Unusual Blood Genetic Characteristics among the Indians of and

By F. M. Salzano,1 F. Pages,2 J. V. Neel,3 H. Gershowitz,3 R. J. Tanis,3 R. Moreno4 and M. H. L. P. Franco1

ABSTRACT

A total of 363 Ayoreo Indians living in throe localities of southern Bolivia and northern Paraguay were studied in relation to 33 genetic systems which are expressed in blood and one in saliva. The degree of intratribal diversity observed is not large, in agreement with the considerable rate of exogamy found among them. They are unusual among South American Indians in showing no variation at the Esterase D locus (Es D\: 1.00), very high frequencies of LMS (MNSs blood groups) and ACPA (acid phos- phatase system), as well as a low frequency off". No Diego (a) or Gin (x) positives were found among them. The frequencies of the other markers do not differ appreciably from those commonly encountered and no rare variants were observed. A six-locus comparison of the Ayoreo with 21 other Middle or South American tribes shows genetic distances that are generally larger than those obtained with any other of these groups.

The Ayoreo (Ayoweo) or Vloro Indians form what is probably the only relatively unacculturated tribe remaining in the southern part of . Therefore, they have been included in a general project of investigation that we have been conducting for many years, which aims at understanding the most salient features of the evolutionary processes which have shaped the gene pool of South American Indians, as well as those of populations living at a similar level of technological development (Neel and Salzano, 1964; Neel et al. 1977b). The Ayoreo speak a language classified as being of the Zamuco stock. They live in nine missions scattered over southern Bolivia and northern Paraguay, with a few families still having an independent life in the mountains. Their habitat can be delimited by a northern-southern axis that extends between 16°S and 22°S, and an eastern-western line that can be set between 58°YV and 63°W. They number about 1,200 individuals.

'Departamento tie Genetica, Institute) de Biociencias, Universidade Federal do Rio Grande do Sul, 90000 Porto Alegre. RS, . 2Consejo Nacional de Investigaciones Cientifieas y Tecnicas, Buenos Aires, . ^Department of Human Genetics, University of Michigan Medical School, 1137 E. Catherine Street, Ann Arbor, Michigan 4H109. Mnstituto de Ciencias Bask-as, Univesidad Nacional de Asuncion, Asuncion, Paraguay.

Human Biology. May 1978, Vol. 50, No. 2. pp. 121-136. • Wayne Slate University Press, 1:978 122 /•'. M. Salzano, et al.

The present report describes data related to 33 genetic systems which are expressed in blood and one in saliva, obtained in three Ayoreo vil- lages. These results are compared with previous, more limited genetic investigations, as well as with other demographic and morphological studies performed on them; and with gene frequencies obtained in other Middle and South American tribes. It will be seen that the Ayoreo pre- sent a series of characteristics that are unusual when we consider previous research done among Indians ol this continent.

MATERIALS AND METHODS

The blood and saliva collections were made in six trips to three localities as follows: 1. Mission of Maria Auxiliadora. It is located 450 km north of Asuncion, in Paraguay, at the margins of the Paraguay River and facing the Brazilian town of Porto Murtinho. This mission was founded in 1963 and at present some 3(K) Indians live near it. 2. Tolrite. Situated 25 km northwest of the railroad station of El Porton, 370 km east of Santa Cruz, this is the oldest of present-day missions having Ayoreo Indians. It was founded more than 16 years ago and is inhabited by 46 families of this tribe. 3. Poso Verde. Located some 9 km south of the railroad station of El Pailon, some 50 km east of Santa Cruz, the Pozo Verde mission was established some 10 years ago and 62 Moro families live there now. Appropriate sampling of such small communities is always a problem (see, for instance, Ward and Neel, 1970). We generally try to study the maximum number of persons in each group, irrespective of stated or known relationships, since with the absence of written records more re- mote links remain undetected. Since the majority of the members of each village are studied, this can be characterized more as an enumerative than a sampling procedure. The statistical problems that appear under these circumstances were discussed by Smith (1969). The samples were collected in vacutainers and chilled as soon as pos- sible. They were then shipped on ice to the testing laboratories. The methods employed in the blood group, enzyme and serum protein de- terminations have been described or referenced elsewhere (Salzano et al. 1974, 1977; Neel et al. 1977a, 1977c). The saliva studies were performed as described in Salzano et al. (1970).

