, 1972-84. , 1986, CMAJ : Canadian Medical Association journal = journal de l'Association medicale canadienne.

[85]  Z. Abdel‐Malek,et al.  Regulation of the human melanocortin 1 receptor expression in epidermal melanocytes by paracrine and endocrine factors and by ultraviolet radiation. , 2002, Pigment cell research.

[86]  R. McKenzie,et al.  Changes in biologically active ultraviolet radiation reaching the Earth's surface. , 1998, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[87]  H G Vogel,et al.  [Mechanical properties of the skin]. , 1972, Archiv fur dermatologische Forschung.

[88]  F. Lees,et al.  Estimating the number of loci determining skin colour in a hybrid population. , 1981, Annals of human biology.

[89]  Steegmann At Frostbite of the human face as a selective force. , 1967, Human biology.

[90]  W. Morison What is the function of melanin? , 1985, Archives of dermatology.

[91]  G. H. Kay,et al.  Vitamin-D deficiency in Asians at home and in Britain. , 1973, Lancet.

[92]  W Westerhof,et al.  The relation between constitutional skin color and photosensitivity estimated from UV-induced erythema and pigmentation dose-response curves. , 1990, The Journal of investigative dermatology.

[93]  M. Holick,et al.  Regulation of cutaneous previtamin D3 photosynthesis in man: skin pigment is not an essential regulator. , 1981, Science.

[94]  N. Jablonski,et al.  The evolution of human skin coloration. , 2000, Journal of human evolution.

[95]  Lars Olof Björn,et al.  Toward Solving the UV Puzzle , 2002, Science.

[96]  J. Weiner 253. A Spectrophotometer for Measurement of Skin Colour , 1951 .

[97]  F. Lees,et al.  Skin colorimetry in Belize. I. Conversion formulae. , 1978, American journal of physical anthropology.

[98]  Hiroyuki Suzuki,et al.  Sequence-specific DNA damage induced by ultraviolet A-irradiated folic acid via its photolysis product. , 2003, Archives of biochemistry and biophysics.

[99]  K. Aoki,et al.  Sexual selection by male choice in monogamous and polygynous human populations. , 1999, Theoretical population biology.

[100]  B. Gessner,et al.  Nutritional rickets among breast-fed black and Alaska Native children. , 1997, Alaska medicine.

[101]  R. Sturm,et al.  Human pigmentation genetics: the difference is only skin deep , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[102]  D. Hewett‐Emmett,et al.  High polymorphism at the human melanocortin 1 receptor locus. , 1999, Genetics.

[103]  T. Fitzpatrick The validity and practicality of sun-reactive skin types I through VI. , 1988, Archives of dermatology.

[104]  P. E. Wheeler The loss of functional body hair in man: the influence of thermal environment, body form and bipedality , 1985 .

[105]  R. Ellis,et al.  The skin of primates. VI. The skin of the gorilla (Gorilla gorilla). , 1962, American journal of physical anthropology.

[106]  C. Garland,et al.  Epidemiologic evidence for different roles of ultraviolet A and B radiation in melanoma mortality rates. , 2003, Annals of epidemiology.

[107]  P. Baker Racial differences in heat tolerance. , 1958, American journal of physical anthropology.

[108]  Lock‐Andersen,et al.  Facultative skin pigmentation in caucasians: an objective biological indicator of lifetime exposure to ultraviolet radiation? , 1998, The British journal of dermatology.

[109]  E. Gunter,et al.  Hypovitaminosis D in medical inpatients. , 1998, The New England journal of medicine.

[110]  M. Holick Vitamin D: A millenium perspective , 2003, Journal of cellular biochemistry.

[111]  H. Randle,et al.  Suntanning: differences in perceptions throughout history. , 1997, Mayo Clinic proceedings.

[112]  M. El-Hazmi,et al.  Exposure to sunlight and vitamin D deficiency in Saudi Arabian women. , 1984, Postgraduate medical journal.

[113]  J. Eaton,et al.  Skin color and nutrient photolysis: an evolutionary hypothesis. , 1978, Science.

[114]  K. Kraning,et al.  Human thermoregulatory responses during heat exposure after artificially induced sunburn. , 1992, The American journal of physiology.

[115]  T. Fitzpatrick,et al.  Tyrosinase in human skin: demonstration of its presence and of its role in human melanin formation. , 1950, Science.

[116]  F. Urbach The negative effects of solar radiation: a clinical overview , 2001 .

[117]  A. Bereket Rickets in developing countries. , 2003, Endocrine development.

[118]  I. Jackson,et al.  Evidence for variable selective pressures at MC1R. , 2000, American journal of human genetics.

[119]  I. Jackson,et al.  Melanocortin 1 receptor variants in an Irish population. , 1998, The Journal of investigative dermatology.

[120]  P. E. Wheeler The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased convective heat loss and cutaneous evaporative cooling , 1991 .

[121]  A. R. Frisancho Human adaptation: A functional interpretation , 1979 .

[122]  C. Antunes,et al.  Color and genomic ancestry in Brazilians , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[123]  A. Brues Rethinking human pigmentation , 1975 .

