Genomic ancestry of rural Africanderived populations from
Transcrição
Genomic ancestry of rural Africanderived populations from
AMERICAN JOURNAL OF HUMAN BIOLOGY 25:35–41 (2013) Original Research Article Genomic Ancestry of Rural African-Derived Populations from Southeastern Brazil LILIAN KIMURA,1ELZEMAR MARTINS RIBEIRO-RODRIGUES,2,3MARIA TERESA BALESTER DE MELLO AURICCHIO,1 JOÃO PEDRO VICENTE,4SIDNEY EMANUEL BATISTA SANTOS,2 AND REGINA CÉLIA MINGRONI-NETTO1* 1 Centro de Estudos do Genoma Humano, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil 2 Laboratório de Genética Humana e Médica, Departamento de Patologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil 3 Instituto de Criminalı́stica, Centro de Perı́cias Cientı́ficas Renato Chaves, Belém, Pará, Brazil 4 Departamento de Pediatria, Instituto da Criança, Hospital das Clı́nicas, Faculdade de Medicina, Universidade de São Paulo, Brazil Objectives: Many Africans were brought to Brazil as slaves. The runaway or abandoned slaves founded isolated communities named quilombos. There are many quilombo remnants in Vale do Ribeira region in the southern part of São Paulo State. The aim of our study was to contribute to understanding the origins of these populations, through admixture studies. Methods: We genotyped 307 unrelated DNA samples obtained from ten quilombo populations from Vale do Ribeira region, using a panel of 48 INDEL polymorphisms. We estimated genetic differentiation between populations (FST) and genomic ancestry from these populations. Our data were compared to a similar study performed in quilombo remnants from the Brazilian Amazon region. Results: Population admixture estimates showed high degree of miscegenation in the quilombo remnants from Vale do Ribeira (average admixture estimates at 39.7% of African, 39.0% of European and 21.3% of Amerindian contribution). The proportions of ancestral genes varied greatly among individuals, ranging from 7.3 to 69.5%, 12.9 to 68.3%, and 7.3 to 58.5% (African, European, and Amerindian, respectively). Genetic differentiation between these populations was low (all FST values <5%), indicating gene flow between them. Both groups of quilombos, from Vale do Ribeira and Amazon, presented similar patterns of admixture. Conclusions: INDEL markers were useful to evidence the triple interbreeding among African, European, and Amerindian in the formation of quilombo populations. The low FST values suggested gene flow among quilombos from Vale do Ribeira. Our data highlight the important role of Amerindians in the formation of quilombo populations. Am. J. Hum. Biol. 25:35–41, 2013. ' 2012 Wiley Periodicals, Inc. INTRODUCTION The present Brazilian population is one of the most genetically heterogeneous populations of the world. Portuguese colonizers first came to Brazil in 1500 and found a heterogeneous native population of around 2,000,000 people. Between 1550 and 1850, about 4,000,000 Africans were brought as slaves from several Sub-Saharan regions, and were distributed among the distinct regions of Brazil (Klein, 1999). The process of admixture in Brazil started soon in 1500 between Portuguese and Amerindians, and continued later, with the arrival of the slave population, since it was extended to Africans. Before the abolition of slavery in Brazil (in 1888), many populations, named quilombos, were founded by runaway or abandoned African slaves. Formed mainly in isolated areas, they are presently known as quilombo remnants. The presence of numerous archaeological sites proves that human occupation in Vale do Ribeira, in southeastern Brazil region, predates the arrival of Portuguese in the 16th century (Neves and Okumura, 2005). This region was a route for Amerindians to reach the cost, centuries before the first incursions of Portuguese into Brazil. In 16th century, Portuguese explorers arrived to Vale do Ribeira, establishing the first settlements in the region. During the 17th century many Africans were brought into the