Solomon Islander skin pigmentation Ultrastructural differences related to genetic variation in Melanesia.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 60:323-326(1983) Solomon Islander Skin Pigmentation: Ultrastructural Differences Related to Genetic Variation in Melanesia RAUL 1. GARCIA, RUTH E. MlTCHELL, JERRY BLOOM,AM) GEORGE SZABO Lubanata~of E k h n M i c ~ m m p yHorwrd , S c M ofDandrJ Medicine, Boston, Maanachuaettrr 02116 (RLG., G.S.), D-nt of, P Saint Gtvrge'a HorrpW, Univcnily of New South Wales, Sydney, N.S. W., Awhrrlia (REMJ,and Department ofbfedicine, BrooMdc H o s p W M e d i a l Center, Bnwklyn, New Yo& 11212 (JBJ KEY WORDS Melanesia, Skin color, Ultrastructure, Melanosomes ABSTRACT Genetic differences between Solomon Islander populations are distinguishableon the basis of melanosomepackaging in epidermal keratinocytes. By electron microscopic study of skin pigmentation in various Melanesian populations, we have found distinct inter-island differences in the mode of melanosome packaging. Melanosomes are found as singlets in the skin of Bougainville Islanders but are found aggregated in melanosomecomplexesin Malaita Islanders and Ontong Javanese. This variation in melanosome packaging represents an important biologic difference found between Solomon Islanders and may reflect the genetic diversity existing in the original Melanesian founding population or populations. Human population differences in phenotypic skin color are due to genetically determined functional Merences in epidermal melanocytes and keratinocytes. Melanin pigment is synthesized and packaged by the melanocyte in a specific cytoplasmic organelle, the melanomme, and is subsequently transferred to adjacent keratinocytes. While the numbers of melanocytes for a particular body region are the same in all races regardless of skin color (Szabo, 19671,dflerences do exist in the number and size of melanmmes produced by the melanocyte and in the manner in which the melanosomes are handled by the keratinocytes (Quevedo, 1973;Szabo et al., 1972). Melanosomes are normally always dispexwd singly in the melanocyte cytoplasm. Following transfer to keratinocytes, however, melanosomesmaybefoundeitherassingletsorgrouped together in membrane-bound aggregates (melanosome complexes). Ultrastructural variation in the mode of melanmme packaging appears to follow racial lines. In Australian Aborigines and African and American Negroes, melanosomes are usually found as singlets, while in Orientals and Asian and European Caucasians they are found as melanosome complexes (Mitchell, 1968; Rosdahl and Szabo, 1976;Szabo et al., 1969). 0 1983 ALAN R.LISS. INC. Skin color variation in Solomon Islanders has been studied using skin refledometry, and it has been shown that Bougainville Islanders are significantly darker skinned than Malaita Islanders (Richardson, 1979,1980). However, the number of epidermalmelanocyteshas been found to be the same for these p u p s (Garcia et al., 1977). Rather, it has been shown that these skin color differences are directly related to Merences in the histologic content of melanin in the epidermis (Garcia et al., 1981),likewise reflecting variation in the number and size of melanosomes synthesized and differences in their handling by keratinocytes. By electron microscopic examination of ekin biopsy specimens from Solomon Islanders,we have been able to further characterize these differences. MATERMS AND METHODS Skin biopsy specimens were obtained by the Harvard Solomon Islands Project expeditions (Damon, 1973,1974)from the palmar aspect of the left forearm of five Nasioi, five Aita, and two Nagovisi, natives of Bougainville Island (lSSoE,6%); of five Lau and three Baegu of R.aind Juruug 6,1081;accqbd Sqtmdmr 10.1982. 324 R.I. GARCIA, R.E.MITCHELL, J. BLOOM, AND G.SZABO Malaita Island (161'E, 9"s);and of five natives of Ontong Java (159.5'E, 7'5); and were processed by us for electron microscopy. Bougainville and Malaita Islands are near the north and south ends, respectively, of the Solomon Islands chain and the natives are Melanesian. Ontong Java is a Polynesian outlier and the natives are mixed Melanesian-Polynesian.The skin specimens were fixed, processed, and embedded for electron microscopic study. Thin sections were cut using a diamond knife with a Porter-Blum MT-2 ultramicrotome, and stained with lead citrate and uranyl acetate before viewing in AEI 6B and AEI Corinth 275 electron microscopes. RESULTS AND DISCUSSION racially distinctive. Single melanosomes in keratinocytes are typical of both African Negroes and Australian Aborigines, who are otherwise unrelated. Thus, comparisons between populations regarding mode of melanosome packaging are limited to characterizingdifferences between groups studied, and cannot be used to establish common genetic origins. The