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Solomon Islander skin pigmentation Ultrastructural differences related to genetic variation in Melanesia.

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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.
. .
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