region as slaves to exploit gold mining. As a consequence of the lack of success of gold exploitation, the abandoned slaves founded quilombos in this region. Nowadays C 2012 V Wiley Periodicals, Inc. there are many quilombo remnants in the Vale do Ribeira region, populations who live at the borders of one of largest remnants of Atlantic rain forest, in the southern part of São Paulo State. The region of Vale do Ribeira is marked by the presence of many Conservation Units, and is one of the most important biological and cultural diversity hotspots of the country. The quilombo remnants survived in locations where the characteristic steep terrain made human occupation peculiarly difficult, maintaining these populations in a certain degree of geographical isolation. Some studies have been performed with quilombo remnants samples in an attempt to estimate the contribution of ancestral populations to their present populations, using classical polymorphisms (Arpini-Sampaio et al., 1999; Bortolini et al., 1997; Guerreiro et al., 1999), polymorphisms of nuclear DNA—VNTRs, STRs, and Alu insertions (Bortolini et al., 1999; Cayres-Vallinoto et al., 2003, Cotrim et al., 2004; Da Silva et al., 1999; Scliar Contract grant sponsors: Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP); Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq). *Correspondence to: Regina C. Mingroni-Netto, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, CP 11461, São Paulo, SP, CEP: 05422-970, Brazil. E-mail: [email protected] Received 22 May 2012; Revision received 2 October 2012; Accepted 5 October 2012 DOI 10.1002/ajhb.22335 Published online 2 October 2012 in Wiley Online Library (wileyonlinelibrary.com). 36 L. KIMURA ET AL. et al., 2009), mitochondrial DNA markers (Bortolini et al., 1999; Carvalho et al., 2008; Ribeiro-dos-Santos et al., 2002) and Y chromosome polymorphisms (Abe-Sandes et al., 2004; Bortolini et al., 1999; Ribeiro et al., 2009, 2011). In general, uniparental markers (mitochondrial DNA and Y chromosome markers) revealed the demographic phenomenon of directional mating of European males to Amerindian and African females; the classic and nuclear DNA polymorphisms showed a tri-hybrid pattern of admixture among African, European and Amerindian, in different proportions. In most cases, the greatest contribution found was that of African genes, as expected. Studies about human genetic variability and human evolutionary history have become more informative and more accurate with the study of DNA polymorphisms, especially polymorphisms named ancestry informative markers (AIMs). AIMs are genetic markers that exhibit significant differences (>40%) in the allelic frequencies between populations of distinct geographical origins (Parra et al., 1998; Santos et al., 2010). More recently, ancestry informative markers of the INDEL type became the focus of several studies to investigate global and individual estimates of the proportion of ancestral genes in many populations, including Brazilians (Lopes Maciel et al., 2011; Pereira et al., 2012; Ribeiro-Rodrigues et al., 2009; Santos et al., 2010; Weber et al., 2002). These markers present many interesting genetic features: (a) they are widely spread throughout all chromosomes, (b) they have low mutation rates, (c) they can be analyzed in short fragments (amplicons), which allows the amplification of degraded DNA, and (d) they can be identified by relatively simple and inexpensive genotyping techniques (Ribeiro-Rodrigues et al., 2009). In the present study, a panel of 48 AIMs was used to estimate individual and population interethnic admixture in unrelated individuals from ten African-derived quilombo populations from Vale do Ribeira, a valley region located in the southern part of São Paulo state. All markers used are INDEL type polymorphisms, which correspond to insertions (IN) or deletions (DEL) of small DNA fragments (between 3 and 40 bp). The INDEL panel used in this investigation was firstly described