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*
Centro de Estudos do Genoma Humano, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências,
Universidade de São Paulo, São Paulo, Brazil
Laboratório de Genética Humana e Médica, Departamento de Patologia, Centro de Ciências Biológicas, Universidade Federal do Pará, Belém,
Instituto de Criminalı́stica, Centro de Perı́cias Cientı́ficas Renato Chaves, Belém, Pará, Brazil
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
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.
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
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
*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
Published online 2 October 2012 in Wiley Online Library
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
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).
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
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 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
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’ [email protected] S, 488 5’ [email protected] W) and Iporanga (248 35’ [email protected] S, 488 35’ [email protected]
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
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
L. KIMURA ET AL.
TABLE 1. Allelic frequencies observed on the ten quilombo populations from Vale do Ribeira
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
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
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
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
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
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
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).
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
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.
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.
Bortolini MC, Da Silva WA, Junior WA, De Guerra DC, Remonatto G, Mirandola R, Hutz MH, Weimer TA, Silva MC, Zago MA, Salzano FM. 1999.
African-derived South American populations: A history of symmetrical
and asymmetrical matings according to sex revealed by bi- and uni-parental genetic markers. Am J Hum Biol 11:551–563.
Bortolini MC, Weimer T de A, Salzano FM, Callegari-Jacques SM, Schneider H, Layrisse Z, Bonatto SL. 1995. Evolutionary relationships between
black South American and African populations. Hum Biol 67:547–559.
Bortolini MC, Zago MA, Salzano FM, Silva-Júnior WA, Bonatto SL, da
Silva MC, Weimer TA. 1997. Evolutionary and anthropological implications of mitochondrial DNA variation in African Brazilian populations.
Hum Biol 69:141–159.
Carvalho BM, Bortolini MC, Batista dos Santos SE, Ribeiro-dos-Santos
AKC. 2008. Mitochondrial DNA mapping of social-biological interactions
in Brazilian Amazonian African-descendant populations. Genet Mol Biol
Cayres-Vallinoto IMV, Vallinoto ACR, Valente CMD, Guerreiro JF. 2003.
Allele frequency distributions of six hypervariable loci (D1S80, APOB,
D4S43, vW1, F13A and DYS19) in two African-Brazilian communities
from the Amazon region. Genet Mol Biol 26:235–240.
Cotrim NH, Auricchio MT, Vicente JP, Otto PA, Mingroni-Netto RC. 2004.
Polymorphic Alu insertions in six Brazilian African-derived populations.
Am J Hum Biol 16:264–277.
Da Silva WA Jr, Bortolini MC, Meyer D, Salzano FM, Elion J, Krishnamoorthy R, Schneider MP, De Guerra DC, Layrisse Z, Castellano HM,
Weimer TD, Zago MA. 1999. Genetic diversity of two African and sixteen
South American populations determined on the basis of six hypervariable loci. Am J Phys Anthropol 109:425–437.
Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50.
Falush D, Stephens M, Pritchard JK. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587.
Falush D, Stephens M, Pritchard JK. 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles.
Mol Ecol Notes 7:574–578.
Guerreiro JF, Ribeiro-dos-Santos AKC, Santos EJM, Vallinoto ACR,
Cayres-Vallinoto IMV, Aguiar GFS, Batista dos Santos SE. 1999.
Genetical-demographic data from two amazonian populations composed
of descendants of African slaves: Pacoval and Curiau. Genet Mol Biol 22:
Klein HS. 1999. The Atlantic slave trade. Cambridge University
Lopes Maciel LG, Ribeiro Rodrigues EM, Carneiro Dos Santos NP, Ribeiro
Dos Santos ?, Guerreiro JF, Santos S. 2011. Afro-derived Amazonian
populations: inferring continental ancestry and population substructure. Hum Biol 83:627–636.
Neves WA, Okumura MMM. 2005. Afinidades biológicas de grupos pré-históricos do vale do rio Ribeira de Iguape (SP): uma análise preliminar.
Revista de Antropologia (São Paulo) v. 48:525–558.
