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Department of Anthropology, The Pennsylvania State University, 409 Carpenter Building, University Park, PA 16802, USADepartment of Geography, The Pennsylvania State University, 409 Carpenter Building, University Park, PA 16802, USA
Variability in skin pigmentation phenotypes in African and African-admixed populations has not been well documented or genetically characterized.
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Afro-textured hair is a shared characteristic of most African and African-admixed people, and may represent an adaptation to protect the brain against thermal stress.
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Vitamin D deficiency is a risk for darkly pigmented people because of the natural sunscreening properties of eumelanin and the increased prevalence of indoor living.
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Use of race categories is ill-advised because of the genetic heterogeneity and socially constructed nature of races.
Our species, Homo sapiens, evolved in Africa, and humanity’s highest levels of genetic diversity are maintained there today.
Underlying genetic diversity combined with the great range of solar regimes and climatic conditions found in Africa has contributed to a wide range of human integumentary phenotypes within the continent. Millions of Africans have moved, both voluntarily and involuntarily, to other continents in the past 2000 years, and the range of integumentary phenotypes among admixed African diaspora populations is enormous. In this contribution, we do not catalog this variation, but provide basic evolutionary background as to how it developed in the first place.
Diversity of integumentary phenotypes within Africa
Africa has been a crucible of human diversification because of the length of human habitation there, and because of the continent’s great size, environmental history, and past and present ecological diversity. Africa is the only continent that spans nearly 70° of latitude, thus containing an enormous range of solar radiation regimes. The continent’s modern environmental mosaic first emerged about 20,000 years before present (BP) with the onset of more arid conditions across the continent. Formation and expansion of sand dunes along the southern margin of the Sahara and dramatic reductions in areas occupied by tropical forests proceeded until about 12,000 years BP.
Phases of increased wetness (“lacustrine phases”) followed, from about 10,000 to 4000 years BP, during which the Sahara shrank and tropical forests rebounded.
Africa today exhibits a long and high elevational rise to the east along the Rift Valley that modifies the predominant global westerly humid air flow and creates a short seasonal monsoon. The specific effects of these environmental changes on human populations in Africa are not understood fully, but there is little doubt that they created opportunities for human biologic and cultural diversification by erecting and then eliminating geographic barriers to north-south and east-west migration. These changes alternately increased opportunities for the action of genetic drift and gene flow, such as across the Sahel corridor,
and created conditions under which biologic and cultural adaptations to rapid environmental change were promoted. Together, these factors contributed to the evolution of a large African population with a highly subdivided genetic structure.
The migration event that contributed most significantly to the establishment of the modern genetic landscape of Africa, including gene flow between once-isolated populations, was the expansion across Africa of the Bantu-language–speaking agriculturalists from near the Nigerian/Cameroonian highlands beginning approximately 3000 years BP.
This series of movements has resulted in overprinting of the original latitudinal cline of skin pigmentation, specifically, in the movement into southern Africa of equatorial peoples who are more darkly pigmented than the original moderately pigmented inhabitants.
Skin pigmentation is visibly different and measurably variable across Africa (Fig. 1). Diversity of environmental conditions, especially of ultraviolet radiation (UVR) regimes, along with population histories (including migrations) are the ultimate evolutionary causes of this diversity, but the specific and proximate genomic causes have not been elucidated fully. Studies of the genetics of skin pigmentation have focused on the significance of the virtual lack of variation in the sequence of the melanocortin 1 receptor (MC1R) locus in Africa,
Between populations and individuals of African or African-admixed ancestry, differences in skin tone and the relative darkness of skin are due primarily to differences in the ratio of eumelanin to pheomelanin in the skin
Subtle differences in skin tone are due to complex mixtures of melanin polymers and to the size and reflectance properties of the melanosomes in which the pigments are packaged.
Phenotypic differences in skin tone among and between people of African ancestry are incompletely known (see Fig. 1) and their genetic basis is inadequately understood.
Fig. 1Variation in human skin tones in Africa, as illustrated by skin reflectance values. The numbers within each polygon are the values for the reflectance of red light (685 nm) from the skin.
(Data from Jablonski NG, Chaplin G. The evolution of human skin coloration. J Hum Evol 2000;39(1):57–106; and Chaplin G. Geographic distribution of environmental factors influencing human skin coloration. Am J Phys Anthropol 2004;125(3):292–302.)
Skin conditions affecting pigmentation produce highly visible disease states in normally darkly pigmented people. Of these, oculocutaneous albinism of the tyrosine-positive type (OCA2) is the most common that afflicts Africans and that has a genetic component. OCA2 has been reported to occur at a prevalence approaching 1 in 1000 in some groups in Zimbabwe and South Africa, because of consanguinity and founder effects.