by Santos et al. (2010) and has been successfully used to assess parental genetic contribution in other populations (Lopes Maciel et al., 2011; Ota et al., 2010; Tarazona-Santos et al., 2011).The data were also used to estimate the genetic differentiation (FST) among the 10 quilombo populations in Vale do Ribeira. Our results were compared to those obtained from quilombos located in Amazonian region (Lopes Maciel et al., 2011). The aim of our study was to contribute to the understanding of the origins of Brazilian southeastern Africanderived populations, focusing on the quilombo remnants from Vale do Ribeira, through admixture studies. Because they remained at least partially isolated, they can be regarded as relics of the original parental populations that gave rise to the current Brazilian population. Our investigation is an elegant example of a study that integrates population history with genetic data, thus contributing to the understanding of the formation of Brazilian population. SUBJECTS AND METHODS Populations Quilombos from the Vale do Ribeira. A sample of 307 unrelated individuals from 10 African-derived quilombo American Journal of Human Biology populations of the Vale do Ribeira region was studied: Abobral (42 individuals), André Lopes (27), Nhunguara (43), Sapatu (32), Pedro Cubas (40), Galvão (11), São Pedro (24), Ivaporunduva (52), Pilões (27), and Maria Rosa (11). The localization of the quilombo populations investigated is shown in Figure 1. Further details about population sizes of the ten quilombos are shown in Auricchio et al. (2007). Quilombos from the Amazonian region. We compared our data with those from another study performed in seven quilombo populations of the Brazilian Amazon region (Lopes Maciel et al., 2011) with the same set of 48 AIMs. The localization of these populations is shown in Lopes Maciel et al. (2011). Parental populations The parental population samples consisted of 593 individuals representative of the three major ancestry groups of Brazilian population: Sub-Saharan Africans—189 individuals from Angola, Mozambique, Zaire, Cameroon, and the Ivory Coast; Europeans—161 individuals (mainly Portuguese); and Native Americans—243 individuals from seven indigenous tribes of the Brazilian Amazon region (Santos et al., 2010). The genotyping data of these samples relating to INDEL panel was used to estimate the individual and population interethnic admixture in the quilombo samples. DNA analysis DNA was extracted from whole blood using standard procedures. DNA samples were genotyped for the 48 biallelic INDEL by means of three 16-plex PCR amplifications, as described previously in Santos et al. (2010). This study was approved by the ethics committee of the ‘‘Instituto de Biociências da Universidade de São Paulo.’’ Informed consent was obtained from all participants in the study. Statistical analysis The statistical analysis for estimating the allele frequencies, the adherence of the observed genotypic frequencies to that expected under Hardy–Weinberg equilibrium (HWE), and the analysis of differentiation between populations (FST) were performed using the Arlequin v.3.1 software package (Excoffier et al., 2005). FST genetic distances were visualized in two-dimensional space using the multidimensional scaling (MDS) method, included in the software SPSS v. 14.0 (SPSS, Chicago, IL). The estimates of individual and global interethnic admixture were achieved using the software STRUCTURE v. 3.2, available free of charge at http://pritch.bsd.uchicago.edu/software.html. The basic algorithm was described by Pritchard et al. (2000) and extensions to the method were published by Falush et al. (2003 and 2007). The individual admixture estimates (IAEs) obtained using STRUCTURE were calculated assuming an Ancestry Model (GENSBACK 5 2 and MIGRPRIOR 5 0.05 under the ‘‘use population information’’ option) in which individuals of known origin (parental populations) were used to classify individuals of