RESULTS

Table 1 presents the phenotypic data related to 13 genetic systems investigated through immunological tests. Table 2 presents those ob- Table 1 Genetic Markers Detected by Immunological Methods studied among the Avoreo Indians

M Auxiliudora Toliite Pozo Verde Total Plienotypes N % N % N % N %

ABO O 185 100 105 100 .56 100 .346 100.0

MNSs1 MS 95 51 4S 46 31 55 174 50.3 MSs 67 .36 .34 32 22 39 123 35.6 Ms 16 9 6 6 2 4 24 6.9 MNSs 7 4 12 11 1 2 20 5.8 MNs 0 0 5 5 0 0 5 1.4 Total 185 100 105 100 .56 100 346 100.0

P2 P. 27 30 15 14 17 30 59 23.5

P2 63 70 90 86 39 70 192 76.5 Total 90 100 105 100 56 100 251 100.0

Rh3 CDe 100 54 50 48 25 45 175 .50.6 cDE 13 i 11 10 5 9 29 8.4 CcDEe 70 38 41 39 26 46 137 39.6 CcDe 2 1 0 0 0 0 2 0.6 CDEe 0 0 3 3 0 0 3 0.8 Total 185 100 105 100 56 100 346 100.0

continued Jo Table 1 (continued)

\1 \uxiliadora Tobite Pozo Verde Total Phenotypes <7R

Kell4 K (-! 185 100 105 100 .56 100 346 100.0 Lewis Le (a—b+) 64 71 31 57 95 66.0 Le (a—b—) 26 29 23 43 49 34.0 Total 90 100 ,54 100 144 100.0 Duffy Fy (a+b-) ,56 62 38 70 91 65.3 Fy (a+b + ) 29 32 16 30 45 31.2 Fy (a-b+) 5 6 0 0 5 3.5 Total 90 100 .54 100 144 100.0 s Fy (a+) 90 95 96 91 2 100 188 93.1 Fy (a-) 5 5 9 9 0 0 14 6.9 Total 95 100 105 100 2 100 202 100.0 Kidd

Jk (a+) 81 90 5 100 50 89 1.36 90.1 Jk la-) 9 10 0 0 6 11 15 9.9 Total 90 100 5 100 56 100 151 100.0 Diego Di (a-) 185 100 102 100 100 341 100.0 Wright Wr (a-) 90 100 — — 54 100 144 100.0

Sec 188 100 - — — — 188 100.0

Cm6 ag 102 100 101 100 .53 98 2.56 99.6 agfl)01 0 0 0 0 1 2 1 0.4 total 102 100 101 100 54 100 257 100.0

1+ 65 64 72 71 23 44 160 62.7 1- 37 36 29 29 29 56 95 37.3 Total 102 100 101 100 52 100 255 100.0

1+3- 26 26 — — — — 26 25.5 1+3 + 39 38 — — — — 39 38.2 1-3+ 37 36 — — — — 37 36.3 Total 102 100 — — — — 102 100.0

'Ninety samples from Maria Auxiliadora were also tested with anti-Mv; no indication of the presence of the Mv antigen was found. These bloods and those from Pozo Verde were all negative for He, M', and Vw. 2 All P2 cells from Maria Auxiliadora and Pozo Verde showed positive reactions with anti-PP, 3All C(+) wre Cw (-). ^Ninety samples from Maria Auxiliadora and all from Pozo Verde were Kp (a—b + ). Those from Pozo Verde were all Js (a—). 5Tests with anti-Fyb not performed. 6All samples tested with anti a, x, g, f. b°, b1. Those from Pozo Verde were also tested with anti-t. The agfb0' sample was found to be positive for b3 also. Table 1 Genetic Markers Detected by Electrophoretic Methods studied among the Avoreo Indians

