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Evolutionary, Biologic, and Social Aspects of Skin Color
Dermatol Clin 25 (2007) 293–302
Evolutionary, Biologic, and Social Aspects of Skin Color Wiete Westerhof, MD, PhD Color Foundation, Landsmeer, the Netherlands
The earth counts a variegated collection of people with a ranging skin color. The skin color is one of the most obvious ways in which humans differ and has been widely used in attempts to define races. The questions are how did it develop, what were the determining factors for the differences in skin color, and what is the significance of it? Hominid and human evolution To answer these questions, one must go back in time. The earth is about 4.6 billion years old. The first 600 million years were needed to cool off. Life began 4 billion years ago with unicellular organisms [1]. Primates developed only recently in the evolutionary process at the beginning of the Cenozoicum, about 65 million years ago. About 5.3 million years ago, at the end of the Tertiary in the Pliocene, the hominids descended from the apes. Many hominid species evolved during the Pliocene until 1.8 million years ago. It is generally accepted that Africa is the cradle of all hominids [2,3]. Eventually, all lines of hominids became extinct. For example, Homo erectus lived in Asia from 800,000 to 20,000 years ago and Homo neanderthalensis in Europe from 400,000 to 30,000 years ago. Of all living apes, the chimpanzee is genetically closest to humans, with a DNA sequence homology of 98%. Although they have a black fur, their underlying skin is white. Initially in young chimpanzees, the hands and face are also white (Fig. 1). At a later age this skin becomes pigmented. This observation is why it is assumed that the first hominids, who were thought to be hairy, also had white
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skin [4]. One characteristic of hominids is their bipedalism (walking upright) [5], which enabled them to become more active. Excavations of bones belonging to Homo australopithecus garhi (Ethiopia), which lived about 2.5 million years ago, indicate their use of stone attributes like arrow heads. These hominids left the forest and started to hunt on the open plains of the savannas. They became so-called ‘‘hunters and gatherers.’’ In their new environments, the body was exposed to extreme heat from the sun and also became overheated as a result of increased exercise. This stress required adaptation that occurred by means of hair loss and an increase in the number of sweat glands. Vaporization of water gives rise to cooling. The nude skins of the hominids were also exposed to intense UV irradiation of the sun. It is assumed that the skin of hominids was initially white, but evolutionary adaptation resulted in stimulation of the pigment cells in the skin to form more pigment, resulting in a better protection against UV radiation [6]. The first modern man (Homo sapiens), who resembles the present day human, descended from tribes of hominids who lived some 200,000 years ago in southern Africa. This period is called the Pleistocene (1.2 million to 10,000 years ago). The modern man who originally came from Africa ousted all hominids and all archaic predecessors of Homo sapiens in every continent as determined from excavations at different places in the world. It is quite likely that early modern man inherited its features from the early hominids from the southern part of Africa. It is assumed that early modern man (like their present day descendants such as the San People and Khoisan) in the forested shelters of southern Africa initially had a light brown skin (Fig. 2A). Consequently, it is suggested that the skin
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moderate climates) initially also had a brown skin; however, they had to adapt to new climatologic and environmental circumstances and developed a lighter skin color. In more recent migrations, such as of the Eskimos (Inuits), the time must have been too short to lead to an adaptation. Alternatively, the necessity to develop a lighter skin color was not there because of other adaptational processes which came instead. Evolutionary cofounding factors in the development of skin color
Fig. 1. Skin color of chimpanzees. (Courtesy of Jan Vermeer, Burgers’ Zoo, Arnhem, the Netherlands.)
pigmentation of these people developed in two directions. The early modern man who migrated to the open planes of equatorial Africa (Niger, Sudan) (Fig. 2B) where UV radiation is most intense developed a deep black skin. The people who moved to northern Africa (Fig. 2C) and out of Africa in the direction of Asia and Europe (the
Black hair, brown eyes, and a dark skin color must be considered the primordial state for humans before transcontinental migration. The selective pressure to retain a darkly pigmented epidermis has been proposed to include the UV light-absorbing properties of melanin, which would protect the skin from sunburn and eventual skin cancer as well as eye damage. Excessive sunburn and skin peeling would most likely limit foraging and hunting. Although skin cancer and premature blindness would be unlikely to occur during the reproductive years, this could affect the longevity of the grandmother and reduce the reproductive success of her daughters or the survival of grandchildren. It has now been recognized that protection of the sweat glands from UV damage is also necessary to ensure thermoregulation. Additionally, deficiency of folic acid is a threat to the survival of the species. This deficiency can develop as a result of photodecomposition of folate due to intense UV radiation. Low folic acid level leads to a decrease in cell division. In newborns, it
Fig. 2. (A) Khoisan woman. (Courtesy of Mike Elliot, Dundee, Scotland.) (B) Luo woman from Western Kenya. (C) Berber woman. (Courtesy of Declan McCullagh, San Francisco, California.)
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gives rise to mortal congenital defects like spina bifida [7] and in adult men to a decrease in fertility as a result of a lower number of spermatozoa [8]. The presence of high levels of melanin in the skin may be involved in protection from fungal infections in steamy tropical climates, providing for an additional selection for darker pigmentation [9]. About 100,000 to 80,000 years ago, modern man moved out of Africa in the direction of the North Pole where the intensity of the sun is less, and the skin of dark people produced too little vitamin D. Additionally, the change in their diet to one consisting predominantly of grains produced by a developing agricultural society (further reducing the vitamin D intake), caused rickets, a deformation of the skeleton. In women with this disease, malformation of the pelvis could give rise to problems during delivery resulting in still birth and death of the mother. Low vitamin D levels also lead to disturbances of the immune system resulting in more infections and higher mortality at birth [4,10]. These effects would result in selection for a lighter skin color to increase the UVinduced synthesis of this vitamin in the skin, especially during pregnancy and lactation. Other selective pressures for a lower epidermal melanin content may have included the susceptibility to frost bite. Eskimos have a brown skin which was often fully covered by their clothing. They could circumvent the problem of hypovitaminosis D by the intake of food rich in vitamin D. People with a light brown skin, such as the Tuaregs from North Africa or inhabitants of the Arab Peninsula, can develop vitamin D deficiency even in tropical areas when they cover their entire body, hands, and face. People with a heavily pigmented skin who live in moderate zones can also easily develop vitamin D deficiency. This event can be prevented by vitamin D substitution in the diet or pills. Sexual selection may also have had a role [11–13]. Available evidence suggests that in each society a lighter-than-average skin color is preferred in a sexual partner.
