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ANNALS OF HUMAN BIOLOGY, 1996, VOL. 23, NO. 3, 189 201
The Wai Wai Indians of South America: history and genetics
S. M. CALLEGARI-JACQUES'~, F. M. SALZANO'~, T. A. WEIMER~', M. H. L. P. FRANCO'~, M. A. MESTRINER~, M. H. HUTZ'~ and L. SCHULERt§
tFederal University of Rio Grande do Sul, Porto Alegre, Brazil ~University of $5.o Paulo, Ribeir'fio Preto, Brazil
§University's Clinical Hospital, Porto Alegre, Brazil
Received 20 August 1995; revised 20 December 1995
Summary. Demographic, medical and genetic information was obtained in a population of Carib-speaking Wai Wai Indians living in northern Brazil. At present mortality is low and fertility moderate, with a low variance in offspring number in completed families. Mobility is high, but about two-thirds of the unions are endogamic. Malaria is the main health problem. Phenotype and allele frequencies were obtained for 27 protein genetic systems. Comparison with six other Carib groups indicates closest affinities with another Amazonian tribe, the Arara. Quantification of the intra- and interpopulation genetic diversity in these seven populations indicate that the variation within groups is only slightly lower than the variation between groups. The level of Carib interpopulation diversity, on the other hand, does not differ significantly from that found in 11 Tupi-speaking populations. In accordance with their history of intermarriage with groups which speak slightly different languages, and consider themselves as distinct, the Wai Wai are clearly more diversified at the intrapopulation level than at least three of the six Carib populations with which they were compared.
1. Introduction The question of the way in which population structure influences the genetic
variability of a given group has been variously considered both at the theoretical and empirical levels, but details of this relationship are far from being elucidated. We therefore decided to study the Wai Wai Indians of Brazil, both at the protein and DNA levels, due to their past history of extensive intercrossing with groups that the Indians themselves distinguish as different. They can therefore serve as a model for the analysis of the interplay between migration, gene flow, fertility, mortality and epidemiological patterns as factors influencing given indices of genetic variability. Another problem frequently considered is that of the relationship between genetic variation and language, and we briefly examine it here also. Specific questions considered were: (a) How does the intrapopulation variation of the Wai Wai (as measured by F-statistics) compare with that of other tribes of the same linguistic group (Caribs)? (b) How can they be classified within that group? and (c) Is the Carib interpopulation variability significantly different from that which occurs in linguistically diverse communities (Tupis)? In addition, we place on record here information about 27 protein genetic systems which may serve as a basis for other analyses of the inter- and intrapopulation diversity of South American Indians.
2. Subjects and methods At present, Wai Wai is a generic identification for a group of people who speak
dialect variations of the linguistic family Parukoto-Charum~, of the Carib stock. Besides living in a common territory (the Mapuera river basin, medium and high
0301-4460/96 $12"00 © 1996 Taylor & Francis Ltd.
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190 S.M. Callegari-Jacques et al.
Nhamundfi, headwaters of the Jatapfl and Trombetas rivers at the frontier between Brazil and Guiana) they present a basic similarity in their way of living and intermarry extensively among themselves. Their history has been aptly described by Fock (1963) and Yde (1965); anthropometric investigations among them were performed as early as the 1920s (Steggerda 1950), and Holden (1938) reported on their blood pressures. Meggers and Evans (1964) furnished genealogical and demographic information about the Wai Wai of Guiana, while Frikel (1958) provided an ethnolinguistic classification of the groups inhabiting the Brazilian-Guiana border. More recently, Gallois and Ricardo (1983) provided a very good general overview of these peoples. Selected genetic information both at the protein (Alc~ntara, Lourengo, Salzano, Petzl-Erler, Coimbra, Santos and Chautard-Freire-Maia 1995) and DNA levels (Bevilaqua, Mattevi, Ewald, Salzano, Coimbra, Santos and Hutz 1995) will be considered together with the results reported here. The following account is based mainly on Gallois and Ricardo (1983).
The first reports about the people who inhabited the Nhamundfi/Mapuera rivers date to the 17th century, and related to attempts made by Catholic priests to evangelize them. Three notable travelers (M. R. Schomburgk, C. B. Brown and H. Coudreau) gave information about the situation of the Wai Wai in the 19th century. Around 1890 they suffered a major demographic decline due to diseases brought by the non-Indian colonizers. At the beginning of the present century the Wai Wai were living in two areas of the Brazilian-Guiana border: in the north in the Acarai mountains and in the east in the high Mapuera river. Conflicts with the Parukoto Indians and other factors led, however, to migrations to the high Essequibo river in Guiana. Beginning in the 1950s profound changes occurred among them. The Unevangelized Fields Mission established a post in the high Essequibo, attracting to Guiana the majority of the population from the Brazilian Mapuera and Nhamundfi rivers. The mission thrived until 1971, when the missionaries were expelled from Guiana. Some of them moved then to Brazil, establishing themselves at the Mapuera river region where they founded another mission. It was in the village of this mission that we contacted the subjects of the present report.
