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Short Review
Development of different human skin colors: A review highlightingphotobiological and photobiophysical aspects
Asta Juzeniene
a,
*
, Richard Setlow
b
, Alina Porojnicu
c
, Arnfinn Hykkerud Steindal
a,c
, Johan Moan
a,d
a
Department of Radiation Biology, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, Montebello N-0310 Oslo, Norway
b
Biology Department, Brookhaven National Laboratory, Upton, NY 11973, USA
c
Centre for Theoretical and Computational Chemistry, Department of Chemistry, University of Troms
ø
, 9037 Troms
ø
, Norway
d
Institute of Physics, University of Oslo, Blindern 0316 Oslo, Norway
a r t i c l e i n f o
Article history:
Received 18 August 2008Received in revised form 10 February 2009Accepted 24 April 2009Available online 3 May 2009
Keywords:
Skin colorSolar radiationVitamin DSkin cancerFolates degradation
a b s t r a c t
Skin color has changed during human evolution. These changes may result from adaptations to solarultraviolet radiation (protection of sweat glands, sunburn, skin cancer, vitamin D deficiency, defenceagainst microorganisms, etc.), and/or sexual selection. Migration to areas with high levels of UV is asso-ciated with skin darkening, while migration to areas with low levels has led to skin lightening. However,other factors may have played roles. Temperature andfood have probably been secondary determinants:heatexchangewiththeenvironmentisdependentonambienttemperature,andahighintakeoffoodrichinvitaminDallowsadarkskincolortopersistevenatlatitudesoflowUVlevels,asexemplifiedbyInuit’sliving at high latitudes. Future studies of human migration will show if skin lightening is a faster processand has a higher evolutionary impact than skin darkening. Maybe due to that some American Indianshave kept a relatively light skin although they live under the equator.The following hypotheses for skin darkening are reviewed: shielding of sweat glands and bloodvesselsin the skin, protection against skin cancer and overproduction of vitamin D, camouflage, adaptation todifferentambienttemperatures, defenseagainstmicroorganisms, protectionagainstfolatephotodestruc-tion. Hypotheses for skin lightening are: sexual selection, adaptation to cold climates, enhancement of vitamin D photoproduction, and changing food habits leading to lower intake of vitamin D. The geneticalprocesses behind some of the changes of skin color will be also briefly reviewed.
Ó
2009 Elsevier B.V. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 942. The origin of humans and their earliest skin color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 943. Hypotheses for skin darkening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 943.1. Protection of sweat glands and cutaneous vasculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 943.2. Skin cancer protection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 953.3. Protection against vitamin D overproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 953.4. Camouflage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 953.5. Defense against microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 953.6. Protection of folates in the blood. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 954. Hypothesis of skin lightening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 954.1. Sexual selection and sexual dimorphism in human skin color. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964.2. Adaptation to colder climates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964.3. The vitamin D hypothesis for skin lightening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964.4. Genetic drift. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 965. The genetics of skin color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 976. The introduction of agriculture and its relation to vitamin D and the Indo-European language . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 977. Health effects of vitamin D . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
1011-1344/$ - see front matter
Ó
2009 Elsevier B.V. All rights reserved.doi:10.1016/j.jphotobiol.2009.04.009
*
Corresponding author. Tel.: +47 22935113; fax: +47 22934270.
E-mail address:
asta.juzeniene@rr-research.no(A. Juzeniene). Journal of Photochemistry and Photobiology B: Biology 96 (2009) 93–100
Contents lists available atScienceDirect
Journal of Photochemistry and Photobiology B: Biology
journal homepage:www.elsevier.com/locate/jphotobiol
8. Skin lightening and skin darkening. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98Acknowledgement. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98
1. Introduction
The ability to change skin color has been of crucial importancefor human evolution. Fluence rates of solar radiation and spatialand temporal changes of the spectral composition of this radiationaremajordeterminantsforthisevolution,whichhastakenplaceinperiodswhenhumans havemigratedor changeddiet. Anumberof hypotheses have been proposed for skin color adaptations. Thesewillbebrieflylistedanddiscussedinthepresentreview. Emphasiswill be put on photobiological and photobiophysical aspects.
