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The evolution of human skin and skin color

Annu. Rev. Anthropol. 2004. 33:585–623  2004 by Annual Reviews. All rights reserved First published online as a Review in Advance on June 21, 2004 THE EVOLUTION OF HUMAN SKIN AND
SKIN COLOR

Nina G. JablonskiDepartment of Anthropology, California Academy of Sciences, San Francisco,California 98103; email: njablonski@calacademy.org Key Words pigmentation, melanin, UV radiation, thermoregulation, race
Abstract Humans skin is the most visible aspect of the human phenotype. It is
distinguished mainly by its naked appearance, greatly enhanced abilities to dissipate
body heat through sweating, and the great range of genetically determined skin colors
present within a single species. Many aspects of the evolution of human skin and skin
color can be reconstructed using comparative anatomy, physiology, and genomics.
Enhancement of thermal sweating was a key innovation in human evolution that allowed
maintenance of homeostasis (including constant brain temperature) during sustained
physical activity in hot environments. Dark skin evolved pari passu with the loss of body
hair and was the original state for the genus Homo. Melanin pigmentation is adaptive
and has been maintained by natural selection. Because of its evolutionary lability, skin
color phenotype is useless as a unique marker of genetic identity. In recent prehistory,
humans became adept at protecting themselves from the environment through clothing
and shelter, thus reducing the scope for the action of natural selection on human skin.
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When humans visualize a body, they see mostly skin. The skin is the body'sdirect interface with the physical environment, conveying a state of health and Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org personal identity. The skin comprises a sheet-like investiture that protects thebody from attack by physical, chemical, and microbial agents. It is the organ thatregulates body temperature through control of surface blood flow and sweating anddetects critical information about the ambient environment and objects touched.
The largest and most massive of the organs of the body, the skin of the averageadult human exceeds 2 m2 yet is generally no thicker than 2 mm (Odland 1991).
The skin also provides a forum for advertising. It provides information about aperson's age, health, and some aspects of ancestry, and furnishes a placard uponwhich further information is placed through temporary and permanent decoration.
Research on the evolution of human skin and skin color has not been com- mensurate with the importance of skin in human evolution. Skin is generally notpreserved in the fossil record and so details of its evolution can be gained only from comparative anatomical and physiological evidence. Skin has also been overlookedas a topic of research interest in anthropology and human biology in recent decadesbecause of the social sensitivity surrounding discussions of skin color and becauseof the use and misuse of skin color in biological and social concepts of race.
The goal of this review is to provide a comprehensive yet economical survey of the biology, evolution, and culture of human skin and skin color, with an emphasison new research—especially on the evolution of skin color. The review beginswith an overview of the basic biology of skin itself, followed by discussions of theevolution of skin and skin color, and of skin color and race.
THE STRUCTURE AND FUNCTIONS OF HUMAN SKIN
The skin serves as an effective physical barrier because its laminar structure ren-ders it relatively resistant to abrasion, puncture, and percutaneous absorption, andbecause its immune cells mount a first line of defense against pathogens comingin contact with the body. Lacking adequate protection from hair, human skin hasundergone numerous adaptive structural changes that give it strength, resilience,and sensitivity (Montagna 1981). The skin of humans, like that of all tetrapods,acts as a sun shield to protect the body from most solar UV radiation (UVR) andis the locus for the initiation of the important, UVR-driven process of vitamin Dproduction in the body.
The laminar structure of human skin comprises two major tissue layers, a thinnerouter layer, the epidermis, and a thicker and more internally complex inner layer,the dermis (Figure 1). The epidermis is a stratified keratinizing epithelium witha smooth, abrasion-resistant surface that is interrupted only by hair follicles andthe pores of sweat glands. The barrier properties of the skin are predicated on theintegrity of the stratum corneum (Elias et al. 2003, Taylor 2002). Keratinocytes arethe principal cell type found in epidermis and are composed largely of filamentous by Stockholm University - Library on 10/03/12. For personal use only.
proteins known as keratins, which are imbedded in an amorphous matrix. Theskin's elasticity and resistance to physical and chemical attack can be attributed Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org to the high elastic modulus and unique amino acid composition of the keratinizedlayer of the epidermis (Marks 1991, Odland 1991). The epidermis also containspopulations of three types of immigrant dendritic cells: melanocytes, Langerhanscells, and Merkel cells. Melanocytes produce the skin's primary pigment, melanin,and are discussed in greater detail below. Langerhans cells are specialized cellsof the immune system that present and respond to antigens coming in contactwith the skin, and Merkel cells are associated with nerve terminals that togetherfunction as slow-adapting mechanoreceptors for touch; they are most common onthe glabrous skin of the fingertips (Chu et al. 2003, Kripke & Applegate 1991,Lynn 1991, Odland 1991). The epidermis is subdivided into four layers fromdeep to superficial: the stratum basale (the germinative layer of keratinocytes), the SKIN AND SKIN COLOR by Stockholm University - Library on 10/03/12. For personal use only.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org Schematic rendering of a cross-section of human skin, showing its laminar structure, main cell types, and appendages.
stratum spinosum, the stratum granulosum, and the stratum corneum. The stratumcorneum consists of flattened, nonviable keratinocytes. In darkly pigmented orheavily tanned individuals, these keratinocytes contain specks of melanin "dust"(Kollias 1995a). The stratum corneum acts as a barrier to the unrestrained passageof water and solutes through the skin, defends against invasion by microorganismsand the penetration of toxic substances, and protects against most mechanicalinjury caused by friction, abrasion, pricks, or arthropod bites (Marks 1991). Thesefunctions are successfully served despite the epidermis being in a constant state ofturnover, as the outermost cornified cells of the stratum corneum are shed as theyare replaced from below.
Differences between human groups in epidermal structure and thickness have been reported, but most studies of this topic have been based on small sampleswith poorly controlled experimental designs, as reviewed elsewhere (Taylor 2002).
Considerable variation in epidermal thickness exists within human populations andis likely related to age and history of sun exposure. The stratum corneum of darklypigmented or heavily tanned people is more compact and consists of more cornifiedcell layers than that of lightly pigmented people; these characteristics enhance thebarrier protection functions of the skin (Taylor 2002).
In all primates, the epidermis of the volar surfaces of the hands and feet exhibit well-developed epidermal ridges or dermatoglyphics, which impart greater resis-tance against friction and help to insure secure purchase on locomotor substratesand on objects being gripped or manipulated. Dermatoglyphics are also found onthe ventral surfaces of the tails of prehensile-tailed New World monkeys and onthe knuckle pads of chimpanzees and gorillas (Ellis & Montagna 1962, Montagna1971).
The melanocytes of the epidermis warrant close attention because of their role in the production of the skin's primary pigment or chromophore, melanin.
Melanocytes are specialized dendritic cells that reside in the stratum basale ofthe epidermis and in the matrix portion of the hair bulb. They originate in theneural crest as melanoblasts proliferate and migrate to the epidermis during theeighteenth week of embryonic development (Rawles 1948). Melanocytes produce by Stockholm University - Library on 10/03/12. For personal use only.
melanins in specialized cytoplasmic organelles called melanosomes, which vary insize and degree of aggregation depending on skin type and pigmentation (Figure 2) Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org (Szabo et al. 1969). The density of melanocytes varies over the surface of the body,and the number of active (melanin-producing) melanocytes varies with age andcan be increased by exposure to UVR (Halaban et al. 2003, Jimbow et al. 1991,Quevedo et al. 1975). The total number of melanocytes is relatively invariant fromone person to another, however, and is not related to variation between humangroups in skin pigmentation (Fitzpatrick et al. 1961, Jimbow et al. 1991, Robins1991, Young & Sheehan 2001). MacKintosh, following Wasserman, has recentlyadvanced the hypothesis that melanocytes, melanosomes, and melanin togetherfunction as part of the immune system against invading microorganisms and that themore darkly pigmented skins of the indigenous peoples of the tropics have evolvedprimarily to serve this function (MacKintosh 2001; Wassermann 1965b, 1974).
SKIN AND SKIN COLOR by Stockholm University - Library on 10/03/12. For personal use only.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org Schematic rendering of cross-sections of lightly and darkly pigmented human skin, showing differences in stratum corneum structure and in the size andaggregation of melanin-containing melanosomes.
Melanocytes project their dendrites into keratinocytes where they then trans- fer mature melanosomes (Figure 2). Melanosomes are ellipsoidal, membrane-bound organelles containing melanin. After melanosomes have been transferredto keratinocytes, they become aggregated and surrounded by a membrane in amelanosome complex (Jimbow et al. 1991, Szabo et al. 1969). In darkly pig-mented skin, melanosomes are large and are not clumped in aggregations, whereasin lightly pigmented skin these organelles are smaller and aggregated (Szabo et al.
1969). Intensity of skin coloration is determined by many factors: (a) The totalnumber of melanosomes in the keratinocytes and melanocytes, and their degreeof dispersion; (b) the rate of melanin production (melanogenesis); (c) the degreeof melanization of melanosomes; (e) the rate of transport and type of incorpo-ration of melanosomes into keratinocytes; (f) the degradation of melanosomeswithin the keratinocytes; and (g) a person's chronological age because the numberof metabolically active melanocytes decreases over time (Halaban et al. 2003,Jimbow et al. 1976, Ortonne 1990, Parker 1981). Larger melanosomes breakdown more slowly in keratinocytes and contribute to higher levels of pigmentation(Sulaimon & Kitchell 2003).
MELANIN PIGMENTATION AND ITS MEASUREMENT
Human skin derives most of its pigmentation from melanin, an extremely dense, virtually insoluble, high molec-ular weight polymer that is attached to a structural protein (Jimbow et al. 1991,Ortonne 2002, Parker 1981, Sulaimon & Kitchell 2003). Human skin contains thetwo types of melanin found in all mammals, the brownish-black eumelanin andthe reddish-yellow pheomelanin (Thody et al. 1991). Higher concentrations ofeumelanin characterize darker skin phenotypes including tanned skin. Concentra-tions of pheomelanin in the skin vary considerably from individual to individualwithin any given human group, but pheomelanin-rich skin phenotypes are morecommon among red-haired northern Europeans, as well as East Asians and Na-tive Americans (Rana et al. 1999, Thody et al. 1991). Melanin is synthesized byoxidation of tyrosine via the enzyme tyrosinase (Fitzpatrick et al. 1950, Jimbowet al. 1976, Ortonne 2002). Eumelanins and pheomelanins arise from a common by Stockholm University - Library on 10/03/12. For personal use only.
metabolic pathway in which dopaquinone is the key intermediate (Ortonne 2002).