In the past the population structure of the Wai Wai was based on a pattern in which families lived in communal houses, with high mobility among villages. The ideal residence pattern was matrilocal, but this was generally observed in the first year of marriage only. Preferential marriage was among cross-cousins. Agricultural practices and fruit gathering were performed mainly by women, while men would deal with hunting and fishing. Under missionary influence this pattern was changed mainly by the grouping of the people in a single place. Communal houses were, however, disfavoured, and at present the Mapuera village is composed of about 130 houses where members of nuclear families plus some relatives live.
The area occupied by the inhabitants of the Mapuera village corresponds to the medium-high Mapuera river, a tributary of the Trombetas, which has its headwaters at the Acarai sierra, frontier with Guiana. The Indian area is included in the county of Oriximinfi, State of Parfi, Brazil. The village is situated on the eastern bank of the Mapuera, 58°00'W, 0°40'S, in a region of difficult access: about 5 hours flying from Bel6m and 2 hours from Manaus and Boa Vista. The nearest Indian community is Cassaufi, which can be reached in 1 day by foot. This village is also inhabited by Parukoto-Charumg groups (about 300 individuals in number), but there the dominant language is Hishkariana, and Almeida (1981) listed only seven Wai Wai Indians living there. The nearest non-Indian locality is called Cachoeira Porteira, at the
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Genetics of South American Indians 191
confluence of the Mapuera and Trombetas rivers. It takes around 4 days by canoe to reach the Mapuera village from there.
Blood samples were collected with anticoagulant, refrigerated shortly afterwards, and flown in this condition to Manaus and Por to Alegre, where they were processed and an aliquot sent to Ribeirfio Preto for further determinations. Most of the methods employed are described or referenced in Salzano, Black, Callegari-Jacques, Santos, Weimer, Mestriner, Pandey, Hutz and Rieger (1988). The exceptions are the isoelectric focusing techniques performed for Gc typings, which are given in Corvello, Franco, Salzano, Black and Santos (1989), and those related to the phosphoglu- comutase 1 subtypes. In the latter case the method used was described by Yuasa, Ikebuchi, Suenaga and Ito (1986), but we introduced the following changes: (a) 0-8 ml of ampholine pH 5 7 only were used; and (b) prefocusing at 1000 V for 15 minutes was done.
The statistical analysis involved the following procedures: (a) calculation of allele frequencies; (b) determination of Nei's (1972) genetic distances and of the corre- sponding dendrogram using the neighbour joining method, the reliability of the tree being tested with 3000 bootstrap replications (Hedges 1992); (c) F-statistics (Wright 1965, 1969, 1978) and other parameters (Nei 1973, 1986, 1987) were used to assess the variability within and between populations. The standard error of F~s was calculated by jack-knifing (one system was subtracted each time and the new total re-evaluated; Efron 1982). The heterogeneity between Carib and Tupi populations was tested as suggested by Workman and Niswander (1970). For all these calculations the DISPAN (Ota 1993) or BIOSYS (Swofford and Selander 1981) programs were used.
3. Results Table 1 presents the age and sex distribution of the individuals living in Mapuera.
For this tabulation we merged the results of our own census, performed in July 1988, with the data collected by Irene Benson, a missionary who at the time was living with these Indians for 27 years, and who keeps a detailed file about the demographic changes occurring in the village. As can be verified, the population pyramid is quite broad, with 42~o of the individuals being 0-14 years of age. The average age is around 22.5 years for both males and females. The sex ratio shows some variation, but on the whole is that expected according to the age groups established.
Considerable effort was expended trying to understand and document the pattern of mobility of these Indians, especially in relation to variables which may affect their genetic variability. As can be verified in table 2, and corroborating the historical
Table 1. Age and sex distribution observed in the Mapuera village of Wai Wai Indians.
Group or characteristic
Age interval Total
0-14 15-30 31 years years years and older
Estimated average age (years) (x ± SD)
Males Females Total Percentage Sex ratio
206 156 127 489 22"4 ± 17.6 196 136 142 474 22.6 ± 17.6 402 292 269 963 22"5± 17.6 42 30 28 --
105 115 89 103
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Table 2.
S. M. Callegari-Jacques et al.
Marriage and previous migratory movements of inhabitants from the Mapuera village of Wai Wai Indians.
Type of marriage Number Percentage
1. Using Mapuera as reference 1.1. Both partners from Mapuera 1.2. One partner from another village 1.3. Both partners from another village
2. Place of origin in general 2.1. Endogamous 2.2. Exogamous
4 5 5 6
69 89
48 62 30 38
The number of localities involved is 28, distributed in the range I°5'S 4°20'N; 56°45'W 60°20'W. This presents an area of 239 198 km 2. Ninety per cent of the localities, however, are restricted to 0°40'S 2°30'N; 56°50'W-59°15'W, an area of 94000 km 2.
Table 3. Tribal composition of the Mapuera Wai Wai village, based on 77 marriages.