M. Auxiliadora Tobite Pozo Ve rde Total PhenoHpes N % N 9 N <7R \ %

Haptoglobins 1-1 .39 19 18 17 19 35 76 20.9 2-1 92 45 53 52 24 43 169 46.6 2-2 74 36 32 31 12 22 118 32.5 Total 205 100 103 100 55 100 363 100.0

Group specific component 1-1 .56 55 •55 38 70 149 .58.0 2-1 45 44 38 38 13 24 96 37.3 2-2 2 2 i . 3 6 12 4.7 Total 103 100 100 100 54 100 257 100.0

Acid phospha- tase A 11 3 — — 1 3 12 9.9 AB 41 49 — — 8 21 49 40.5 B 32 38 — — 28 76 60 49.6

Total 84 100 — — 37 100 121 100.0

Phosphoglu- comutase 1 1-1 59 70 35 69 30 60 124 67.0 2-1 22 26 12 23 20 40 54 29.2 2-2 3 4 4 8 0 0 1 3.8 Total 84 100 51 100 50 100 185 100.0 Phosphoglu eomutase 2 1-1 84 100 49 100 50 100 183 100.0 6-PhosphogIuco- nate dehydroge- nase A 71 100 54 100 .50 100 175 100.0 lactate dehydro- genase Normal 84 100 51 100 50 100 1»5 1000 Adenylate kinase 1-1 83 100 49 100 50 100 182 100.0 Malate dehydrogenase Normal 85 100 51 100 50 100 186 100.0 Adenosine deaminase 1-1 82 100 49 100 50 100 181 100.0 Transferrin C 103 100 102 100 54 100 259 100.0 Ceruloplasmin B 103 100 101 100 54 100 258 100.0 Albumin1 A 198 100 105 100 55 100 358 100.0 Peptidase A 1-1 &3 100 43 100 12 100 138 100.0

continued Table 2 (continued)

M Auxiliadora Tobite Pozo Verde Total Phenotypes N <2 N N <7c N %

Peptidase B 1-1 8.5 100 51 100 50 100 186 100.0

Phosphohexo.se isomerase 1-1 85 100 51 100 .50 100 186 100.0

Isocitrate dehydrogenase Normal 85 100 .50 100 50 100 185 100.0

Esterase D2 1-1 111 100 30 100 141 100.0

Esterases A,

A2, A3, B Normal 111 100 30 100 141 100.0

Carbonic anhy- drases I and 11 Normal 111 100 30 100 141 100.0

Hemoglobin A 182 100 104 100 56 100 342 100.0

'Three samples from Tobite and one sample from Pozo Verde showed suggestions of variants in one of the buffer systems used. New collections in two of the Tobite persons involved could not confirm the presence of a variant 'The data from Maria Auxiliadora have been already reported in Mestriner et id. (1976). The number of individuals studied is 111 and not 112 as was indicated there by mistake. 1.33 Ayoreo Blood Genetics tained by electrophoretic methods. The total number of samples collected was 363, but due to a variety of reasons (transportation problems, un- availability of reagents in one laboratory, etc.) there is variation in the number studied for the different genetic markers. Gene frequencies for the systems which showed variation are presented in Table 3. The degree of intratribal diversity is not very large: in only five of the 18 alleles considered are the differences greater than 10% (AC'PA, Inv', Hp\ Ftja, and Le). The localities which showed the greatest similarity in gene fre- quencies were Maria Auxiliadora and Tobite, while those that are closer geographically are Pozo Verde and Tobite. It should be noted, however, that we are dealing with highly mobile individuals, and that the missions have been founded at a relatively recent time. Data to be reported else- where (Perez Diez and Salzano, 1978) also show considerable exogamy in all groups considered. Turning now to intertribal comparisons, we see that the Ayoreo pre- sent unusual frequencies for six of 22 alleles which show variability among South American Indians and were studied here. Only Es D1 was found in the individuals tested (Table 2), while investigations in other tribes of the continent presented values of Es Dl ranging from 0.36-0.86 (Mestriner et al. 1976). Allele LMS was observed in a frequency of 0.71, while previous studies involving sample sizes equal to or larger than 90 individuals showed values varying from 0.05 to 0.46. The ACPA gene frequency (0.30) is also high, the largest frequency observed in South American Indians for this allele so far being 0.23. On the other hand, P1 presented a very low prevalence (0.12; earlier studies: 0.28-0.91) and Gmax did not appear. In relation to the latter, only one other South America tribe in 25 (the Chipaya) showed a similar absence, the allele reaching as high a fre- quency as 0.54 among the Palikour (references in Salzano et al. 1973). Special mention should be made of the absence of Diego a-positives. Up to now some 1(X) South American Indian tribes have been studied in relation to this antigen and only four besides the Ayoreo showed its absence when sample sizes higher than 100 persons were investigated: the Venezuelan Bari, Warao and Yanomama (Layrisse and Wilbert, 1966 and unpublished; Ward et al. 1975) and the Colombian Noanama (Kirk et al. 1974). To these we should add the Panamanian Cuaymi (Matson and Swanson, 1965; unpublished data from the Michigan group). The other frequencies were not very different from those usually en- countered. Se, C'pB, R' and JhB showed numbers in the upper third of the observed range in other tribes; PCM1,, F[/a, Gc1, Inv1 and R2 presented values in the middle portion of this range; andLNS, Rz, fl°orr, LNs, Le and Hp1 in its lower third. 130 F. M. Salzano, et al.

