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114 In: Solar Radiation and Human Health Espen Bjertness, editor. Oslo: The Norwegian Academy of Science and Letters, 2008. The evolution of different skin colours Arnfinn Hykkerud Steindal1 and Johan Moan1,2 1 Norwegian Radium Hospital, Oslo, Norway, 2 University of Oslo, Oslo, Norway Correspondene: Arnfinn Hykkerud Steindal, Department of Radiation Biology, Institute for Cancer Research, Norwegian Radium Hospital, Montebello, N-0310 Oslo, Norway, E-mail: [email protected] Telephone: +47 22934443 Fax: +47 22934270 Abstract Skin colour is a phenotype that has been widely used to separate humans into different races. A dark skin colour is mainly due to high levels of melanin, a pigment that absorbs ultraviolet radiation (UV), visible light and infrared radiation. Hence, darkly pigmented skin absorbs more radiation than lightly pigmented skin and reduces the penetration depth of it into skin. Skin colour of a human population correlates strongly with latitude and with the intensity of ultraviolet radiation reaching the Earth’s surface where the population lives. The mechanisms behind the evolution of human skin colour are not yet fully understood. Several theories have been proposed, most of them being related to UV radiation. The skin of the first hominids was probably light and covered with dark hair, as that of the chimpanzee today. Very early in the evolution of the genus Homo, the body hair was lost and a dark skin colour evolved. Since then, the colour has probably been modulated by migration towards or away from the Equator. It has been suggested that dark skin is advantageous in regions with high UV fluences because of protection against sunburn and skin cancer. However, skin cancer use to develop late in life, after the reproductive age. Recently, it was proposed that protection of folate against photolysis is more important. Folate is an essential vitamin for proper development of the fetus, and folate deficiency may lead to neural tube defects. Therefore, if folate is degraded in the human body by UV exposure, the degradation will constitute an evolutionary pressure, favouring dark skin near the Equator. Since humans get almost all their vitamin D from sun exposure, a total protection from UV is not desirable. This means that lightly pigmented skin is necessary in areas of low annual UV exposure to allow production of enough vitamin D, and that the colour of the skin at different areas on earth is evolutionarily developed to 115 balance folate photodegradation and vitamin D photoproduction. These phenomena are discussed. Introduction There is a strong correlation between skin colour of humans and UV radiation intensity (1, 2), indicating that the variation in skin pigmentation with latitude is a result of adaptation to different UV environments via natural (1) and/or sexual (3, 4) selection. Melanin is the main pigment in human skin. Melanin is produced by melanocytes, a cell type in the lower part of the epidermis. The melanin is stored in melanosomes and redistributed to neighboring keratinocytes in the basal layers of the epidermis (5). Melanocytes produces two different types of melanin: the yellow/red pheomelanin and the brown/black eumelanin (6). Both these types are produced from an oxidation of the amino acid tyrosine by the use of the enzyme tyrosinase. The human skin colour is a result of the varied production, distribution and packaging of the two classes of melanin. A dark skin colour is due to high concentration of eumelanin, but there is normally no correlation between pheomelanin concentration in the epidermis and skin type, except in the case of red-haired persons that seem to have a higher concentration of pheomelanin than other people (7). The melanocyte densities are remarkably similar between people with different skin colours, but the cells melanin production activity varies. The history of humans Our common ancestors with those of chimpanzees lived around six million years ago in Africa. During the period from six to about two million years ago, species belonging to the genus Australopithecus lived. They looked more ape-like, and had body hair. The earliest known members of the genus Homo is at least 1.2 million years old, and belong to the species Homo erectus (8). They had larger bodies, larger brains and longer lower limbs than their ancestors. Therefore, they were able to walk and run longer distances. Because of higher activity levels and, consequently, longer daylight exposure, they developed hairlessness and high density of eccrine sweat glands to be able to get rid of body heat (9). What separate us the most from other primates is our large brain. Our brain is heat sensitive, and the temperature of the brain follows the temperature of the arterial blood (10). In other words, the brain temperature follows the core temperature of the body. A whole body cooling system was therefore required for the development of larger brain and increased activity level, and for our ancestors to be able to survive on the savannahs of Africa (1, 11). Our closest 116 relatives, the chimpanzees, lack eccrine sweat glands and can not