Differences in Human Pigmentation: Measurement, Geographic Variation, and Causes* G

DIFFERENCES IN HUMAN PIGMENTATION: MEASUREMENT, GEOGRAPHIC VARIATION, AND CAUSES* G. AINS WORTH HARRISON, PH.D.

INTRODUCTION affected b y o nly a s ingle pair of ge nes. Since most of the genetic studies of populati T he racial differences in pi gmentation t hat have on differences in pigmentation relate to skin color, I been studied by ant hropolog ists are t he readily shall , for the most part, confine my d isc ussion to it. observable o nes t hat occur in skin, ha ir, a nd t he eye. T he co lor of t h ese structures is due to a THE MEASUREM ENT OF SKIN CO LOR number of factors, but variation in them, espe For a long time, t he study o f skin co lor variation cia lly as it occurs between popu l at i m~s, ~p pe ~ r s to. in fi eld sit uations was beset with difficult prob be largely due to the amount and dtstn butwn of lem of m easurement. At first, measurements involv t he pigment melanin. This was first _most firml y_ ed visual co mpari son with sets of co lor standards such established fo r skin in t he now classtcal work of as the Va n Luschan t iles or the colored papers Edwards and Duntley (1939) and has subsequently used by Gates ( 1949) . These were hi ghly unsatisfactory been demonstrated fo r hair and the iris diaphragm not onl y because of the subjectivity of of the eye. Hair color, however, may be influenced visual matching, but also because of t he necessity by a totally different pigment, t ri chosiderin, which of imposing discrete units upon a natural co is concerned with the red shades (Barnicot, 1956a, ntinuum. Furthermore, it was a lmost impossible to b). Histologic (Gates and Zimmermann, 1953; m atch t he texture of the skin with the texture of ei Gates, 1961) a nd electron microscopic studies t her tiles or papers; t hose who have used t hese (Barnicot et a l. , 1955; Birbeck et al. , 1956) have tech niques know t he difficul ty of fin ding a n_y show n h ow t he mela nin pigment is organized into corre spondence between the standa rds a nd discrete encapsul ated gra nules in skin and ha ir. s ~m color. H arrison and Salza no (1966) , workmg wtth South Little attention has been given recently to t he basis American Indian populations, fou nd li tt of eye color differences, but it has been established le corre spondence between measurements m t hat much of t he color vari ation in the iris is due ade with Van to Luschan tiles and t hose m different a moun ts of phys ical refr ade with a s pectropho action which tometer. depend upon how t he melanin is di stributed in t he The sit uation was so t issues (Coon et a l. , 1950). mewhat improved by the use of the Milton Bradley color top In the development o f skin color, melanin is in which segments of four colored papers-black, wh synthesized solely by melanocytes in the basal ite, red. and yellow-were arra nged in differin g amoun layer of t he epid ermis from which pigment e nters ts so that wh en t he top was spun t he blendin t he neighboring epidermal cell s of t he stratum g of the colors produced a visual range varying Malpighi (Bi llingha m and Medawar, 1948). There fr om dark to li cr ht brow n . This at least presented a co fore, in a ny consideration of racial va ri ation and ntinuous s;ale of measurements, but it still retain ed the the ge netics of skin color, the ul timate concern ts fundamental disadvantage of visual subjectivi t he hereditary fa ctors that regulate melanin sy n ty. H ow to co mbine t he amounts of t he t hesis a nd distribution by the skin melanocytes. four color discs, which corresponded to any particula r However, the activit ies of these melanocytes them skin color, into a s ingle measurement o f t hat selves are a ffected by numerous external factors, color wa never adequately solved . At first, t he exte especia ll y exposure to ultraviolet radiation . Hence nt of expos ure of t he black disc was taken skin color in man i s a typical, quantitatively as the measurement, but it was later show n that th varying character dependent wit hin and between e red disc itself contained black pi gment a nd t h populations upon both hered itary an? envir at allow on ance had to be made for mental factors and poss tbly o n a t his. n mteractton The fi eld of stud between them. y o f skin color vari ation on a geogra phic basis has been revo~ut Al t hough ha ir a nd eye color appear to be less i o ni ze d in t he last decades by the development of t he portable reflect affected by norma l enviro nmental factors, t hey are ance spectrophotometer. This instrument in£1 uenced by age and sex differences; and ha tr oYer came practicall y a ll the earli er problems color, of course, is often artifi cia lly c hanged. Even by provid ing a measure o f color on a continuous after a ll owance has been made for t hese factors, _ and objective scale of measurement. A vane_ty both tend to show quantitative variations wit hin of such instruments have been used in [i eld stud1 es, but populations. Red ha ir (Reed, 1952) a nd i he more all work on essentiall y t he sa me principle. marked differences in eye color such as blue versus Li ght is e mitted from a standa rd source brown (Brues, 1946) behave as t hough t hey were and passes on to the surface of the skin t h1:ough any one of a series of co lor fil ters, • From the An thropology Laboratory , D wh1ch typtcall y samp l~ epa rtment of t he visual Human Anatomy, Un iversity of Oxford, Oxford, Eng spectrum. The re11 ected light is the11 land . picked up by a photocell a nd measured on a 418 DIFFERENCES IN HUMAN PIGMENTATION 419