Individuals affected by albinism experience all the harmful effects of UVR exposure, including skin cancer, and face significant social ostracism, even death, because of their condition.
It has recently been suggested that the deleterious OCA2 allele may be maintained in African populations as a balancing polymorphism, with the common deletion allele possibly conferring resistance to susceptibility to leprosy.
including the diversity that exists within Africa. Differences in hair color within Africa are minor and may represent pleiotropic effects of skin pigmentation genes.
Slight differences in hair form, growth characteristics, and susceptibility to breakage exist but have not been documented systematically. Sub-Saharan Africans generally exhibit tightly curled or Afro-textured hair and northern populations exhibit less tightly or loosely curled hair, but in all African populations, the hair shaft is elliptical in cross-section. The curliness of the hair shaft is caused by retrocurvature of the hair bulb, which gives rise to an asymmetrical S-shape of the hair follicle.
The continent-wide distribution of Afro-textured hair indicates that this is the ancestral condition for modern humans. Hrdy, who was one of the first to systematically characterize the morphology of human hair, speculated that hair form was determined by multiple genes, and that the tightly curly hair form had evolved convergently in African and Melanesian populations.
but the genetic basis of hair form is still largely unknown. Symmetric hair follicles and generally straighter scalp hair shafts characterize Eurasian populations; the straight and thick hair shafts common to most East Asians are caused by a variant of the ectodysplasin receptor, EDARV370A.
The influence of natural selection on integumentary phenotypes
Throughout most of the history of the genus Homo, roughly 2 million years, naked skin has been the primary interface between our bodies and the environment.
The major speciation events leading to the emergence of Homo sapiens occurred at or near the equator in Africa, where levels of UVR are high throughout the year. Within the tropics, UVR levels potentially can be lowered by clouds and humidity, but otherwise the equinoctial peaks of UVB (medium wavelength UVR) caused by the earth’s orbit around the sun are the most biologically significant sources of variation.
The intensity of UVB in sunlight is not perfectly correlated with heat produced by sunlight. Africa’s UVB regimes vary according to latitude, but also are affected greatly by humidity and cloud cover (Fig. 2). High levels of atmospheric moisture contribute to generally lower levels of UVR, especially UVB, over western and central equatorial Africa, whereas negligible levels of atmospheric moisture contribute to extremely high levels over the Sahara and the Namib, and much of eastern and northeastern Africa.
Fig. 2Variation in UVB (305 nm) levels across Africa at the Autumnal Equinox (22 September), based on remotely sensed data collected by the NASA TOMS 7 satellite. Details of methodology are discussed elsewhere.
The many deleterious effects of UVR on biologic systems have promoted the evolution of complex processes of protection and repair, including protective pigmentation, DNA repair mechanisms, and means of neutralizing reactive oxygen species. Variation in UVR accounts for 86% of the observed variation in human skin pigmentation as measured by skin reflectance.
The stable clinal arrangement of human skin pigmentation that existed before the modern era of human migrations indicates the action of stabilizing selection over a spatially varying optimum condition.
The evolution of darkly pigmented, eumelanin-rich, naked skin, which is capable of tanning on exposure to UVR, was one of the key innovations of human biologic evolution. Constitutive dark pigmentation and capabilities for development of facultative dark pigmentation through tanning evolved independently in multiple human lineages
), but conservation of folate is supported by the largest body of evidence. The unique and critical roles played by folate and its metabolically active form, 5-methyltetrahydrofolate (5-MTHF), in DNA biosynthesis, repair, and methylation
imply that mechanisms to conserve folate and 5-MTHF in the presence of UVR would have been promoted by natural selection. Exposure of unprotected skin to UVR creates high demand for folate and 5-MTHF, which is further heightened during periods of rapid cell division, such as embryogenesis and spermatogenesis.
Serum folate levels undergo statistically significant decline in people following exposure to clinical doses of narrow-band UVB administered over the course of 3 weeks,
Wavelength-specific photolysis appears to affect circulating levels of folate and 5-MTHF, but these levels are also certainly influenced by many other factors, including the polymorphic genes regulating folate and 5-MTHF metabolism, epigenetic modification of such genes, dietary folate consumption, and other factors, such as ethanol consumption.
Solar cycle predicts folate-sensitive neonatal genotypes at discrete phases of the first trimester of pregnancy: a novel folate-related human embryo loss hypothesis.