Type of marriage Number Percentage
Wai Wai + Wai Wai 23 30 Wai Wai x Katuena 8 10 Wai Wai x Xereu 4 5 Wai Wai x Hishkariana 3 4 Wai Wai x Mawayana 3 4 Wai Wai x Wapishana ! 1 Wai Wai x Mura/Neo-Brazilian ! 1 Wai Wai x unknown 1 - Katuena x Katuena 14 19 Katuena x Xereu 2 3 Katuena × Mawayana 1 1 Katuena x unknown 1 Xereu x Xereu 9 12 Xereu x Mawayana 1 1 Hishkariana x Hishkariana 3 4 Hishkariana x Mawayana 2 3 Hishkariana x Wayana 1 1 Mawayana x Mawayana 1 1
Total 79 100
information, since the village is of recent origin, in only 5~o of the marriages have both partners been bo rn locally, with another 6 ~ of unions being ones in which one par tner was born in Mapue ra and the other in a different place. Consider ing all marriages, abou t two-thirds of them are endogamous . The total n u m b e r of localities men t ioned by marr ied persons is 28, distr ibuted over an area of abou t 239 000 km 2. This area is, however, much reduced (94 000 km 2) when a few outliers are excluded.
In format ion abou t the tr ibal identification of spouses in 79 marriages is given in table 3. Consider ing the 77 in which both spouses provided the information, it can be seen that four other P a r u k o t o - C h a r u m ~ groups are represented (Katuena, Xereu, Hishkar iana and Mawayana) , and that un ions outside the P a r u k o t o - C h a r u m f i complex (with one Wapishana , one Mura /Neo-Braz i l i an and one Wayana) are very rare. Sixty-six per cent of the marriages were contracted with members of the same social unit, and 55~o involved at least one Wai Wai subject.
Ferti l i ty and morta l i ty data are given in table 4. The percentage of premature deaths (before age 15), 9"3~o, is very low for hunter gatherers with incipient
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Genetics of South American Indians
Table 4. Fertility and mortality in the Mapuera village of Wai Wai Indians.
193
Unit considered Number of Number of Mean Premature females live births + SD deaths ( ~ ) t
All families 81 364 4.5 ± 2-4 9.3 Completed families+ 15 88 5.9 ± 2.2
Opportunity for selection: l m = 0"10, I f - -0 '14, lf/ps -- 0"15, and I = 0'25. I,,, = pd/ps, where p d - premature deaths and ps = proportion surviving or (l - pd). If = Vr/x ~, where Vf = variance in offspring number in completed sibships and x = mean number of live births per woman who completed her reproduction. I - Ira -r- lf/ps -- index of opportunity for selection (Crow 1958). t Before age 15.
From females who were 40 years of age or older.
agriculture, fertility is moderate (about six children per women who completed reproduction) with a low variance in offspring number. As a consequence the index of opportunity for selection is also very low (I = 0-25), with similar contributions of mortality (I m = 0.10) and fertility (If = 0.14).
Systematic physical examinations performed by one of us (L.S.) indicated a generally healthy population. The main health problem in Mapuera, according to Irene Benson, is malaria, and both Plasmodium falciparum and Plasmodium vivax were identified in thick blood smears of two and 10 individuals, respectively. We also observed 14 persons with symptoms compatible with malaria, from whom blood was collected for parasite analysis. Two boys (aged 5 and 15) were found to be affected by Down syndrome, and a 29-year-old woman presented with peripheral polyneuritis. She and her husband, with a painful tumour in the left hip, went to Manaus with us for specialized treatment. Irene Benson, in addition, reported the occurrence of an individual with severe cleft lip and palate, who has been operated on several times in Bauru and Manaus, and of another child with a milder cleft lip. She also mentioned a subject born with spina bifida, who died at 2 years of age. Other pathologies observed by us involved a tumour clinically similar to a lipoma in the foot of a 25-year-old woman, and a case with purulent skin lesions in the thorax of unknown aetiology. Twenty-five children and one adult female showed different types of infectious problems, including a child with measles.
Phenotype and allele frequencies for 27 genetic systems are given in table 5. A comparison of the results presented here and the allele averages obtained among Amazonian Indians in general (reported in Callegari-Jacques, Salzano, Weimer, Hutz, Black, Santos, Guerreiro, Mestriner and Pandey 1994) indicate that the Wai Wai show high prevalences of L*NS (193/o vs 9~o), L*Ns (27~o vs 15~o), RH*R! (64~o vs 52'~), ACP*A (23~o vs 11~o) and ESD*I (82~ vs 72~o). Low frequencies, on the other hand, were obtained for L ' M S (10~ vs 24~), P*I (35~ vs 47~), RH*R2 (13~o vs 37~), and FY*a (36~ vs 68~o). Only two other Brazilian tribes have been tested for the phosphoglucomutase-1 subtypes (Sim6es, K6mpf, Ritter, Luckenbach, Zischler and Salzano 1989), and the values obtained here are intermediate between those observed in these groups. Also of interest is the finding, in 4 ~ of the Wai Wai, of an esterase A variant previously observed in two of 31 (6~o) Karara6 Indians.
How do the Wai Wai genetic results compare with those obtained previously in other Carib groups? To assess this we compared them with the information available on six other Carib tribes, living in different places of the Amazon region (figure !). Sixteen genetic systems were studied in all of them (bibliographic references in the Appendix) and the resulting dendrogram is presented in figure 2. The Wai Wai show
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194 S.M. Callegari-Jacques et al.
Table 5. Phenotype and allele frequencies for 27 genetic systems studied in the Wai Wai Indians.
