Sexual selection as a cause of human skin colour variation: Darwin's hypothesis revisited

Annals of Human Biology

Volumn 29, Issue 6, 2002, Pages 589-608

  Aoki, Kenichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN RECEPTOR; MELANOCORTIN RECEPTOR;

COLOR; SEXUAL SELECTION; SKIN;

CULTURAL FACTOR; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HUMAN; POPULATION GENETICS; REVIEW; RICKETS; SEXUAL BEHAVIOR; SKIN PIGMENTATION;

CROSS-CULTURAL COMPARISON; GENETICS, POPULATION; HUMANS; RECEPTORS, CORTICOTROPIN; RECEPTORS, MELANOCORTIN; RICKETS; SELECTION (GENETICS); SEXUAL BEHAVIOR; SKIN PIGMENTATION; VARIATION (GENETICS);

EID: 0036866115     PISSN: 03014460     EISSN: None     Source Type: Journal    
DOI: 10.1080/0301446021000019144     Document Type: Review

References (104)

1. Aoki, K., Feldman, M. W., and Kerr, B., 2001, Models of sexual selection on a quantitative genetic trait when preference is acquired by sexual imprinting. Evolution, 55, 25-32.
2. Arnold, J. E., 1996, The archaeology of complex hunter-gatherers. Journal of Archaeological Method and Theory, 3, 77-126.
3. Baldwin, J. C., and Damon, A., 1973, Some genetic traits in Solomon Island populations V. Assortative mating, with special reference to skin color. American Journal of Physical Anthropology, 39, 195-202.
4. Banerjee, S., 1985, Assortative mating for colour in Indian populations. Journal of Biosocial Science, 17, 205-209.
5. 3). Photochemistry and Photobiology, 25, 519-527.
6. Bhattacharyya, A. K., 1992, Nutritional rickets in the tropics. In Nutritional Triggers for Health and in Disease, World Review of Nutrition and Diet, vol. 67, edited by A. P. Simopoulos (Basel: Karger), pp. 140-197.
7. Binet, A., and Kooh, S. W., 1996, Persistence of vitamin D-deficiency rickets in Toronto in the 1990s. Canadian Journal of Public Health, 87, 227-230.
8. Borgerhoff Mulder, M., 1987, Resources and reproductive success in women with an example for the Kipsigis of Kenya. Journal of Zoology, London, 213, 489-505.
9. Box, N. F., Wyeth, J. R., O'Gorman, L. E., Martin, N. G., and Sturm, R. A., 1997, Characterization of melanocyte stimulating hormone receptor variant alleles in twins with red hair. Human Molecular Genetics, 6, 1891-1897.
10. Brace, C. L., 1973, A nonracial approach towards the understanding of human diversity. In Man in Evolutionary Perspective, edited by C. L. Brace and J. Metress (New York: Wiley), pp. 341-363.
11. Branda, R. F., and Eaton, J. W., 1978, Skin color and nutrient photolysis: An evolutionary hypothesis. Science, 201, 625-626.
12. Buss, D. M., 1989, Sex difference in human mate preferences: Evolutionary hypotheses tested in 37 cultures. Behavioral and Brain Sciences, 12, 1-49.
13. Byard, P. J., 1981, Quantitative genetics of human skin color. Yearbook of Physical Anthropology, 24, 123-137.
14. Chhajlani, V., and Wikberg, J. E. S., 1992, Molecular cloning and expression of the human melanocyte stimulating hormone receptor cDNA. FEBS Letters, 309, 417-420.
15. 3. Lancet, 1, 74-76.
16. Cone, R. D., Lu, D., Koppula, S., Vage, D. I., Klungland, H., Boston, B., Chen, W., Orth, D. N., Pouton, C., and Kesterson, R. A., 1996, The melanocortin receptors: Agonists, antagonists, and the hormonal control of pigmentation. Recent Progress in Hormone Research, 51, 287-318.
17. Darwin, C., 1871, The Descent of Man (London: Murray).
18. Darwin, C., 1874, The Descent of Man, 2nd Edn (London: Murray).
19. Dawodu, A., Dawson, K. P., Amirlak, I., Kochiyil, J., Agarwal, M., and Badrinath, P., 2001, Diet, clothing, sunshine exposure and micronutrient status of Arab infants and young children. Annals of Tropical Paediatrics, 21, 39-44.