galvano meter unit . The a mount of li ght refl ected melanin concentration, it probably arises from from t h e skin is compared with t hat ref1 ected from different li fe styles and different exposure to sun a pure white standard such as magnesium oxide or light. Age differences t hat have been reported magnesium carbonate, or in some cases with a (some rather complicated ) have been assumed to more robust standard which itself has been ca li be related to hormonal balance. brated against what is regarded as 100% ref1 ect The use of spectrophotometers hi ghlights some ance. T he two photometers most commonly used of the problems inherent in the measurement of in field studies are t he EEL (Weiner, 1952), large ly a ny continuously varin g t rait, for one seldom has used by British, Cont in ental, a nd Indian investiga t he opportunity to measure t he same c haracter tors, and the P hotovolt (Lasker, 1954), used by directly on such totally different scales as t hose orth Ameri cans. These instruments are obtaina afforded b y t he various wavelengths of t he differ ble with many different fi lters. The EEL is nor ent fi lters. Within most popul ations, t he variation mally s upplied with a standard set of nine. Photo in skin color tends to be sli ght and when graph volt offers a considerable variety from which to ically plotted does not detectably depart from a choose. Unfortunately, because t he filters differ Gaussian distribution. Where t he within-popula not only in their dominant wavelength but also in tion variabili ty is high (e.g., in hybrid groups and many other optical properties, it is difficul t to between p arental populations differing markedly mak e direct comparisons between t he two instru in color), a non-Gaussia n distribution may be due ments. Filters have been designed for many spec i to other factors tha n the scale of measurements, fic purposes; for example, for color analys is a nd, such as the differing contributions of t he parental like t h e set of nine provided wi th the EEL instru populations o r assortative mating. men t, for m easuring ref1ecta nce over a narrow Only when populations differing markedly in waveband. In using t hese instruments, one must skin color a re studied on t he diffe rent scales of never forget exactly what is being measured. wavelength d oes the problem of scale itself become Typical refle ctance curves measured with t he clear. For example, Figure 2 compares a European EEL instrument are shown in Figure 1. Refl ectance whi te population, an African black population, values depend not only on t he particul ar instru and an F 1 hybrid population in terms of t he ment a nd fi lter u sed, bu t a lso body s ite. Most reflectance of blue light with that of red li ght. Note investigators measure at one or more of t hree that one wou ld have to come to totally diffe rent sites- t h e fo rehead, t he inner aspect of t he fore conclusions about t he potence of t he genes on the arm, a nd t he inner aspect of the upper a rm two scales. This is clearly a matter of great concern (generally t he left); the latter is most commonly wh en t he nature of t he hereditary difference be used because it is easily accessible, is protected tween populations is bein g a na lyzed. somewhat more t han t he others f rom exposure to sunlig h t, and is less likely to be tanned. There is a GEOGHAP HI C VAR IAT ION IN SKI N COLOR correlati o n between retlection at t hese t hree sites Among a ll t he quantitatively varying human and at other pa rts of the body t hat have been tra its, skin color is remarkable in t hat t he within measured (Garnet a!. , 1956 ; Leguebe, 1961). But population va riabili ty is small compared with t hat t he correlation i s by no mea ns exact, partly, but between populations. Not only is t here frequently not entire ly, because of different ia l tanning. More no overl ap between the distribution in different over, in a ny genetic study the results ca nnot be populations, but a lso t here is after a marked range assumed to apply to parts of the s kin surface not of separation between the I ightest individua l in one examined. In populations with li ttle variability group and t he darkest in a nother. Unlike t he within t he group, a sex difference has ge nerall y patterns of hair a nd eye color, those of skin tend to been found, with women tending at a ny g ive n vary on a world -wide scale. In the former, most of wavele n gth to show hi gher refl ectance t han m en. t he a pparent vari ation occurs when populations of T his is l argely due to such factors as skin texture European descent are co mpared with each other and b lood supply, but even when it is due to a nd wit h those elsewhere; differences in sk in color are more on a continental basis. S kin color and ~ 70 latit ude a re o bviously co rrelated: t he a mounts of ~ 10 20 30 40 R 425 m}J ~ 50 ~' ~ 30 ~ ~ Q. 10