Human skin color is the product of 2 clines produced by natural selection to adjust levels of constitutive pigmentation to levels of UVR. Protective, eumelanin-rich skin pigmentation was the original condition for the genus Homo and has been maintained by stabilizing selection on combinations of different genes as an adaptation to high levels of UVR. Dark pigmentation is not disadvantageous from a thermoregulatory perspective to individuals living and exercising in sunny or arid environments. The heat-absorbing properties of eumelanin lead to darkly pigmented individuals showing higher core temperatures than lightly pigmented individuals after prolonged vigorous exercise, but no difference in evaporated sweat or in heat storage, which is balanced by increased long-wave radiation to the environment.
The continuously varying cline of eumelanin pigment in human skin from the equator to the poles is best explained as an adaptation for the maintenance of adequate levels of vitamin D in the body under conditions of seasonal or low UVR.
Vitamin D3 is made in the skin when UVB (290–310 nm) penetrates the skin and is absorbed by 7-dehydrocholesterol (7-DHC) in the epidermis and dermis to form previtamin D3. The potential for photosynthesis of vitamin D3 in the skin depends on many environmental and personal factors: solar zenith angle (which varies according to season, latitude, and time of day), local humidity and pollution levels and weather conditions, the amount and distribution of eumelanin in the skin, and the thickness of the stratum corneum.
Because the vitamin D endocrine system is involved in the regulation of many independent biologic processes, including bone metabolism, the innate immune response, cell proliferation, and differentiation,
positive selection for maintenance of vitamin D production capability under highly seasonal or low average UVB levels has been a major determinant of human skin pigmentation phenotypes.
Dark pigmentation can be a risk factor for vitamin D deficiency when individuals do not receive sufficient UVR exposure to produce adequate levels of vitamin D. This can be the result of migration, indoor living, lack of outdoor activity, routine wearing of concealing clothing, or combinations of these factors that often exist in urban environments.
The clinical presentation of vitamin D deficiency depends not only on sun exposure and diet, but on genetic factors that affect the production, metabolism, and storage of vitamin D. The vitamin D endocrine system is regulated by many genes, including the vitamin D receptor locus (VDR), the vitamin D binding protein locus (VDBP), and those controlling the production of enzymes required for vitamin D synthesis and metabolism, such as CYP27B1 and CYP24A1.
Variants in the vitamin D pathway, serum levels of vitamin D, and estrogen receptor negative breast cancer among African-American women: a case-control study.
Vitamin D deficiency manifests itself in different ways depending on its duration, severity, and the interval in the life course when it strikes. Among the most serious potential consequences of vitamin D deficiency established for African, African diaspora, or African-admixed populations are elevated risks of nutritional rickets in children,
Prevalence of vitamin D insufficiency and risk factors for type 2 diabetes and cardiovascular disease among African migrant and refugee adults in Melbourne: a pilot study.
; patterns of comorbidity between vitamin D deficiency and type 2 diabetes mellitus and tuberculosis are not well understood.
In contrast to the situation for skin pigmentation, considerably less has been researched or written on the evolution of hair color and hair form. Most studies to date have dealt with the proximate genetic mechanisms responsible for producing lightly colored hair variants, and have focused especially on characterization of polymorphic MC1R loci and their associated phenotypes.
but not rigorously tested. Even less has been documented on the functional and evolutionary significance of hair form. Although hair form is almost certainly related to thermoregulation and the importance of keeping the head cool during exercise and under hot environmental conditions,
comparative studies of the effects of different hair forms on scalp and body temperature have not been conducted. Studies of the properties of bird plumage and mammal coats indicate that the color and the microstructure and micro-optical properties of feathers or hairs, as well as the degree to which these appendages can be elevated by piloerection or passive lofting, contribute to the radiative heat loads that homeotherms acquire from solar radiation.
Humans evolved functional hairlessness on most of their bodies probably as the result of selection for enhanced eccrine sweating and the cooling benefits associated with the evaporation of sweat.
In the only experimental study of its kind, hair length and style were found to affect sweat rate and total body mass when humans were exposed to high environmental temperatures in a climate chamber.
Kim MJ, Choi JW, Lee HK. Effect of hair style on human physiological responses in a hot environment. Paper presented at: Environmental Ergonomics: Proceedings of the 13th International Conference on Environmental Ergonomics. Boston, MA, August 2–7, 2009.
Kim MJ, Choi JW, Lee HK. Effect of hair style on human physiological responses in a hot environment. Paper presented at: Environmental Ergonomics: Proceedings of the 13th International Conference on Environmental Ergonomics. Boston, MA, August 2–7, 2009.