move freely during the dry, sunny season. They are restricted to areas with water and shade (11). As a consequence of reduced body hair density and increased number of eccrine sweat glands, the skin of early humans had to be protected against harmful UV radiation (1). The modern Homo sapiens developed in Africa, according to the “single origin” hypothesis (12). It was evolved in East-Africa around 100.000 years ago, and started to move from there and out into the world 80.000 years ago. Europe was populated around 40.000 years ago, and from about the same time Neanderthals started to decline and disappear (13). Modern human replaced the populations of older species, like Homo erectus, Homo neanderthalensis and Homo heidelbergensis, with little or no interbreeding. The modern human was adapted to different conditions and developed a wide spread of skin colours. The “single origin” hypothesis is well supported by genetic (14) and phenotypic (15) evidence. Human Skin Colour Genetics Recent advances in modern gene technology have been crucial to solve some of the mysteries concerning evolution of human skin colour (13). Molecular genetics suggests that the development of different skin colours is an adaptation to local environments (16). The genes controlling human skin colour are mainly related to the production of melanin, and to skin distribution of eumelanin and pheomelanin. This production includes several genes, and mutations in some of them leads to albinism. The gene that is most known to have an impact on skin colour variations is MC1R, a gene encoding for the melanocortin 1 receptor. The melanocortin 1 receptor (MC1R) regulates the production of eumelanin and pheomelanin in the melanocytes (17), and polymorphisms of the MC1R gene varies between different populations. African people are mostly the “wild type”(17, 18). Japanese, Inuits and American Indians have mostly the Arg163Gln genotype, while “red-heads” have a lot of variations, such as Arg151Cys (36%) and Arg160Trp (24%) (18). A functional MC1R seems to be important for dark skin (17, 18) and the MC1R diversity among fair-skinned people can be explained by natural mutations and is not due to evolutionary pressure (18). In other words it seems like the MC1R gene is not important for the evolution of pale skin, but only for the dark skin and for the variation within populations (19). An exception is people with red hair. 117 A couple of years ago, MC1R was the only gene found to be related to normal skin colour variations (20). Several “new” genes have been found recently. SLC24A5, MATP and TYR have been linked to the evolution of European pale skin, while polymorphisms in ASIP and OCA2 are related to skin colour variation all over the world (21). MC1R and ASIP are both involved in the production of the two different melanins. The gene SLC24A5 encodes for a protein that is a member of the potassiumdependent sodium-calcium exchanger (22). This regulates the calcium level in the melanosomes. It has been suggested that melanogenesis and the development of the melanosomes are dependent on calcium level (23). In almost all Africans and Asians the amino acid 111 in the third exon of SLC24A5 are alanine, but in European samples the allele encodes threonine (21, 23). SLC24A5 is a pigmentation-related gene accounting for 25 to 38% of the difference in skin colour between Europeans and Africans (23). It seems that the light skin of Europeans and Asians was developed independently (21), and that the light skin of Europeans was developed as recently as 3.000 to 12.000 years ago (24). Hypotheses Several hypotheses have been proposed to explain the different skin colours in humans. There is a high correlation between colour variation and annual average UVMED (1). In people migrated to a given area a long time ago (over 10–20 thousand years) their skin colour is very close to expected values, while populations recently migrated into certain areas do not correlate very well with UVMED (1). Why do people have dark skin? The dark skin colour is mainly due to melanin. A highly melanised skin absorbs most of the ultraviolet radiation and visible light, and protects people from the damaging effects of such radiations. It is well known that UV radiation induces DNA damages and leads to several types of skin cancers. The melanin is localized around the basal cell nuclei. Therefore, a protective role against the mutagenic effects of ultraviolet radiation is plausible. However, as stated by Blum, skin cancer rarely kills people before their reproductive age and may not be the driving force of dark skin (25), even though in the extreme case of albinos living near the Equator many of them are affected by skin cancers early in their adult life (26). Older people can also have a positive influence on the overall survival of a population, and favour dark skin (27). 