40 R685 m}' 400 500 600 700 WAVELENGTH m}J F IG. 2. Co mparative s imilari ties of Afri ca ns, Euro pea ns, and F, hyb rids as measured at two different F IG. 1. S kin color refl ectance curves as measured wi th wave lengths with an EEL refl ectance spectrophotometer. an EEL spectrophotometer. Percent refl ectance is pl otted fo r eac h wavelength. 420 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY

pigment tend to diminish from tropical zo nes to sumed that African and at least Northwest Euro temperate ones a nd to increase again in arctic pean populations can be regarded as being essen populations. Alt hough sha rp breaks in this pattern tially homozygous for sets of alternative ge nes at occur, the distribution ca n be broadly categori zed the skin color loci. T his is not an unreasonable as clinal and corresponds to the natural l evels of assumption, at least as far as the major ge ne loci t he incidence of ul traviolet radiation. The clina l involved are conce rned, in view of the lack of distribut ion i s not inconsistent with the marked overlap and marked separation in the skin color differences between some populations, because distributions o f Africans and Europeans. It i , although neighborin g populations tend to be simi however, worth noting that between the various lar to one a nother, the overall diversity is great. Europea n a nd African populations compounded in Population d ata obtained with spectrophotometers the American Negro, differences in skin color h ave are still very limited. The Ta ble summa ri zes the be en r ecorded (Table), so me parts of which are available mean values recorded with a red fil ter . almost certainly ge netic in ori gin. Related to this is Some of t he photovolt va lues ca n be converted by the difficulty o f estimating the degrees of h ybridi the cali bration formulae of Garrard eta!. (1967) to zation. Many different European and African EEL values and vice versa. groups, not to men tion the Amerindian contribu tion, have been invo lved to uncertain degrees in THE GENETICS OF S KIN COLOR VA RIATION the formation of the Ameri can Negro population. Most of the work on t he ge netic nature of Furthermore, the levels of hybridization within the population differences has been concerned with the America n Negro clearl y differ from region to re differences between p eo ple of Africa n and E uro gion, a nd there are problems arising from fo und er pean descent, probably because they represent the principle, drift, and diffe ring selection since the maxim 11 l differences between different geog raphic beginning of the formation of the hybrid popu la populations with no overlap in their distribution, tion. As a lready indicated, differences in the esti and there are many hybrid groups between them, mates of levels of intermixture profo undly affect especia lly in the New World. The earliest work was the nature of the model distributions. Stern also carried out by Davenport and Danielson (1913) on had to assume essent ially ra ndom mating within West India n groups. They concluded from pedigree the hybrids t hemselves ; a nd there is evidence, a ana lysis that two pairs of ge nes were responsible Stern points out in his ow n d ata and from other for African/European differences. Later Gates hybrid groups, that marriage is o ften assortative (1949, 1953), also using a pedigree approach on with respect to skin color. Because of t he long American Negro populations a nd employ ing his existence of t he American Negro hybrid pop ul ation colored paper standards, concluded that three sets and the impossibility of establishing genealogie of ge nes of uneq ual effect were involved. Hersko back to the original miscegenation, Stern had to vits (1926, 1930), usin g t he color top, made an assume that t he scale of measurements provided extensive study o f the American Negro on a by the color top was a ppropriate for a genetic population basis, and subsequently Stern (1953 ), analysis. The requirements of such a scale are that in a most important paper, reexamined these data there should be neither environmental/genetic in and co mpared the actual distribution of co lor in teraction n or in terl