80,000 years ago, caused the coverage with ice of large parts of the Northern Hemisphere as well as the most southern part of the Southern Hemisphere. At the same time, extreme drought developed in southern Africa. This event forced the people living there to move to more fertile areas. Because the ice was stacked up in great heaps on the land, the sea level was about 80 m lower than nowadays, which caused the Continental plateaus to rise above the sea level. At that time (from 80,000 to 100,000 years ago), people could walk overland via the Arabian peninsula, India, Indonesia, and New Guinea except through narrow straits to reach Australia 40,000 to 50,000 years ago. Based on the similarity of archeological finds (utensils, cave paintings made by Cro–Magnons) from sites in Spain and France and places in north, west, and south Africa [16] and the evidence derived from the Berber-Ibero-Basque language complex [17], Europe was most probably invaded from north Africa about 35,000 to 40,000 years ago, with the invaders defeating the Neanderthalers. The New World became populated relatively late. During the last ice age, about 20,000 to 15,000 years ago, the Bering Strait fell dry. This event enabled the Eskimos (Inuits) to make the crossing from Siberia to Alaska. In only a few thousand years the descendents of these Eskimos, which are the present day Indians, spread out over North and South America. The original native primitive inhabitants of China were black Africans who arrived there about 80,000 to 100,000 years ago and who dominated the region until a few thousand years ago when the Mongol advance into that region began. Indeed, archeology and genetic studies confirm that China’s first two dynasties, the Xia and the Chang/Chang, were largely constituted of black people with negroid characteristics [18]. In most of these areas, the original negroid people were replaced (through assimilation or defeat) by later arriving tribes.
Early migrations of people
Present situation
Based on skeletal findings, genetic research theories have been developed to explain the migration of modern man out of Africadthe ‘‘out of Africa’’ theory [14,15]. In Fig. 3 the migration of people is indicated by arrows. The related times are estimations. There could have been more than one migration wave. The fore last ice age, about
Are we still able to see traces of ancient migrations out of Africa? Anthropology teaches us that people with negroid features, the so-called ‘‘Negritos,’’ are living in the Andaman Islands, in Burma, Thailand, Malaysia, central Borneo, the Philippines, and the islands of Melanesia, that is, Papua/New Guinea, the Bismarck Archipelago,
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Fig. 3. Early migration of people out of Africa.
the Solomon Islands, Vanuatu (New Hebrides), New Caledonia, and Australia (Fig. 4) [19]. The Andaman Islands are a fascinating group of islands in front of the coast of Thailand. They are inhabited by Negritos, who were until 1920 never in contact with the surrounding peoples and continued living in the Stone Age. Although close to the mainland of South East Asia, the islands were not colonized until the beginning of 1800 by the British, who established a penal settlement. They belong now to India. The various tribes settled here possibly 80,000 years ago (Fig. 5). They appear to have external features and genetic traits in common with other Paleolithic people, namely, the pygmies [20,21]. Since 1920, migration from India, especially of convicts, to the Great Andaman Island has threatened the original tribes with extinction [22]. Of the Great Andamese tribe, there are about 50 persons left. Of the Jarawas, only 300 people are alive. The Onge tribe counts 45 people. Nobody knows exactly how many people are living on North Sentinel Island. It is extraordinary that they have been successful in banning other people from their territory and have continued to live undisturbed on an island that is not more than 65 km2. An estimated hundred members
belonging to the Sentinelese tribe live in harmony with nature. There is no overpopulation and no deforestation on their relatively small island. They have not fished their surrounding sea empty. They have not killed each other, neither have they conquered or suppressed others on neighboring islands. This situation has existed for about 80,000 years. These people are considered primitive because they still live in the Stone Age; however, many people today would like to know more about their wisdom and their vision on life. Genes and gene products in human pigmentation The biochemical pathways underlying melanin synthesis have been elucidated with the help of mouse coat color mutations. Almost 100 genes have been identified that affect mouse coat color. More than 40 of the genes underlying these traits have been cloned [23], and many of them have corresponding human phenotypes. In nearly all of these genes, a mutation leads to a multisystem defect that includes a pigmentation abnormality, such as the different forms of oculocutaneous albinism and Waardenburg syndrome type 1. Only a minority of these gene mutations are known to affect ‘‘normal’’ variation in human skin
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Fig. 4. Areas where the direct descendants of the first migration from Africa still live. (Courtesy of W. Westerhof, MD, PhD, Amsterdam, the Netherlands.)
color. Chief among the genes known to affect normal variation is the melanocortin 1 receptor (MC1R) gene. Mutations in this gene affect not only human pigmentation but also that of wild animals, mice, and many domestic animals, including cattle, horses, sheep, pigs, dogs, and chickens [24]. The gene product lies in the cell membrane of the melanocyte and is the receptor for a-melanocyte stimulating hormone. MC1R encodes a 317–amino acid G-coupled receptor that controls the relative amounts of the two major melanin classes, eumelanin and pheomelanin. Receptor stimulation leads to an elevation of the intracellular concentration of cyclic AMP (cAMP), a signaling molecule, inducing changes in protein activity through phosphorylation, altered gene expression, and, ultimately, the generation of a mature eumelanogenic melanosome. In the absence of a signal via MC1R, the eumelanosome cannot form, and, instead, the immature pheomelanosome persists, with a consequent phenotype of reduced pigmentation. Most persons with red hair are homozygous for alleles of the MC1R gene that show varying
degrees of diminished function. More than 65 human MC1R alleles with nonsynonymous changes have been identified, and current evidence suggests that many of them vary in their physiologic activity such that a graded series of responses can be achieved on the basis of (1) dosage effects (of one or two alleles) and (2) individual differences in the pharmacologic profile in response to ligand. A single locus identified within a mendelian framework can contribute significantly to human pigmentary variation [25]. Three of these loci have been shown to be associated with red hair, fair skin, and freckling [26–28], and a fourth has been associated with fair skin and blonde hair [28]. These variants map to the intracellular part of the protein, and the first three have been shown to reduce the ability of MC1R to stimulate increases in the concentration of the intracellular messenger molecule cAMP. The mode of inheritance of red hair has been thought to be autosomal recessive, and the inheritance of the variant alleles is broadly consistent with this [29]. There is a general association of the number of MC1R variants carried in skin color as well as
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Fig. 5. Nigrito people. (A) Jarawas from South Andaman. (Courtesy of Deepak Johnson, Port Blair, Andaman Islands.) (B) Mani from (Malay Peninsula) South Thailand. (Courtesy of Alice Everett, the Andaman Association, Switzerland.) (C) Aeta from Luzon, Philippines. (Courtesy of Wiete Westerhof, the Netherlands.)