variation in the ultrastructure of Solomon Islander skin pigmentation that we have found represents a well-defined biologic difference between Solomon Islander populations, and correlates with reported linguistic, anthropometric, and serologic variation in Melanesians (Damon, 1973, 1974; Friedlaender, 1971, 1975; Howells, 1970, 1973, 1976). For example, the Bougainvilleans, characterized by single melanosomes, speak PapudnonAustronesian (NAN) dialects, while the Malaitans and OntongJavanese, characterized by melanosome complexes, speak Melanesian/ Austronesian (MN) dialects. Similarly, a northsouth cline was found in Inv gammaglobulin allotype fbquencies, with the lowest frequencies in MN-speakingMalaitans and the highest frequencies in NAN-speaking Bougainvilleans (Steinberg et al., 1972). It has been suggested that a similar cline exists in the Solomons for Gm gammaglobulin allotypes (Steinberget al., 1972).Giles et al. (1966)have distinguished other Melanesian populations speaking MN dialectsfromthoee &NAN dialects on the basis of Gm allotype frequencies. Rhoads (19771, using distance statistics to analyze population genetic data from the Solomons, showed that NAN-speakers cluster separately and are distinct from MN-speakers. Ofthe various traits studied, he found the best fit with linguistic differences to be anthropometric dif€erences.Rhoads (1977)believes that We have found that melanosemes are distributed more frequentlyas singlets in the keratinocytesof the Bougainvilleans studied (Fig. 1). Melanosome complexes containing two or three melanosomes are occasionally found. In the skin of the Malaitans and Ontong Javanese, melanosomes are most often found in large aggregates with each melanosome complex typically containing three or more melanosomes (Fig. 2). Single melanosomes are less frequently found (Table 1). It has been shown that melanosome size determines their mode of packaging by the keratinocyte (Jimbow et al., 1976; Quevedo, 1973; Szabo et al., 1969, 19721, and we have found that the melanommes in Malaitan and Ontong Javanese skin are typically smaller than those in Bougainvillean skin. These differences in melanosome packaging in Solomon Islanders also correlate with variation in phenotypic skin color, as shown by skin reflectance data, with Bougainvilleansbeing significantlydarker skinned than Malaitans (Richardson, 1979, 1980; Garcia et al., 1981). The mode of melanosome packaging by keratinacytes is not modified by natural environ- TABU 1. Distribution of melasuurome packaging modes in mental fadons such as ultraviolet radiation, Solomon lalander akin and is believed to be genetically determined P a modee Mean % & S.D. (Quevedo, 1973; Szabo et al., 1969,1972). Sun exposure and artificial ultraviolet irradiation 1 2 3 >3 (UVB: 290-320 nm) both increase the number Bougainville 74 f 9 21 * 7 4 f3 12 1 of melanosomes produced by melanocytes, but Malaita 1724 2926 40213 1428 do not alter the racial differences in packaging OntongJava 21 2 6 926 13 f 7 57 f 7 within keratinocytes (Szabo et al., 1969). Dif1o.ooo x magni6fation50ld.Y wer0 exEmmed . fromrlinrpecferences in the distribution of melanosomes in ssparats imenn of each of three Bougainvilleana, three M d l i h , and three keratinocytes are present in neonatal skin Onton#Javanwe. M e l a ~ u ~ mim n basal LentinOeJrtsn w m k n c ~ r d i l l g t o m o d e a f p a c k e i n e i n f o u r u t 8 ~I3ingIe 1(Rosdahland Szabo, 19761, are stable through- ~msluuwome, 2 = mel.nosome complex mntainiw t m melmamomee, out life, and may serve in distinguishing the 3 melanmme complex mntainiq three melmmome41. and >3 = racial origin of a biopsy specimen (Szaboet al., m e h w o m e mmplex mnta-i mom tbur three melanolomw. The dimhibution for eaeh pacLaeine typn wan obtained for each 1972). However, the distribution of melano- pexmnt individual exmind Data era m u t a d ae the mdllll percent * 8.D. somes as singlets or complexes is not always r o d C a to the nearsst w b l e number. - ULTRASTRUCTURE OF SOLOMON ISLANDER SKIN 325 Fig. 1. Electron micrograph of epidermal keratinccyte in Bougainville Islander skin. Numerom single melanoBomea are evident. x 27,600. Fig. 2. Electron micrograph of epidermal keratinmyte in Malaita Mander skin. Melanmmea are found aggre gated within membrane.-boundcomplexes x 27,500. 