oc us interaction, or that such the population, as measured b y t he co mponents of interactions be know n a nd allowed for in the black in the color top, with the distributions to be estimation procedures. Unless there is some as yet expected when different numbers of equal and unexa mined relationship between scales of addi addit ive gene pairs a re in volved. T he freq uency of tive ge ne action and scales of evolu tionary change, African and European skin color ge nes in the there is no reason to suppose t hat conditions of Ameri can Negro, which are req uired f or calcu lat nonin teraction would be fulfill ed on a visual or ing t he theoretical distributions, were obtained reflectance-type scale. In principle it would seem from the estimates of the extent of the hybridiza just as likely, if not more so, that the genes a re tion as judged from gene frequencies in those acting in terms of mela nin concentration or rate of polymorphic systems that distin guish African from melanin synthesis. T he a ddition of a s mall amount European populations. On the basis that 30 per of mel a nin to a li ght skin would be strikingly cent of the ge nes in the American Negro are evident, but the a ddition of a s imilar a mount of derived from Caucasia n a ncestors, Stern first co n melanin to an already da rk skin might go • unno cluded that between four a nd six gene pairs were ticed. in volved in the pa rental skin color difference. More The problem of scale , at least fo r the EEL recently he (Stern, 1970) has used Reed 's revised spectrophotometer and the differences that distin estimate of 20 percent in termixture, and on the guish Europeans from Africans, was reso lved bY basis of this finds that models involvi ng t hree or Harrison and Owen (1964) in their study of Live; fo ur additive ge ne pairs best fit the observed pool hybrids. They were fortunate enough to find a distribution . hybrid population in the process of formation, in It is worthwhile considering t he various assum p which it was possible to identify first-generation tions upon whi ch these conclusions are based. hybrids between West Africa ns a nd local Liverpool First, Stern and a ll other investigators have as- Whites, first-generation backcrosses both to the DIFFERENCES IN HUMAN PIGMENTATION 421

TABLE M ean percentage refl ectance of red light in various populations (Measurements mainly on adult and subadult samples, on medial aspect of upper arm, and with an EEL spectrophotometer.)

Population Filter No. of Male No. of Female Reference D.W . m~< Males Mean Females Mean AFRICA Africa (South) Bantu Okavango Kuangali 685 50 21.7 38 22.0 Weiner et al. (1964) Bantu Okavango M 'Bukushu 685 15 22.6 23 22 .2 Weiner eta\. (1964) Bantu Xhosa 685 104 32.1 100 38.9 Wassermann & Heyl (1968) Hottentots 685 50 43.7 84 46.8 Weiner eta\. (1964) Bushmen 685 88 42.2 59 42 .8 Weiner eta\. (1964) Bushmen 685 42 42.5 46 43.6 Tobias (1961) Black Bushmen 685 13 28 .2 25 29.4 Wei ner eta\. (1964) South African White 685 108 63.5 109 64.4 Wassermann & Hey! (1968) Cape Coloured 685 103 49.2 107 52.1 Wassermann & Hey\ (1968) Cape Coloured 685 187 50.1 112 51.3 Wein er eta\. ( 1964) Rehoboth Bastaards 685 10 47.9 21 51.9 Weiner eta\. ( 1964) Africa (West) Yoruba' 685 100 23 .6 94 26.1 Barnicot (1958) Ibo' 685 52 28.2 Barnicot (1958) Nigeria (mainly N & E) 685 108 32.5 Ojikutu (1965) Dog on 685 27 31.4 19 36.7 Huizinga (1965) Africa (East) Ethiopia (Highlands) 685 43 31.4 13 35.7 Harrison et al. (1969) Ethiopia (Lowlands) 685 61 30.2 33 33.2 Harri so n et al. (1969) EUROPE English (Liverpool) 2 685 62.3 62.3 Harrison & Owen (1964) English (London)' 685 50 61.5 50 63.1 Barnicot (1958) Germany (German & 685 74 66.9 Ojikutu (1965) American White) American Negro 685 12 43.9 Oj ikutu (1965) West-African (Liverpool) 685 106 34.7 Harrison & Owen (1964) ASIA Jordon Chechen 685 23 55.0 7 51.9 Sunderland (1967) Druze 685 42 52.8 Sunderland (1967) Arab 685 30 52.2 3 48.0 Sunderland (1967) India Brahmin 685 100 49.7 Das & Mukherjee (1963) Brahmin 685 76 49.9 Biichi (1957) Brahmin 685 27 53 .6 Tiwari (1963) Kayastha 685 58 48.6 Biichi (1957) Kayastha 685 47 52.3 Tiwari (1963) Vaidya 685 19 50.7 Biichi (1957)