118 We lost our body hair and developed sweat glands because of thermoregulation. Dark skin may also have been developed for the same reason. Our large brain is very sensitive to overheating. At a brain temperature of about 40°C you get delirium, and unconsciousness and death may take place at 42°C for a period of time (9). The thermoregulation in pale skinned human is strongly disrupted when exposed to ultraviolet radiation (28). A protection from the UV radiation on the bodies thermoregulation may therefore be a reason for the dark skin (29). Folate is a vitamin necessary for the production of DNA, and therefore, essential for cell division (30). Folate deficiency may lead to neural tube defects (anencephaly, spina bifida) (31). Neural tube defects are among the most common severe congenital malformations (31) and anencephaly (1/3 of all NTD) is always lethal (32). Ultraviolet radiation degrades folate (33). In a mathematical model the incidents of NTD correlates with ultraviolet radiation, in places with more sun light there are more children born with NTD (34). In 1996, Lapunzina found that three women giving birth to children with NTD had used sun beds early in their pregnancies (35). The incidence of NTD varies with season, with the highest conception rates in May–June (36). Dark skin colour may protect the folate in the human body from photodegradation. Highly pigmented skin will therefore be favoured in areas with much ultraviolet radiation, i.e. near the Equator. Native South Americans are a group of people that are much lighter than predicted by the model of Jablonski and Chaplin (1). There may be several explanations for this exception. It may be due to their relatively recent migration, their cultural behaviour, or that it may be more difficult in an evolutionary point of view to gain darker skin than to develop pale skin. Why do people have light skin? By looking at the gene MC1R, it was stated that the light skin of Europeans was due to neutral selection (37), but recent years of genetic research have concluded that the evolution of pale skin is not just a relaxation of evolutionary pressure (19, 21, 23, 38, 39). Therefore, there has to be a driving evolutionary force behind the development of pale skin. Two theories have been proposed, sexual (3, 4) and natural (1, 40) selection. In many societies, people prefer a light skin colour. The evolution of lighter skin colour may, therefore, be driven by sexual selection (4). If the pale skin of people was developed because men preferred light skinned females, the sexual dimorphism in skin colour would have been larger in populations living near the poles than closer to Equator. Madrigal and Kelly did not find any evidence for the sexual selection hypothesis when they studied sexual dimorphism in human skin colour, i.e. the difference in skin colour between men and women in different populations (41). 119 Charles Darwin proposed sexual selection to explain light skin colour based on, among other things, the fact that Asian people living near Equator had the same skin colour as Inuits living near the poles: The Esquimaux live exclusively on animal food; they are clothed in thick fur, and are exposed to intense cold and to prolonged darkness; yet they do not differ in any extreme degree from the inhabitants of Southern China, who live entirely on vegetable food and are exposed almost naked to a hot, glaring climate (3, p. 246). Even though they have almost the same skin colour, Darwin mentioned that they ate different types of food. This leads us to the evolutionary hypothesis accepted by most of the scientists as the driving force in the development of pale skin, the photoproduction of vitamin D. Previtamin D3 is produced in the epidermis and dermis from 7dehydrocholesterol when the skin is exposed to ultraviolet B radiation, 280–315 nm (42, 43). In 1934, Murray formulated the theory that light skin was evolved to produce enough vitamin D (40). Melanin pigmentation reduces the production of vitamin D in the skin after UV exposure (44, 45). The light skin of Europeans was developed as short time as 3.000 to 12.000 years ago (24). This is a strong support for the vitamin D hypothesis, since the human population started with agriculture at this time in history. When they started eating vegetables they also reduced the intake of fish and meat. Therefore, they needed more of their vitamin D from the sun and it was an evolutionary force for lighter skin. The food historically eaten by Inuits is rich on vitamin D, and, therefore, the need of producing it through ultraviolet radiation was not that important. The only known benefit humans have from being exposed to ultraviolet radiation from the sun is the production of vitamin D in the skin. There are mainly two exceptions, Europeans and equatoriel Native Americans are both lighter than predicted according to the ultraviolet exposure from the sun. Europeans are lighter than any other group on Earth. Europeans started farming and agriculture around ten thousand years ago in the Near East and spread to the Baltic proximally five thousand years ago. Their diet was then shifted from animal rich, including fish, to a diet with mostly grain and vegetables. Therefore, the Europeans dietary intake of vitamin D was reduced, the photoproduction of vitamin D in their skin was not sufficient because of dark skin, and they developed their characteristic European pale skin. 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