Table 3

Gene Frequencies in the Systems which showed Variation among the Ayoreo Indians

Gene Maria Pozo frequencies Auxiliadora Tobite Verde Total

MNSs J MS 0.71 0.68 0.76 0.710 J Ms 0.27 0.24 0.23 0.2.54 0.00 0.00 0.00 0.000 0.02 0.08 0.01 0.036

P P' 0.16 0.07 0.17 0.125

Rh R' 0.73 0.69 0.68 0.711 R' 0.26 0.30 0.32 0.282 R' 0.00 0.01 0.00 0.004 R" or r 0.01 0.00 0.00 0.003

Lewis

U 0.46 — 0.35 0.417

Duffy Fy" 0.78 0.71 0.85 0.766

Kidd

Jk> 0.68 — 0.67 0.685

Cm Cm" 1.00 1.00 0.99 0.998 Cm"' 0.(X) 0(H) 0.01 0.002

Inv Inv1 0.45 0.46 0.25 0.390

Haptoglobins lip' 0.41 0.43 0.56 0.442 Group-specifie component Gc' 0.24 0.26 0.18 0.234

Acid phosphatase A ACP 0.37 — 0.14 0.302

Phosphogluco- mutase 1 PCM\ 0.83 0.80 0.80 0.816 Table 1 Six-locus Genetic Distances (x 103) between 22 Middle or South American Indian Tribes

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

2. 257 3. 290 420 4 .300 295 421 5. 244 243 284 308 6. 351 222 479 2S1 296 7. 514 389 654 489 536 339 8. 321 276 420 267 279 338 470 9. 310 252 452 390 215 293 501 352 10. 246 197 338 286 182 205 402 .311 258 11. 334 242 382 339 230 236 469 401 321 149 12. 318 363 430 324 •310 408 532 202 332 345 467 13 255 246 339 224 226 312 453 199 345 221 299 270 14. 392 a59 414 4S6 254 465 670 438 282 385 3S4 466 395 15. 291 317 300 389 222 357 601 419 .341 290 262 468 323 312 16. 288 216 ,362 299 129 207 467 265 190 190 237 320 247 300 243 17. 330 313 387 364 251 359 581 367 314 349 352 438 315 247 230 232 18. 374 244 446 342 228 223 430 277 216 251 302 346 304 334 366 143 291 19 460 377 474 401 472 408 423 410 586 397 407 557 360 610 490 4.56 495 464 20 450 322 •169 •324 327 235 467 355 409 301 285 478 365 481 407 270 388 248 366 21. 276 171 413 260 219 295 495 270 292 218 239 341 205 352 311 24 S 336 .308 427 22. 532 497 655 336 .544 410 574 462 542 535 576 502 495 662 584 473 490 468 580