1 Measurements from t he forearm. 2 Sexes combined. • Found evidence for social class differences in skin colour-a phenomenon indicated in other data, but which may be entirely due to varying habits. 'Measurements involved an instrument calibration. • Measurements made with a Photovolt instrument. 422 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY

TABLE-Co ntinued

Filter No. of Male No. of Female Reference Population D.W. ml' Males Mea n Females Mean

India- Co nt. Va idya 685 8 5 1.1 Tiwari (1963) Ma har 685 100 41.3 Das & Mukherjee (1 963) Low Caste 685 40 44 .8 Bi.ichi (1957) Khatris 685 249 56. 1 238 56.4 Ka ll a ( 1969) Aroras 685 171 55.8 209 56. 1 Kall a ( 1969) Bado Gada ba 685 100 32.3 Das & Mukherjee (1963) Bareng Paroja 685 100 3l .8 Das & Mukherjee (1963) India ns 685 23 53.1 Tiwa ri (1963) Sout h Indians 650 22 40.0 Walsh (1963) Europeans 685 23 63.0 Tiwari (1963) Europeans 685 10 64 .2 Bi.ichi (1 957) Mixed Indians 685 71 52.0 Tiwari (1963) Paki stan 650 39 47. 1 Walsh (1963) Goa 650 4 8 39.6 Walsh (1963) Cambodia Vi etna mese 660 105 51.3 Carbonnel & Olivier (1966) Khmers 660 75 50.2 Carbonnel & Olivier (1966) Chinese 660 106 56 .6 Carbonnel & Olivier (1966) Hong- Kong Chinese 650 70 50. 6 Wa lsh (1963) Japan North 685 54 54 .1 50 55.7 Hulse (1967)' Cent ral 685 54 53.3 61 55.7 Hulse (1967) South-West 685 116 51.6 68 55.5 Hulse (1967) Tokyo 650 69 50.7 Wa lsh (1963) Philippines (Ma nila) 650 49 46.6 Wa lsh (1963) AU STRALASIA A ustralia Abori gines 650 41 1 3.3 Walsh (1963) Whi tes 650 19 57.8 22 58.5 Wa lsh (1963) N ew Guinea Goroka Asaria 650 38 24.7 Walsh (1963) Goroka Gahuku 650 36 29.1 Wa lsh (1963) M t. Hagan 650 47 28 .3 56 29.4 Wa lsh (1963) Port Moresby Hanuabada 650 55 34.3 Wa lsh (1963) AM E RI CAS Aguaruna ' 685 40 42.8 52 42.9 Weiner et al. (1963) Caingang 685 60 48.1 40 50 .7 Harrison & Salzano (1966) Guarani 685 23 47 .9 10 46.5 Ha rrison & Salzano (1966) Gua hibos' 575 100 24.6 Diaz Ungri a (1965) Brazilia n White 685 216 57.9 268 59.2 Harrison et a l. (1967) Brazilia n Negro 685 68 42.9 117 46.0 Harrison et al. (1967) Baha mi an N egro' 590 35 10. 6 35 13.1 Mazess (1967 ) Mex ican M estizo lnternado' 650 86 43.6 Lasker (1954) Mex ican M estizo P arachoan' 650 41 44.7 46 44.1 Lasker (1954)