20. Diamond, J., 1997, Guns, Germs, and Steel (New York: Norton).
21. Ellis, G., Woodhead, J. S., and Cooke, W. T., 1977, Serum-2-hydroxyvitamin-D concentrations in adolescent boys. Lancet, 1, 825-828.
22. Emlen, S. T., and Oring, L. W., 1977, Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215-223.
23. Feinman, S., and Gill, G. W., 1978, Sex differences in physical attractiveness preferences. Journal of Social Psychology, 105, 43-52.
24. Feleke, Y., Abdulkadir, J., Mshana, R., Mekbib, T.-A., Brunvand, L., Berg, J. P., and Falch, J. A., 1999, Low levels of serum calcidiol in an African population compared to a North European population. European Journal of Endocrinology, 141, 358-360.
25. Fisher, R. A., 1958, The Genetical Theory of Natural Selection (New York: Dover).
26. Follis, R. H., Jr, Park, E. A., and Jackson, D., 1952, The prevalence of rickets at autopsy during the first two years of age. Bulletin of the Johns Hopkins Hospital, 91, 480-490.
27. Ford, J. A., McIntosh, W. B., Butterfield, R., Preece, M. A., Pietrek, J., Arrow-Smith, W. A., Arthurton, M. W., Turner, W., O'Riordan, J. L. H., and Dunnigan, M. G., 1976, Clinical and subclinical vitamin D deficiency in Bradford children. Archives of Disease in Childhood, 51, 939-943.
28. Frändberg, P.-A., Doufexis, M., Kapas, S., and Chhajlani, V., 1998, Human pigmentation pheno-type: A point mutation generates nonfunctional MSH receptor. Biochemical and Biophysical Research Communications, 245, 490-492.
29. Frisancho, A. R., Wainwright, R., and Way, A., 1981, Heritability and components of phenotypic expression in skin reflectance of Mestizos from the Peruvian lowlands. American Journal of Physical Anthropology, 55, 203-208.
30. Frost, P., 1994, Preference for darker faces in photographs at different phases of the menstrual cycle: Preliminary assessment of evidence for a hormonal relationship. Perceptual and Motor Skills, 79, 507-514.
31. Gantz, I., Konda, Y., Tashiro, T., Shimoto, Y., Miwa, H., Munzert, O., Watson, S. J., Delvalle, J., and Yamada, T., 1993, Molecular-cloning of a novel melanocortin receptor. Journal of Biological Chemistry, 268, 8246-8250.
32. Goel, K. M., Sweet, E. M., Logan, R. W., Warren, J. M., Arneil, O. C., and Shanks, R. A., 1976, Florid and subclinical rickets among immigrant children in Glasgow. Lancet, 1, 1141-1145.
33. Harding, R. M., Healy, E., Ray, A. J., Ellis, N. S., Flanagan, N., Todd, C., Dixon, C., Sajantila, A., Jackson, I. J., Birch-Machin, M. A., and Rees, J. L., 2000, Evidence of variable selective pressures at MC1R. American Journal of Human Genetics, 66, 1351-1361.
34. Harrison, G. A., and Owen, J. J. T., 1964, Studies on the inheritance of human skin color. Annals of Human Genetics, 28, 27-37.
35. Henderson, J. B., Dunnigan, M. G., McIntosh, W. B., Abdul-Motaal, A. A., Gettinby, G., and Glekin, B. M., 1987, The importance of limited exposure to ultraviolet radiation and dietary factors in the aetiology of Asian rickets: A risk-factor model. Quarterly Journal of Medicine, New Series, 63, 413-425.
36. 1-3. American Journal of Clinical Nutrition, 61, 638S-645S.
37. Holick, M. F., 2000, Sunlight and vitamin D: The bone and cancer connections. Radiation Protection Dosimetry, 91, 65-71.
38. 3 photosynthesis in man: Skin pigment is not an essential regulator. Science, 211, 590-593.
39. Holmes, A. M., Enoch, B. A., Taylor, J. L., and Jones, M. E., 1973, Occult rickets and osteomalacia amongst the Asian immigrant population. Quarterly Journal of Medicine, New Series, 42, 125-149.