As is discussed in greater detail below, production of melanins is regulated by Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org pigmentation genes, hormones, and UVR (Fitzpatrick & Ortonne 2003, Sulaimon& Kitchell 2003, Thody & Smith 1977). A balance of many regulatory factors isessential for normal pigment production in the melanocyte, and derangements ofthese factors can lead to anomalies of cutaneous pigmentation such as albinismpiebald spotting, and various types of hyperpigmentation (Robins 1991, Sulaimon& Kitchell 2003, Thody & Smith 1977).
The optical and chemical properties of melanins have been studied in detail (Ito 2003, Kollias et al. 1991, Ortonne 2002, Prota 1992c), but detailed chemicalcharacterization of the compounds has been difficult to obtain because melaninpolymers are composed of many different units connected through strong carbon-carbon bonds (Ito 2003). The optical properties of natural melanin in vivo are SKIN AND SKIN COLOR related to its abilities to absorb, scatter, and reflect light of different wavelengths(Kollias et al. 1991, Ortonne 2002). The melanins in human skin are a hetero-geneous mixture of melanin polymers, precursors, and metabolites, character-ized by a continuous absorption capacity in the UV range and exponentiallydeclining absorption capacity from the UV to the visible range (Kollias 1995b,Sarna & Swartz 1998). Natural protection against sunburning (photoprotection)is due to the absorption and scattering of UVR by melanin (Kaidbey et al. 1979;Kollias 1995a,b). Both processes are influenced by the density and distributionof melanosomes within keratinocytes (Figure 2), with the larger, singly dispersedand heavily melanized melanosomes of darkly pigmented skin absorbing moreenergy than the smaller, less dense, and lightly melanized melanosomes of lightlypigmented skin (Kaidbey et al. 1979).
Melanin was long considered to act as a passive screening filter against UVR, but it is by no means inert (Fitzpatrick et al. 1961). Photodegradation (photolysis)and/or oxidative polymerization of melanin may occur when it absorbs photons(Ortonne 2002). Recent evidence indicates that the photoprotective role of melaninin darkly pigmented skin may be augmented by its ability to scavenge oxygen-derived radicals (reactive oxygen species), such as superoxide anion and hydrogenperoxide, which are cytotoxic compounds generated by the interaction of UV pho-tons with membrane lipids and other cellular components (Ortonne 2002, Prota1992c, Sulaimon & Kitchell 2003, Young & Sheehan 2001). At the physiologicallevel, the protective role of melanin pigmentation against UVR exposure derivesfrom its ability to prevent direct and indirect (oxidative) damage to DNA at wave-lengths where it is most vulnerable (Cleaver & Crowley 2002, Kielbassa et al.
1997, Shea & Parrish 1991).
Melanin pigmentation in human skin is considered as either constitutive skin color or facultative skin color (Quevedo et al. 1975). Constitutive skin color isthe amount of genetically determined cutaneous melanin pigmentation that is gen-erated without any influence of solar radiation (Jimbow et al. 1976, Quevedoet al. 1975). Facultative skin color or "tan" constitutes the short-lived, immedi-ate, and delayed tanning reactions elicited by exposure to UVR (Jimbow et al.
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1991, 1976; Quevedo et al. 1975). Lighter constitutive pigmentation is associ-ated with a higher sunburn response, a lower tanning response, and a greater Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org susceptibility to skin cancers (Kollias et al. 1991, Sturm 2002, Wagner et al.
2002).
Objective and reproducible assessment of melanin pigmentation has long been a goal of anthropology and dermatology. In anthropology, verbal descriptions ofskin colors ("white," "yellow," "black," "brown," and "red") were replaced bycolor-matching methods during the early twentieth century (Olivier 1960, vonLuschan 1897). The most popular of these methods was the von Luschan scale,based on the use of colored tablets or tiles of different colors and hues with whichthe colors of unexposed skin were matched. These and similar matching meth-ods could not be consistently reproduced, however, and were swiftly abandonedwhen reflectance spectrophotometry was introduced in the early 1950s (Lasker 1954, Wassermann 1974). Reflectance spectrophotometry remains the method ofchoice for the objective study of skin pigmentation, color definition, and the spec-tral reflectance curves of skin because the incident light used and the distancebetween the light source and the subject are invariable and because subjectivefactors inherent in the visual matching methods are excluded (Wassermann 1974).
All instrumental approaches to skin color evaluation depend on the illuminationof the skin site by a standard light source at a fixed relative angle that minimizesthe reflected light from the stratum corneum. The detector collects light re-emittedby the skin site from a particular angle and with a chosen color filter (Kollias1995a). Because of the importance of assessing constitutive skin color on a partof the body that is not routinely exposed to sun, the inner (medial) surface ofthe upper arm has long been the standard reference site for studies of skin color.
Portable reflectance spectrophotometers came into use with Weiner's (1951) study,with two types of instruments being commonly employed in anthropology dur-ing the latter part of the twentieth century. The instrument manufactured by theEvans Electroselenium Company (EEL) has been the most widely used, espe-cially in studies of the skin colors of Old World peoples (Wassermann 1974),whereas that made by the Photovolt Corporation was more widely used in studiesof New World peoples. Unfortunately, the skin reflectance measurements obtainedby these two instruments are not directly comparable, requiring conversion for-mulae to make them so (Lees & Byard 1978). Research is now underway that maymake possible the conversion of skin color assessments made by von Luschancolor tablets to values comparable with those derived from reflectance spectropho-tometry (M. Henneberg, personal communication).
In clinical medicine, constitutive skin color and skin sensitivity has been clas- sified commonly according to skin phototypes or sun-reactive skin types, fromType I (very sensitive, easily burned, with little or no potential for tanning)to Type VI (insensitive, never burns, and deeply pigmented) (Fitzpatrick 1988,Fitzpatrick & Ortonne 2003, Jimbow et al. 1991). Skin type does not correspondwell to constitutive skin color, however, and has limited applicability with respectto the responses of moderately or deeply pigmented skin (Kollias et al. 1991, Prota by Stockholm University - Library on 10/03/12. For personal use only.
1992c, Taylor 2002, Wagner et al. 2002, Westerhof et al. 1990). Despite theselimitations, skin phototyping has been widely embraced by many clinicians be- Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org cause assessments can be made without instrumentation. In recent years, highlysensitive diffuse reflectance spectrophotometers such as the DermaSpectrometerand the Datacolor International Microflash as well as chromaticity meters havebeen used increasingly to measure skin pigmentation and skin response to UVR(Kollias 1995a, Wagner et al. 2002).
The photoprotective benefits of melanin have been assessed using several dif- ferent measures including minimal erythemal dose (MED), DNA damage, andincidence of skin cancer (Kollias et al. 1991). The MED represents the minimumamount of UVR necessary to bring about a slight visible reddening of lightly pig-mented skin. It is the easiest and most common method of assessing skin reactionsto UVR but is difficult to determine for deeply pigmented individuals in whom SKIN AND SKIN COLOR visual redness is difficult to assess (Kaidbey et al. 1979, Ortonne 2002, Shono et al.
1985).
Exposure of human skin to UVR results in a profound alteration of the meta- bolism, structure, and function of epidermal cells. These activities include in-creased activation of melanocytes, augmentation of melanosome production, anincrease in the size of melanosome complexes incorporated within keratinocytes,and initiation of vitamin D synthesis (Parker 1981, Prota 1992a, Urbach 2001).
The erythema response or sunburn reaction is related to constitutive skin color:Dark-skinned individuals can tolerate longer sun exposure than light-skinned indi-viduals can. The skin of individuals with dark constitutive pigmentation exhibits asun protection factor (SPF) of 10–15, whereas that of moderately pigmented peo-ple (e.g., from the circum-Mediterranean) achieves an SPF of only 2.5 (Kaidbeyet al. 1979, Kollias et al. 1991, Ortonne 2002). In vitro studies of the reactions ofhuman melanocytes to UVR have shown that heavily pigmented melanocytes havea greater capacity to resume cell division after irradiation with short wavelengthUVR (UVB) than do their lightly pigmented counterparts, which suggests that theysuffered less damage to their DNA (Barker et al. 1995). In contrast, UVB damagesthe immune system of the skin regardless of constitutive pigmentation by depletingboth heavily and lightly pigmented skin of Langerhans cells (Cleaver & Crowley2002, Kripke & Applegate 1991). The protective role of melanin in connection withskin cancer thus derives from its role in preventing damage to DNA in the first place,not in protecting against damage to the cutaneous immune system (Vermeer et al.
1991). Tanning or facultative pigmentation induced by UVR is photoprotective tosome degree against the deleterious effects of further UVR exposure, but it does notsignificantly increase the SPF of individuals with light constitutive pigmentationor protect the DNA of their skin from UVR-induced damage (Kaidbey et al. 1979,Ortonne 2002). Although repeated exposure of tanned skin to UVR increases thenumber of metabolically active melanocytes and the intensity of melanogenesis(Lock-Anderson et al. 1998), the increased concentration of melanin in the tannedskin of inherently lightly pigmented people does not approach the photoprotectionconferred by natural melanin in intrinsically darker-skinned people (Kaidbey et al.
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1979). Individuals with lightly to moderately pigmented skin, who are repeatedlyexposed to UVR, experience premature aging (photoaging) of the skin, which is Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org characterized by wrinkling and anomalies of pigmentation (Chung 2001, Fisheret al. 2002, Kollias et al. 1991). This process is initiated by the photochemicalgeneration of reactive oxygen species causing degradation of structural proteinsin the dermis that confer strength and resiliency to the skin (Fisher et al. 2002).
The dermis is a thick, dense fibroelastic connective tissue composed of collagenfibers, elastic fibers, and an interfibrillar gel composed of glycosaminoglycans,salts, and water. The primary cells of the dermis are collagen-rich fibroblasts.
Collagen, which constitutes 77% of the fat-free dry weight of skin, largely accounts for the tensile strength of the skin's fabric and for some of the ability of the dermisto scatter visible light (Kollias 1995a, Shea & Parrish 1991). Interwoven with thecollagen is a network of abundant elastic fibers that restore the skin to its normalconfiguration after stretching. The dermis is equally thick in people with dark orlight constitutive pigmentation (Taylor 2002).
The dermis encloses a widely ramifying network of blood vessels, an extensive nerve network, sweat glands, and a pilosebaceous complex of hair follicles andsebaceous glands (Figure 1). Of these, only the sweat glands are addressed in detailin this review because of their importance in thermoregulation.