326 R.I. GARCIA, R.E. MITCHELL,J. BLOOM, AND G. SZABO the cultural-linguistic divisions correspond to population subsystemsthat have at least some internal coherence and historical stability. The origin of the linguistic and genetic diversity in Melanesia is unclear. Earlier invest i g a h attemptedto discerna workable scheme of separate racial types in order to represent ancestral strains in these populations. They suggested that variation in Melanesia was due to genetically distinct founding groups that settled Melanesia in different waves of migration from Southeast Asia (Howells, 1970,1973, 1976).Recently,more attention has been given to possible effectsof local adaptation, selection, and genetic drift in accountingfor the observed diversity. Howells (1973) believes that the varying physiques of Melaneaia, as well as other genetic variation, reflect varying samplings or founding groups derived from a single basic original population. Our finding of a basic biologic difference between Bougainville and Malaita Islanders in regard to skin pigmentation is reflective of the considerable genetic variation in Melanesia. It is unclear to what degree such diversity may have existed in only one original foundingpopulation, A possible explanation is that more than one ance&al population, perhaps blended to some degree by subsequent “hybridization,” may be responsible for the presently observed variation. Friedlaender, JS (1976)Pattern of Human Variation: The Demography, Geneties and Phenetica of Bougainville b landera.Cambridge: Harvard University h, pp. 252. Garcia, RI, Mitehell, RE, Bloom, J, and Saebo, G (1977) N u m b e r o f e p i d e r m a l ~hairrollielae, , andmeat duda in #kin of Solomon Islanders. Am. J. Phys. Anthropol. 47:427434. Garcia, RI,, i R RE, and Smbo, G (1981)Skin color variation in Solomon Islandem:rdectometry, histoloey, and ultra~tmcture.In M Seiji (ed):Pigment Cell 1981: Phenowic E x p M o n in Pigment Celb. Tokyo:Univer& of Tokyo Rese, pp. 19S206. files, E,O m E, and Sbinbrg, AG (1966)G--glObulin faetore (Gm and Inv) in New Guinea:anthropological .seiaee, 1~0:115aii60. ~ E Howelb, WW (1970)Anthqmnetric p u p i n g ~ Y C I of Pacific peoples. Archeol. Phys. Anthropol. Oceania 6:192-217. Howells,WW (1973)The Pacific blandern. New York Scribner, pp. 299. Howelb, WW (1976)Multivariate analyaia in the problem of Awtralian origins. In RL Kirk and AG Thorme (eds): The Origin ofthe Auntralians. Canberra: Au~tralianInetitute Of Aboriginal studim, pp. 141-160. Howelb, WW (1976)Explaining modern man: mlutioniets vemu migmtioni~ts.J. Hum.Evol. 6:477-496. Jimbow, K,Que.vedo, WC, Jr., Fitzpatrick,TB, and Saebo, G (1976)Some aepects of melanin biology. J. Inveet. Dermatol. 67:72-89. Mitchell, RE (1968)The skin of the Australian Aborigine: A light and eleetronrm‘cnmcopicnl study. Aurt. J. Dermatol. 9:314-328. Quevedo, WC, Jr. (1973)Genetic control of melanin metabolinm within the melanin unit of mammalian epidermis. J. Invent. Dermatol. 60:407-417. Rhoads, J G (1977)Genetics, growth, and microevolution: The- E of geographic variation in Solomon bland p o ~ u l a t iPhD ~ . D M t i a , HarvardU n i ~ e QUII, publiied. Richdmm, RE (1979)Skin pigmentation in Solomon IsACKNOWLEDGMENTS landern: Microanatomic and reAeetometric study of intrapopulation and interpopulation variation in #kincolor. The authors gratefully acknowledge the asThe&, Harvard Univernity, unpublished. sistance of Evelyn Flynn and Ann Hawthorne, R i e , RE (1980)comparieon of euntanning capacity in light- and dark-akinned Solomon Islandem. Am. J. and the invaluable advice and cooperation of Phy~. Anthropol. (Ab~tmct)62:247. the late Dr.Albert Damon. This research waa I, and Szabo, G (1976)Ultradructureof the human supported by a grant from the Milton Fund of Roadahl, melanoeytesysteminthenewborn,withspecialrefereace Harvard University, and by USPHS Grant AMto racial differemm. In V Riley (ed):Pigment Cell, Vol. 3.B m l : Kager,pp. 1-12. 20669 from the National Institute of Arthritis, Diabetes, and Digestive and Kidney Diseases. Steinberg, AG, Damon, A, and Bloom, J (1972)Gammaglobulin allotypee of Melanesians from Malaita and BouThe Harvard Solomon Islands Project was s u p gainville, Solomon bland^. Am. J. Phy~.Anthropol. ported by USPHS Grant GM-13482 from the 36:17-&6. National Institute of General Medical Sciences saabo,G (1967)The regional anatomy ofthe human int8gument with special reference to the distribution of hair and was a part of the Human Adaptability Secfollicles, sweat glendn and m e w . Phil. Trans. Roy. tion of the International Biological Program. 8oc. Lond. 262B:447485. &ah,G, Gerald, AB, Pathak, M A, and Fitzpatrick, T B LITERATURE ClTED (1969)Racial Meremm in the fate of melanotmmea in human epidermis. Nature 222:1081-1082. Damon, A (1973)Some genetic traits in Solomon bland saabo, 0, Gerald, AB, Pathak, M A, and Fitzpntrick, T B populations. Am.J. P h p Anthmpol. 39:169-178. (1972)The -lu of racial color M e r e n c e ~in Damon. A (1974)Human ecology in the Solomon I~lanQ. man. In V Riley (4) pigmentation: : Its G~IUAE and BiBiomedical oteervation~among fiour tribal mcietieu Hum. ologic control. New York Appleton-Century-Cmfts,pp. E d . 2:191-215. 23-41. Eedlnender, JS (1971)The population structure of SouthCentral Bougnhville. Am.J. Phy~.Anthropol.36:13-26. . .