System No. Phenotypes No. Allele or Gene tested found found haplotype frequency
ABO 166 MNSs 166
P 166
Rh 166
Kell 166 Duffy 150
Diego 166
Haemoglobin A 165 Haemoglobin A2 165 Phosphogluconate dehydrogenase 166 Phosphoglucomutase 1 165
Glucose-6-phosphate dehydrogenase Males: 74 Females: 92
Adenylate kinase 165 Acid phosphatase 166
Glutamate pyruvate 101 transaminase
Esterase A 159
Esterase D 146
Glyoxalase I 166
Carbonic anhydrase 2 164 Peptidase A 154 Peptidase B 159 Peptidase C t 59 Haptoglobin 166
O 166 ABO*O 1"000 MSs 10 L ' M S 0"096 Ms 37 L ' M s 0"446 MNS 15 L*NS 0"187 MNSs 29 L*Ns 0"271 MNs 42 NS 7 NSs 11 Ns 15 P1 97 P*I 0"355 P2 69 CDE 7 RH*RZ 0"124 CDEe 20 RH*R1 0.644 CDe 76 RH*R2 0-132 CcDE 5 RH*RO 0.100 CcDEe 17 CcDe 27 cDE 11 cDEe 2 cDe 1 K - 166 KELL*K- 1-000 a + 89 FY*a 0.362 a - 61 a + 65 DI*a 0.220 a - 101 A 165 HB*A 1.000 A2 165 HB*A2 1.000 A 166 PGD*A 1-000 1A 16 PGMI*IA 0.255 1A1B 41 PGMI*IB 0.551 1A2B 11 PGMI*2B 0.194 1B 53 1B2B 35 2B 9
B 74 G6PD*B 1"000 B 92 1-1 165 AK*I 1"000 A 6 ACP*A 0"229 AB 64 B 96 1-1 47 GPT*I 0"653 2-I 38 2-2 16 1-1 152 ESA*I 0.978 1-K;~ 7 1-1 98 ESD*I 0-818 2-1 43 2-2 5 1-1 19 GLO*I 0.322 2-1 69 2-2 78 1-I 164 CA2*I 1.000 1-1 154 PEPA*I 1"000 1-1 159 PEPB*I 1.000 1-1 159 PEPC* 1 1"000 1-1 65 HP*I 0'609 2-1 66 2-2 30 0 5
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Genetics of" South American lndians
Table 5 (continued)
195
System No. Phenotypes No. Allele or Gene tested found found haplotype frequency
Transferrin 166 BC 17 TF*C 0"949 C 149
Ceruloplasmin 166 B 166 CP*B 1.000 Albumin 166 A 166 ALB*A 1-000 GC 162 1F 13 G C * I F 0.272
1F-1S 46 GC*IS 0.497 1S 40 GC*2 0.231 2-1F 16 2-1S 35 2 12
Serum cholinesterase i t 165 A 0 BCHE*A 0.000 165 F 0 BCHE*F 0.000
Serum cholinesterase 2t 163 C5 + 24 - -
+ Results reported in Alc~ntara et aI. (1995). 1-Karara6. Same variant described in Callegari-Jacques et al. (1994),
Karara6 Indians. found previously in two of 31
70 ° o o ¢ + so"
+ I0 °
~ J
0 °
" [ J g2,
%°.t..~ '?
40 ° "t- 0 °
10 °
Figure 1. Geographic location of the seven Carib tribes considered ill the genetic distances and diversity analyses. Key to the tribal names: APA: Apalai; ARA: Arara; MAC: Macushi; MAK: Makiritare; TIR: Tiriyo; WWA: Wai Wai: WAY: Wayana. Insert: the region's location in South America's map.
closest affinities with the Arara, and both can be clearly separated from the other five populations. This corresponds well with their geographic distribution, the Wai Wai and Arara living at the south and all the others north of the equator.
Comparison of the genetic diversity encountered in these groups was performed using eight codominant genetic loci which are polymorphic in at least one of these communities (ACP, ALB, Ce(RH), Ee(RH), HP, PGD, PGM1 and TF), and the
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196 S.M. Callegari-Jacques et al.
58 Apalai
39 69 5~iriuo
Hacushi
Wayana Hakiritaro
A F t r a
Waiuai Figure 2. Dendrogram obtained for seven Carib Indian tribes considering 16 protein genetic systems (ABO, ACP, ALB, DI, FY, GC, G6PD, HB, HP, KELL, MNSs, P, PGD, PGM1, RH, and TF).
Table 6. Measures of genetic diversity (_+ standard errors) for eight loci in seven Carib-speaking Indian populations.