African and t he European parents, as well as a matin g c ircle o f the African-derived h ybrids, and ce rtain number of second-ge neration hybrids. Un t he number of those whose ancestry co uld be fort unately, from the a nalytical point o f view, directly t raced b ack to the o nset of hybridization shortly after the establishment o f this hybrid was small. Nevertheless, Harrison and Owen were population a large West India n immigration oc a ble to test for the requirements of scale. The curred which co nsiderably expa nded the possible majori ty of the West Africans in Liverpool came DIFFERENCES IN HUMAN P IGMENTATION 423

from N igeria and we re of Yoruba descent, a nd and disc rimination of the EEL instrument ; if so, Harrison and Owen assumed that they, like the the transformations sui table fo r the Liverpool local Liverpoo l Whites, were homozygous fo r skin study wi ll probably be widely applicable. However, colo r genes. T herefore, it woul d be ex pected that in it would not be surprising if there were a general the absence of enviro nmental interaction, the environmental genotype interaction, since given var iability wit hin the Afri cans, t he Europeans, and any part icular exposure to ultraviolet radiation , the first-ge neration hybrids wo uld be entirely envi more melanin is likely to be produced by a geneti ronmental and of eq ual magnitude in the a bsence cally light-skinned person than by a ge netica lly of e n v i ronmental genotype interaction. But in dark-skinned one, espec ially since the melanin of stead t h ey fou nd that t his ex pectation was not the latter would shield the melanocytes fro m the realized on percentage refl ectance va lues with t he rad iation. There does not seem to be any info rma E EL s p ectrophotometer at 425 IDJ.L a nd 685 IDJ.L , tion on this point, although it is known that t hou g h a pprox imate equali ty occurred at 545 IDJ.L . Negroes tan. Vario u s empirical transformations of the 425 mil Because of the known nature of the Liverpoo l data were tested, a nd a logarithmic transformation hybrids, Harrison and Owen were able to extend at t h e b lue and an antilog tra nsformation at the their analys is and partition the variation into its red removed much of the interaction. three principal components: (a) that due to envi Interlocus interaction can be tested by compar ronmental factors, (b) that due to the segregation ing t h e mean refl ectances of hybrids of known of the genes responsible for the parental differe nce, genetic constitution. T hus, for example, on a n i.e. fixa ble variation, and (c) that due to the ad d itive scale, one would expect twice the back average dominance of the different gene pairs, i.e. cross E uropean mean to equal the sum of t he F 1 unfixable vari ation. Because of the limited nature mean a nd the parental European mean. Similarly, of the F 2 data, they based their analysis exclusively one would ex pect fo ur t imes the mean of the on info rmation fro m the first-ge neration a nd back secon d-generation hybrids to equal the sum of cross hybrids and therefore had to assume in their twice t h e F, mean plus the Afri can mean plus t he estimations of unfixable variation that any domi European mean. Using such criteri a , Harrison and nance was isodirectional, i.e., that at all the skin Owen found (as they had fo r the environmental color loci the E uropean ge nes were dominant to the genotyp e situation) that reflectance at 545 