unknown origin (the quilombo populations), considering either correlated or independent ‘‘allele frequency 37 GENOMIC ANCESTRY OF AFRICAN-BRAZILIANS Fig. 1. (A) São Paulo state localization in Brazil. (B) Geographical location of Vale do Ribeira region in São Paulo. The black area corresponds to the location of the ten quilombo populations and the neighboring towns of Eldorado and Iporanga, showed in details in C. (C) Location of the ten quilombo remnants investigated and of the neighboring towns of Eldorado (248 30’ 7@ S, 488 5’ 6@ W) and Iporanga (248 35’ 14@ S, 488 35’ 41@ W); the black dots (EL and IP) represent the urban centers of Eldorado and Iporanga, respectively. GA (Galvão); IV (Ivaporunduva); SP (São Pedro); NH (Nhunguara); AN (André Lopes); PS (Pilões); TU (Sapatu); AB (Abobral); PC (Pedro Cubas); MR (Maria Rosa). models.’’ All runs were performed with 100,000 burn-in steps followed by 100,000 Markov Chain Monte Carlo (MCMC) replications, with K 5 3, which corresponds to the historical data on the tri-hybrid formation of mixed Brazilian population. RESULTS AND DISCUSSION Observed allelic frequencies relating to 48 autosomal INDEL markers in the ten African-derived populations from Vale do Ribeira are presented in Table 1. Individual genomic ancestry The data of ancestral populations from a previous study (Santos et al., 2010) was used to estimate the interethnic admixture present in each individual. The individual admixture estimates (IAEs) for the representatives of each population obtained using structure are presented in Figure 2. On the bar plot, each vertical line represents one individual and the correspondent admixture proportion. On the triangle plot, each edge of the triangle represents a parental subpopulation. Individuals from the quilombo remnants were plotted in the triangle (colored dots). It is clearly indicated that individuals of ten quilombo populations have a trihybrid genetic composition, with African and European contributions being higher than Amerindian genetic contribution (triangle plot—2A). Figure 2 also indicates a large heterogeneity in the ancestral composition among individuals from the quilombos (bar plot—2B). The individuals from the ten quilombos presented a proportion of African ancestry that ranged from 7.3 to 69.5%, the European contribution ranged from 12.9 to 68.3% and Amerindian genetic contribution was estimated between 7.3 and 58.5%. These estimates clearly indicate that individuals of the ten quilombo populations are largely heterogeneous regarding genomic ancestry. Population genomic ancestry Table 2 shows the genetic admixture estimates from each quilombo population. There is a high degree of admixture in all of the quilombo populations. The average admixture estimate was: 39.7% of African, 39.0% of European and 21.3% of Amerindian contribution. Galvão was the population with the greatest contribution of African ancestry (46%), Sapatu presented the highest contribution of European genes (46.2%), and Maria Rosa showed the highest percentage of Amerindian ancestry (25.2%). Some of the populations (Abobral, Galvão, São Pedro, Pedro Cubas, Pilões, and Maria Rosa) were previously investigated with four polymorphic Alu insertions (Cotrim et al., 2004), and the presence of Amerindian contribution had already been detected. However, the estimates based on the present 48 AIMs set of markers is surely more efficient to estimate the Amerindian contribution, since it was developed on a significant amount of information about genotypes from different Amerindian populations (Santos et al., 2010). The significant proportion of genetic material from Europe evidenced by INDEL markers demonstrates the historical importance of European contribution to the origin of these populations. There are two possible explanations for the European genetic contribution in quilombos: (1) part of the slaves who founded the quilombos was already European descendant or (2) in the maintenance of