2. The origin of humans and their earliest skin color
When the physical characteristics of the environment change,the individuals who are best adapted to the new conditions havea survival advantage. Over many generations, evolution by naturalselection will lead to changes in the genetic and phenotypic com-position of the species. In fragmented environments, some mem-bers of the species may adapt better to different environmentalcircumstances than others. This may eventually lead to the forma-tion of new species[1].During the last 15–10 million years there has been a cooling of the global climate, mostly expressed as a drying close to the equa-tor[2]. Archeological and molecular evidences suggest that com-mon ancestor of humans diverged about 6–7 million years ago inAfrica[3–5]. One of the oldest known hominids from that timewas found in Chad[3,6]. He may have walked upright[4,7]. The
African apes did probably change less than the human ancestors[5]. They have, and probably had, light skin under their dark hair.Skin in areas with little hair is light, but turns brown and getsfreckles in the sun[8]. Many researchers believe that 7 millionyears ago the human ancestors resembled chimpanzees, as theyappear today, with respect to characteristic features of hair andskin[8].One of the oldest known human skeletons belongs to ‘‘Lucy”,who lived in East Africa more than 3 millions years ago[9]. Later,1.5 millions years ago, the ‘‘Turkana” boy lived in the same area[9,10]. He had longer legs than ‘‘Lucy”. The hot sun of Africa mayhave led to modifications of the skin of early humans in order toavoid overheating of their brain[11]. The dense capillary networkin the brain assures that its temperature closely follows arterialtemperature and is controlled through systemic thermoregulation,independent of head surface temperature[12]. The brain can func-tionoptimallyonlywithinanarrowrangeofphysiologicaltemper-atures. To reduce the chance of overheating, early humansprobably lost most of their body hair and developed sweat glands[13]. Furthermore, bacteria and fungi are easier to fight in a hair-less skin[14]. However, this may not be correct since we still havehair on our heads and on other vital body areas.Before about 1.8 million years ago human evolution occurredonly in Africa. Afterwards, humans migrated out of Africa for thefirst time and probably populated Asia first and Europe somewhatlater,inhabitingnon-equatorialregionsforthefirsttime[15].Fig.1
is a sketch of one of the models for the later part of human evolu-tion[16].Fig. 2demonstrates the relationship between mean ge-
netic diversity of human populations computed on the basis of autosomal microsatellite markers and their geographic distancesin km from East Africa[17]. This figure shows genetic evidencedocumenting much later migrations out of Africa, only about50,000years ago[17]. These migrations lead to the spread of mod-ern humans (Homo sapiens) throughout the world, and, as theyspread, they largely replaced other human species, such as Nean-derthals, whose ancestors had migrated from Africa 1.8 millionyearsago.Thisisthemigrationwhichisrelevantforunderstandingthe present-day patterns of skin color.
3. Hypotheses for skin darkening
At least six hypotheses have been proposed for skin darkening:(1) protection of sweat glands and cutaneous blood vessels, (2)protection against skin cancer, (3) protection against vitamin Doverproduction, (4) camouflage, (5) combating microorganisms,and (6) protection of vital structures and molecules such as folatesin the blood.
3.1. Protection of sweat glands and cutaneous vasculature
The strong African sun can easily damage sweat glands andblood vessels in a naked skin. Thus, thermoregulation will be im-paired, and development of a dark, protective skin color may havebeen inevitable[18].Fig. 3shows the characteristics of different
humanskintypes[19]. Beforeitgetsburnt,darkskintoleratessev-eral times more solar radiation than light skin does[20,21]. The
Fig. 1.
Fig. 2.
A. Juzeniene et al./Journal of Photochemistry and Photobiology B: Biology 96 (2009) 93–100
melanin is produced by melanocytes in the basal layer of the epi-dermis, from where it moves upwards as the basal cells divideand migrate to the stratum corneum, and, thus, protects all layersof the skin, as well as the blood vessels under it against sun dam-age[21–23]. However, it is a paradox that dark skin absorbs moresolar radiation and gets warmer than light skin does[24].
3.2. Skin cancer protection
The hypothesis that the main purpose of a dark skin color is toprotect against skin cancer is rather unlikely, because skin cancerusually develops late in human life, after the reproductive age[25–27], which was low for early humans[28]. The incidence rate
of all types of skin cancer increases rapidly with age[25–27].Furthermore,itispossiblethatolderindividualsmayhelptoin-crease the overall success of reproduction of their kin with theirknowledge or by providing for them. Individuals who remain aliveand escape skin cancer would be able to help their family. Thismightleadtosome selectionfor resistanceagainstdevelopingskincancer.