40. Ihara, Y., and Aoki, K., 1999, Sexual selection by male choice in monogamous and polygynous human populations. Theoretical Population Biology, 55, 77-93.
41. Ingman, M., Kaessmann, H., Pääbo, S., and Gyllensten, U., 2000, Mitochondrial genome variation and the origin of modern humans. Nature, 408, 708-713.
42. Iwasa, Y., Pomiankowski, A., and Nee, S., 1991, The evolution of costly mate preferences. II. The 'handicap' principle. Evolution, 45, 1431-1442.
43. Jablonski, N. G., and Chaplin, G., 2000, The evolution of human skin color variation. Journal of Human Evolution, 39, 57-106.
44. Jimbow, K., Quevedo, W. C., Jr, Fitzpatrick, T. B., and Szabó, G., 1993, Biology of melanocytes. In Dermatology in General Medicine, 4th Edn, edited by T. Fitzpatrick, A. Eisen, K. Wolff, I. M. Freedberg and R. F. Austen (New York: McGraw-Hill), pp. 261-289.
45. Jones, D., 1995, Sexual selection, physical attractiveness, and facial neoteny: Cross-cultural evidence and implications. Current Anthropology, 36, 723-748.
46. Jones, D., 1997, An evolutionary perspective on physical attractiveness. Evolutionary Anthropology, 5, 97-109.
47. Kimura, M., 1983, The Neutral Theory of Molecular Evolution (Cambridge: Cambridge University Press).
48. Kirkpatrick, M., 1982, Sexual selection and the evolution of female choice. Evolution, 36, 1-12.
49. Klein, R. G., 1999, The Human Career, 2nd Edn (Chicago: University of Chicago Press).
50. Kreiter, S. R., Schwartz, R. P., Kirkman, H. N., Jr, Charlton, P. A., Calikoglu, A. S., and Davenport, M. L., 2000, Nutritional rickets in African American breast-fed infants. Journal of Pediatrics, 137, 153-157.
51. Lande, R., 1981, Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences USA, 78, 3721-3725.
52. Loomis, W. F., 1967, Skin-pigment regulation of vitamin-D biosynthesis in man. Science, 157, 501-506.
53. Lynch, M., and Walsh, B., 1998, Genetics and Analysis of Quantitative Traits (Sunderland: Sinauer).
54. Matsuoka, L. Y., Wortsman, J., Haddad, J. G., Kolm, P., and Hollis, B. W., 1991, Racial pigmentation and the cutaneous synthesis of vitamin D. Archives of Dermatology, 127, 536-538.
55. Mawer, E. B., Backhouse, J., Holman, C. A., Lumb, G. A., and Stanbury, S. W., 1972, The distribution and storage of vitamin D and its metabolites in human tissues. Clinical Science, 43, 413-431.
56. McDonald, J. H., and Kreitman, M., 1991, Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652-654.
57. Mitchell, F. T., 1930, Incidence of rickets in the south. Southern Medical Journal, 23, 228-235.
58. Mountjoy, K. O., 1994, The human melanocyte stimulating hormone receptor has evolved to become 'super-sensitive' to melanocortin peptides. Molecular and Cellular Endocrinology, 102, R7-R11.
59. Mountjoy, K. G., Robbins, L. S., Mortrud, M. T., and Cone, R. D., 1992, The cloning of a family of genes that encode melanocortin receptors. Science, 257, 1248-1251.
60. Murray, F. G., 1934, Pigmentation, sunlight and nutritional disease. American Anthropologist, 36, 438-445.
61. Nakayama, K., 2001, Genetic Diversity of Melanocortin 1 Receptor in Asia. M.Sc. thesis, Department of Biological Sciences, University of Tokyo.
62. Nei, M., 1985, Human evolution at the molecular level. In Population Genetics and Molecular Evolution, edited by T. Ohta and K. Aoki (Tokyo: Japan Scientific Societies Press), pp. 41-64.
63. O'Donald, P., 1980, Genetic Models of Sexual Selection (Cambridge: Cambridge University Press).
64. Parker, G. A., and Simmons, L. W., 1996, Parental investment and the control of sexual selection: Predicting the direction of sexual competition. Proceedings of the Royal Society London B, 263, 315-321.