populations, admixture with European descendants continued to occur. These two hypotheses are not mutually American Journal of Human Biology 38 L. KIMURA ET AL. TABLE 1. Allelic frequencies observed on the ten quilombo populations from Vale do Ribeira INDEL MID1357 MID273 MID1684 MID818 MID1172 MID1176 MID1358 MID1785 MID1271 MID789 MID494 MID625 MID1379 MID2011 MID1726 MID473 MID619 MID1448 MID1923 MID856 MID99 MID93 MID1716 MID682 MID1039 MID1780 MID1470 MID132 MID1098 MID1558 MID217 MID568 MID1952 MID476 MID275 MID152 MID196 MID778 MID1603 MID1386 MID660 MID575 MID216 MID481 MID913 MID350 MID988 MID184 AB AN GA IV MR NH PC PS SP TU 0.407 0.535 0.360 0.512 0.209 0.581 0.756 0.395 0.500 0.547 0.616 0.628 0.860 0.547 0.523 0.512 0.558 0.256 0.267 0.524 0.779 0.419 0.512 0.674 0.465 0.581 0.326 0.512 0.381 0.326 0.321 0.349 0.360 0.291 0.686 0.256 0.640 0.651 0.360 0.256 0.488 0.151 0.698 0.093 0.023 0.058 0.279 0.570 0.500 0.407 0.315 0.308 0.259 0.685 0.615 0.259 0.648 0.685 0.558 0.444 0.870 0.577 0.346 0.442 0.611 0.288 0.442 0.519 0.769 0.556 0.537 0.778 0.315 0.667 0.241 0.426 0.240 0.241 0.185 0.296 0.259 0.167 0.630 0.241 0.630 0.722 0.296 0.278 0.463 0.111 0.685 0.148 0.019 0.111 0.148 0.426 0.227 0.727 0.227 0.455 0.364 0.636 0.682 0.182 0.500 0.545 0.682 0.545 0.909 0.409 0.591 0.773 0.591 0.150 0.409 0.591 0.545 0.227 0.545 0.682 0.273 0.182 0.318 0.364 0.091 0.364 0.136 0.182 0.091 0.182 0.545 0.091 0.773 0.818 0.455 0.136 0.318 0.045 0.727 0.045 0.000 0.136 0.182 0.682 0.404 0.462 0.442 0.548 0.375 0.625 0.702 0.423 0.442 0.538 0.625 0.481 0.875 0.548 0.462 0.654 0.654 0.202 0.365 0.644 0.654 0.337 0.615 0.808 0.317 0.567 0.327 0.433 0.468 0.385 0.221 0.404 0.327 0.279 0.731 0.240 0.692 0.712 0.346 0.279 0.587 0.058 0.769 0.115 0.010 0.067 0.317 0.548 0.545 0.682 0.500 0.455 0.273 0.636 0.727 0.591 0.773 0.591 0.409 0.773 0.727 0.545 0.545 0.682 0.682 0.100 0.250 0.455 0.727 0.500 0.500 0.773 0.409 0.182 0.318 0.409 0.318 0.273 0.182 0.364 0.682 0.182 0.591 0.227 0.409 0.545 0.409 0.136 0.318 0.045 0.500 0.045 0.000 0.227 0.182 0.636 0.360 0.465 0.453 0.453 0.360 0.733 0.570 0.291 0.581 0.547 0.558 0.733 0.849 0.512 0.477 0.535 0.570 0.233 0.395 0.674 0.744 0.419 0.419 0.640 0.256 0.616 0.256 0.558 0.305 0.256 0.174 0.131 0.302 0.314 0.535 0.291 0.616 0.651 0.314 0.360 0.430 0.163 0.791 0.093 0.000 0.209 0.116 0.407 0.388 0.550 0.313 0.575 0.438 0.688 0.525 0.400 0.513 0.600 0.550 0.600 0.725 0.475 0.488 0.575 0.463 0.263 0.308 0.481 0.763 0.350 0.513 0.713 0.288 0.525 0.363 0.513 0.346 0.163 0.400 0.325 0.300 0.388 0.713 0.288 0.700 0.575 0.388 0.188 0.525 0.100 0.825 0.100 0.075 0.088 0.225 0.563 0.444 0.556 0.259 0.444 0.315 0.537 0.389 0.463 0.407 0.704 0.648 0.667 0.796 0.500 0.593 0.519 0.611 0.185 0.346 0.759 0.704 0.667 0.481 0.815 0.370 0.370 0.222 0.593 0.296 0.204 0.278 0.167 0.407 0.222 0.574 0.296 0.481 0.796 0.352 0.185 0.574 0.167 0.796 0.204 0.000 0.019 0.204 0.296 0.521 0.625 0.396 0.625 0.458 0.604 0.583 0.208 0.500 0.604 0.688 0.583 0.875 0.479 0.500 0.500 0.729 0.333 0.396 0.688 0.667 0.521 0.604 0.833 0.250 0.500 0.313 0.396 0.375 0.313 0.125 0.188 0.292 0.125 0.521 0.250 0.688 0.792 0.458 0.271 0.417 0.042 0.833 0.042 0.000 0.125 0.188 0.521 0.641 0.469 0.328 0.422 0.313 0.641 0.672 0.344 0.719 0.797 0.703 0.750 0.797 0.547 0.453 0.438 0.500 0.188 0.266 0.766 0.781 0.344 0.609 0.844 0.281 0.531 0.266 0.563 0.344 0.344 0.484 0.328 0.250 0.250 0.641 0.234 0.547 0.688 0.438 0.188 0.484 0.109 0.806 0.125 0.000 0.109 0.438 0.323 AB (Abobral); AN (André Lopes); GA (Galvão); IV (Ivaporunduva); MR (Maria Rosa); NH (Nhunguara); PC (Pedro Cubas); PS (Pilões); SP (São Pedro); TU (Sapatu). exclusive. The first hypothesis is supported by genetic evidence coming from our study with Y chromosome markers. We found a high contribution of Y chromosome of European origin (Kimura et al., unpublished data). Probably the genetic material of Europeans was originally introduced mainly by male slaves, who were descendents