Population Mean Mean no. of Percentage of Observed Fls sample alleles per loci showing mean (intrapopulation size per l o c u s polymorphism heterozygosity genetic diversity) locus
Apalai 127 1.8 _+ 0-2 75 0.252 _+ 0.073 0.041 + 0.020 Arara 60 1-6 _+ 0.2 63 0.204 _+ 0.068 -0.076 _+ 0.011 Macushi 918 2.0 _+ 0.3 75 0.223 _+ 0.082 0.001 _+ 0.008 Makiritare 743 2-1 _+ 0.2 88 0.225 _+ 0.076 0.011 -+- 0.013 Tiriyo 555 1.9 _+ 0.2 75 0.246 _+ 0.077 0.045 _+ 0.017 Wayana 377 2-4 + 0.3 100 0.269 _+ 0.068 0.037 _+ 0.014 Wai Wai 165 1.8 _+ 0.2 75 0.213 _+ 0-057 0.109 _+ 0.034
x 2 for heterogeneity among populations: 1713.65; d.f. = 90; 0 < 0.00001.
results are shown in table 6. The mean number of alleles per locus varied between 1-6 and 2.4, the percentage of loci showing po lymorph ism between 63~o and 100~o, and the observed mean heterozygosi ty between 0.204 and 0.269, in all cases the extreme values being observed respectively in the Arara and Wayana . But the differences among these three parameters are clearly non-significant, as evaluated by their s tandard errors and, in relation to the percentage of loci showing polymorphism, by chi-square analysis (Z2: 4-01; 6 d.f.; p < 0.50).
The quantification of intra- and interpopulat ion genetic diversity can also be done using Wright 's F-statistics (Wright 1965, 1969, 1978, see also Nei 1987). The correlat ion between gametes that unite to produce the individuals (I) relative to the gametes of the total popula t ion is represented by F~ T. The average over all subdivisions of the correlat ion between uniting gametes relative to those of their own subdivision is F~ s. The correlat ion between r a n d o m gametes within subdivisions, relative to gametes of the total populat ion, is FST. In practice, what is used is the observed heterozygosity versus that expected under Hardy-Weinberg equilibrium, considering the different units (in this case, Carib as a whole and the five tribes). The results obtained with the data of table 6 (values and their s tandard errors obtained by jack-knifing) are as follows: FIT: 0"098 _+ 0'006; F~s: 0"042 _+ 0"008; FST: 0'059 _+ 0"002. The in t rapopulat ion diversity (F~s) is therefore only slightly lower than the inter- popula t ion diversity (FsT). The latter is statistically highly significant 0~2: 1714; 90 d.f.; p < 0.001). The other question, as to whether the in t rapopula t ion diversities of each tribe are different among themselves, can be answered by an inspection of the
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Genetics of South American Indians 197
last column of table 6. The Wai Wai value (0.109 + 0.034) is the highest, signi- ficantly different from those obtained among the Arara ( -0 .076 _+ 0.011), Macushi (0.001 + 0.008) and Makiritare (0.011 _+ 0.013).
A final question can be asked: Is the interpopulation diversity found among the Carib different from that observed in linguistically different groups? To test this point we compared the present FsT information with that obtained in 11 Tupi populations (Arawet6, Asurini-Koatinemo, Asurini-Trocarfi, Cinta Larga, Emerillon, Karitiana, Parakanfi, Sater6-Maw6, Surui, Urubu-Kaapor and Wai~pi; references describing their genetic data are given in the Appendix). Since albumin is monomorphic among the Tupi we had to restrict the analysis to seven loci only (ACP, Cc(RH), Ee(RH), HP, PGD, PGM1 and TF). Following Workman and Niswander (1970) this can be tested by an F ratio, considering the summed chi-squares for these seven loci and their degrees of freedom. The results are as follows: Carib, )~2: 1653.78; 78 d.f., p < 0.000001; Tupi: 1693.04; 100 d.f., p < 0.000001; F ratio: 1653.78/78 + 1693.04/100 = 1.25, p > 0.20. That is, in relation to these loci the interpopulation differences of Carib and Tupi are statistically non-significant.
4. Discussion At the outset it is important to summarize in which way the Wai Wai results depart
from or agree with the picture observed among other South American Indians. In terms of demography they generaUy show age and sex distributions, and endogamy levels similar to those observed among hunter gatherers with incipient agriculture (cf. Salzano and Callegari-Jacques 1988). But their estimated index of opportunity for selection is quite low (I: 0-25; range in 25 other tribes: 0-38 3.16; Salzano and Callegari-Jacques 1988; Salzano, Callegari-Jacques, Mestriner, Weimer, Franco, Schiller, Harada, Schneider, Hutz and Freitas 1990). The Wai Wai distribution range seems to be large, indicating high mobility. No less than 28 localities were identified as birthplaces of spouses, spread over an area of 239 000 km 2. To place this result in perspective we should remember that the whole country of Guiana has 214 969 km 2, and the United Kingdom 258 256 km 2.
In terms of.qenetics the Wai Wai do not depart markedly from other Amazonian Indians, only nine of the 39 alleles or haplotypes listed in table 5 showing some departure (10~o or more) from the Amazonian Indian averages listed in Callegari- Jacques et al. (1994). As a matter of fact, only the Fy*a allele showed a difference of more than two standard deviations from the Amazonian average (Wai Wai: 0.36; Amazonian Indians in general: 0.68 _+ 0.13). Since it has been known for almost 20 years that the F y ( a - b ) phenotype confers resistance to infection by the malarial parasite Plasmodium vivax (Miller, Mason, Clyde and McGinniss 1976), and that this disease is prevalent among the Wai Wai, it is possible that at least part of the difference may be due to this association. Results in 16 genetic systems, on the other hand, place the Wai Wai together with the Arara, clearly separated from other five Carib groups, as expected by their geographic distribution.