65. Pathak, M. A., Fitzpatrick, T. B., Greiter, F., and Kraus, E. W., 1987, Preventive treatment of sunburn, dermatoheliosis, and skin cancer with sun-protective agents. In Dermatology in General Medicine, 3rd Edn. edited by T. Fitzpatrick, A. Eisen, K. Wolff, I. M. Freedberg and R. F. Austen (New York: McGraw-Hill), pp. 1507-1522,
66. Perrett, D. I., May, K. I., and Yoshikawa, S., 1994, Facial shape and judgments of female attractiveness. Nature, 368, 239-242.
67. Pfitzner, M. A., Thacher, T. D., Pettifor, J. M., Zoakah, A. I., Lawson, J. O., Isichei, C. O., and Fischer, P. R., 1998, Absence of vitamin D deficiency in young Nigerian children. Journal of Pediatrics, 133, 740-744.
68. Pomiankowski, A., Iwasa, Y., and Nee, S., 1991, The evolution of costly mate preferences. I. Fisher and biased mutation. Evolution, 45, 1422-1430.
69. Ramsay, M., and John, P. R., 2000, MC1R gene variation in normally pigmented South African individuals. American Journal of Human Genetics, 67 (suppl. 2), 237.
70. Rana, B. K., Hewett-Emmett, D., Jin, L., Chang, B. H.-J., Sambuughin, N., Lin, M., Watkins, S., Bamshad, M., Jorde, L. B., Ramsay, M., Jenkins, T., and Li, W.-H., 1999, High polymorphism at the human melanocortin 1 receptor locus. Genetics, 151, 1547-1557.
71. Relethford, J. H., 1997, Hemispheric differences in human skin color. American Journal of Physical Anthropology, 104, 449-458.
72. Roberts, C., and Manchester, K., 1995, Archaeology of Disease, 2nd Edn (Ithaca: Cornell University Press).
73. Roberts, D. F., and Kahlon, D. P. S., 1972, Skin pigmentation and assortative mating in Sikhs. Journal of Biosocial Science, 4, 91-100.
74. Roberts, D. F., and Kahlon, D. P. S., 1976, Environmental correlations of skin colour. Annals of Human Biology, 3, 11-22.
75. Robins, A. H., 1991, Biological Perspectives on Human Pigmentation (Cambridge: Cambridge University Press).
76. Sano, S., 2002, Theoretical Study of Sexual Selection in a Finite Population. M.Sc. thesis, Department of Biological Sciences, University of Tokyo.
77. Schiöth, H. B., Phillips, S. R., Rudzish, R., Birch-Machin, M. A., Wikberg, J. E. S., and Rees, J. L., 1999, Loss of function mutations of the human melanocortin 1 receptor are common and are associated with red hair. Biochemical and Biophysical Research Communications, 260, 488-491.
78. Shi, P., Lu, X. M., Luo, H. R., Xiang-Yu, J.-G., and Zhang, Y. P., 2001, Melanocortion-1 receptor gene variants in four Chinese ethnic populations. Cell Research, 11, 81-84.
79. Singh, D., 1993, Adaptive significance of female physical attractiveness: Role of waist-to-hip ratio. Journal of Personality and Social Psychology, 65, 293-307.
80. Singh, D., and Young, R. K., 1995, Body weight, waist-to-hip ratio, breasts, and hips: Role in judgments of female attractiveness and desirability for relationships. Ethology and Sociobiology, 16, 483-507.
81. Specker, B. L., Valanis, B., Hertzberg, V., Edwards, N., and Tsang, R. C., 1985, Sunshine exposure and serum 25-hydroxyvitamin D concentrations in exclusively breast-fed infants. Journal of Pediatrics, 107, 372-376.
82. Stern, C., 1953, Model estimates of the frequency of white and near-white segregants in the American Negro. Acta Genetica, 4, 281-298.
83. Stern, C., 1970, Model estimates of the number of gene pairs involved in pigmentation variability of the Negro-American. Human Heredity, 20, 165-168.
84. Sturm, R. A., Box, N. F., and Ramsay, M., 1998, Human pigmentation genetics: The difference is only skin deep. BioEssays, 20, 712-721.