Oliveira AN Jr, Stucchi D, Chagas MF, Brasileiro SS. 2000. Comunidades
Negras de Ivaporunduva, São Pedro, Pedro Cubas, Sapatu, Nhunguara,
André Lópes, Maria Rosa e Pilões. In: Andrade T, Pereira CAC, Andrade
MRO, editors. Negros do Ribeira: reconhecimento étnico e conquista do
território. ITESP: Páginas e Letras. São Paulo, SP, Brasil: Editora
Ota VK, Belangero SI, Gadelha A, Bellucco FT, Christofolini DM, Mancini
TI, Ribeiro-dos-Santos AK, Santos SE, Mari Jde J, Bressan RA, Melaragno MI, Smith Mde A. The UFD1L rs5992403 polymorphism is associated with age at onset of schizophrenia. J Psychiatr Res 2010; 44:
Pacheco dos Santos KM, Tatto N. 2008. Agenda socioambiental de comunidades quilombolas do Vale do Ribeira. Instituto Socioambiental.
Parra EJ, Marcini A, Akey J, Martinson J, Batzer MA, Cooper R, Forrester
T, Allison DB, Deka R, Ferrell RE, Shriver MD. 1998. Estimating African American admixture proportions by use of population-specific alleles. Am J Hum Genet 63:1839–1851.
Pereira R, Phillips C, Pinto N, Santos C, dos Santos SE, Amorim A, Carracedo Á, Gusmão L. 2012. Straightforward inference of ancestry and
admixture proportions through ancestry-informative insertion deletion
multiplexing. PLoS One 7:e29684.
Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945–959.
Raymond M, Rousset F. 1995. Genepop version 1.2: population genetics
software for exact tests and ecumenicism. J Hered 86:248–249.
Ribeiro D. 2000. The Brazilian people: the formation and meaning of Brazil. Florida: University Press of Florida.
Ribeiro GG, Abe-Sandes K, Barcelos Rda S, Klautau-Guimarães Mde N,
Junior WA, Oliveira SF. 2011. Who were the male founders of rural Brazilian Afro-derived communities? A proposal based on three populations.
Ann Hum Biol 38:237–240.
Ribeiro GG, De Lima RR, Wiezel CE, Ferreira LB, Sousa SM, Rocha DM,
Canas Mdo C, Nardelli-Costa J, Klautau-Guimarães Mde N, Simões AL,
Oliveira SF. 2009. Afro-derived Brazilian populations: male genetic constitution estimated by Y-chromosomes STRs and Alu YAP element polymorphisms. Am J Hum Biol 21:354–356.
Ribeiro-dos-Santos AK, Pereira JM, Lobato MR, Carvalho BM, Guerreiro
JF, Batista Dos Santos SE. 2002. Dissimilarities in the process of formation of Curiaú, a semi-isolated Afro-Brazilian population of the Amazon
region. Am J Hum Biol 14:440–447.
Ribeiro-Rodrigues EM, dos Santos NP, dos Santos AK, Pereira R, Amorim
A, Gusmão L, Zago MA, dos Santos SE. 2009. Assessing interethnic
admixture using an X-linked insertion-deletion multiplex. Am J Hum
Salzano FM, Freire-Maia N. 1967. Populações Brasileiras: aspectos demográficos, genéticos e antropológicos. Companhia Editora Nacional.
Santos NP, Ribeiro-Rodrigues EM, Ribeiro-Dos-Santos AK, Pereira R, Gusmão L, Amorim A, Guerreiro JF, Zago MA, Matte C, Hutz MH, Santos
SE. 2010. Assessing individual interethnic admixture and population
substructure using a 48-insertion-deletion (INSEL) ancestry-informative marker (AIM) panel. Hum Mutat 31:184–190.
Scliar MO, Vaintraub MT, Vaintraub PM, Fonseca CG. 2009. Brief communication: admixture analysis with forensic microsatellites in Minas Gerais, Brazil: the ongoing evolution of the capital and of an African-derived
community. Am J Phys Anthropol 139:591–595.
Souza IR, Culpi L. 2005. Valongo, genetic studies on an isolated Afro-Brazilian community. Genet Mol Biol 28:402–406.
Tarazona-Santos E, Castilho L, Amaral DR, Costa DC, Furlani NG, Zuccherato LW, Machado M, Reid ME, Zalis MG, Rossit AR, Santos SE,
Machado RL, Lustigman S. 2011. Population genetics of GYPB and association study between GYPB*S/s polymorphism and susceptibility to P.
falciparum infection in the Brazilian Amazon. PLoS One 6:e16123.
Weber JL, David D, Heil J, Fan Y, Zhao C, Marth G. 2002. Human diallelic
insertion/deletion polymorphisms. Am J Hum Genet 71:854–862.
American Journal of Human Biology