hair color; however, sharing of identical MC1R haplotypes among people with very different pigmentation phenotypes indicates that other loci must be involved [30,31]. Apart from MC1R, the identification of genes influencing normal pigmentation without accompanying pathologic features has been difficult. The P protein is involved in eumelanogenesis through its role in reduction of acidity within the melanosome. A study of a Tibetan population [32] showed no association between skin color and two single nucleotide polymorphisms in the P gene or three single nucleotide polymorphisms in the MC1R gene. Nevertheless, an epistatic model allowing for interaction between genes did show a statistically significant effect upon skin color of the two genes acting in concert. The author and his colleagues studied a Hindustani family who demonstrated in three generations an autosomal dominant neurocutaneous syndrome known as the Westerhof syndrome. Besides disturbances of the central nervous system, the patients also exhibited light and dark macules on their bodies. Electron microscopic research showed that
the dark macules had typical characteristics of negroid skin, whereas the light macules showed signs of caucasoid skin. Together with their own normal Asiatic skin, these patients had three main skin types represented in a single person [33]. This finding might indicate that only variations of a single gene are responsible for the differences in skin color. Unfortunately, in 1978 we were unable to carry out molecular biology. Genetic proof of the out of Africa theory Some scientists support a multiregional hypothesis of the origin of mankind; however, most researchers are in favor of the out of Africa theory [34,35]. In people who have been living for a long duration in an isolated geographic area, genetic studies can demonstrate distinctions between various groups, suggesting that living in isolation can lead to the development of unique genetic properties. Many genetic studies have been conducted in people with varying skin colors. Some studies have made use of DNA of the Y chromosome, whereas others have used mitochondrial
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DNA. The Y chromosome, which occurs only in males, gives a perspective of the inheritance in the masculine lineage. The mitochondrial DNA is inherited from the mother and allows studying genetic properties in the female lineage. By using the investigations of scientists such as CavalliSforza and Wells, the migration of the people throughout the world can be reconstructed. These researchers had the brilliant idea that our DNA carries the history of mankind. The puzzle is still being sorted out in greater detail. At this moment, it is clear that a man from Uzbekistan is a descendent of an African who migrated there about 100,000 to 80,000 years ago. He bears characteristics of all the populations living in Eurasia (bordered by the Ural and the Himalayas) [36]; therefore, one of his forefathers must have been the person from whom all people from Europe and Asia descend. It is said that if Africa is the cradle off mankind, then Asia is the maternity room. It is assumed that early modern man migrated out of Africa in small numbers (a few thousands) as gatherers and hunters [37]. If selection has been acting on human pigmentation genes, the signal of that selection may be discernible in patterns of haplotype diversity. The only gene that has been studied from this perspective is MC1R. A study of MC1R variation based on resequencing of the gene revealed a striking difference in the distribution of haplotypes between African and Eurasian populations [30]. There were only five African haplotypes in the sample and a complete absence of nonsynonymous base substitutions. In Eurasia, by contrast, there were 13 haplotypes, with 10 nonsynonymous mutations and 3 synonymous ones [38]. There also appeared to be some MClR polymorphic alleles of higher frequency in the Asian community. There must have been disparate selective pressures acting upon human pigmentation during migrations into Europe and Asia with the associated climatic changes, and a later adaptation to an agrarian economy must also be considered. With lower incident UV light, it is possible that the strong positive selection for darker complexions in Africa was reduced, allowing for lighter skin color in Northern European populations, with Asia perhaps somewhere in the middle. More likely was a reciprocal positive selection for lower levels of epidermal melanin in Europeans acting through the evolution of multiple lower strength MC1R alleles. In addition, there are major differences in the allele strength or frequency of the two genes for oculocutaneous albinism in human populations, with weaker OCA2
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alleles associated with the skin lightening and blue eyes seen in Europeans and strong OCA2 alleles responsible for brown eyes and darker skin. The finding of an exclusive Leu374Phe amino acid change within the OCA4 allele of most Europeans must also be considered functionally significant and indicative of an early selective pressure for depigmentation. Comparing these findings with the known number of synonymous and nonsynonymous changes between the human consensus sequence and the chimpanzee sequence shows that the high degree of amino acid sequence conservation in Africa is highly unlikely to have arisen by chance. It probably reflects a strong functional constraint in Africa, where any diversion from eumelanin production is strongly deleterious. Despite the vitamin D hypothesis discussed earlier, which could provide a mechanism for selection, the pattern in Eurasia seems compatible with low selective constraint rather than selective enhancement of diversity. In contrast to the extraordinary conservation of the wild-type MC1R genotype in Africa, indicative of a strong selective pressure to retain dark skin, there is extensive allelic polymorphism within this locus in light-skinned European populations, with over 30 MC1R alleles reported thus far [38]. Skin color and society Does race exist? After many migrations during 200,000 years, people have spread out all over the world and mixed with each other; therefore, clear distinctions cannot be made. This observation is supported by genetic research. Formerly much harm was done by people like Linnaeus to the image of people with dark skin. In his passion to classify everything, he grouped the Hottentot people (Khoisan and San) together with the monsters (Fig. 6). The church, which suppressed free thinking and science, defended the inferiority of people with dark skin with quotations from the Bible. These attitudes were responsible for crimes against humanity such as the slave trade and slavery during more than three centuries. It is ironic to realize that, today, scientists are of the opinion that modern man descended from the Hottentots. A recent study demonstrates the need to be cautious when using pigmentation as a proxy for genetic ancestry or race [39]. Admixture and admixture mapping is also a key factor to elucidate the genetic basis of skin pigmentation variation in human populations [40]. Objective measures of
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Fig. 6. Classification of primates by Linnaeus.