The rich vascular supply of the skin is responsible for supplying the needs of the sweat glands, hair follicles, and rapidly multiplying epidermal cells in the stratumbasale. The density of cutaneous blood vessels varies throughout the body's surfaceand is related to temperature and blood pressure regulation and the relative amountsof intermittent physical pressure different parts of the body must withstand, withthe highest concentrations found in the skin covering the head, nipples, palms,soles, and ischial tuberosities (Edwards & Duntley 1939). The perineal skin offemale macaques, baboons, and chimpanzees is richly suffused with blood vessels(Montagna 1967, Montagna 1971) that create large sexual swellings advertisingthe female's state of reproductive receptivity and lifetime reproductive potential(Domb & Pagel 2001). The oxygenated and deoxygenated forms of hemoglobincarried in the skin's blood vessels are some of the skin's main pigments, witha person's skin color determined mainly by the skin's melanin and hemoglobincontent (Edwards & Duntley 1939). The erythema or strongly red appearance ofthe skin caused by exposure to UVR is the result of increases in the number anddiameter of vascular capillaries through which blood is flowing and an increase inthe blood flow through each capillary (Kollias 1995a). Sunburned skin feels hot tothe touch because of the increased vascularization of the skin and the inflammatoryresponse mounted by the skin as it works to repair UVR-induced damage (Ryan1991, Shea & Parrish 1991).
The nerve supply of the skin is highly complex because the skin is a ma- jor sensory surface that contains varied types of receptors sending signals to the by Stockholm University - Library on 10/03/12. For personal use only.
central nervous system about the external environment and the internal state ofthe skin (Chu et al. 2003, Lynn 1991). These receptors include two types of Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org temperature sensors, diverse mechanoreceptors associated with both hairy andglabrous skin, and an important group of cutaneous sensory cells (nociceptiveafferents) specialized for the detection of tissue-threatening stimuli or the pres-ence of injury or inflammation (Lynn 1991). The glabrous skin of the hands andfeet of primates is densely packed with sensory nerve endings that permit highlysensitive tactile discrimination and exquisite differentiation of temperature andtexture (Chu et al. 2003, Lynn 1991, Martin 1990). These attributes greatly en-hance the manipulative functions of these appendages, especially the hand (Martin1990).
Numerous hairs, which grow from hair follicles located in the dermis, are as- sociated with mechanoreceptors and sebaceous glands. Hair performs a range of SKIN AND SKIN COLOR functions from insulation, to protection against the sun, enhancement of cutaneoussensation to communication of emotion (through piloerection), and ornamenta-tion (Lavker et al. 2003; Montagna 1967, 1971; Wheeler 1984, 1985). Humansare unique among primates in possessing effectively naked skin, except on thescalp, the male chin, the axilla, and the groin. Although human skin bears mil-lions of hairs, most of them are so small as to be nearly invisible (Montagna1981).
SWEAT GLANDS
Human dermis contains two main types of sweat glands, eccrine and apocrine. The former are widely distributed throughout the surface of the body,whereas the latter are concentrated in the axilla, perineum, and external auditorycanal. Eccrine glands are tubular in form (Figure 1) and lie in the outer portion ofthe dermis. They produce copious amounts of dilute, watery fluid expressed to thesurface of the skin through an individual pore. Humans have two to four millioneccrine glands on the surface of their bodies, with an average distribution rangingfrom ∼150–340/cm2 (Folk & Semken 1991, Goldsmith 2003). Both apocrine andeccrine sweat glands are stimulated by the sympathetic division of the autonomicnervous system and produce sweat in response to thermal stimulation (thermalsweating). In contrast, the eccrine glands of the palms and soles respond only toemotional stimuli, whereas those of the face and axilla respond to both (Folk &Semken 1991, Zihlman & Cohn 1988).
Considerable attention has been placed on comparisons of the quantity, struc- ture, and function of sweat glands between human groups. The number of strictlycontrolled comparisons between members of different populations after equivalentperiods of deliberate acclimatization is quite small (Weiner 1977). The results ofmost rigorous comparative study of sweat gland densities in humans (Knip 1977)indicate that only small differences in the total number and average density of sweatglands exist between disparate human populations. As yet it has proven virtuallyimpossible to design studies that can determine conclusively whether differencesin sweating performance between human groups are due to genetic influences or by Stockholm University - Library on 10/03/12. For personal use only.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org The Skin in Thermoregulation
Dissipation of heat is the function that most conspicuously distinguishes humanskin from that of all other animals (Montagna 1981). The reasons for the evolutionof this unique capacity are discussed in the following section. Humans encounterheat stress more or less year round in equatorial areas and for varying lengthsof time in the rest of the world except for circumpolar and alpine environments.
Heat stress is exacerbated by prolonged or rigorous exercise. Maintenance ofhomeostasis requires that the body's core temperature remain close to a neutralpoint, which varies from about 36.8 to 37.2◦C, in order to permit uninterruptedfunctioning of the temperature-sensitive cells of the human central nervous system.
If the rates of production or loss of heat are excessively out of balance, core temperature can quickly increase or decrease to dangerous levels (Kraning 1991,Wenger 2003).
Temperature regulation in humans includes involuntary (physiologic) and vol- untary (behavioral) activity (Wenger 2003). Voluntary temperature regulation in-volves the conscious actions taken by people to maintain thermal comfort, includ-ing the seeking of shade and shelter, and the wearing or shedding of clothing.
Involuntary temperature regulation in the skin has been studied in great detail in the past 50 years by both physiologists and anthropologists, and only a superficialsummary of this corpus of work is presented here. Regulation of temperature by theskin is accomplished through its roles in (a) perceiving and transmitting its owntemperature to the central nervous system; (b) regulating heat transfer betweenthe body's core and the skin through the cutaneous circulation; (c) serving as asuperficial casing through which body heat is conducted from the vascular layersto the surface; (d) acting as an interface for the loss or gain of heat to or from theenvironment by radiation, convection, or conduction; and (e) acting as a surface forthe spreading of sweat necessary for evaporative cooling (Frisancho 1981, Kraning1991). The relative role of the four avenues of heat loss (radiation, convection,conduction, and evaporation) depends on the interaction of the ambient temperatureand humidity (Chaplin et al. 1994; Frisancho 1981; Wenger 2003; Wheeler 1984,1991b). The ability of sweat glands to respond to heat stress is adversely affectedby sunburn (Pandolf et al. 1992). Protection of the integrity of sweat glands againstdamage caused by UVR, therefore, has been of great importance during the longcourse of human habitation of the tropics.
Experimental studies and simulations undertaken to determine how thermal homeostasis is maintained under the stressful environmental conditions of thetropics have shown that heat loss is maximized in people with a high ratio ofskin surface area to body weight, such as Nilotic tribespeople, the Kung San, andAustralian Aborigines (Frisancho 1981; Wheeler 1991a,b, 1992). This relationshipsupports Allen's Rule in mammals, which states that mammals living in coldregions will minimize the size and surface area of their extremities, whereas thoseinhabiting hot areas will increase the relative size of appendages.
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Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org The Role of the Skin in Vitamin D Biosynthesis
Synthesis of vitamin D in the skin of vertebrates is the only unanimously agreedpositive effect of UVR exposure. Vitamin D3 is the form of vitamin D that is syn-thesized by vertebrates, whereas vitamin D2 is the primary form found in plants(Holick 2003). Vitamin D3 is more accurately characterized as a prosteroid hor-mone than as a vitamin because, in mammals, it is derived from a cholesterol-likeprecursor (7-dehydrocholesterol) found in the skin (Holick 2003). Vitamin D is aunique natural product thought to have first occurred on Earth as a photosyntheticproduct in marine phytoplankton more than 750 mya (Holick 1995). Although thephysiological role of vitamin D in plants and invertebrates is not clear, vitaminD was essential for the evolution of terrestrial vertebrates (Holick 1991, 1995).
SKIN AND SKIN COLOR Holick has reasoned that early tetrapods depended on vitamin D for the efficient useof scarce dietary calcium to preserve their rigid calcified skeletons (Holick 1995).
Vitamin D can be synthesized only by a photochemical process, so early tetrapodscould only satisfy their body's vitamin D requirements by exposing themselvesto sunlight to photosynthesize vitamin D in their own skin or by ingesting foodscontaining vitamin D (Holick 1995).
Vitamin D3 synthesized in the skin requires successive hydroxylations in the liver and kidney to be converted to its biologically active form, 1α, 25-dihydroxy-vitamin D3 (Holick 1991, Jones et al. 1998). This functionally active form isimportant for the regulation of calcium and phosphorus metabolism, skeletal de-velopment and mineralization, the regulation of normal cell growth, and the inhi-bition of cancer cell growth (Holick 1991, 2001). The production of vitamin D3is optimally stimulated by UVR wavelengths of 295–300 nm, in the UVB range(MacLaughlin et al. 1982). High-energy UVB photons penetrate the skin and areabsorbed by the 7-dehydrocholesterol in the keratinocytes of the epidermis (espe-cially of the strata basale and spinosum) and fibroblasts of the dermis, catalyzingthe formation of previtamin D3 (Holick 2001, Webb et al. 1988). Once formed inthe skin, previtamin D3 can undergo isomerization to vitamin D3 at body temper-ature and then undergo further chemical conversions to 1α, 25-dihydroxyvitaminD3. The conversion of previtamin D3 or vitamin D3 to the functionally activeform is rate-limited, however. In the presence of biologically sufficient amountsof 1α, 25-dihydroxyvitamin D3 in the circulation, previtamin D3 and vitamin D3are transformed by UVA or UVB into a variety of inert byproducts, thus avertingoverproduction of the biologically active form and subsequent "vitamin D intox-ication" (Holick 2001, Holick et al. 1981). This finding disproves the hypothesisthat dark constitutive skin pigmentation evolved in the tropics as an adaptation toprotect against the overproduction of 1α, 25-dihydroxyvitamin D3 (Loomis 1967).
Melanin pigments are highly effective at absorbing and scattering the UVB wavelengths that catalyze vitamin D3 synthesis. Thus, high concentrations ofmelanin in the skin result in a decrease in the efficiency of conversion of 7-dehydrocholesterol to previtamin D3; pigmentation slows but does not prevent by Stockholm University - Library on 10/03/12. For personal use only.
cutaneous production of the vitamin (Holick et al. 1981, Webb et al. 1988). In-dividuals with very deep constitutive pigmentation often require 10 to 20 times Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org longer exposure to sunlight than those of lighter pigmentation in order to promotean adequate synthesis of vitamin D3 (Holick et al. 1981). This finding explainswhy dark-skinned individuals living at high latitudes with low levels of envi-ronmental UVB are at greater risk of vitamin D3–deficiency diseases than arelight-skinned people (Clemens et al. 1982, Holick 2001, Mitra & Bell 1997). Theevolutionary significance of this observation is discussed further below. The pho-toconversion of 7-dehydrocholesterol to previtamin D3 in the skin is also adverselyaffected by increasing age (Holick 1995), the wearing of clothing (Matsuoka et al.