How much diversity occurs at the intra- and interpopulation levels? This problem has been variously considered by many researchers, and good reviews can be found in Wills (1991), Chakraborty and Jin (1994), and Cavalli-Sforza, Menozzi and Piazza (1994). These analyses suggest that the results can be much influenced by differences in clustering, the type of method used, and the classes of polymorphisms considered. Our specific results considering the Carib as a whole suggest not much difference between the intra- and interpopulation diversities in relation to eight polymorphic
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loci. However, the Wai Wai are clearly more diversified at the intrapopulation level than at least three of the six other Carib populations with which they were compared, including the Arara, in accordance with their history of extensive intermarriage with groups who distinguish themselves as different and who speak diverse dialects. The present analysis, on the other hand, did not reveal differences in interpopulation diversity between Carib- and Tupi-speaking populations, in disagreement with previous findings, based on genetic distances (Callegari-Jacques and Salzano 1989, Aguiar 1991). The reviews mentioned at the beginning of this paragraph also emphasized the fact that results obtained with a given set of markers will not necessarily be replicated with another set. In this connection it should be mentioned that Bevilaqua et al. (1995), examining the beta-globin gene cluster haplotype distribution, at the DNA level, of six Brazilian Indian tribes, verified that the Wai Wai presented intermediate values of haplotypic diversity in relation to the others (three Tupi-, one G~- and one Yanoama-speaking tribes). Extension of these studies to other Carib populations, and the investigation of the variability at other nuclear DNA and mitochondrial DNA systems, will be awaited with interest.
Acknowledgements We thank the Fundagfio Nacional do indio (FUNAI) for permission to study the
Indians and for logistic assistance, given by the head of the Post, Luiz I. M. Sousa, nurse Ana M. Sousa and health attendants Eraldo and Rocivaldo. The Miss5o Central Amazonas (MEVA) missionaries were also very helpful, especially Irene Benson, who gave us much useful information, and provided access to her census data. The Indian leaders and the subjects of the investigation were adequately informed about the aims of the study and gave their approval, which is also gratefully acknowledged. Financial aid was provided by Financiadora de Estudos e Projetos (FINEP) and Conselho Nacional de Desenvolvimento Cientifico e Tecnol6gico (CNPq).
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Address for correspondence: Professor Francisco M. Salzano, Departamento de Gen~tica, Instituto de Biociencias, Universidade Federal do Rio Grande do Sul, Caixa Postal 15053, 91501-970 Porto Alegre, RS, Brazil.
Appendix: List of papers reporting primary data used in the genetic comparisons between Carib and Tupi indians ARENDS, T., 1963, Frecuencia de hemoglobinas anormales en poblaciones humanas suramericanas. Acta
Ciem(fica Venezolana, Supl. 1, 46-47.
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ARENDS, T., 1964, Search for abnormal hemoglobins in South American Indians living in malarious zones. Proceedings, VII International Congress of Tropical Medicine and Malaria, 4, 179-182.
ARENDS, T., and GALLANGO, M. L., 1960, Haptoglobin types in a Paraujano Indian population. Vox Sanguinis, 5, 452-461.
ARENDS, T., and GALLANGO, M. L., 1962, Haptoglobin and transferrin groups in Venezuela. Proceedings, VIII Congress of the International Society of Blood Transfusion, Tokyo, pp. 379-382.
ARENDS, T., and GALLANGO, M. L., 1965, Hemoglobin types and blood serum factors in British Guyana Indians. British Journal of Haematology, 11, 350 359.
ARENDS, T., WEITKAMP, L. R., GALLANGO, M. L., NELL, J. V., and SCHULTZ, J., 1970, Gene frequencies and microdifferentiation among the Makiritare Indians. II. Seven serum protein systems. American Journal of Human Genetics, 22, 526 532.
BLACK, F. L., SALZANO, F. M., BERMAN, L. L., GABBAY, Y., WEIMER, T. A., FRANCO, M. H. L. P., and PANDEr, J. P., 1983, Failure of linguistic relationships to predict genetic distances between the Waifipi and other tribes of lower Amazonia. American Journal of Physical Anthropology, 60, 327-335.
BLACK, F. L., SALZANO, F. M., LAYR1SSE, Z., FRANCO, M. H. L. P., HARRIS, N. S., and WEIMER, T. A., •980, Restriction and persistence of polymorphisms of HLA and other blood genetic traits in the Parakan~ Indians of Brazil. American Journal of Physical Anthropology, 52, 119-132.
BLACK, F. L., SANTOS, S. E. B., SALZANO, F. M., CALLEGARI-JACQUES, S. M., WEIMER, T. A., FRANCO, M. H. L. P., HUTZ, M. H., R1EGER, T. T., KUBO, R. R., MESTRINER, M. A., and PANDEY, J. P., 1988, Genetic variation within the Tupi linguistic group: new data on three Amazonian tribes. Annals of Human Biology, 15, 337-351.
BOlS, E. P., 1967, Les Am6rindiens de la Haute-Guyane Frangaise. Societk de Pathologie Exotique, Monographie 7 (Paris: Desclge), pp. 1-180.