pigmentation fail to correlate with race [41]. The conclusion is that skin color is not the same thing as race [42]. Genetic studies have demonstrated that people of African American descent frequently have a closer relationship to the population of northern Europe than to an ethnic African [43]. Evolutionary effects on skin color might have evolved over thousands of years in static isolated populations. The intermingling of people today, with the quick means of transportation, clearly abolishes the past influences of environment on genetic drifts. Also in daily life we know that a black phenotype can change through intermarriage in a few generations into the other extreme. Conversely, a white skin can dissolve in the gene pool of a black community. It is interesting to speculate about the role of skin color in ancient societies. The first modern man had black skin and black curly hair. He was the first to populate Africa and Asia. Later migrations to China of people with light skin were most likely from central Asia or the Middle East, thereby mixing with the residing black population or possibly ousting them. Because of ice ages and other untoward environmental circumstances, Europe was populated much later. In isolated geographic regions, people with a lighter skin evolved for reasons explained earlier. The population of northern Europe may have descended from migrated brown-skinned northern
Africans, who adapted by a mutation of the MC1R gene to their new environment with a more moderate climate (Cro–Magnons 40,000 years ago). It is clear from the present day situation that the black population, who remained gatherers and hunters, was almost everywhere overruled by the newcomers. Only in remote or inaccessible areas were they able to survive and maintain their customs and beliefs until today. During the last 100,000 years, countless migrations took place backward and forward over the entire globe. It may soon become possible using contemporary molecular biology techniques to trace back these routes of migration, which will deepen the knowledge of our past. One classic example of white-skinned domination is known from recent history [44]. About 3700 years ago, the light-skinned Aryans moved from the borders of the Caspian Sea in the Caucasus to Northern India. They defeated the residing people, who had a black skin and curly hair, the Dravidians [45]. The Aryans established the Vedic civilization, which lead to the foundation of Hinduism [46,47]. The oldest literature in India, the Rig Veda, contains the religious praise poems. The later Vedic period is dominated by the Brahmans, or priestly book, which was composed sometime between 1000 and 850 BC. The Rig Vedic peoples originally had only two social classes, nobles and commoners. Eventually, they added a third class, Dasas or ‘‘darks.’’ These people were, we presume, the darker-skinned people they had conquered. By the end of the Rig Vedic period, social class had settled into four rigid castes, the caturvarnas or ‘‘four colors.’’ In Sanskrit the word ‘‘varna’’ has two meaningsdcaste as well as color. At the top of the caturvarnas were the priests, or Brahmans, with the lightest skins. Below the priests were the warriors or nobles (Kshatriya), the craftspeople and merchants (Vaishya), and the servants (Shudra), who made up the bulk of society. These economic classes were legitimated by an elaborate religious system and were eventually subdivided into a huge number of economic subclasses which we call ‘‘castes.’’ Social class by the end of the Rig Vedic period became completely inflexible; there was no such thing as social mobility. Not belonging to any caste are the untouchables (Dalit), who have the darkest skin color. The further remote from the cultural heart of India (Northern India), the darker the skin color of the people. The Tamils have a nearly black skin. There are still people with black curly hair amongst them. They belong
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to the Dravidian minority. Here religion was the driving force for over 3700 years to support discrimination based on skin color. More recent examples are the Apartheid in South Africa and the racial segregation (Color bar) in the United States. Currently, racism to a varying degree lingers on almost everywhere in the world, with or without governmental or religious inspirations. As a dermatologist, I have been confronted with dramatic skin problems due to the use of skin-lightening agents. The Netherlands has a multi-ethnic society. The most frequent users of these skin-lightening agents are people of African descent (recent immigrants from Ghana and Nigeria) and people from Surinam, especially of Hindustani origin [48]. The use of skin-lightening agents is surrounded by taboos; therefore, it is very difficult to get an idea about the extent of the misuse and the side effects. Anthropological investigations have shown that people with a darker skin belonging to the lower classes reach for these agents to make them resemble the dominant class so that the chances for a better marriage and labor increase [49–51]. Although people have been mixing with each other since the beginning of mankind, it is an amazing to see how the lines between the different ethnic groups can still be drawn. In many respects this diversity can be seen as an advantage. The existence of colorful people means diverse and interesting cultures. It only requires respect for each other’s culture. Looking at the news from the media we see how difficult this is nowadays. It is apparently impossible to tolerate so many beliefs, opinions, and habits. Harlon L. Dalton writes about this touchy matter [52], ‘‘We people, white or black, must learn to speak openly about our racial beliefs to overcome fear and mistrust. This could help to remove the terrible division between people with various skin shades.’’ A possible solution might be to stimulate migration and assimilation. In a few hundred years we would all have a brown skin. Then only the real qualities of a man would matter!
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consequences of polymorphic variation. Genetica 2001;277:49–62. Parra EJ, Kittles RA, Shriver MD. Implications of correlations between skin color and genetic ancestry for biomedical research. Nat Genet 2004;36(Suppl 11):S54–60. Hoggart CJ, Shriver MD, Kittles RA, et al. Design and analysis of admixture mapping studies. Am J Hum Genet 2004;74:965–78. Chan JL, Ehrlich A, Lawrence RC, et al. Assessing the role of race in quantitative measures of skin pigmentation and clinical assessments of photosensitivity. J Am Acad Dermatol 2005;52:609–15. Silver SE. Skin color is not the same thing as race. Arch Dermatol 2004;140:361. Adelman L. Racedthe power of an illusion. Available at: http://www.newsreel.org/guides/race/what diff.htm. Accessed June 7, 2007. Wilson J. Indian Caste, vols. 1 & 2. Elibron Classics. Boston: Adamant Media Corporation; 2001 (facsimile of 1st edition by Times of India; William Blackwood & Sons, Bombay; Edinburgh and London. 1877). Thanseem I, Thangaraj K, Chaubey G, et al. Genetic affinities among the lower castes and tribal groups of India: inference from Y chromosome and mitochondrial DNA. BMC Genet 2006;7:42. Kamat V. The caste system: introduction, myths, and reality. Available at: http://www.kamat.com/ indica/caste/. Accessed June 7, 2007. Available at: http://experts.about.com/e/c/ca/Caste. htm. Accessed June 7, 2007. Menke HE, Gomes PD, Lamur H, et al. Een tintje lichter. Nederland: Medisch Contact 2001;56:89–91. Westerhof W. A few more grains of melanin. Int J Dermatol 1997;36:573–4. Gomes PD, Westerhof W. Het gebruik van chemische huidbleekmiddelen onder Chanese vrouwen in Amsterdam-Zuidoost. Tijdschrift voor Genderstudies 2001;4:20–33. Gomes PD, Westerhof W. Het gebruik van chemische huidbleekmiddelen onder Indiase vrouwen in Bangalore. Medische Antropologie 2002; 14:353–74. Dalton HL. Racial healing: confronting the fear between blacks and whites. New York: Doubleday; 1995.