1992), and by the use of topical sunscreens, which block the UVB wavelengthsresponsible for both sunburn and vitamin D3 production (Holick 1997, Webb et al.
1988).
THE EVOLUTION OF MODERN HUMAN SKIN
Reconstruction of the evolution of human skin relies on evidence provided bycomparative anatomy and physiology, as well as study of the evolution of thegenes and gene complexes that determine the function and pigmentation of skin.
Using basic principles of historical morphology, one can reconstruct the majorsteps in the evolution of human skin by utilizing a well-established phylogeny toexamine historical transformations of structure and function (Jablonski & Chaplin2000). This method leads to the reconstruction of the probable appearance of theskin in the last common ancestor of the human and chimpanzee lineages as beinglightly pigmented and covered with dark hair, like most catarrhine primates today(Jablonski & Chaplin 2000).
The skin of modern humans is distinguished from that of other primates mainly by its naked appearance, its greatly enhanced abilities to dissipate body heatthrough sweating, and by the great range of genetically determined skin colorspresent within a single species. Most investigators have considered these attributesto be adaptations forged by natural selection.
The Evolution of the Thermoregulatory Properties
of Human Skin

Human skin is not hairless, but—as discussed above—the hairs over most of thebody's surface are so fine and present at a sufficiently low density that the skinappears essentially naked. Explanations for the evolution of human hairlessnesshave been many, varied, and often highly creative. The most cogent explanationsare based on the importance of a functionally naked skin in maintaining bodytemperature in hot environments.
Many animals, including primates, which live in hot environments, have heavy coats of insulating fur or feathers. In the heat caused by strong sunlight, suchinsulation reduces environmental heat gain (Folk & Semken 1991, Walsberg 1988).
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This is the case even for black coats, which absorb short-wave radiation near or atthe surface of the fur and reradiate large amounts of long-wave radiation before it Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org reaches the skin (Dmi'el et al. 1980). The effectiveness of fur insulation in reducingenvironmental heat gain is lessened by sweating. The most efficient evaporativecooling occurs at the skin's surface; in heavily furred animals, water vapor istransferred through the fur to the atmosphere (Folk & Semken 1991). If the fur iswet from sweating, however, maximum evaporation occurs at the surface of thefur, and heat from the blood vessels cannot be transferred as efficiently to the site ofevaporation (Folk & Semken 1991). Under these circumstances, much more watermust be used for evaporative cooling. Thermal sweating as a method of coolingbecomes more important as environmental temperatures rise or as activity levelsincrease because the lower gradient between core and environmental temperaturesrestricts the amount of heat loss that can be achieved by radiation, convection,and conduction (Frisancho 1981, Wheeler 1991b). Removal of excess heat is, SKIN AND SKIN COLOR therefore, greatly facilitated by the loss of body hair because it increases thermalconductance and permits additional heat loss through sweating (Wheeler 1985,Zihlman & Cohn 1988).
A strong case can be made for the evolutionary loss of apocrine sweat glands in humans because these sweat glands are most common in heavily furred animals(Folk & Semken 1991). The African apes exhibit a ratio of approximately 40%apocrine sweat glands to 60% eccrine; the great preponderance of eccrine sweatglands in modern humans probably evolved under the strong influence of natu-ral selection, following the loss of the apocrine component to sweating (Folk &Semken 1991, Montagna 1981, Zihlman & Cohn 1988). This process was proba-bly propelled by increases in body size and activity levels associated with modernlimb proportions and striding bipedalism, which occurred in the transition from theprimitive hominins of the late Miocene to the genus Homo of the Plio-Pleistocene(Chaplin et al. 1994; Folk & Semken 1991; Jablonski & Chaplin 2000; Montagna1981; Schwartz & Rosenblum 1981; Wheeler 1984, 1996).
The importance of body cooling through the skin in modern humans has been emphasized repeatedly by both physiologists and anthropologists because of theprimacy of preventing hyperthermia and attendant damage to the central nervoussystem (Cabanac & Caputa 1979, Falk 1990, Wheeler 1984, Zihlman & Cohn1988). The temperature of the brain closely follows arterial temperature, requir-ing that the temperature of the circulating blood be carefully regulated (Nelson &Nunneley 1998). This process became increasingly important as activity levels andbrain size increased in the genus Homo through the Pleistocene. Simulations andexperimental studies have confirmed that maintenance of stable core temperatureunder conditions of increased environmental heat load or exercise is best accom-plished via recruitment of a whole-body cooling system, involving cooling ofperipheral blood vessels through sweating (Desruelle & Candas 2000, Nelson &Nunneley 1998). A recently mooted hypothesis that human hairlessness evolvedlate in human evolution as a result of the adoption of clothing and the need to reducethe load of external parasites (Pagel & Bodmer 2003) finds no support in light ofthe overwhelming evidence of the importance of hairlessness in thermal sweating by Stockholm University - Library on 10/03/12. For personal use only.
and whole-body cooling in maintaining stable core temperature and homeostasis.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org The Evolution of Human Skin Pigmentation
RECONSTRUCTION OF SKIN COLOR IN EARLY HOMO
The early members of the genus Homo from the late Pliocene and Early Pleistocene of Africa exhibitedlarger bodies, relatively larger brains, and relative longer lower limbs than didtheir australopithecine predecessors (McHenry & Berger 1998; Ruff et al. 1993,1997). The higher activity levels and larger day ranges reconstructed for them(Wheeler 1991a, 1992) would have required that their skin be functionally nakedand endowed with a high density of eccrine sweat glands in order to facilitateheat loss (Jablonski & Chaplin 2000, Wheeler 1984). This situation created a newphysiological challenge for human skin: protection of a naked integument against UVR. Dense hairy coats protect the skin of mammals from UVR-induced damageto the skin because the hairs themselves absorb or reflect most short-wavelengthsolar radiation. In mammals with sparse coats of hair, however, 3%–5% of inci-dent UVR is transmitted to the skin (Walsberg 1988). Nonhuman mammals thatare active in hot, sunny environments exhibit sparse coats because they facilitatepassive heat loss; they also display highly melanized skin on their exposed (dorsal)surfaces to effectively block the UVR transmitted to the skin (Walsberg 1988). Thisevidence clearly indicates that hair loss in the human lineage was coupled withincreased melanization of the skin as activity levels in hot environments increased.
The early members of the genus Homo, the ancestral stock from which all laterhumans evolved, were, thus, darkly pigmented (Jablonski & Chaplin 2000). Thisinterpretation has recently been supported by genetic evidence demonstrating thatstrong levels of natural selection acted about 1.2 mya to produce darkly pigmentedskin in early members of the genus Homo (Rogers et al. 2004).
Heavily pigmented skin does not, in fact, perceptibly increase the body's heat load under conditions of intense solar radiation (Baker 1958, Walsberg 1988).
This is because for half of the solar radiation reaching the Earth's surface—in theinfrared—there is essentially no difference in absorption between dark and lightskin (Baker 1958, Daniels 1964). This evidence negates the claim by Blum (1961)and others (Morison 1985) that heavily melanized pigmentation in humans couldnot be adaptive in the hot tropics because of the increased heat load caused bygreater amounts of absorbed solar radiation.
SKIN PIGMENTATION IN MODERN HUMAN POPULATIONS
Many of the accounts of travelers and explorers from the fifteenth century onward include reports of theskin color of the peoples they encountered. As natural historians and humangeographers—mostly from Europe—ventured into Asia, Africa, Australia, and theAmericas and began to study the indigenous human populations in detail, mapsdepicting the worldwide distribution of human skin color were slowly assembled.
The best known of these maps is that composed by the Italian geographer Renato by Stockholm University - Library on 10/03/12. For personal use only.
Biasutti, which was based on the von Luschan skin color scale. This map hasgained broad circulation in several widely distributed publications (Barsh 2003, Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org Lewontin 1995, Roberts 1977, Walter 1971), despite the fact that, for areas withno data, Biasutti simply filled in the map by extrapolation from findings obtainedin other areas (Robins 1991). A more accurate and exhaustive compilation of theskin colors of indigenous peoples based only on published skin reflectance mea-surements is now available (Jablonski & Chaplin 2000). Both maps show similartrends, with darkly pigmented peoples found near the Equator and incrementallylighter ones found closer to the Poles. A larger percentage of people with dark skinis found in the Southern Hemisphere as compared with the Northern Hemisphere(Relethford 1997) because of a latitudinal bias in the distribution of land masses(Chaplin & Jablonski 1998).
The data compiled by Jablonski and Chaplin also provide conclusive evidence of sexual dimorphism previously observed in human skin pigmentation (Frost SKIN AND SKIN COLOR 1988, van den Berghe & Frost 1986), with females being consistently lighter thanmales in all populations studied (Jablonski & Chaplin 2000).
One of the major problems encountered in assembling data on the distribu- tion of human skin color in indigenous populations is determining exactly whatan indigenous population represents. For most anthropologists and human geog-raphers, an arbitrary cutoff date of 1500 has been adopted to distinguish nativeor indigenous peoples from immigrant populations. This date is reasonable withrespect to the inauguration of the modern era of European colonization but fails torecognize the several major movements of human groups within continents (suchas the so-called Bantu expansion within Africa) that occurred before 1500. Thesemovements, along with European colonization and the increasingly rapid and dis-tant migrations of human populations through time, have fundamentally alteredthe human landscape established in prehistoric times. This has made the interpre-tation of geographically and biologically significant trends in human populationsmuch more difficult.
ENVIRONMENTAL CORRELATES OF HUMAN SKIN COLOR
The skin pigmentation of indigenous human populations shows remarkable regularity in its geographic dis-tribution. Darker skins occur in more tropical regions and lighter skins in tem-perate, although the gradient is less intense in the New World as compared tothe Old World. Even within Africa, the continent with the largest equatorial landmass, there is considerable heterogeneity of skin color, with the deepest colorsoccurring not in the lowest latitudes but in the open grasslands (Chaplin 2001,Roberts 1977). The strong latitudinal signal in skin color led most early work-ers to conclude that skin pigmentation represented an adaptation to sunlight orother solar-driven phenomena such as temperature. Walter (1958, 1971) was thefirst researcher to suggest that the pigmentation gradient observed was linked tothe intensity of UVR, and he established this relationship by calculation of cor-relation coefficients between skin color (as measured on the von Luschan scale)and estimated UVR. The relationship between skin color and environment was by Stockholm University - Library on 10/03/12. For personal use only.
further explored by studies in which the relationship of skin color, as measuredby reflectance spectrometry, to latitude, temperature, and humidity was studied Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org by correlation and regression analyses (Roberts 1977, Roberts & Kahlon 1976).