Tribal designation: 1: Aymara; 2: Cakchiquel; 3: Cashinaua; 4: Cayapa; 5: Cayapo; 6: Cuna; 7: Guaymi; 8. Jivaro; 9: Makiritare; 10: Macushi, 11: Pemon, 12: Piaroa, 13: Quechua; 14: Shipibo; 15: Trio; 16: Wapishana; 17: Wajana; 18: Xavante; 19: Yanomama; 20: Yupa; 21: Kraho; 22: Ayoreo. 132 /•'. M. Salzano, et al.

No rare variants were observed witb respect to phosphoglucomutase 2, 6-phosphogluconate dehydrogenase, lactate dehydrogenase, adenylate kinase, malate dehydrogenase, adenosine deaminase, transferrin, ceruloplasmin, albumin, peptidases A and B, phosphohexose isomerase, isocitrate dehydrogenase, esterase A,,2.3 or esterase B, carbonic anhy- drases I and II and hemoglobin. As is indicated in the footnote of Table 2, three samples from Tobite and one from Pozo Verde showed suggestions of albumin variants in one laboratory (either Ann Arbor or Porto Alegre) which could not be confirmed in the other. New collections in two of the Tobite persons involved could not confirm the unusual pattern. We there- fore decided to consider the previous results as artifacts. The absence of rare phenotypes is somewhat at variance witb our previous studies, but it should be noted that tbe number of samples tested for some of these systems was not high (Table 2). Ward et al. (1975) recently obtained a 6-locus (Rh, MNSs, Kidd, Duffy, Diego and Haptoglobin) matrix of genetic distances for 20 tribes of Middle and South America. We have now extended that matrix to include the Kraho (cf. Salzano et al. 1977) and the Ayoreo (these data). At the same time, the matrix lias been updated to take advantage of more recent data on the Macushi and Wapishana (Neel et al. 1977a), plus the now published data of Geerdink et al. (1974a, b) on the Trio and Wajana. Rh gene frequencies have been computed on the assumption that only four alleles are present (ft1, R2, Rz and R" or r). Finally, tbe distances are now "chord distances rather than the "stereographic projections of these distances (cf. Edwards, 1971) which were employed by Ward et al. (1975) (Table 4). The Ayoreo show distances that are generally higher than those calculated when we compare other groups. As a matter of fact, their average (0.52) is larger than those obtained for any other tribe (range: 0.28-0..50; mode: 0.35). No clear pattern can be discerned when we try to correlate these genetic with the geographic distances. For instance, the smallest value (0.34) was observed between the Ayoreo and the Cayapa. who live in the northern part of South America, and the largest (0.66) between them and the Shipibo, whose villages are located much closer to the Ayoreo territory. If we consider these facts concerning genetic dis- tance in conjunction with the unusual gene frequencies mentioned above at the AGP, ESI). ('.111 and P' loci, the outlying position of the Ayoreo is even more apparent. Unfortunately, because of lack of data on many of the tribes treated in 'fable 4, the matrix cannot yet be extended to include these loci. Ayoreo Blood Genetics 1.33