of unions between Portuguese men and African or Amerindian females. This type of directional mating is easily documented by historical records about Brazilian population (Ribeiro, 2000; Salzano and Freire-Maia, 1967). Concerning the second hypothesis, additional European contribution could have been introduced later, through few European-derived individuals who moved later to quilombos. However, the lack of European mitochondrial DNA lineages (Rincon et al., unpublished data) supports the idea that European DNA came almost exclusively from males. Comparing our results to other Brazilian Africanderived populations, the contribution of African genes in quilombo populations from Vale do Ribeira (39.7%) is American Journal of Human Biology lower than in African-derived populations of Southern (Bortolini et al., 1999; Souza and Culpi, 2005), Northeastern (Arpini-Sampaio et al., 1999; Bortolini et al., 1999) and Northern (Bortolini et al., 1995, 1999; Cayres-Vallinoto et al., 2003; Guerreiro et al., 1999; Lopes Maciel et al., 2011) Brazil, estimated on different sets of autosomal markers. In only one study (Lopes Maciel et al., 2011) the same panel of autosomal INDEL markers was employed. It is predictable that there should be high contribution of Amerindian genes in the Amazonian and Northeastern African-derived populations: in fact, some of these populations presented more than 32% of Native American genetic ancestry. This was evidenced in several studies with classic markers and/or autosomal hipervariable loci (Arpini-Sampaio et al., 1999; Bortolini et al, 1995; CayresValinoto et al., 2003; Guerreiro et al., 1999; Lopes Maciel et al., 2011). The estimated contribution of Amerindian genes to the quilombo populations from Vale do Ribeira was also high (21.3% in average), different from other 39 GENOMIC ANCESTRY OF AFRICAN-BRAZILIANS Fig. 2. Schematic representation of the IAEs in the 10 quilombo populations, using structure v3.2 software for K 5 3. (A) Triangle plot: each individual is represented by a colored point, and the correspondent admixture proportions are indicated by the distance to the edges of the triangle. Red, green, and blue colors correspond to individuals from the parental populations (African, European and Amerindian, respectively), and individuals from quilombo populations are plotted in colored dots. (B) Bar plot: each vertical line represents one individual and the correspondent African (1—red), European (2—green), and Amerindian (3—blue) admixture proportions (4 5 Abobral; 5 5 André Lopes; 6 5 Galvão; 7 5 Ivaporunduva; 8 5 Maria Rosa; 9 5 Nhunguara; 10 5 Pedro Cubas; 11 5 Pilões; 12 5 São Pedro; 13 5 Sapatu). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] TABLE 2. Global estimate of ancestry in ten quilombo populations from Vale do Ribeira % of admixture estimates Quilombo populations Abobral André Lopes Galvão Ivaporunduva Maria Rosa Nhunguara Pedro Cubas Pilões São Pedro Sapatu Total quilombos African European Amerindian N 0.369 0.395 0.460 0.408 0.394 0.424 0.415 0.393 0.398 0.316 0.397 0.408 0.400 0.346 0.394 0.354 0.359 0.381 0.403 0.396 0.462 0.390 0.224 0.204 0.194 0.198 0.252 0.217 0.204 0.204 0.207 0.222 0.213 42 27 11 52 11 43 40 26 24 31 307 N 5 number of subjects studied in each locality. estimates (not exceeding 13%) found in studies with samples from the South (Bortolini et al., 1999) and Southeast of Brazil (Scliar et al., 2009). Inclusion of Amerindian women in the quilombos from Vale do Ribeira The preferential inclusion of indigenous women into Amazonian African-derived groups was previously suggested by Ribeiro-dos-Santos et al. (2002). Mitochondrial DNA investigations performed by us in the same quilombos from Vale do Ribeira here reported (Rincon et al., unpublished data) revealed a high frequency of Amerindian (50%) and African (48%) mtDNA lineages and a small frequency of European contribution (from 1 to 2%). On the other hand, our Y-chromosome investigations (Kimura et