These analyses showed the dominant association of skin reflectance with latitude,which was then deduced to be an effect related to the intensity of UVR (Roberts1977, Roberts & Kahlon 1976).
In recent years, studies of the relationships between morphological and physio- logical variation and attributes of the physical environment have been advanced bythe availability of remotely sensed data on levels of UVR, total solar radiation, tem-perature, humidity, precipitation, and other environmental variables at the Earth'ssurface. These data, which were not widely available to workers before 1990,have permitted correlation, regression, and other analyses of skin reflectance to beconducted against actual measurements, rather than estimates, of environmentalvariables (Chaplin 2001, 2004; Jablonski & Chaplin 2000).
Using data on the minimal erythemal dose of UVR (UVMED) at the Earth's surface collected by the NASA TOMS 7 satellite, Jablonski & Chaplin were able toestablish a conclusive correlation between latitude and annual average UVMED,and thence between annual average UVMED and skin reflectance (Jablonski &Chaplin 2000). This publication was followed by a study in which the influence ofminimum, maximum, and seasonal levels of UVR, as well as other directly mea-sured environmental variables, relative to skin reflectance were studied (Chaplin2001, Chaplin 2004). This study showed that skin reflectance was correlated withautumn levels of UVMED, and that skin reflectance could be almost fully mod-eled as a linear effect of this variable alone (Chaplin 2001, 2004). This studyalso showed that the relationship between summer levels of UVMED and skinreflectance appeared to reach a threshold past which higher levels of UVR werenot correlated with incrementally lower skin reflectance (darker pigmentation)(Chaplin 2001, 2004).
Low reflectance values for human skin (dark pigmentation) are primarily a func- tion of UVMED (Jablonski & Chaplin 2000), with regression analysis demonstrat-ing that autumn UVMED levels have the strongest effect. This indicates that skincolor is more strongly correlated with UVA, which is consistently higher through-out the year at all latitudes, than with UVB (Chaplin 2001, 2004). MaximumUVMED had the next most significant effect (Chaplin 2001, 2004). Winter lev-els of precipitation have the opposite effect, being positively correlated with highreflectance values (light pigmentation) (Chaplin 2001, 2004). Multiple regressionformulae relating skin reflectance to these environmental parameters can then beused to derive a map of predicted human skin colors, with the colors shown beingrealistic approximations of the true color of skin (Chaplin 2001, 2004) (Figure 3).
This map depicts an idealized situation in which humans worldwide are assumedto have inhabited their respective regions for the same lengths of time, and havefollowed similar cultural practices that could affect skin color (e.g., diet, activityschedules, use of clothing and shelter).
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NATURAL SELECTION AND THE EVOLUTION OF HUMAN SKIN PIGMENTATION
geographical distribution of human skin colors has invited many explanations, Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org most of which have claimed melanin pigmentation to be an adaptation to someattribute of the physical environment that varies primarily by latitude. Ever sincethe harmful effects of UVR began to be appreciated by scientists, explanations forthe evolution of deeply melanized skin have centered on the importance of resis-tance to sunburn, solar degeneration, and skin cancer (Daniels et al. 1972). Equallypopular has been the vitamin D hypothesis, which stated that lightly pigmentedskins were necessary outside of the tropics in order to permit vitamin D biosyn-thesis in the skin by low levels of UVR, whereas darkly pigmented skin affordedprotection against production of toxic doses of vitamin D in equatorial regions(Loomis 1967). Lightly pigmented skin has also been explained as an adaptationto resist cold injury, on the basis of experimental and epidemiological data thathave documented more severe injuries incurred by pigmented skin exposed to SKIN AND SKIN COLOR freezing conditions (Post et al. 1975, Steegmann 1967). Other explanations haveimputed highly melanized skin as providing effective concealment in habitats suchas tropical forests with differing light intensities and environmental illumination(Cowles 1959, Morison 1985), and still others have reasoned that tropical diseasesand parasites rather than tropical climate were the major selective forces lead-ing to the evolution of differential pigmentation in humans (MacKintosh 2001;Wassermann 1981, 1965a).
Although adaptive explanations for human pigmentation have dominated the literature, others have downplayed or discounted the role of adaptation by naturalselection. Some workers have emphasized the role of sexual selection, especiallyby way of explaining the lighter constitutive pigmentation of females relative tomales (Aoki 2002, Frost 1988). Deol claimed that differences in skin color betweenhuman populations were the pleiotropic byproducts of natural selection on otherfunctions of pigmentation genes (Deol 1975). Others have simply discouragedthe "amusing pastime" of adaptive reconstruction in the absence of data on thedifferential survival and reproduction of varying skin pigmentation phenotypes(Blum 1961, Lewontin 1995). Adaptive explanations "for" any given phenotypictrait require demonstration that the trait increases the real or probable reproductivesuccess of the organism. Although such evidence is often difficult to muster inthe case of traits borne by long-lived mammals, it is incumbent that adaptivereconstructions be tethered by this responsibility.
In the past, adaptive explanations for different levels of melanin pigmentation in human skin have suffered from an inability to demonstrate probable or realdifferences in survivorship and reproduction of different skin color phenotypesunder the same environmental conditions. Blum introduced this mode of criticalappraisal of competing hypotheses when he drew attention to the fact that dark skinpigmentation could not have evolved primarily as adaptive protection against skincancer because such cancers rarely cause death during peak reproductive years(Blum 1961, Jablonski & Chaplin 2000). Other adaptive explanations for lightor dark skin pigmentation (e.g., protection against cold injury; camouflage) havesimilarly failed to demonstrate real or probable increases in reproductive success by Stockholm University - Library on 10/03/12. For personal use only.
as a result of possession of these phenotypes.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org MELANIN AS A REGULATOR OF THE PENETRATION OF UVR INTO THE SKIN Recen-
tly, Jablonski & Chaplin (2000) published a new adaptive hypothesis for the evo-
lution of human skin pigmentation stating that melanin pigmentation evolved to
regulate the penetration of UVR into the skin in order to prevent the photolysis of
photo-labile compounds while permitting the photosynthesis of others. This hy-
pothesis was based on two equally important observations: (a) that the B vitamin
folate is destroyed by long wavelength UVR (UVA), and that folate deficiencies
can markedly reduce individual reproductive success by adversely affecting cell
division; and (b) that vitamin D3 is synthesized in the skin by short wavelength
UVR (UVB) and that severe vitamin D deficiencies adversely affect reproduc-
tive success by interfering with normal calcium metabolism (Jablonski & Chaplin
2000). Natural selection has produced two opposing clines of skin pigmentation.
The first is a cline of photoprotection that grades from darkly pigmented skin atthe Equator to lightly pigmented skin near the Poles. The second is a cline ofvitamin D3 photosynthesis that grades from lightly pigmented near the Poles todarkly pigmented at the Equator. In the middle of the two clines we find peopleswith enhanced abilities to develop facultative pigmentation according to seasonalUVR levels.
THE FOLATE HYPOTHESIS
The potential importance of dark skin pigmentation in protecting folate from UVR-induced photolysis was first recognized upon discov-ery that folate undergoes photolysis in vitro when subjected to UVA (360 nm) andthat serum folate levels of human subjects dramatically declined when humansunderwent long-term exposure (minimum of 3 months) to the same wavelength,for 30–60 min once or twice a week (Branda & Eaton 1978). The potential sig-nificance of the finding to the evolution of human skin pigmentation was echoedlater, but a causal mechanism was not mooted (Zihlman & Cohn 1988).
Few nutrients compare with folate (folic acid) for its impact on health. Adequate folate status is vital for the synthesis, repair, and expression of DNA, and thereforefor all processes involved in cell division and homeostasis (Kesavan et al. 2003,Lucock et al. 2003, Suh et al. 2001). The subtle influence of folate on the cell'sgenomic machinery has led to the realization that even marginal folate deficien-cies may have significance in developmental disorders and degenerative diseasesassociated with high morbidity and mortality (Lucock et al. 2003). Now that folatedeficiency is widely acknowledged as a risk factor for neural tube defects, recurrentearly pregnancy loss, and other complications of pregnancy, the maintenance ofadequate folate status in women of reproductive age has become a primary publichealth concern (Bower & Stanley 1989, Fleming & Copp 1998, Minns 1996, Suhet al. 2001). Folate's importance in spermatogenesis also highlights its importantrole in maintaining male reproductive competence (Cosentino et al. 1990, Mathuret al. 1977).
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The recognition of folate's pivotal roles in DNA synthesis and repair—and thus most processes associated with reproductive success in both sexes—has underlined Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org the importance of protecting the body's folate stores from physical or chemicaldegradation. Because folate is susceptible to oxidative damage as a result of expo-sure to UVR and ionizing radiation (Branda & Eaton 1978, Hirakawa et al. 2002,Kesavan et al. 2003), the primary evolutionary function of melanin in regions re-ceiving high annual UVR is to protect folate from photodegradation (Jablonski& Chaplin 2000). Photolysis of folate has been experimentally demonstrated at340 nm and 312 nm, in the UVA and near-UVA wavelengths (Hirakawa et al. 2002,Lucock et al. 2003). With skin reflectance being most closely correlated with au-tumn levels of UVMED dominated by UVA, one can conclude that the longerwavelengths of UVR, which are capable of penetrating deep into the dermis ofthe skin, have been the most important agents of natural selection in connectionwith the evolution of skin pigmentation (Chaplin 2001) (Figure 4). The results of SKIN AND SKIN COLOR by Stockholm University - Library on 10/03/12. For personal use only.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org The effects of UV radiation on the skin. Different wavelengths of UVR penetrate to different thicknesses in the skin, with UVA penetrating more deeply thanUVB. UVC generally does not penetrate the Earth's atmosphere.
a recent study (Gambichler et al. 2001) did not confirm the photolytic effect ofUVA on serum folate levels in a small number of human volunteers. This findingruns counter to the results of previous in vivo and in vitro studies demonstratingprofound photodegradation of folate upon exposure to UVR (Hirakawa et al. 2002,Lucock et al. 2003) and to X- and γ -irradiation (Kesavan et al. 2003). A true andstatistically robust test of the folate hypothesis would require a case-control studyinvolving a large number of human volunteers experiencing long-term (once ortwice a week for a minimum of three months) exposure to UVR, with measurementof more labile folate species such as specific red cell folate coenzymes (Lucocket al. 2003).
SKIN PIGMENTATION AND VITAMIN D BIOSYNTHESIS
In the millennia prior to about 1.6 mya, the earliest members of the genus Homo appear to have beenrestricted in their distribution to the high-UVR regimes of equatorial Africa. Un-der these environmental conditions, possession of highly melanized skin wascritical for survival. As populations of early Homo moved both northward andsouthward, they began to experience different schedules and intensities of UVRexposure.