DISCUSSION

The first historical documents about the Zamucoan tribes date back to the end of the 17th century. Detailed accounts about them can be found in Metraux (1946) and Kelm (1963). According to the former, the Ayoreo (Moro) undoubtedly are the remnants of the ancient Zamucoan Morotoco and Guaranoca. Kelm (1963) goes further, suggesting that the Ayoreo are a product of the fusion of several Zamucoan-speaking groups. Population estimates about the latter are available for the beginning of the 18th and 19th centuries, and amount to about 2,000 individuals. Since the now number some 1,200 persons, we should probably conclude that they have not had much demographic decline during these three centuries (especially if we consider that the numbers cited in historical sources can generally be viewed as approximate only). If to this informa- tion we add the data we have, indicating a high rate of exogamy, it is difficult to suggest genetic drift as an explanation for the unexpected genetic features of the Ayoreos. \latson et al. (1968) studied 36 Ayoreo from Maria Auxiliadora, and their figures are similar to those we obtained for LMS, P1 and Dia. How- ever, the frequency they obtained for Jka (0.20) is much lower than the one found here (0.67). Brown et al. (1974) tested 73 persons from this same locality. Their results are in agreement with ours in relation to LMS and Pl, while only one in 71 individuals proved to be Gm (ax); unfortu- nately, they have not done studies in the Diego and Kidd systems. Neither of these two investigations showed data on the Esterase D (dis- covered in 1973) or acid phosphatase polymorphisms. We are left, there- fore, without confirmatory evidence for the unusual Es Dl and ACPA observations. Matson et al. (1968) also studied 88 persons who were living at the time near Bahia Negra and Fuerte Olimpo, at the margins of the Paraguay River. They were members of the , the only other extant Zamucoan-speaking tribe. Two individuals were non-O (ABO system), suggesting some admixture in this group; but its amount seems to be sufficiently small to allow safe comparisons with the Ayoreo. Similarities were observed in the Rh, Duffy and haptoglobin systems, but somewhat different values in the MNSs, P, Kidd and Lewis blood groups. Two of the 86 persons tested for Diego showed the Dia antigen; since this could be due to intercrossing with other tribes, there is a possibility that all Zamu- coan tribes were Diego a-negatives. 134 /•'. M. Salzano, et al.

Are the Ayoreo unusual in relation to other characteristics, besides the genetic markers already mentioned? To test that we compared the an- thropometric data obtained by Vellard (1972) among the Ayoreo of Maria Auxiliadora (66 males and 72 females) with the information compiled by Comas (1971) on other South American Indians (scries with at least 30 individuals of each sex). Results concerning just one measure and six indices were available for comparison: stature, cephalic index, length- height cephalic index, breadth-height cephalic index, morphological facial index, nasal index and cormic index; and interestingly enough, for three of the seven characteristics the Ayoreo showed values outside the range commonly found among Indians of this continent! They have a very low cephalic index (72.5 in males (M); 72.6 in females (F); range in South American Indians (SAI): 74.5-84.0 and 75.2-84.8 in the two sexes, respec- tively). As for the length-height cephalic index the numbers were: M:64.2; F:61.2; SAI:65.7-73.3 and 67.8-70.5; and for the nasal index: M:90.3; F:91.9; SAI:62.2-84.9 and 62.0-80.1. They can be characterized, therefore, as extremely dolieocephalic, hypsicephalic and platyrrhine; that is, they have long and high heads, but, curiously, broad noses. The genetic distances compiled comparing Middle and South Ameri- can tribes two by two show a wide range of variation (from 0.13 to 0.67). The Wapishana present the lowest average (0.28), and the Ayoreo, as mentioned, the largest (0.52). There is no clear tendency for these aver- age distances to cluster around some group of values. The number of tribes studied simultaneously for the six chosen alleles is still small; there- fore, the correlations that we can make between this pattern of variation and those of their languages or cultures are limited. We are still far away from establishing a coherent picture of the complex chain of events that led to the present genetic diversity of American Indians.

ACKNOWLEDGEMENTS

Thanks are due to A. A. Perez Diez for help in the field work; to C. V. Simoes, F. A. de Sa and M. Regina Borges Osorio for laboratory help; and to members of the missions ol M. Auxiliadora, Tobite and Pozo Verde who aided us in many ways. This research was supported by the Camara Especial de Pos-graduagao e Pesquisa da Universidade Federal do Rio Grande do Sul, Conselho Nacional de Desenvolvimento Cientifico e Tec- nologico (Programa Integrado de Genetica), Coordenagao do Aperfeigo- amento de Pessoal de Nivel Superior, Fundayao de Amparo a Pesquisa do Estado do Rio Grande do Sul, Consejo Nacional de Investigaciones 1.33 Ayoreo Blood Genetics

Cienti'ficas y Tecnicas (Argentina), the Energy Research and Development Administration and the National Science Foundation.

Received: 25 April 1977. Revision Received: 1 September 1977.

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