3.3. Protection against vitamin D overproduction
In 1967 Loomis proposed that a dark skin color had developedtopreventagainstvitaminDintoxication[29]. Alreadyatthattimeit was known that solar radiation, notably at equatorial fluencerates, was an extremely efficient vitamin D producer and that highdoses of vitamin D might have toxic effects[29]. This proposal iswrong because once previtamin D
3
is formed from 7-dehydrocho-lesterol in the skin, it either can isomerize to vitamin D
3
or absorbUVB radiation and isomerize into biologically inactive products,outofwhichlumisterolisthemostabundantone[30].Forthisrea-son vitamin D intoxication from sun-exposure has never been ob-served[31].
3.4. Camouflage
Camouflage plays a vital role for the survival of some animals,and for this purpose melanin is used[32]. Melanin pigments canget darker through a reversible, photochemical process or throughspatial rearrangements of melanin structures. In human skin suchrapid darkening is called immediate pigment darkening, IPD. Ittakesplace withinminutesuponexposureto UVAandvisibleradi-ation, reaches a maximum within 1–2h and then fades[33–37].IPDismostpronouncedinindividualswithadarkbaseline(consti-tutive) pigmentation[34]. No photoprotective effects of the IPD,such as less skin cancers or sunburns, have been observed[36].The evolutionary significance and the biological role of such dark-ening for humans can at present only be speculated on[35–37].The early humans would have had to rely on concealment duringhunting[38]. Maybe IPD acted as camouflage and led to decreasedvisibility in the sun?
3.5. Defense against microorganisms
Melanin producing cells may have immunological functions,and some scientists think that melanocytes should be regardedas true members of the immune system[39]. Bacteria and fungiare more abundant and troublesome in tropical regions than incold regions. This supports the defense hypothesis, since peopleliving in tropical regions usually have more melanin and a darkerskin color than people living in colder regions at high latitudes[39].Studies of populations living at low latitudes and high alti-tudes with a cold climate, as in Tibet, may help to evaluate thishypothesis.
3.6. Protection of folates in the blood
Theso-called‘‘folate-hypothesis”fordarkeningof skinwaspro-posed in 1978 by Branda and Eaton[40]. Folates are vitamin Bderivatives of utmost importance in DNA synthesis; i.e. in the bio-synthesis of pyrimidines. Folate deficiency leads to infertility inmen and neural tube defects of babies and other disorders of evi-dent evolutionarysignificance[41–46]. Since a substantial fractionofthefolatesinhumansareflowingintheblood,eitherinserumorin red cells, and since folates absorb and can be degraded by UVBradiation, and since blood is flowing in dermal microvessels thatcan be reached by solar UVB, brown or dark skin may have beendeveloped to protect folates[8,40,47]. Some, but not all, in vivoinvestigations aimed at elucidating this question, indicate that in-tensesolarradiationorartificialUVBradiationasusedinthetreat-ment of psoriasis, can lead to folate degradation, similar to what isfound in test tubes[48,49]. Since folate antagonists, such as meth-otrexate, are used in cancer therapy with the hope that they canslow down tumor growth selectively[50], we have proposed thatthe observed variation of internal cancer prognosis with seasonof diagnosis can be related to folate photodegradation in the sum-mer season[41]. Thus, prognosis is best when treatment starts insummeror autumn[51–54]. However, wefoundnodecreaseof fo-late levels in summer in Norway, and proposed that the prognosiswas more likely to be related to vitamin D levels, which are signif-icantly larger in the summer season than in the winter season[51,55].Morework,bothmeasurementsofpenetrationofUVandvisiblelight to dermal vessels of dark and light skin and studies of folatephotobiology are needed before the ‘‘folate hypothesis” can be fi-nally evaluated.
4. Hypothesis of skin lightening
From the fact that skin lightening has occurred several times inthe evolutionary history of humans[8], we can conclude that thisprocess is an important factor in evolution. Four main hypothesesfor skin lightening will be reviewed: that of the hypothesis of sex-ualselection,thatofadaptationtocolderclimatesthroughchangesof heat exchange with the environment, that of need of more effi-cientvitaminDphotosynthesisathighlatitudesandthatofgeneticdrift.
Fig. 3.
Different skin types (adapted from Ref.[19]). Human skin of all types havethe same total number of melanocytes, but the number, size, aggregation anddistribution of melanosomes within the keratinocytes vary. Melanosomes inkeratinocytesofdarkskinarelarge,heavilypigmentedanddistributedindividually,whereasthoseinkeratinocytesofCaucasianskinaresmaller,havelessmelaninanddistributed in clusters. More melanosomes are in dark skin.
A. Juzeniene et al./Journal of Photochemistry and Photobiology B: Biology 96 (2009) 93–100
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