UVR levels at the Earth's surface are affected by latitude, altitude, season, moisture content, cloud cover, the depth of the ozone column, orbital parameters,and other factors (Hitchcock 2001, Madronich et al. 1998). Short wavelengthUVR (UVB, 280–315 nm) is more effectively absorbed by atmospheric ozonethan are longer wavelengths (UVA, 315–400). Thus, as one moves away from theEquator and the angle of solar elevation decreases, the thickness of the atmosphere(including the ozone layer), through which sunlight must pass, increases. Thisresults in a greater attenuation of UVR, especially of UVB, by scattering andabsorption by ozone, and consequently very low levels of UVB in high-latitudeecosystems (Caldwell et al. 1998). Very small increments or decrements of UVBlead to substantial biological effects (Madronich et al. 1998); thus, it is highlybiologically significant that regions north and south of 50◦ latitude receive onlytiny doses of UVB, and only then at the peak of summer (Caldwell et al. 1998, by Stockholm University - Library on 10/03/12. For personal use only.
Chaplin 2001, Johnson et al. 1976, Neer 1985).
As discussed earlier, deeply melanized skin confers excellent protection against Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org the deleterious effects of UVR, but it also greatly slows the process of vitaminD3 synthesis in the skin. As hominins moved out of the tropics, their exposureto UVR—especially to vitamin D–inducing UVB—was dramatically reduced.
Levels of UVR at the Earth's surface are not thought to have been appreciablydifferent in the Pleistocene as compared to today because similar conditions ofsolar emissivity and orbital parameters existed at the time, and similar levels ofUVR have been reconstructed from biological proxies (Rozema et al. 2002). Evenbefore remotely sensed data on UVB levels outside of the tropics were available,theorists surmised that early humans living in high latitudes with deeply pigmentedskin would have not been able to produce sufficient vitamin D3 in their skin to meettheir physiological demands and that strong selective pressure for depigmentation SKIN AND SKIN COLOR of the skin had been exerted in order to facilitate photosynthesis of vitamin D3(Loomis 1967, Murray 1934, Neer 1975).
Using known values of UVMED at the Earth's surface (Herman & Celarier 1996) and the precise dosage of UVB necessary to catalyze vitamin D synthesis inhuman skin at a specific latitude (Webb et al. 1988), researchers can calculate theworldwide potential for vitamin D3 synthesis for lightly pigmented skin (Jablonski& Chaplin 2000) (Figure 5). Zone 1 (shown without hachure in Figure 5) corre-sponds closely to the tropics and represents an area in which there is adequateUVR throughout the year to catalyze vitamin D3 synthesis in the skin (Jablonski& Chaplin 2000). Zone 2 (area covered by vertical hachure in Figure 5) representsthe region in which there is insufficient UVR during at least one month of the yearto produce vitamin D3, and Zone 3 (cross-hatched area of Figure 5) represents thatin which there is insufficient UVR, as averaged over the entire year, to photosyn-thesize vitamin D3 in the skin (Jablonski & Chaplin 2000). The configuration ofvitamin D synthesis zones for darkly pigmented skin differs markedly from this de-piction, with Zone 1 being greatly reduced in area, and Zones 2 and 3 significantlyexpanded because of the attenuation of UVB absorption by dark melanin pig-mentation and concomitant prolongation of the length of UVB exposure requiredfor vitamin D3 biosynthesis (Jablonski & Chaplin 2000). This analysis clearlydemonstrates the profound impact of constitutive pigmentation on the potentialfor vitamin D3 synthesis in the skin. An empirical demonstration of this was re-cently provided by a school population of darkly pigmented and albino children inSouth Africa, in which the former group of children required a significantly higherdietary intake of vitamin D3 to attain the same levels of vitamin D3 and plasmacalcium than did the albinos (Cornish et al. 2000). The importance of the synthesisand physiological activity of vitamin D have been further born out by studies ofthe worldwide polymorphism in the vitamin D–binding protein (or group-specificcomponent, Gc) that show a clear relationship between the frequency of specificGc alleles and levels of sunlight (OMIM 2003).
Vitamin D3 insufficiency and deficiency can exert sinister effects on the body throughout life and have the demonstrated potential to reduce fitness when they by Stockholm University - Library on 10/03/12. For personal use only.
afflict children and adolescents. The most serious and notorious of the vitaminD3–deficiency diseases is rickets, caused by a failure of mineralization in the Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org cartilaginous matrix of developing bones as a result of calcium and phosphatemalabsorption (Shaw 2003, Wharton & Bishop 2003). Comprehensive clinical de-scriptions of rickets (Bereket 2003, Holick 1995, Shaw 2003, Wharton & Bishop2003) catalog the devastating osseous and nonosseous effects of the disease onchildren and adolescents, including the delayed closure of fontanelles, bowing ofthe lower limb bones, and narrowing of the pelvic outlet in females, which cancause obstructed labor and a high incidence of infant and maternal morbidity andmortality. Vitamin D3 deficiency in adults produce osteomalacia, a softening ofthe bone matrix, but inadequate vitamin D3 status in pregnant women contributesto hypocalcemia and rickets in their babies (Wharton & Bishop 2003). The dele-terious effects of vitamin D3 deficiency encompass a suite of problems affecting evolutionary fitness, including those involving the formation and maintenance ofthe skeleton, control of normal cell growth, inhibition of cancerous cell growth,and maintenance of normal immune system function (Grant 2002; Holick 1991,2001; Wharton & Bishop 2003). An important, but little reported consequence ofvitamin D deficiency in laboratory mice and rats is a marked reduction in femalefertility and female reproductive failure apparently due to failure of vitamin D tointeract normally with its receptor on the ovary (Jones et al. 1998).
An abundance of clinical and epidemiological evidence now supports the ar- gument that depigmentation of the skin evolved in humans living outside of thetropics because of the importance of maintaining adequate vitamin D3 productionin the skin for as long as possible throughout the year. Alterations in the functionof the vitamin D endocrine system in darkly pigmented people as a consequence ofdiminished exposure to sunlight result in vitamin D3 insufficiency and deficiency,as recently reviewed elsewhere (Mitra & Bell 1997, Wharton & Bishop 2003).
These problems potentially afflict dark-skinned people who have migrated to orwho inhabit UVB-poor regions (e.g., northern Europe, the northern United States,or Canada) or darkly pigmented people living in sunny regions who habitually stayindoors or consistently wear concealing clothing when outdoors (Atiq et al. 1998,Bereket 2003, Brunvand & Haug 1993, Fogelman et al. 1995, Fonseca et al. 1984,Gessner et al. 1997, Hodgkin et al. 1973, Holick 1995, Wharton & Bishop 2003).
In these populations, vitamin D3 deficiency is exacerbated by breast feeding be-cause of the low concentration of vitamin D3 in human breast milk (Gessner et al.
1997, Shaw 2003, Wharton & Bishop 2003).
Vitamin D3 insufficiency and deficiency also afflict lightly pigmented people who are not exposed to sufficient sunlight because of occupation, advanced age, orhospitalization, or people who consistently wear protective clothing or sunscreenwhen outdoors (Holick 1995, 1997, 2001; Thomas et al. 1998). Rickets (knownto many as the English disease) was, in fact, first recognized as a disease of light-skinned children living in dark, multistoried structures devoid of sunlight (Holick1991, 1995).
Brace (1963) argues that depigmentation of human skin occurred not as the by Stockholm University - Library on 10/03/12. For personal use only.
result of active selection for lighter pigmentation, but because of the relief ofselective pressure on pigmentary systems as humans populated increasingly high Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org latitudes where dark pigmentation was no longer required as a shield againstUVR. This structural reduction hypothesis is based on the "probable mutationeffect" whereby mutations in the genes controlling melanin pigmentation wouldaccumulate, leading to reduction of or failure to produce melanin (Brace 1963).
A recent variation on this argument states that where natural selection for darkskin is sufficiently weak, a sexual preference for lighter skin could have driven theevolution of light skin (Aoki 2002, Ihara & Aoki 1999) (see below also). Thesearguments find limited support today with respect to the evolution of human skincoloration in light of the impressive body of recent clinical evidence cited abovethat attests to the many and highly significant functions of vitamin D3 in humans,which directly impact human health and reproductive competence.
SKIN AND SKIN COLOR Strong natural selection for vitamin D3 production in human skin was likely a powerful factor influencing the evolution of skin pigmentation in human popula-tions at high latitudes. Preliminary study of the distribution of paleontological andarchaeological sites for the genus Homo in relationship to the vitamin D3 synthe-sis zones described above indicates that year-round hominin habitation of Zone3, i.e., latitudes generally higher than 50◦, occurred only after human populationshad developed the technological competence to harvest fish, marine mammals, orother sources of food [such as reindeer lichen, or reindeer meat, organs, or milk(Bjorn & Wang 2000)] rich in vitamin D3 (N. Jablonski, G. Chaplin & D. Tyler,manuscript in preparation). This capability is associated almost primarily withUpper Paleolithic peoples, living approximately 15,000–10,000 years ago, whoare known to have made extensive use of fish hooks, fish traps, nets, harpoons, andother implements for the harvesting of marine animals.
SEXUAL DIMORPHISM IN HUMAN SKIN COLOR The observation that females exhi-
bit lighter skin pigmentation than do males in all populations examined (Jablonski
& Chaplin 2000, van den Berghe & Frost 1986) has invited speculation that the
phenomenon may be due to infantile mimicry, sexual selection, or a combination
of both factors (Aoki 2002, Frost 1988, Ihara & Aoki 1999, van den Berghe &
Frost 1986). These hypotheses are based on the observations that the attraction of
human infants and human females is partly due to their lighter pigmentation, and
that lighter-colored adult females are perceived as more feminine than are darker
females, and therefore are preferred as partners (Frost 1988). Jablonski & Chaplin
(2000) have advanced the idea that sexual dimorphism in skin pigmentation is
primarily due to natural selection, on the basis of the need of females to maximize
cutaneous vitamin D3 production in order to meet their absolutely higher calcium
requirements of pregnancy and lactation. Also, darker pigmentation may have been
the object of natural selection in males because of the importance of maintaining
optimal levels of folate in order to safeguard sperm production, a process depen-
dent on folate for DNA synthesis (G. Chaplin, personal communication). Sexual
selection is thus considered to have played a role in increasing the disparity in
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skin color between the sexes in some societies through preference for more lightlypigmented females, but this was not its ultimate cause (Jablonski & Chaplin 2000).