85. Takahata, N., 1990, Allelic genealogy and MHC polymorphisms. In Population Biology of Genes and Molecules, edited by N. Takahata and J. F. Crow (Tokyo: Baifukan), pp. 267-286.
86. Takahata, N., and M. Nei, 1990, Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics, 124, 967-978.
87. Tasa, G. L., Murray, C. J., and Boughton, J. M., 1985, Reflectometer reports of human pigmentation. Current Anthropology, 26, 511-512.
88. Ten Cate, C., and Bateson, P., 1988, Sexual selection: The evolution of conspicuous characteristics in birds by means of imprinting. Evolution, 42, 1355-1358.
89. Ten Cate, C., and Bateson, P., 1989, Sexual imprinting and a preference for 'supernormal' partners in Japanese quail. Animal Behaviour, 38, 356-358.
90. Thody, A. J., Higgins, E. M., Wakamatsu, K., Ito, S., Burchill, S. A., and Marks, J. M., 1991, Pheomelanin as well as eumelanin is present in human epidermis. Journal of Investigative Dermatology, 97, 340-344.
91. Thompson, L. A., 1989, Romans and Blacks (Norman: University of Oklahoma Press).
92. Thomson, M. L., 1951, The cause of changes in sweating rate after ultraviolet radiation. Journal of Physiology, 112, 31-42.
93. Thomson, M. L., 1955, Relative efficiency of pigment and horny layer thickness in protecting the skin of Europeans and Africans against solar ultraviolet radiation. Journal of Physiology, 127, 236-246.
94. Underhill, P. A., Shen, P., Lin, A. A., Jin, L., Passarino, G., Yang, W. H., Kauffman, E., Bonné-Tamir, B., Bertranpetit, J., Francalacci, P., Ibrahim, M., Jenkins, T., Kidd, J. R., Mehdi, S. Q., Seielstad, M. T., Wells, R. S., Piazza, A., Davis, R. W., Feldman, M. W., Cavalli-Sforza, L. L., and Oefner, P. J., 2000, Y chromosome sequence variation and the history of human populations. Nature Genetics, 26, 358-361.
95. Valverde, P., Healy, E., Jackson, I., Rees, J. L., and Thody, A. J., 1995, Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nature Genetics, 11, 328-330.
96. van den Berghe, P. L., and Frost, P., 1986, Skin color preference, sexual dimorphism and sexual selection: A case of gene culture coevolution? Ethnic and Racial Studies, 9, 87-113.
97. Vigilant, L., Stoneking, M., Harpending, H., Hawkes, K., and Wilson, A. C., 1991, African populations and the evolution of human mitochondrial DNA. Science, 253, 1503-1507.
98. Voisey, J., and van Daal, A., 2002, Agouti: From mouse to man, from skin to fat. Pigment Cell Research, 15, 10-18.
99. Wagatsuma, H., 1967, The social perception of skin color in Japan. Daedalus, 96, 407-443.
100. 3 synthesis in human skin. Journal of Clinical Endocrinology and Metabolism, 67, 373-378.
101. Welch, T. R., Bergstrom, W. H., and Tsang, R. C., 2000, Vitamin D-deficient rickets: The reemergence of a once-conquered disease. Journal of Pediatrics, 137, 143-145.
102. Wells, C., 1975, Prehistoric and historical changes in nutritional diseases and associated conditions. Progress in Food and Nutrition Science, 1, 729-779.
103. Yao, Y.-G., Lü, X.-M., Luo, H-R., Li, W.-H., and Zhang, Y.-P., 2000, Gene admixture in the Silk Road region of China: Evidence from mtDNA and melanocortin 1 receptor polymorphism. Genes and Genetic Systems, 75, 173-178.
104. Zerjal, T., Dashnyam, B., Pandya, A., Kayser, M., Roewer, L., Santos, F. R., Schiefenhövel, W., Fretwell, N., Jobling, M. A., Harihara, S., Shimizu, K., Semjidmaa, D., Sajantila, A., Salo, P., Crawford, M. H., Ginter, E. K., Evgrafov, O. V., and Tyler-Smith, C., 1997, Genetic relationships of Asians and northern Europeans, revealed by Y-chromosomal DNA analysis. American Journal of Human Genetics, 60, 1174-1183.