fill did African ones or vice versa. In fact, on t his assump not sign i fi cantly differ fro m ex pectation but that tion, the estimate of the co mponent of unfixable ther e was evid ence of in teraction on ref1ectances at vari ation was very small indeed a nd suggested 425 m J.L a nd 685 mil. Aga in, however, log transfor either zero dominance or a balanced dominance in mation of the fo rmer a nd ant ilog of the latter the pa rental ge nes. On t he diffe rent scales of greatly improved the sit uation. T he best scale measurements-refl ectance at 545 mil, log of re obtain ed was t he a nt il og transformation at 685 mJL. f1 ectance at 425 IDJ.L , and ant il og of re f1 ectance at T his is the main reason why ret1ectance values 685 mil-it was estimated that environmental obtain ed wi th a red fil ter have been cited for the factors caused between 36 and 27 percent of the variou s popul ations in the Ta ble, though it is also vari ance and the component of genetically fixable impor tan t that differences in skin blood supply variation was between 63 and 72 percent. minimally affect reflectance of the longe r wave T here is obviously nothing absolu te about these lengths ( H a rmse, 1964). A better idea of t he skin pro po.rtions, whi ch vary according to the environ color affinities of t he populat ions fo r which EEL mental circumstances under which a population. is 685 ffiJ.L d ata are avail able can probably be ob livi ng. Wi thin a si ngle city, the estimate of the tained by converting t he ret1ectance means in t he environmental contribution obtained by Harrison Tab le to a nt il ogs, though, of co urse, the ant il og of a and Owen may seem large ; but subjects were mean is not the same as the mean of in dividua l measured at different times of the year, and, as antilogs. F urthermore, vari ous amoun ts of tanning already mentioned, there is almost certainly ge must c learly affect the values for the differe nt netic vari ation wi thin the parental groups, whi ch populations which were measured under ve ry di f in this a nalysis has been included in the environ fe ren t situ ations. Note also that scales are sought mental component. empirically and that when di fferent environments Harrison and Owen also estimated the number or gen otypes are concerned, a change of scale may of "effective factors" responsible for t he Africa n/ be requir ed. However, the interactions that we re European diffe rence in ski n color si nce this num fo und o n ref1 ectance at 425 mil and 685 IDJ.L are ber equals the squa re of the difference between the probably not indicative of biochemical in teractions parental populations divi ded by fo ur times the in mela n in synthesis. If they were, they woul d also fixable vari ation. T he estimate they obtained on tend to be ma nifest at 545 m JL. However, a complex the scale of re f1 ectance of 545 mJL was a bout 3; on relationship, probably of a reciprocal function log 525 mil and antilog 685 mil, about 4. T he nature, exists between melanin co ncentration a nd a nalysis co uld be taken only to the level of effective reflectance (H arrison a nd Owen, 1956) . In fact, the factors because there was no in fo rmation on second interaction s are almost certainly mainly inherent and later- generation hybrids from whi ch levels of in th e spectrophotometry and in t he sensitivity lin kage could be ascertained. T herefore a ll that 424 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY

can be deduced from this study is that 3 or 4 pairs groups which are in the process of formation and of chromosomes are probably concerned in carry which, if they differ both in skin color and the ing the genes responsible for the skin color differ frequency of polymorphic genes, afford the most ences between Africans and Europeans. Of course, ideal situation for the detection of linkage in man. if only one locus per chromosome is involved, then No doubt it wi ll also ultimately prove possible to the number of effective factors equals the number determine how the polygenic loci, already identi of gene loci. fied, work at t he biochemical level. Further confirmation of the small number of genes involved in African/European skin color CAUSES FOR RACIAL DIFFERENCES IN HUMA N differences comes from work on the Brazilian PIGMENTATION Negro which has been carried out with an EEL No discussion of racial differences in pigmenta spectrophotometer, with the scales that have been tion would be complete without some mention of established for t hat instrument, but with Stern's the causes for the distinctive patfern of geographic methodology. In these studies, Harrison et al. variation in skin color. In fact, many theories have (1967) were able to measure skin color variation in been proposed to account for this phenomenon practically the same population that had been (Daniels et al. , 1969) , and there seems li ttle doubt examined for calculating the levels of hybridiza that natural selection (Livingstone, 1969) ha tion. On the basis of 50 percent in termixture in played a critical role, though most of the evidence southern Brazil, they fou nd that the best fit is indirect. Despite the contentions of Blum ( 1961) between observed and expected distributions was to the contrary, most anthropologists subscribe to also obtained on three or four locus models of equal the_,Yiew that a prime selective factor has been the and additive genes. environmental l evels of ultraviolet radiation; it i All the recent studies of African/European dif hardly coincidental that ultraviolet stimulates m e ferences in skin color are t herefore remarkably lanocytes to synthesize melanin. Indeed, skin color concordant. T hose on the American and Brazilian affords an interesting example not only of the Negro, among whom one would have expected relationship between individual adaptability and considerable break-up in racial linkage groups, genetic selection in man but possibly of genetic might be taken to indicate that the effective assimilation as well (Waddington, 1957) . factors identified in the Liverpool study are in fact We now have impressive evidence that heavy individual gene loci. Conversely, the latter study pigmentation in areas of high solar radiation pro can be thought of as validating many of the tects the skin from the burning and carcinogenic assumptions that Stern had to make in his pioneer effects of ultraviolet radiation (reviewed in Harri ing work. There is, however, t he possibility of son, 1961). Much attention has been given to the internal error compensations, and it is perhaps latter but among naked primitive populations surprising that the analyses of the American Negro protection from burning has probably been, in and Brazilian Negro lead to such agreement in evolutionary terms, much more important. Hun view of the skin color differences in the parental ter- gatherers would probably have been severely contributing populations, for example, the Por handicapped in their daily lives if left with no other tuguese and Northwestern Europeans. protection aga inst ultraviolet radiation than the It would seem, nevertheless, that more is now skin-thickness response shown by albinos in the known about the inheritance of skin color differ tropics. Nevertheless, heavy pigmentation in these ences than about any other quantitatively varying regions is not an unmixed blessing. Theoretically character in man. However, much remains to be (Heer, 1952) and experimentally (Baker, 195 ) done. Clearly, differences between many other dark skin has been shown to increase considerably populations must be examined and, with increas the solar heat load. In regions of low sunlight , like ing . levels of hybridization between the world's those in the temperate regions of Europe, there is populations, groups are now forming that should the converse problem of facilitating ultraviolet allow thi s. Of some particular interest will be the penetration of the epidermis and thereby of in cases involving people of simil ar color but of very creasing the capacity of the body to synthesize different ancestry. We cannot, for example, as vitamin D. Before the addition of vitamins to fo od sume that Melanesians difJer in their skin color heavily pigmented children in urban areas of from Europeans the same way as African popula North America and Europe were more prone to tions do. It also seems unlikely that Indian groups, rickets than wh ite children on comparable diets. whi ch lie intermediate in skin color, share homozy Moreover, pigmentation in arctic regions supports gously some of their genes with Europeans and the view that it protects against ultraviolet radia Africans . Allelic series may, in fact, occur. Kalla tion since levels of such radiation can be high. The (1968) has conpluded that five gene pairs are on ly environmental circumstances where pigment involved in Indian(Punjabi)/European differ level is apparently not co in cidental with levels of ences. The problem also remains of id entifying the ul traviole t radiation are in the equatorial forest chromosomal location of the skin color genes, and especially of t he Old World. Here one finds quite linkage studies with gene markers in polymorphic dark skins (though usuall y not so dark as in systems should be undertaken, especially in hybrid neighboring savannah areas) with low levels of DIFFERENCES IN HUMAN PIGMENTATION 425

ultraviolet which probably have not changed much new theo ry o f skin colour inheri tance. Int. An nary t imes. Va ri ous s uggestions thropol. Ling. Rev., 1:15- 67. in rece n t e volutio Gates, R. R. (1961). The histology of skin pigmentation. have b een proposed f or this a pparent a nomaly. J . R. Microsc. Soc. , 80:1 21- 130. Perha p s t he most persistent has been the view that Gates, R. R. , a nd Zimmermann, A. A. (1953). Compa ri he avily pigmented skin in one o f a number of son of skin color with melanin content. J. Invest. tates heat loss under the dif Dermatol. , 21:339- 348. possible ways facili Gl ass, B. , a nd Li , C. C. (1 953). The dyna mi cs of racial fic ult conditions of high humidity co mbined with intermixture- an analysis based on t he Am eri can temperatures just below that of the body. The Negro. Am. J . Hum. Genet., 5:1- 20. evidence for this, though far from impressive, Harmse, N. S. (1 964). Retlec tometry o f t he bl oodless et. 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