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org TANNING AND BLEACHING
The temporary development of increased melanin pig- mentation through exposure to UVR is called facultative pigmentation or tanning.
Individuals with very light constitutive pigmentation (skin phototypes I and II)never tan or tan minimally, whereas those with moderate to dark constitutive pig-mentation (phototypes V and VI) tan profusely (Taylor 2002). Considerable vari-ation in tanning potential exists even between people with ostensibly very similarlevels of constitutive pigmentation (Lee & Lasker 1959). Tanning develops in twostages (immediate and delayed) over the course of several hours or days, dependingon the wavelength and duration of UVR exposure (Ortonne 1990). Exposure toUVA causes tanning to develop quickly (Ortonne 1990), possibly as an adaptation to protect against photodegradation of essential biomolecules. Facultative pig-mentation is probably most important in areas such as the circum-Mediterraneanthat receive low levels of UVB but receive moderate levels of UVA that causephotodegradation of folate, DNA, and vitamin D3.
The practice of recreational tanning has been eschewed by health care workers in the past 20 years because of the explosion in skin cancer rates due to increasedUVR exposure. A tanned skin is still viewed by many as fashionable or as a signof well-being, however, and this positive image has spurred the development of asimulated tanning industry in Europe, the Americas, and Australia (Brown 2001,Randle 1997).
In many countries, however, tanned or dark skin does not connote member- ship in a fashionable class, and the possession of light skin—especially amongwomen—was and still is viewed as highly desirable and indicative of higher socialstanding. In many Asian countries, most women practice sun avoidance diligently.
In other countries where constitutive pigmentation is darker, skin-bleaching agents(including potent topical corticosteroids and hydroquinone formulations) have be-come popular (Taylor 2002).
THE MULTIFACTORIAL DETERMINATION OF SKIN PIGMENTATION IN MODERN HU-
The evolution of skin pigmentation in humans has been determined by many factors (Figure 6). By far the most important of these is the UVR regimeof the environment because intensity of UVR has been the main selective fac-tor influencing the evolution of melanin pigmentation in the skin. Through time,the number of factors influencing the evolution of human skin pigmentation hasincreased, and culture clearly has reduced the scope for the action of natural se-lection on human skin. Cultural behaviors such as the wearing of clothes and theutilization of shelter have become more common through time and have affectedthe evolution of skin pigmentation in some populations because of their effects ofreducing an individual's UVR exposure. Related to this phenomenon is the lengthof time that a population has inhabited an area with a particular UVR regime and by Stockholm University - Library on 10/03/12. For personal use only.
the latitudinal distance traversed from the ancestral to the new homeland. Thereis certainly a considerable lag time between the time of settlement of an area and Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org time that a population reaches its "optimum" skin color for the UVR conditionsof the area. The length of that lag period for any population is not known butwould depend on the intensity of natural selection exerted on the population byenvironmental influences. In early prehistory, humans possessed a simpler materialculture, spent considerable time accumulating food, and had fewer cultural trap-pings to buffer themselves against the environment. Under these conditions, naturalselection would have promoted mainly biological adaptations to the environment—including changes in skin coloration, body proportions, and regulation of thermalcooling. With increasing cultural competence over time, cultural solutions to theenvironmental challenges of sun, heat, and cold became preeminent. The oft-citedexample of the skin colors of the native populations of equatorial South America isworth revisiting in this connection. These populations have long been recognized SKIN AND SKIN COLOR by Stockholm University - Library on 10/03/12. For personal use only.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org The factors influencing human skin pigmentation, through evo- lutionary time and during the course of a human lifetime.
as being more lightly pigmented than are their counterparts at similar latitudesand altitudes in the Old World (Frisancho 1981, Jablonski & Chaplin 2000). Thisfact is almost certainly due to the recency of populations' migration into SouthAmerica from Asia (within the past 10,000–15,000 years) and the fact that the im-migrant populations into South America possessed many cultural behaviors andaccoutrements that protected them from high UVR exposure (Jablonski & Chaplin2000).
Diet has also played a part in the evolution of human skin pigmentation in very recent human history, as is well illustrated by the Eskimo-Aleut peoplesof the northeast Asian and North American Arctic. Eskimo-Aleuts exhibit skinpigmentation darker than would be predicted on the basis of the UVMED in theirhabitats (Jablonski & Chaplin 2000). Several factors have likely contributed tothis phenomenon, including the relative recency of their migration to the far northfrom a lower-latitude Asian homeland and its implication that their skin colorhas not caught up with their current location. This is almost certainly not theentire story, however. The UVR regime of the latitudes in which Eskimo-Aleutsreside comprises almost exclusively UVA throughout the year, with virtually novitamin D–inducing UVB except for extremely small doses in the summer months(Chaplin 2001, Johnson et al. 1976). Habitation of this latitude (Figure 5, Zone 3)by humans would be impossible without reliance on a highly vitamin D–rich diet.
The major components of the aboriginal Eskimo-Aleut diet—marine mammals,fish, and caribou—provide vitamin D3 in abundance. Much of the dietary vitaminD3 is stored in body fat (Mawer et al. 1972), denoting a possible evolutionaryconnection between the development of generous subcutaneous fat stores andvitamin D3 storage in these populations. With selection pressure on depigmentationapparently relaxed because of diet, Eskimo-Aleuts have evolved darker skin toprotect themselves from high levels of UVA as a result of direct solar irradiationand reflection from snow and ice. This scenario is supported by epidemiologicalstudies showing that departure from traditional diets in Eskimo-Aleut populationshas resulted in a high prevalence of vitamin D3–deficiency diseases, especiallyrickets (Gessner et al. 1997, Haworth & Dilling 1986, Moffatt 1995).
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Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org THE GENETICS OF HUMAN SKIN COLORATION
The study of genetics of human skin pigmentation has lagged considerably behind the study of the diversity andcausation of diverse human skin color phenotypes. This situation is now changingrapidly as comparative genomics, especially detailed studies of the genes regu-lating coat color pigmentation in mice (Barsh 1996, Sturm et al. 2001), begin topermit identification of the genes responsible for the pigmentation of human hair,skin, and eyes. Sixty of the 127 currently recognized pigmentation genes in themouse appear to have human orthologs (Bennett 2003).
Human skin pigmentation has long been considered a polygenic trait that fol- lows a quasi-Mendelian pattern of inheritance (Brues 1975, Byard 1981, Byard& Lees 1981), with a few major genes of dramatic effect and additional modi-fier genes (Sturm et al. 2001). Because pigmentation is a trait determined by the SKIN AND SKIN COLOR synchronized interaction of various genes with the environment (John et al. 2003),determination of the relative roles of variant genes and varying environments hasproven extremely challenging (Sturm et al. 1998). Classical genetic studies of in-heritance of human skin coloration have shed little light on the molecular basisof skin color variation, beyond showing that interbreeding between light and darkskin color phenotypes produces offspring of intermediate pigmentation (Robins1991; Sturm et al. 1998, 2001). As a result of recent advances in the understand-ing of the chemistry and enzymology of the biosynthesis of melanins, the geneticregulation of the many steps in melanin production is now beginning to be under-stood. Among the numerous mutations affecting melanocyte function in humanpopulations are the P-gene and members of the TYRP and SILV gene families,which direct the assembly and maturation of melansomes within melanocytes(Sturm et al. 2001). Investigation of the influence of these genes on skin pigmen-tation phenotypes is just beginning (Akey et al. 2001), however, and it remainsto be demonstrated whether polymorphism in these gene systems correlates withpigmentary differences between populations.
To date, the greatest scholarly attention has been focused on the melanocortin-1 receptor (MC1R) gene, which is the human homologue of the Agouti locus thatin mice regulates the production of the eumelanin and pheomelanin pigments ofthe coat (Barsh 1996, Rana et al. 1999). In humans, the synthesis of eumelanin isstimulated by the binding of α-melanotropin (α-melanocyte-stimulating hormone)to the functional MC1R expressed on melanocytes (Scott et al. 2002). The MC1Rappears to be one of the major genes involved in the determination of human hairand skin pigmentation, with MC1R polymorphisms in northern European popula-tions associated with red hair and fair skin, reduced tanning ability, and high riskof melanoma and nonmelanoma skin cancer (Healy et al. 2001, Scott et al. 2002,Smith et al. 1998). The MC1R locus is characterized by high levels of polymor-phism in light-skinned individuals outside of Africa and lower levels of variationin dark-skinned individuals within Africa (John et al. 2003, Rana et al. 1999).
This is opposite the pattern observed in most other loci, where Africans are mostpolymorphic (Shriver et al. 1997). The observed pattern of variation in the MC1R by Stockholm University - Library on 10/03/12. For personal use only.
suggests that different selective pressures among individuals with dark and lightskin have shaped the genetic variation at this locus, with functional constraints Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org operating to limit variation in African populations (John et al. 2003). The numer-ous MC1R polymorphisms in light-skinned individuals were originally thoughtto denote relaxation of selection for production of eumelanin outside of tropicallatitudes (Harding et al. 2000). A reinterpretation of these data indicates, however,that adaptive evolution for sun-resistant MC1R alleles began when humans firstbecame hairless in tropical Africa, and that human movement into the less sunnyclimes of Eurasia favored any mutant MC1R allele that did not produce dark skin(Rogers et al. 2004). Recent study of the MC1R promoter function casts doubt onthe relaxation hypothesis and suggests instead the possible action of purifying ordiversifying selection on some MC1R variants in Asian and Europeans (Makovaet al. 2001). A study comparing populations in southern Africa of Bantu-language speakers and San people showed some variation in MC1R sequences, but investi-gators concluded that although some MC1R mutants are tolerated in Africa, thisgene has been the object of purifying selection and has played an important rolein the maintenance of dark pigmentation in Africans (John et al. 2003). The pres-ence of higher levels of MC1R variation in dark-skinned populations subjected tolower levels of UVR in southern Africa (as compared to equatorial Africa) sup-ports the notion that number and kinds of MC1R variants are strongly influencedby purifying selection (John et al. 2003). Further genetic studies of more Africanpopulations are needed to determine if the great diversity of skin color observedin populations in sub-Saharan Africa (Relethford 2000) can be related to specificpatterns of MC1R or other polymorphisms that evolved in response to the region'sconsiderable heterogeneity of UVR and precipitation regimes (Chaplin 2001).
The study of the genetics of human skin pigmentation is still in infancy, and much remains to be learned about the levels, effects, and interactions of polymor-phisms in the loci influencing skin color phenotype. The production of eumelaninis under strong functional constraint as a result of natural selection in regions ofthe world with high levels of UVR (Sturm et al. 2001), and there is increasingevidence that at least MC1R variation is an adaptive response to selection for dif-ferent alleles in different environments (Makova et al. 2001, Sturm et al. 2001).