Evolutionary, Biologic, and Social Aspects of Skin Color Wiete Westerhof, MD, PhD Color Foundation, Landsmeer, the Netherlands
The earth counts a variegated collection of people with a ranging skin color. The skin color is one of the most obvious ways in which humans differ and has been widely used in attempts to define races. The questions are how did it develop, what were the determining factors for the differences in skin color, and what is the significance of it? Hominid and human evolution To answer these questions, one must go back in time. The earth is about 4.6 billion years old. The first 600 million years were needed to cool off. Life began 4 billion years ago with unicellular organisms [1]. Primates developed only recently in the evolutionary process at the beginning of the Cenozoicum, about 65 million years ago. About 5.3 million years ago, at the end of the Tertiary in the Pliocene, the hominids descended from the apes. Many hominid species evolved during the Pliocene until 1.8 million years ago. It is generally accepted that Africa is the cradle of all hominids [2,3]. Eventually, all lines of hominids became extinct. For example, Homo erectus lived in Asia from 800,000 to 20,000 years ago and Homo neanderthalensis in Europe from 400,000 to 30,000 years ago. Of all living apes, the chimpanzee is genetically closest to humans, with a DNA sequence homology of 98%. Although they have a black fur, their underlying skin is white. Initially in young chimpanzees, the hands and face are also white (Fig. 1). At a later age this skin becomes pigmented. This observation is why it is assumed that the first hominids, who were thought to be hairy, also had white
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skin [4]. One characteristic of hominids is their bipedalism (walking upright) [5], which enabled them to become more active. Excavations of bones belonging to Homo australopithecus garhi (Ethiopia), which lived about 2.5 million years ago, indicate their use of stone attributes like arrow heads. These hominids left the forest and started to hunt on the open plains of the savannas. They became so-called ‘‘hunters and gatherers.’’ In their new environments, the body was exposed to extreme heat from the sun and also became overheated as a result of increased exercise. This stress required adaptation that occurred by means of hair loss and an increase in the number of sweat glands. Vaporization of water gives rise to cooling. The nude skins of the hominids were also exposed to intense UV irradiation of the sun. It is assumed that the skin of hominids was initially white, but evolutionary adaptation resulted in stimulation of the pigment cells in the skin to form more pigment, resulting in a better protection against UV radiation [6]. The first modern man (Homo sapiens), who resembles the present day human, descended from tribes of hominids who lived some 200,000 years ago in southern Africa. This period is called the Pleistocene (1.2 million to 10,000 years ago). The modern man who originally came from Africa ousted all hominids and all archaic predecessors of Homo sapiens in every continent as determined from excavations at different places in the world. It is quite likely that early modern man inherited its features from the early hominids from the southern part of Africa. It is assumed that early modern man (like their present day descendants such as the San People and Khoisan) in the forested shelters of southern Africa initially had a light brown skin (Fig. 2A). Consequently, it is suggested that the skin
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moderate climates) initially also had a brown skin; however, they had to adapt to new climatologic and environmental circumstances and developed a lighter skin color. In more recent migrations, such as of the Eskimos (Inuits), the time must have been too short to lead to an adaptation. Alternatively, the necessity to develop a lighter skin color was not there because of other adaptational processes which came instead. Evolutionary cofounding factors in the development of skin color
Fig. 1. Skin color of chimpanzees. (Courtesy of Jan Vermeer, Burgers’ Zoo, Arnhem, the Netherlands.)
pigmentation of these people developed in two directions. The early modern man who migrated to the open planes of equatorial Africa (Niger, Sudan) (Fig. 2B) where UV radiation is most intense developed a deep black skin. The people who moved to northern Africa (Fig. 2C) and out of Africa in the direction of Asia and Europe (the
Black hair, brown eyes, and a dark skin color must be considered the primordial state for humans before transcontinental migration. The selective pressure to retain a darkly pigmented epidermis has been proposed to include the UV light-absorbing properties of melanin, which would protect the skin from sunburn and eventual skin cancer as well as eye damage. Excessive sunburn and skin peeling would most likely limit foraging and hunting. Although skin cancer and premature blindness would be unlikely to occur during the reproductive years, this could affect the longevity of the grandmother and reduce the reproductive success of her daughters or the survival of grandchildren. It has now been recognized that protection of the sweat glands from UV damage is also necessary to ensure thermoregulation. Additionally, deficiency of folic acid is a threat to the survival of the species. This deficiency can develop as a result of photodecomposition of folate due to intense UV radiation. Low folic acid level leads to a decrease in cell division. In newborns, it
Fig. 2. (A) Khoisan woman. (Courtesy of Mike Elliot, Dundee, Scotland.) (B) Luo woman from Western Kenya. (C) Berber woman. (Courtesy of Declan McCullagh, San Francisco, California.)
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gives rise to mortal congenital defects like spina bifida [7] and in adult men to a decrease in fertility as a result of a lower number of spermatozoa [8]. The presence of high levels of melanin in the skin may be involved in protection from fungal infections in steamy tropical climates, providing for an additional selection for darker pigmentation [9]. About 100,000 to 80,000 years ago, modern man moved out of Africa in the direction of the North Pole where the intensity of the sun is less, and the skin of dark people produced too little vitamin D. Additionally, the change in their diet to one consisting predominantly of grains produced by a developing agricultural society (further reducing the vitamin D intake), caused rickets, a deformation of the skeleton. In women with this disease, malformation of the pelvis could give rise to problems during delivery resulting in still birth and death of the mother. Low vitamin D levels also lead to disturbances of the immune system resulting in more infections and higher mortality at birth [4,10]. These effects would result in selection for a lighter skin color to increase the UVinduced synthesis of this vitamin in the skin, especially during pregnancy and lactation. Other selective pressures for a lower epidermal melanin content may have included the susceptibility to frost bite. Eskimos have a brown skin which was often fully covered by their clothing. They could circumvent the problem of hypovitaminosis D by the intake of food rich in vitamin D. People with a light brown skin, such as the Tuaregs from North Africa or inhabitants of the Arab Peninsula, can develop vitamin D deficiency even in tropical areas when they cover their entire body, hands, and face. People with a heavily pigmented skin who live in moderate zones can also easily develop vitamin D deficiency. This event can be prevented by vitamin D substitution in the diet or pills. Sexual selection may also have had a role [11–13]. Available evidence suggests that in each society a lighter-than-average skin color is preferred in a sexual partner.