CABANNES, R., BEURR1ER, A., and LARROUY, G., 1965, La thallassgmie chez les indiens de Guyane Fran9aise. NouveUe Revue Frangaise d'Hematologie, 5, 617-630.
CABANNES, R., BEURRIER, A., and MONNET, B., 1965, Etude des prot6ines, des haptoglobulines et des transferrines chez les indiens de Guyane Frangaise. Nouvelle Revue Franqaise d'Hematologie, 5, 247-260.
CALLEGARI-JACQUES, S. M., SALZANO, F. M., WEIMER, T. A., HUTZ, M. H., BLACK, F. L., SANTOS, S. E. B., GUERRE1RO, J. F., MESTR1NER, M. A., and PANDE¥, J. P., 1994, Further blood genetic studies on Amazonian d ive r s i t y~a ta from four Indian groups. Annals of Human Biology, 21, 465-481.
GEERDINK, R. A., BARTSTRA, H. A., and VAN VEEN, J. M. S., 1974, Serum proteins and red cell enzymes in Trio and Wajana Indians from Surinam. American Journal of Human Genetics, 26, 581-587.
GEERDINK, R. A., N1JENHUIS, L. E., VAN LOGHEM, E., and SJOE, E. L. F., 1974, Blood groups and immunoglobulin groups in Trio and Wajana Indians from Surinam. American Journal of Human Genetics, 26, 45-53.
GERSHOWITZ, H., LAYRISSE, M., LAYRISSE, Z., NELL, J. V., BREWER, C., CHAGNON, N., and AYRES, M., 1970, Gene frequencies and microdifferentiation among the Makiritare Indians. I. Eleven blood group systems and the ABH-Le secretor traits: a note on Rh gene frequency determinations. American Journal of" Human Genetics, 22, 515-525.
KELLER, J., PI SUNYER, X., PLANT, T., and MARKS, P. A., 1960. Incidence of erythrocyte glucose-6- phosphate dehydrogenase among different population groups in Surinam. Unpublished data, cited by Motulsky (1960).
LARROUY, G., MARTI, Y., and RUFFII~, J., 1964, l~tude h~motypologique des populations indiennes de la Guyane Frangaise. I. Les groupes 6rythrocytaires. Bulletin et Mkmories de la Societ~ d'Anthropologie de Paris, XI s6rie, 7, 107-117.
LAVRISSE, M., LAYR1SSE, Z., and WILBERT, J., t963, The blood groups of northern continental Cafibs. Human Biology, 35, 140-166.
MATSON, G. A., SUTTON, H. E., PESSOA, E. M., SWANSON, J., and ROBINSON, A., 1968, Distribution of hereditary blood groups among Indians in South America. V. In Northern Brazil. American Journal of Physical Anthropology, 28, 303 330.
MOTULSKY, A. G., 1960, Metabolic polymorphisms and the role of infectious diseases in human evolution. Human Biology, 28, 28-62.
NELL, J. V., GERSHOWITZ, H., SPIELMAN~ R. S., M1GLIAZZA, E. C., SALZANO, F. M., and OLIVER, W. J., 1977, Genetic studies of the Macushi and Wapishana Indians. II. Data on 12 genetic polymorphisms of the red cell and serum proteins: gene flow between the tribes. Human Genetics, 37, 207- 219.
NELL, J. V., MOHRENWE1SER, H. W., ROTHMAN, E. D., and NAIOU, J. M., 1986, A revised indirect estimate of mutation rates in Amerindians. American Journal of Human Genetics, 38, 649 666.
SALZANO, F. M., BLACK, F. L., CALLEGARI-JACQUES, S. M., SANTOS, S. E. B., WEIMER, T. A., MESTRINER, M. A., KUBO, R. R., PANDEr, J. P., and HUTZ, M. H., 1991, Blood genetic systems in four Amazonian tribes. American Journal of Physical Anthropology, 85, 51-60.
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Genetics o f South Amer i can Indians 201
SALZANO, F. M., BLACK, F. L., CALLEGARI-JACQUES, S. M., SANTOS, S. E. B., WE1MER, T. A., MESTRINER, M. A., PANDEY, J. P., HUTZ, M. H., and RIEGER, T. T., 1988, Genetic variation within a linguistic group: Apalai-Wayana and other Carib tribes. American Journal of Physical Anthropology, 75, 347-356.
SALZANO, F. M., MOHRENWEISER, H., GERSHOWITZ, H., NEEL, J. V., MESTR1NER, M. A., SIMOES, A. L., CONSTANS, J., and FREITAS, M. J. M., 1984, New studies on the Macushi Indians of northern Brazil. Annals of Human Biology, 11, 337-350.
SALZANO, F. M., WEIMER, T. A., FRANCO, M. H. L. P., Hu'rz, M. H., MESTRINER, M. A., S1M()ES, A. L., and FREITAS, M. J. M., 1985, Demography and genetics of the Sater6-Maw6 and their bearing on the differentiation of the Tupi tribes of South America. Journal of Human Evolution, 14, 647-655.