Together with the evidence from studies of heat gain and loss in birds and nonhuman mammals, these findings suggest that short, curly, Afro-textured hair evolved because it can maintain a boundary layer of cooler, dryer air near the scalp, and thereby protect the thermogenic and thermosensitive brain. This hypothesis warrants experimental testing.
Integumentary phenotypes and race
Skin color has been the primary feature used to classify people into groups or races. The first scientific classification of humans, written by Carolus Linneaus and published in 1738, placed people into 4 unranked “types” based on skin color and continent of origin. By 1758, Linneaus’ classification further defined people by eye color and hair texture, and by general traits of character and disposition that accorded with the prevailing climatic theory of human diversity.
These ideas were embraced and extended by the philosopher Immanuel Kant, who was the first to define human “races” as fixed natural entities in his essay of 1775, “On the different human races.”
Kant’s classification differed from that of Linneaus in being explicitly hierarchical and based on skin color, which Kant viewed as a trait that denoted personality and morality. Kant equated skin color with character, and propagated ideas that lighter-colored races were superior and darker-colored ones inferior.
Because of his immense reputation, Kant was instrumental in establishing the “color meme,” which profoundly affected attitudes toward the nature and meaning of human physical differences.
The persistence of racism and colorism has contributed to the promotion of skin lightening and the widespread use and abuse of skin bleaching agents among African and African-admixed populations worldwide.
The nonexistence of human races is a scientific fact, which is based on the observations that similar “racial characteristics,” such as skin color, have evolved multiple times, that such characteristics are generally not genetically linked to one another, and that patterns of phenotypic and genotypic diversity are not exclusive but extensively overlapping. Genomic research has revealed geographic clustering of some traits, but social factors alone have constructed and maintained races at different times and in different places.
There is an urgent need for clinical researchers and practicing physicians to recognize that the continued use of racial categories in medicine is inaccurate and irresponsible because it reinforces the existence of socially constructed categories, and fails to recognize the highly genetically heterogeneous nature of most human populations, including African and African-admixed groups. Most human populations today are heterogeneous and genetically admixed, and self-identified ancestry often does not reflect genetic ancestry accurately.
Many of the world’s largest cities today on all inhabited continents have large proportions of people with African ancestry, and the genetic heterogeneity of this group must not be underestimated.
Summary
Africa is home to the highest levels of human genetic diversity because of our species’ long evolutionary history there, and because of the continent’s large size, environmental diversity, and complex histories of human migration and isolation. The diversity of human skin pigmentation and hair texture phenotypes within Africa has not been well documented. Skin pigmentation within Africa generally varies by latitude, but the pattern has been overprinted by the migration of equatorial Bantu-language–speaking agriculturalists into eastern and southern Africa in the past 5000 years. The genetic basis of different skin tones among people of African ancestry has not been elucidated thoroughly. Dark pigmentation confers excellent protection against high levels of UVR, but predisposes individuals to vitamin D deficiency, especially those with indoor lifestyles. Afro-textured hair characterizes all African populations and is the likely ancestral condition for humans. It may have evolved as thermoregulatory adaptation to help keep the scalp and brain cool under conditions of high environmental heat and strenuous exercise. The evolution of integumentary phenotypes is characterized by widespread parallelism. For this and other reasons, skin color and hair texture cannot be used to classify people into races. The use of race to classify human groups in clinical contexts is ill-advised because of the highly genetically heterogeneous nature of most human populations, including African and African-admixed groups, and because races are socially constructed categories specific to particular times and places.
Acknowledgments
We are grateful to Nonhlanhla Khumalo for inviting us to contribute to this special issue of Dermatologic Clinics. We thank Tess Wilson for help in obtaining bibliographic materials, and for all logistical matters related to manuscript preparation and submission. Jablonski is grateful to Ophelia Dadzie for discussions on the evolution and functional significance of Afro-textured hair.
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The genetic structure and history of Africans and African Americans.
Solar cycle predicts folate-sensitive neonatal genotypes at discrete phases of the first trimester of pregnancy: a novel folate-related human embryo loss hypothesis.
Variants in the vitamin D pathway, serum levels of vitamin D, and estrogen receptor negative breast cancer among African-American women: a case-control study.
Prevalence of vitamin D insufficiency and risk factors for type 2 diabetes and cardiovascular disease among African migrant and refugee adults in Melbourne: a pilot study.
Kim MJ, Choi JW, Lee HK. Effect of hair style on human physiological responses in a hot environment. Paper presented at: Environmental Ergonomics: Proceedings of the 13th International Conference on Environmental Ergonomics. Boston, MA, August 2–7, 2009.
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