al., unpublished data) revealed, despite the African contribution (30%), a significant fraction of European ancestry (61%), and only a small portion of Y chromosomes had an Amerindian origin (9%). In the present study, using autosomal INDEL markers, we highlight an important Amerindian contribution (21.3%), with intermediate values, when compared to estimates obtained by mitochondrial and Y chromosome markers. The contribution of Amerindian genes would not be expected to be high, at first, in African-derived populations from southeast of Brazil, as found in Amazon groups (Lopes Maciel et al., 2011). However, the ancient occupation of Vale do Ribeira was marked by the presence of indigenous groups. The region was populated by Carijós, Guarani and Kaingang (or Guainás) population groups that formed small clusters located at the coast or near the Ribeira river shores (Oliveira Jr. et al., 2000; Pacheco dos Santos and Tatto, 2008). Furthermore, Vale do Ribeira was a route for Amerindians that crossed the region towards the coast during the winter, searching for areas where they could fish (Oliveira Jr. et al., 2000). Thus, we found that African-derived people living in the Vale do Ribeira presented a similar pattern of admixture to African-derived populations from the Amazon region, emphasizing the important role of indigenous women in setting and establishing the quilombo populations. Differentiation among quilombos from Vale do Ribeira The genetic distances (FST) analysis indicated that the 10 populations studied, geographically close, have a low degree of genetic differentiation (none of the FST values found was superior to 5%). The greatest differentiation American Journal of Human Biology 40 L. KIMURA ET AL. Fig. 3. Multidimensional scaling (MDS) plot based on genetic differentiation (FST) values among the ten quilombo populations from Vale do Ribeira and the three ancestral populations. (STRESS 5 0.0520, RSQ 5 0.9954). AME (Amerindian); AFR (African); EUR (European); GA (Galvão); IV (Ivaporunduva); SP (São Pedro); NH (Nhunguara); AN (André Lopes); PS (Pilões); TU (Sapatu); AB (Abobral). PC (Pedro Cubas); MR (Maria Rosa). occurs between Galvão and Sapatu (>4%). We compared the genetic distances by an exact differentiation test (Raymond and Rousset, 1995) and no significant statistical differences were found (P > 0.05) between the studied populations. Because all the FST values found are very small, the results suggest a high degree of gene flow among all populations studied. Because of geographic proximity among quilombos from Vale do Ribeira (see Fig. 1), gene flow among them could be favored. According to the oldest inhabitants of the populations studied, severe communities from Vale do Ribeira were founded by a small number of couples. Furthermore, according to our genealogical data, we observed that some founder individuals are present in the history of more than one population. Genetic distances (FST) were visualized in two-dimensional space using the MDS (multidimensional scaling) method (Fig. 3). Parental populations (European, African, and Amerindians) were included in this analysis. The figure shows that all the ten quilombo populations practically formed one cluster, grouped closer to the African and the European quadrants. This is explained by the fact that all populations presented a greater contribution of these two ancestries and a lower contribution of Amerindian genes. Fig. 4. MDS plot based on genetic differentiation (FST) values between 17 afro-derived populations (Stress 5 0.160; RSQ 5 0.880). GA: Galvão. IV (Ivaporunduva); SP (São Pedro); NH (Nhunguara); AN (André Lopes); PS (Pilões); TU (Sapatu); AB (Abobral). PC (Pedro Cubas); MR (Maria Rosa); PCV (Pacoval); MRJ (Marajó); TRB (Trombetas); CUR (Curiaú); PON (Pontal); MAZ (Mazagão); PTD (Pitimandeua). Into the full line are shown the quilombos from Vale do Ribeira. Into the dashed line are shown the Amazonian quilombos. the other hand, the populations from Vale