[124]  Susan C. Taylor,et al.  Skin of color: biology, structure, function, and implications for dermatologic disease. , 2002, Journal of the American Academy of Dermatology.

[125]  Wen-Hsiung Li,et al.  DNA Polymorphism and Selection at the Melanocortin‐1 Receptor Gene in Normally Pigmented Southern African Individuals , 2003, Annals of the New York Academy of Sciences.

[126]  B. Epe,et al.  Wavelength dependence of oxidative DNA damage induced by UV and visible light. , 1997, Carcinogenesis.

[127]  A. T. Steegmann, Frostbite of the human face as a selective force. , 1967, Human biology.

[128]  HUMAN PIGMENTATION , 1961 .

[129]  J. Chung Chapter 4 - The effects of sunlight on the skin of Asians , 2001 .

[130]  F. Stanley,et al.  Dietary folate as a risk factor for neural‐tube defects: evidence from a case‐control study in Western Australia , 1989, The Medical journal of Australia.

[131]  T. Fitzpatrick,et al.  Some aspects of melanin biology: 1950-1975. , 1976, The Journal of investigative dermatology.

[132]  U. Mathur,et al.  The effect of aminopterin-induced folic acid deficiency on spermatogenesis. , 1977, Fertility and sterility.

[133]  G. Walsberg,et al.  Consequences of skin color and fur properties for solar heat gain and ultraviolet irradiance in two mammals , 2004, Journal of Comparative Physiology B.

[134]  C. Ruff,et al.  Body mass and encephalization in Pleistocene Homo , 1997, Nature.

[135]  E. Haug,et al.  Vitamin D deficiency amongst Pakistani women in Oslo , 1993, Acta obstetricia et gynecologica Scandinavica.

[136]  N. Jablonski,et al.  Physiology, thermoregulation and bipedalism , 1994 .

[137]  M. E. Rawles Origin of melanophores and their role in development of color patterns in vertebrates. , 1948, Physiological reviews.

[138]  A. Zihlman,et al.  The adaptive response of human skin to the savanna , 1988 .

[139]  M. Pagel,et al.  A naked ape would have fewer parasites , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[140]  R. B. Cowles Some Ecological Factors Bearing on the Origin and Evolution of Pigment in the Human Skin , 1959, The American Naturalist.

[141]  J. V. D. van den Berg,et al.  Effects of ultraviolet B light on cutaneous immune responses of humans with deeply pigmented skin. , 1991, The Journal of investigative dermatology.

[142]  B. Kitchell,et al.  The biology of melanocytes. , 2003, Veterinary dermatology.

[143]  James Varani,et al.  Mechanisms of photoaging and chronological skin aging. , 2002, Archives of dermatology.

[144]  R. Minns Folic acid and neural tube defects , 1996, Spinal Cord.

[145]  T. Fitzpatrick,et al.  Racial Differences in the Fate of Melanosomes in Human Epidermis , 1969, Nature.

[146]  Peter Frost,et al.  Human Skin Color: A Possible Relationship Between Its Sexual Dimorphism and Its Social Perception , 2015, Perspectives in biology and medicine.

[147]  K. Toda,et al.  The relationship of skin color, UVB-induced erythema, and melanogenesis. , 1985, The Journal of investigative dermatology.

[148]  I. Jackson,et al.  Functional variation of MC1R alleles from red-haired individuals. , 2001, Human molecular genetics.

[149]  R. Anderson,et al.  Spectral character of sunlight modulates photosynthesis of previtamin D3 and its photoisomers in human skin. , 1982, Science.

[150]  J. Mackintosh The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. , 2001, Journal of theoretical biology.

[151]  Clothing prevents ultraviolet-B radiation-dependent photosynthesis of vitamin D3. , 1992 .

[152]  M. Deol,et al.  Racial differences in pigmentation and natural selection , 1975, Annals of human genetics.

[153]  N Kollias,et al.  The physical basis of skin color and its evaluation. , 1995, Clinics in dermatology.

[154]  P. J. Byard Quantitative genetics of human skin color , 1981 .

[155]  N Kollias,et al.  Photoprotection by melanin. , 1991, Journal of photochemistry and photobiology. B, Biology.

[156]  W. Grant An estimate of premature cancer mortality in the U.S. due to inadequate doses of solar ultraviolet‐B radiation , 2002, Cancer.

[157]  R. Sturm,et al.  Skin colour and skin cancer - the genetic link , 2001 .

[158]  Donal E. Muir Race: The Mythic Root of Racism , 1993 .

[159]  A. Suria,et al.  Maternal vitamin‐D deficiency in Pakistan , 1998, Acta obstetricia et gynecologica Scandinavica.

[160]  M. Pagel,et al.  Sexual swellings advertise female quality in wild baboons , 2001, Nature.

[161]  V. Candas,et al.  Thermoregulatory effects of three different types of head cooling in humans during a mild hyperthermia , 2000, European Journal of Applied Physiology.

[162]  H. Mchenry,et al.  Body proportions of Australopithecus afarensis and A. africanus and the origin of the genus Homo. , 1998, Journal of human evolution.

[163]  K. Aoki Sexual selection as a cause of human skin colour variation: Darwin's hypothesis revisited , 2002, Annals of human biology.