From what is known of the timing and nature of movements of groups of earlyHomo species and of Homo sapiens in prehistory, it appears that populations ofhumans have moved in and out of regions with different UVR regimes over thecourse of thousands of years. This finding would suggest that natural selectionwould have favored the evolution of dark and light skin pigmentation in disparateplaces at different times, resulting in the independent evolution of dark and lightskin phenotypes and possibly involving recurrent episodes of repigmentation anddepigmentation (Jablonski & Chaplin 2000). This phenomenon would have beenpronounced in the early history of the genus Homo (including the early history ofHomo sapiens) when cultural buffers against the environment were less effectiveand sophisticated.
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SKIN COLOR AND RACE
Skin color is the most obvious visible attribute of the human body. It has been the primary characteristic used to classify people into Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org purportedly genetically distinct geographic groups or "races." The biological ba-sis of skin pigmentation in humans, however, strongly argues against its use as adiagnostic classificatory trait. Critical examination of the distribution of skin colorphenotypes in humans leads to the conclusion that skin pigmentation is adaptive,and its evolution in specific populations has been strongly influenced by the envi-ronmental conditions (the UVR regimes, in particular) of specific places. Highlyadaptive phenotypic characteristics of organisms are of little use in classificationbecause they are subject to homoplasy (parallelism or convergent evolution) andare extremely labile. Emerging genetic evidence indicates that the evolution ofpigmentation genes has been driven by purifying and diversifying selection work-ing to produce adaptive responses in different environments (Makova et al. 2001, SKIN AND SKIN COLOR Rogers et al. 2004, Sturm et al. 2001). This evidence indicates that similar skincolors have evolved independently in human populations inhabiting similar en-vironments. Darkly or lightly pigmented skin, therefore, provides evidence onlyabout the nature of the past environments in which people have lived, renderingskin pigmentation useless as a marker for membership in a unique group or "race." The continued social importance of skin color in human affairs reflects a high degree of sensitivity to skin color, brought about by historic and complex culturalattitudes toward skin colors (Ehrlich & Feldman 1969, Lewontin 1995, Parra et al.
2003). The apparent existence of a difference between so-called human races andsubgroups is predicated on an exaggerated perception and heightened sensitivityto a visually obvious attribute of human appearance. The enormity of this bias isrevealed when the small amounts of actual genetic variation within purported racialgroups are revealed (Lewontin 1995, Marks 2002). Overall, human populations areremarkably similar to one another, with the greatest fraction of human variationbeing accounted for by differences between individuals (Lewontin 1972, 1995;Marks 2002). This collective evidence militates that the concept of biologicalrace be abandoned and publicly disavowed (Lewontin 1995, Marks 2002, Muir1993). Race thus emerges as a cultural construct devoid of explanatory power anddestructive of human and social relations (Lewontin 1972, 1995; Muir 1993).
The past decade has witnessed a tremendous advance in the understanding of theevolution of human skin and especially skin color, largely as a result of two phe-nomena. First is availability of remotely sensed environmental data that permithypotheses about the adaptive value of properties of skin to be thoroughly tested.
Second is the proliferation of studies of the molecular genetics of the skin colorthat are permitting new insight into the origins of skin color phenotypes and themechanisms by which they have evolved. Growth is anticipated in both of these by Stockholm University - Library on 10/03/12. For personal use only.
areas, and great potential exists for their interaction, in particular for the testing ofhypotheses of adaptation through the simultaneous and detailed study of patterns Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org of phenotypic, genotypic, and environmental variation, such as has been done inthe study of butterfly pigmentation (Watt et al. 2003). The study of the evolution ofhuman skin and skin color will also be advanced by the documentation of differen-tial survival of well-defined phenotypes and genotypes in different environmentalregimes through the use of epidemiological data, as has been undertaken recentlyin the study of geographic patterns of melanoma (Garland et al. 2003).
Continued study of the evolution of human skin and skin color is important not only to our realization of a more complete picture of human evolution, butalso it is important because the skin is involved in so many aspects of human well-being. Many humans now live in regions far distant from their ancestral homelands,but they retain a covering of skin adapted to remote Pleistocene conditions. Asis evidenced by modern rates of skin cancer and vitamin D deficiencies, human behavior and culture are not perfect buffers against the effects of these majortranslocations. An appreciation of the many roles of skin will improve human healthand attitudes toward diversity and will promote the fundamental understanding ofwhy it is that people look the way they do.
Conversations and discussions with many colleagues in the months and yearsleading up to the writing of this review greatly enriched the content of this paper.
These include Walter Alvarez, Carol Boggs, Carol Bower, C. Loring Brace, JimCleaver, Paul Ehrlich, Roberto Frisancho, Cedric Garland, Maciej Henneberg, thelate Gabriel Lasker, Charles Oxnard, Bill Nye, Lynn Rothschild, Donald Tyler, andWard Watt. I thank Rachel Wolf for helping to assemble references. Figures 1, 2,3, and 6 were produced by Jennifer Kane, whom I thank for her skillful renderingsand patient revisions. I thank George Chaplin for producing Figures 4 and 5, and formore than ten years worth of challenging and inspiring discussions on the evolutionof human skin and skin coloration. The spatial analyses and maps summarized herewere made possible by generous donations of geographical information systemssoftware to the California Academy of Sciences from Charles Convis and theConservation Program of the Environmental Systems Research Institute (ESRI).
The Annual Review of Anthropology is online at http://anthro.annualreviews.org
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and photosensitivity estimated from UV- Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org



HI-RES-AN33-24-Jablonski.qxd 9/8/04 1:34 AM Page 1 SKIN AND SKIN COLOR Figure 3 Human skin coloration as predicted from multiple regression formulae. See text
for discussion.
by Stockholm University - Library on 10/03/12. For personal use only.
Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org Figure 5 The potential for synthesizing vitamin D3 in the skin relative to levels of annual
average UVMED. The highest UVMED levels are indicated in deep violet, with incremen-
tally lower levels indicated in shades of red, orange, yellow, green, and gray. Zone 1 (area
without hachure enclosing the tropics
) represents the region with adequate UVR throughout
the year to catalyze vitamin D3 synthesis. Zone 2 (vertical hachure) represents the area in
which there is insufficient UVR during at least one month of the year to produce vitamin D3.
Zone 3 (cross-hatched area) represents the region in which there is insufficient UVR aver-
aged over the entire year to photosynthesize vitamin D3. See text for further description.
Annual Review of Anthropology Volume 33, 2004 The Whole Person and Its Artifacts, Marilyn Strathern The Archaeology of Ancient State Economies, Michael E. Smith Political Economic Mosaics: Archaeology of the Last Two Millennia in Tropical Sub-Saharan Africa, Ann Brower Stahl Primary State Formation in Mesoamerica, Charles S. Spencer and Elsa M. Redmond The Archaeology of Communication Technologies, Stephen D. Houston Origins and Development of Urbanism: Archaeological Perspectives, George L. Cowgil Early Dispersals of Homo from Africa, Susan C. Ant´on and Carl C. Swisher, III Social Status and Health in Humans and Other Animals, Robert M. Sapolsky The Peopling of the New World: Perspectives from Molecular by Stockholm University - Library on 10/03/12. For personal use only.
Anthropology, Theodore G. Schurr The Evolution of Human Skin and Skin Color, Nina G. Jablonski Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org LINGUISTICS AND COMMUNICATIVE PRACTICES
Language Revitalization and New Technologies: Cultures of Electronic Mediation and the Refiguring of Communities, Patrick Eisenlohr New Technologies and Language Change: Toward an Anthropology of Linguistic Frontiers, Susan E. Cook Language Birth and Death, Salikoko S. Mufwene Talk and Interaction Among Children and the Co-Construction of Peer Groups and Peer Culture, Amy Kyratzis INTERNATIONAL ANTHROPOLOGY AND REGIONAL STUDIES
Christianity in Africa: From African Independent to Pentecostal-Charismatic Churches, Birgit Meyer Anthropology in Area Studies, Jane I. Guyer Music and the Global Order, Martin Stokes The Globalization of Pentecostal and Charismatic Christianity, Joel Robbins Hang on to Your Self: Of Bodies, Embodiment, and Selves, Steven Van Wolputte The Body Beautiful: Symbolism and Agency in the Social World, Erica Reischer and Kathryn S. Koo Inscribing the Body, Enid Schildkrout Culture, Globalization, Mediation, William Mazzarella The World in Dress: Anthropological Perspectives on Clothing, Fashion, and Culture, Karen Tranberg Hansen Anthropology and Circumcision, Eric K. Silverman Thinking About Cannibalism, Shirley Lindenbaum THEME I: THE BODY AS A PUBLIC SURFACE
Hang on to Your Self: Of Bodies, Embodiment, and Selves, Steven Van Wolputte The Body Beautiful: Symbolism and Agency in the Social World, Erica Reischer and Kathryn S. Koo Inscribing the Body, Enid Schildkrout The World in Dress: Anthropological Perspectives on Clothing, Fashion, and Culture, Karen Tranberg Hansen by Stockholm University - Library on 10/03/12. For personal use only.
Anthropology and Circumcision, Eric K. Silverman Annu. Rev. Anthropol. 2004.33:585-623. Downloaded from www.annualreviews.org The Evolution of Human Skin and Skin Color, Nina G. Jablonski THEME II: NEW TECHNOLOGIES OF COMMUNICATION
Language Revitalization and New Technologies: Cultures of Electronic Mediation and the Refiguring of Communities, Patrick Eisenlohr Music and the Global Order, Martin Stokes New Technologies and Language Change: Toward an Anthropology of Linguistic Frontiers, Susan E. Cook The Archaeology of Communication Technologies, Stephen D. Houston Culture, Globalization, Mediation, William Mazzarella Cumulative Index of Contributing Authors, Volumes 25–33 Cumulative Index of Chapter Titles, Volume 25–33 An online log of corrections to Annual Review of Anthropologychapters may be found at http://anthro.annualreviews.org/errata.shtml by Stockholm University - Library on 10/03/12. For personal use only.
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Equine Drugs & Medications Presented by Kathy Ott, DVM – Cleary Lake Veterinary Hospital December 13, 2010 A) Commonly Used Drugs 1) Anti-inflammatories (NSAIDs) 2) Antibiotics 3) Sedatives 4) Steroids Therapeutic Hormonal 5) Muscle Relaxants 6) Antihistamines 7) Blocking Agents 8) Reproductive Drugs 9) Anti-ulcer Drugs 10) Eye medications 11) Dewormers 12) Topicals 13) Diuretics 14) Miscellaneous