do Ribeira did not appear to form well-defined groups, suggesting that their composition was more homogenous and reinforcing the idea that there was a high degree of gene flow among them. Both groups of quilombos (from Vale do Ribeira and Amazonian region) present a similar trihybrid pattern of admixture: besides the African genetic contribution, an expressive European and a high Amerindian ancestry were detected. However, there are considerations to be made: since the type of molecular markers used (INDEL) is not able to discriminate subtle geographical differences (they just discriminate continental ancestry), even though the source of Portuguese genetic contribution could be similar, the Amerindian populations that participated in the formation of the quilombos (from Vale do Ribeira and Amazonian region) were certainly different. Besides, the African component can also be distinct, since the slaves brought to Brazil originated from many different parts of Africa and were distributed in different patterns among the regions of our country (Klein, 1999). CONCLUSIONS Comparing quilombos from North and Southeast of Brazil investigated with the panel of INDEL We calculated genetic distances (FST) of 17 quilombos populations (Fig. 4). It is apparent that quilombos from Vale do Ribeira are more similar to each other than to the populations from Amazonian region. This scenario would suggest that the genetic composition of populations from Vale do Ribeira was more homogeneous, reinforcing that there was a high degree of gene flow among them. Gene flow might have been be favored in populations of Vale do Ribeira because they are geographically close, a different situation from most populations in the Amazon region. Our own genealogical collection of data confirms this trend of exchange of individuals between close populations. The Amazonian quilombos formed three well-defined clusters, and they are grouped according to their ancestry composition (see Fig. 2 in Lopes Maciel et al., 2011). On American Journal of Human Biology The autosomal INDEL ancestry-informative markers provide genetic evidence that corroborates historical records of triple interbreeding (European, African and Amerindian) in the formation and maintenance of the African-derived quilombo populations in Vale do Ribeira— São Paulo. FST values estimated between the quilombo remnants populations were low, indicating that the 10 populations from Vale do Ribeira are genetically very similar, a phenomenon that may explained by high degree of gene flow among them. Comparing our results to another study with Amazonian quilombos, we found a similar pattern of admixture, reinforcing the role of Amerindian in the formation of the quilombos also in African-derived populations from Southeast of Brazil. Our results reinforce the utility of the INDEL ancestry-informative markers in the investigation of the patterns of admixture in Brazilian populations. GENOMIC ANCESTRY OF AFRICAN-BRAZILIANS ACKNOWLEDGMENTS The authors thank the people living in the quilombo for their willingness to participate. They also thank L.M. Macedo-Souza, C.B. Angeli, E. Pardono, D. Rincon, and N.H. Cotrim for helping with the genealogical inferences and with the collection of genealogical data, and Renan Barbosa Lemes for helping with the maps of quilombos. They thank the physicians Roberto C. Maluf Filho and Franklin A. S. Kono for clinical assistance. LITERATURE CITED Abe-Sandes K, Silva WA Jr, Zago MA. 2004. Heterogeneity of the Y chromosome in Afro-Brazilian populations. Hum Biol 76:77–86. Arpini-Sampaio Z, Costa MC, Melo AA, Carvalho MF, Deus MS, Simões AL. 1999. Genetic polymorphisms and ethnic admixture in Africanderived black communities of northeastern Brazil. Hum Biol 71:69–85. Auricchio MTBM, Vicente JP, Meyer D, Mingroni-Netto RC. 2007. Frequency and origins of HBB*S mutation in African-derived Brazilian populations. Hum Biol 79:667–678. 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