SALZANO, F. M., WOODALL, J. P., BLACK, F. L., WE~TKAMP, L. R., and FRANCO, M. H. L. P., 1974, Blood groups, serum proteins and hemoglobins of Brazilian Tiriyo Indians. Human Biology, 46, 81-87.
SANTOS, S. E. B., GUE~REIRO, J. F., and AGUIAR, G. F. S., 1987, Polimorfismos prot6icos em indigenas da Amaz6nia: tribos Arawet6, Karara6 e Karitiana. Ci~ncia e Cultura, 39 (Supl.), 757.
SCHAAD, J. D. G., 1960, Epidemiological observations in Bush Negroes and Amerindians in Surinam. Tropical and Geographical Medicine, 12, 38 46.
TANIS, R. J., NEEL, J. V., DOVEY, H., and MORROW, M., 1973, The genetic structure of a tribal population, the Yanomama Indians. IX. Gene frequencies for 18 serum protein and erythrocyte enzyme systems in the Yanomama and five neighboring tribes: nine new variants. American Journal of Human Genetics, 25, 655-676.
TCHEN, P., BOlS, E., LANSET, S., and FEINGOLD, N., 1981, Blood group antigens in the Emerillon, Wayampi, and Wayana Amerindians Of French Guiana. Human Heredity, 31, 47 53.
TC~E~, P., Bors, E., SEGER, J., GRENANO, P., FEINGOLD, N., and FEINGOLD, J., 1978, A genetic study of two French Guiana Amerindian populations. I. Serum proteins and red cell enzymes. Human Genetics, 45, 305-316.
WARD, R. H., GERSHOWITZ, H., LAYRISSE, M., and NEEL, J. V., 1975, The genetic structure of a tribal population, the Yanomama Indians. XI. Gene frequencies for 10 blood groups and the ABH-Le Secretor traits in the Yanomama and their neighbors; the uniqueness of the tribe. American Journal of ttuman Genetics, 27, 1 30.
WEIMER, T. A., CORVELLO, C. M., and SALZANO, F. M., 1984, The acid phosphatase polymorphism: new data and review of results in Amerindians. Interciencia, 9, 401-403.
WErrKAMP, L., and NEEL, J. V., 1970, Gene frequencies and microdifferentiation among the Makiritarc Indians. III. Nine erythrocyte enzyme systems. American Journal of Human Gene~ics, 22, 533-537.
Zusammenfassung. In einer Carib sprechenden Bev61kerung von Wai Wai lndianern aus dem n6rdlichen Brasilien wurden demographische, medizinische und genetische Daten gesammelt. Gegenwfirtig ist die Mortalitfit goring und die Fertilitfit moderat mit ciner geringen Varianz der Zahl der Nachkommen in kompletten Familien. Die Mobilit/it ist hoch, dennoch sind etwa zwei Drittel der Ehen endogam. Malaria stellt das gr613te Gcsundheitsproblem dar. Ein Vergleich mit sechs anderen Carib-Gruppen liel3 die gr613ten Affinit/iten zu einem anderen Amazonasstamm, den Arara, erkennen. Eine Quantifizierung der Genetic Diversity innerhalb und zwischen den sieben Populationen zeigt, daB die Variationen innerhalb der Gruppen nur geringf/igig niederiger sind als die Variation zwischen den Gruppen. Andererseits ist der Grad der Diversity zwischen den Carib sprechenden Populationen nicht signifikant von dem verschieden, der ffir 11 Tupi sprechende Populationen beobachtet werden konnte. In Ubereinstimmung mit der Geschichte der Heiraten zwischen den Gruppen sind die Wai Wai, die sich selbst als getrennte Gruppe betrachten, innerhalb der Bev61kerung deutlich st/irker differenziert als zumindest drei der sechs Carib Bev61kerungen, mit denen sie verglichen wurden.
Resum& Des informations d6mographiques, m6dicales et gbndtiques ont 6t6 recueillies dans une population d'indiens Wai Wai de langue caraibe, vivant au nord du Brbsil. La mortalitb y est actuellement basse et la f6condit6 mod6r~e, avec une faible variance du nombre d'enfants dans les families compl6t6es. La mobilit+ est 61evde mais environ deux-tiers des unions sont endogames. Le paludisme est le principal probldme sanitaire. Des fr~quences all61iques et ph~notypiques ont ~t6 obtenues pour 25 systemes g6n6tiques et de prot6ines. Leur comparaison avec six autres groupes caraibes indique des affinit6s plus marqu6es avec une autre tribu amazonienne, les Arara. La quantification de la diversit6 g~n6tique intra- et inter-populationnelle dans ces sept populations, indique que la variation intra-groupe est seulement 16g6rement inf6rieure ~. la variation inter-groupe. Par ailleurs, le niveau de la diversit6 interpopulationnelle caraibe ne diffdre pas signifieativement de celui qui est trouv6 parmi 11 populations de langue Tupi. En conformit6 avec leur histoire d'intermariages avec des groupes qui parlent des langues 16gdrement diff~rentes et qui se consid&rent distincts, les Wai Wai pr6sentent une diversit6 intrapopulationnelle plus forte que celles d'au moins trois des six populations caraibes avec lesquelles ils sont compar6s.
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