80,000 years ago, caused the coverage with ice of large parts of the Northern Hemisphere as well as the most southern part of the Southern Hemisphere. At the same time, extreme drought developed in southern Africa. This event forced the people living there to move to more fertile areas. Because the ice was stacked up in great heaps on the land, the sea level was about 80 m lower than nowadays, which caused the Continental plateaus to rise above the sea level. At that time (from 80,000 to 100,000 years ago), people could walk overland via the Arabian peninsula, India, Indonesia, and New Guinea except through narrow straits to reach Australia 40,000 to 50,000 years ago. Based on the similarity of archeological finds (utensils, cave paintings made by Cro–Magnons) from sites in Spain and France and places in north, west, and south Africa [16] and the evidence derived from the Berber-Ibero-Basque language complex [17], Europe was most probably invaded from north Africa about 35,000 to 40,000 years ago, with the invaders defeating the Neanderthalers. The New World became populated relatively late. During the last ice age, about 20,000 to 15,000 years ago, the Bering Strait fell dry. This event enabled the Eskimos (Inuits) to make the crossing from Siberia to Alaska. In only a few thousand years the descendents of these Eskimos, which are the present day Indians, spread out over North and South America. The original native primitive inhabitants of China were black Africans who arrived there about 80,000 to 100,000 years ago and who dominated the region until a few thousand years ago when the Mongol advance into that region began. Indeed, archeology and genetic studies confirm that China’s first two dynasties, the Xia and the Chang/Chang, were largely constituted of black people with negroid characteristics [18]. In most of these areas, the original negroid people were replaced (through assimilation or defeat) by later arriving tribes.
Early migrations of people
Present situation
Based on skeletal findings, genetic research theories have been developed to explain the migration of modern man out of Africadthe ‘‘out of Africa’’ theory [14,15]. In Fig. 3 the migration of people is indicated by arrows. The related times are estimations. There could have been more than one migration wave. The fore last ice age, about
Are we still able to see traces of ancient migrations out of Africa? Anthropology teaches us that people with negroid features, the so-called ‘‘Negritos,’’ are living in the Andaman Islands, in Burma, Thailand, Malaysia, central Borneo, the Philippines, and the islands of Melanesia, that is, Papua/New Guinea, the Bismarck Archipelago,
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Fig. 3. Early migration of people out of Africa.
the Solomon Islands, Vanuatu (New Hebrides), New Caledonia, and Australia (Fig. 4) [19]. The Andaman Islands are a fascinating group of islands in front of the coast of Thailand. They are inhabited by Negritos, who were until 1920 never in contact with the surrounding peoples and continued living in the Stone Age. Although close to the mainland of South East Asia, the islands were not colonized until the beginning of 1800 by the British, who established a penal settlement. They belong now to India. The various tribes settled here possibly 80,000 years ago (Fig. 5). They appear to have external features and genetic traits in common with other Paleolithic people, namely, the pygmies [20,21]. Since 1920, migration from India, especially of convicts, to the Great Andaman Island has threatened the original tribes with extinction [22]. Of the Great Andamese tribe, there are about 50 persons left. Of the Jarawas, only 300 people are alive. The Onge tribe counts 45 people. Nobody knows exactly how many people are living on North Sentinel Island. It is extraordinary that they have been successful in banning other people from their territory and have continued to live undisturbed on an island that is not more than 65 km2. An estimated hundred members
belonging to the Sentinelese tribe live in harmony with nature. There is no overpopulation and no deforestation on their relatively small island. They have not fished their surrounding sea empty. They have not killed each other, neither have they conquered or suppressed others on neighboring islands. This situation has existed for about 80,000 years. These people are considered primitive because they still live in the Stone Age; however, many people today would like to know more about their wisdom and their vision on life. Genes and gene products in human pigmentation The biochemical pathways underlying melanin synthesis have been elucidated with the help of mouse coat color mutations. Almost 100 genes have been identified that affect mouse coat color. More than 40 of the genes underlying these traits have been cloned [23], and many of them have corresponding human phenotypes. In nearly all of these genes, a mutation leads to a multisystem defect that includes a pigmentation abnormality, such as the different forms of oculocutaneous albinism and Waardenburg syndrome type 1. Only a minority of these gene mutations are known to affect ‘‘normal’’ variation in human skin
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Fig. 4. Areas where the direct descendants of the first migration from Africa still live. (Courtesy of W. Westerhof, MD, PhD, Amsterdam, the Netherlands.)
color. Chief among the genes known to affect normal variation is the melanocortin 1 receptor (MC1R) gene. Mutations in this gene affect not only human pigmentation but also that of wild animals, mice, and many domestic animals, including cattle, horses, sheep, pigs, dogs, and chickens [24]. The gene product lies in the cell membrane of the melanocyte and is the receptor for a-melanocyte stimulating hormone. MC1R encodes a 317–amino acid G-coupled receptor that controls the relative amounts of the two major melanin classes, eumelanin and pheomelanin. Receptor stimulation leads to an elevation of the intracellular concentration of cyclic AMP (cAMP), a signaling molecule, inducing changes in protein activity through phosphorylation, altered gene expression, and, ultimately, the generation of a mature eumelanogenic melanosome. In the absence of a signal via MC1R, the eumelanosome cannot form, and, instead, the immature pheomelanosome persists, with a consequent phenotype of reduced pigmentation. Most persons with red hair are homozygous for alleles of the MC1R gene that show varying
degrees of diminished function. More than 65 human MC1R alleles with nonsynonymous changes have been identified, and current evidence suggests that many of them vary in their physiologic activity such that a graded series of responses can be achieved on the basis of (1) dosage effects (of one or two alleles) and (2) individual differences in the pharmacologic profile in response to ligand. A single locus identified within a mendelian framework can contribute significantly to human pigmentary variation [25]. Three of these loci have been shown to be associated with red hair, fair skin, and freckling [26–28], and a fourth has been associated with fair skin and blonde hair [28]. These variants map to the intracellular part of the protein, and the first three have been shown to reduce the ability of MC1R to stimulate increases in the concentration of the intracellular messenger molecule cAMP. The mode of inheritance of red hair has been thought to be autosomal recessive, and the inheritance of the variant alleles is broadly consistent with this [29]. There is a general association of the number of MC1R variants carried in skin color as well as
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Fig. 5. Nigrito people. (A) Jarawas from South Andaman. (Courtesy of Deepak Johnson, Port Blair, Andaman Islands.) (B) Mani from (Malay Peninsula) South Thailand. (Courtesy of Alice Everett, the Andaman Association, Switzerland.) (C) Aeta from Luzon, Philippines. (Courtesy of Wiete Westerhof, the Netherlands.)
hair color; however, sharing of identical MC1R haplotypes among people with very different pigmentation phenotypes indicates that other loci must be involved [30,31]. Apart from MC1R, the identification of genes influencing normal pigmentation without accompanying pathologic features has been difficult. The P protein is involved in eumelanogenesis through its role in reduction of acidity within the melanosome. A study of a Tibetan population [32] showed no association between skin color and two single nucleotide polymorphisms in the P gene or three single nucleotide polymorphisms in the MC1R gene. Nevertheless, an epistatic model allowing for interaction between genes did show a statistically significant effect upon skin color of the two genes acting in concert. The author and his colleagues studied a Hindustani family who demonstrated in three generations an autosomal dominant neurocutaneous syndrome known as the Westerhof syndrome. Besides disturbances of the central nervous system, the patients also exhibited light and dark macules on their bodies. Electron microscopic research showed that
the dark macules had typical characteristics of negroid skin, whereas the light macules showed signs of caucasoid skin. Together with their own normal Asiatic skin, these patients had three main skin types represented in a single person [33]. This finding might indicate that only variations of a single gene are responsible for the differences in skin color. Unfortunately, in 1978 we were unable to carry out molecular biology. Genetic proof of the out of Africa theory Some scientists support a multiregional hypothesis of the origin of mankind; however, most researchers are in favor of the out of Africa theory [34,35]. In people who have been living for a long duration in an isolated geographic area, genetic studies can demonstrate distinctions between various groups, suggesting that living in isolation can lead to the development of unique genetic properties. Many genetic studies have been conducted in people with varying skin colors. Some studies have made use of DNA of the Y chromosome, whereas others have used mitochondrial
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DNA. The Y chromosome, which occurs only in males, gives a perspective of the inheritance in the masculine lineage. The mitochondrial DNA is inherited from the mother and allows studying genetic properties in the female lineage. By using the investigations of scientists such as CavalliSforza and Wells, the migration of the people throughout the world can be reconstructed. These researchers had the brilliant idea that our DNA carries the history of mankind. The puzzle is still being sorted out in greater detail. At this moment, it is clear that a man from Uzbekistan is a descendent of an African who migrated there about 100,000 to 80,000 years ago. He bears characteristics of all the populations living in Eurasia (bordered by the Ural and the Himalayas) [36]; therefore, one of his forefathers must have been the person from whom all people from Europe and Asia descend. It is said that if Africa is the cradle off mankind, then Asia is the maternity room. It is assumed that early modern man migrated out of Africa in small numbers (a few thousands) as gatherers and hunters [37]. If selection has been acting on human pigmentation genes, the signal of that selection may be discernible in patterns of haplotype diversity. The only gene that has been studied from this perspective is MC1R. A study of MC1R variation based on resequencing of the gene revealed a striking difference in the distribution of haplotypes between African and Eurasian populations [30]. There were only five African haplotypes in the sample and a complete absence of nonsynonymous base substitutions. In Eurasia, by contrast, there were 13 haplotypes, with 10 nonsynonymous mutations and 3 synonymous ones [38]. There also appeared to be some MClR polymorphic alleles of higher frequency in the Asian community. There must have been disparate selective pressures acting upon human pigmentation during migrations into Europe and Asia with the associated climatic changes, and a later adaptation to an agrarian economy must also be considered. With lower incident UV light, it is possible that the strong positive selection for darker complexions in Africa was reduced, allowing for lighter skin color in Northern European populations, with Asia perhaps somewhere in the middle. More likely was a reciprocal positive selection for lower levels of epidermal melanin in Europeans acting through the evolution of multiple lower strength MC1R alleles. In addition, there are major differences in the allele strength or frequency of the two genes for oculocutaneous albinism in human populations, with weaker OCA2
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alleles associated with the skin lightening and blue eyes seen in Europeans and strong OCA2 alleles responsible for brown eyes and darker skin. The finding of an exclusive Leu374Phe amino acid change within the OCA4 allele of most Europeans must also be considered functionally significant and indicative of an early selective pressure for depigmentation. Comparing these findings with the known number of synonymous and nonsynonymous changes between the human consensus sequence and the chimpanzee sequence shows that the high degree of amino acid sequence conservation in Africa is highly unlikely to have arisen by chance. It probably reflects a strong functional constraint in Africa, where any diversion from eumelanin production is strongly deleterious. Despite the vitamin D hypothesis discussed earlier, which could provide a mechanism for selection, the pattern in Eurasia seems compatible with low selective constraint rather than selective enhancement of diversity. In contrast to the extraordinary conservation of the wild-type MC1R genotype in Africa, indicative of a strong selective pressure to retain dark skin, there is extensive allelic polymorphism within this locus in light-skinned European populations, with over 30 MC1R alleles reported thus far [38]. Skin color and society Does race exist? After many migrations during 200,000 years, people have spread out all over the world and mixed with each other; therefore, clear distinctions cannot be made. This observation is supported by genetic research. Formerly much harm was done by people like Linnaeus to the image of people with dark skin. In his passion to classify everything, he grouped the Hottentot people (Khoisan and San) together with the monsters (Fig. 6). The church, which suppressed free thinking and science, defended the inferiority of people with dark skin with quotations from the Bible. These attitudes were responsible for crimes against humanity such as the slave trade and slavery during more than three centuries. It is ironic to realize that, today, scientists are of the opinion that modern man descended from the Hottentots. A recent study demonstrates the need to be cautious when using pigmentation as a proxy for genetic ancestry or race [39]. Admixture and admixture mapping is also a key factor to elucidate the genetic basis of skin pigmentation variation in human populations [40]. Objective measures of
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Fig. 6. Classification of primates by Linnaeus.
pigmentation fail to correlate with race [41]. The conclusion is that skin color is not the same thing as race [42]. Genetic studies have demonstrated that people of African American descent frequently have a closer relationship to the population of northern Europe than to an ethnic African [43]. Evolutionary effects on skin color might have evolved over thousands of years in static isolated populations. The intermingling of people today, with the quick means of transportation, clearly abolishes the past influences of environment on genetic drifts. Also in daily life we know that a black phenotype can change through intermarriage in a few generations into the other extreme. Conversely, a white skin can dissolve in the gene pool of a black community. It is interesting to speculate about the role of skin color in ancient societies. The first modern man had black skin and black curly hair. He was the first to populate Africa and Asia. Later migrations to China of people with light skin were most likely from central Asia or the Middle East, thereby mixing with the residing black population or possibly ousting them. Because of ice ages and other untoward environmental circumstances, Europe was populated much later. In isolated geographic regions, people with a lighter skin evolved for reasons explained earlier. The population of northern Europe may have descended from migrated brown-skinned northern
Africans, who adapted by a mutation of the MC1R gene to their new environment with a more moderate climate (Cro–Magnons 40,000 years ago). It is clear from the present day situation that the black population, who remained gatherers and hunters, was almost everywhere overruled by the newcomers. Only in remote or inaccessible areas were they able to survive and maintain their customs and beliefs until today. During the last 100,000 years, countless migrations took place backward and forward over the entire globe. It may soon become possible using contemporary molecular biology techniques to trace back these routes of migration, which will deepen the knowledge of our past. One classic example of white-skinned domination is known from recent history [44]. About 3700 years ago, the light-skinned Aryans moved from the borders of the Caspian Sea in the Caucasus to Northern India. They defeated the residing people, who had a black skin and curly hair, the Dravidians [45]. The Aryans established the Vedic civilization, which lead to the foundation of Hinduism [46,47]. The oldest literature in India, the Rig Veda, contains the religious praise poems. The later Vedic period is dominated by the Brahmans, or priestly book, which was composed sometime between 1000 and 850 BC. The Rig Vedic peoples originally had only two social classes, nobles and commoners. Eventually, they added a third class, Dasas or ‘‘darks.’’ These people were, we presume, the darker-skinned people they had conquered. By the end of the Rig Vedic period, social class had settled into four rigid castes, the caturvarnas or ‘‘four colors.’’ In Sanskrit the word ‘‘varna’’ has two meaningsdcaste as well as color. At the top of the caturvarnas were the priests, or Brahmans, with the lightest skins. Below the priests were the warriors or nobles (Kshatriya), the craftspeople and merchants (Vaishya), and the servants (Shudra), who made up the bulk of society. These economic classes were legitimated by an elaborate religious system and were eventually subdivided into a huge number of economic subclasses which we call ‘‘castes.’’ Social class by the end of the Rig Vedic period became completely inflexible; there was no such thing as social mobility. Not belonging to any caste are the untouchables (Dalit), who have the darkest skin color. The further remote from the cultural heart of India (Northern India), the darker the skin color of the people. The Tamils have a nearly black skin. There are still people with black curly hair amongst them. They belong
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to the Dravidian minority. Here religion was the driving force for over 3700 years to support discrimination based on skin color. More recent examples are the Apartheid in South Africa and the racial segregation (Color bar) in the United States. Currently, racism to a varying degree lingers on almost everywhere in the world, with or without governmental or religious inspirations. As a dermatologist, I have been confronted with dramatic skin problems due to the use of skin-lightening agents. The Netherlands has a multi-ethnic society. The most frequent users of these skin-lightening agents are people of African descent (recent immigrants from Ghana and Nigeria) and people from Surinam, especially of Hindustani origin [48]. The use of skin-lightening agents is surrounded by taboos; therefore, it is very difficult to get an idea about the extent of the misuse and the side effects. Anthropological investigations have shown that people with a darker skin belonging to the lower classes reach for these agents to make them resemble the dominant class so that the chances for a better marriage and labor increase [49–51]. Although people have been mixing with each other since the beginning of mankind, it is an amazing to see how the lines between the different ethnic groups can still be drawn. In many respects this diversity can be seen as an advantage. The existence of colorful people means diverse and interesting cultures. It only requires respect for each other’s culture. Looking at the news from the media we see how difficult this is nowadays. It is apparently impossible to tolerate so many beliefs, opinions, and habits. Harlon L. Dalton writes about this touchy matter [52], ‘‘We people, white or black, must learn to speak openly about our racial beliefs to overcome fear and mistrust. This could help to remove the terrible division between people with various skin shades.’’ A possible solution might be to stimulate migration and assimilation. In a few hundred years we would all have a brown skin. Then only the real qualities of a man would matter!
References [1] Welcome to the UCMP Web Lift for Geologic Time! Available at: http://www.ucmp.berkeley.edu/help/ timeformold.html. Accessed June 7, 2007. [2] Human ancestry. Available at: http://www.archaeo logyinfo.com/. Accessed June 7, 2007. [3] Becoming human. Available at: http://www.beco minghuman.org/. Accessed June 7, 2007.
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[4] Jablonski NG, Chaplin G. The evolution of human skin coloration. J Hum Evol 2000;39:57–106. [5] Jablonski NG, Chaplin G. Becoming bipedal: how do theories of bipedalization stand up to anatomical scrutiny? In: Anapol F, German RZ, Jablonski NG, editors. Shaping primate evolution: form, function and behavior. Cambridge: Cambridge University Press; 2004. p. 281–96. [6] Jablonski NG. The evolution of human skin and skin coloration. Annu Rev Anthropol 2004;33: 585–623. [7] Mathur U, Datta SL, Mathur BB. The effect of aminopterin-induced folic acid deficiency on spermatogenesis. Fertil Steril 1977;12:1356–60. [8] Jablonski NG. A possible link between neural tube defects and ultraviolet light exposure. Med Hypotheses 1999;52:581–2. [9] Mackintosh JA. The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J Theor Biol 2001;211:101–13. [10] N Loomis WF. Skin-pigment regulation of vitaminD biosynthesis in man. Science 1967;157:501–6. [11] Darwin C. The descent of man and selection in relation to sex. London: John Murray; 1871. [12] Harpending H, Rogers A. Genetic perspective on human origins and differentiation. Annu Rev Genomics Hum Genet 2000;1:361–85. [13] Aoki K. Sexual selection as a cause of human skin colour variation: Darwin’s hypothesis revisited. Ann Hum Biol 2002;6:589–608. [14] Available at: http://en.wikipedia.org/wiki/Out_of_ Africa_theory. Accessed June 7, 2007. [15] Oppenheimer S. Out of Africa: peopling of the world. London: Constable & Robinson; 2004. [16] Tattersall I. Special exhibitionsdAfrica: continent of origins. Available at: http://www.metmuseum.org/ special/Genesis/tattersall_lecture.asp?printFlag¼1&; refPage¼1. Accessed June 7, 2007. [17] Leonard RC. Linguistic connections: a Paleolithic language. Available at: http://www.atlantisquest. com/Linguistics.html. Accessed June 7, 2007. [18] Zhao TM, Lee TD. Gm and Km allotypes in 74 Chinese populations: a hypothesis of the origin of the Chinese nation. Hum Genet 1989;2:101–10. [19] Omoto K. The Negritos: genetic origins and microevolution. Acta Anthropogenet 1984;8(1–2):137–47. [20] Thangaraj K, Singh L, Reddy AG, et al. Genetic affinities of the Andaman Islanders, a vanishing human population. Curr Biol 2003;13:86–93. [21] Endicott P, Gilbert MT, Stringer C. The genetic origins of the Andaman Islanders. Am J Hum Genet 2003;72:178–84. [22] Thangaraj K, Chaubey G, Kivisild T, et al. Reconstructing the origin of Andaman Islanders. Science 2005;308(5724):996. [23] Oetting WS, Bennett D. Mouse coat color genes. Vol. 2003. The albinism database. Available at: http://www.cbc.umn.edu/tad/genes.htm. Accessed June 7, 2007.
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