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Brief communication Admixture analysis with forensic microsatellites in Minas Gerais Brazil The ongoing evolution of the capital and of an African-derived community.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 139:591–595 (2009)
Brief Communication: Admixture Analysis With
Forensic Microsatellites in Minas Gerais, Brazil: The
Ongoing Evolution of the Capital and of an
African-Derived Community
Marı́lia O. Scliar,1* Marco T. Vaintraub,2 Patrı́cia M.V. Vaintraub,2 and Cleusa G. Fonseca1
1
Departamento de Biologia Geral, ICB, Universidade Federal de Minas Gerais. Caixa Postal 486,
31270-910 Belo Horizonte, MG, Brazil
2
GENETICENTER—Centro de Genética e Reprodução. Alameda da Serra 500, 34000-000 Nova Lima, MG, Brazil
KEY WORDS
population admixture; African Brazilians; Belo Horizonte
ABSTRACT
We report the estimated allele frequencies for 13 and 14 microsatellite loci in two populations
of Minas Gerais, Brazil as follows: Belo Horizonte (the
capital) and Marinhos (an African-derived community).
Analysis of the African, Amerindian, and European
genetic contributions to both populations, together with
historical information, revealed distinct differences
between the two populations. Estimates for Belo Horizonte revealed a higher-European (66%) than African
(32%) contribution, and a minimal Amerindian contribution. These results are consistent with the peopling of
the city mainly by people from the Minas Gerais hinterland, a people highly admixed but with more European
ancestry. Estimates for Marinhos confirmed the highAfrican component of the population. However, a temporal analysis of two datasets—CURRENT (representing
the population living in Marinhos today) and ORIGINAL
(representing families, who have lived in Marinhos since
the onset of the 20th century),—identified a diminishing
of the population’s African ancestry from 92% in the
ORIGINAL group to 67% in the CURRENT group. This
change is here interpreted as a consequence of the growing migration into the village of people with more
European ancestry and subsequent admixture with the
local population. Am J Phys Anthropol 139:591–595,
2009. V 2009 Wiley-Liss, Inc.
The constitution of the modern Brazilian population
began with the arrival of Portuguese colonizers in 1500.
About 100,000 Portuguese settled in Brazil in the ensuing 200 years. They found a heterogeneous native population of around 2,000,000 people. Afterward, between
1550 and 1850, about 4,000,000 Africans from several
Sub-Saharan regions were brought to Brazil (IBGE,
2000; Salzano and Bortolini, 2002).
The process of admixture soon started between Portuguese men and Amerindian women, and later, with the
arrival of the slave population, it was extended to African women (Ribeiro, 1995). This asymmetric mating has
been confirmed by research on uniparental markers—mitochondrial DNA (mtDNA) and Y-chromosome—in individuals of different ancestries and regions of Brazil
(Alves-Silva et al., 2000; Carvalho-Silva et al., 2001;
Hünemeier et al., 2007). That is, although twice as many
African males as females were brought to Brazil
(Resende and Villalta, 2007), and the Amerindian population contained similar frequencies of men and women,
the greatest part of Brazilian genetic inheritance was
introduced by Portuguese men and Amerindian and African women. Among the factors affecting the lower degree
of contribution from African men are high-mortality and
low-reproductive rates. This can be demonstrated by contrasting the number of slaves that entered Brazil
(4,000,000) with their number in 1870 (1,500,000), 20
years after the abolishment of the slave trade; in contrast, 400,000 African slaves entered the United States
over two centuries and in 1860 this population had
increased to 4,000,000 (Florentino, 1997). Portuguese
social domination over the African and Amerindian
populations created barriers to the reproduction of men
and made the women available, leading to unequal admixture.
At the same time, many communities of African descendants were formed in Brazil. These were founded by
escaped slaves in isolated locations (quilombos), and by
liberated slaves, mainly after abolition in 1888. Many of
these communities have preserved much of their original
heritage, presenting various degrees of cultural and
genetic interethnic exchange.
Following this pattern, regional variation in the process of colonization created diverse histories of admixture across the country. In the southeastern state of
Minas Gerais, the discovery of gold in the last decade of
C 2009
V
WILEY-LISS, INC.
C
Additional Supporting Information may be found in the online
version of this article.
Grant sponsors: GENETICENTER, Coordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior, Fundação de Amparo à Pesquisa do Estado de Minas Gerais.
*Correspondence to: Marı́lia O. Scliar, Departamento de Biologia
Geral, ICB, Universidade Federal de Minas Gerais. Caixa Postal
486, 31270-910 Belo Horizonte, MG, Brazil.
E-mail: mariliascliar@icb.ufmg.br
Received 19 August 2008; accepted 16 January 2009
DOI 10.1002/ajpa.21046
Published online 6 April 2009 in Wiley InterScience
(www.interscience.wiley.com).
592
M.O. SCLIAR ET AL.
the 17th century began the Gold Cycle, during which
started the effective peopling of the region. In this period, Minas Gerais became the most populous area of
Brazil: six times more Portuguese came in 50 years than
in the previous 200 years, most settling in Minas Gerais;
a massive immigration of Brazilians, a population resulting from the preceding two centuries of admixture,
occurred; and the greatest contingent of slaves arrived
from the ports of Bahia and Rio de Janeiro and from
plantations of the northeastern region (Souza, 1994;
Resende and Villalta, 2007). The mining industry began
to decline around 1760, but as Minas Gerais had diversified its economy with agriculture and livestock production, the population dispersed from the mining villages
into the state’s hinterlands (Resende and Villalta, 2007).
The largest European immigration to Brazil occurred
between 1850 and 1950, with the entry of 1,500,000 Italians, 1,485,000 Portuguese, and 1,000,000 people from
other nations. This, however, had little influence in
Minas Gerais (IBGE, 2000). The greatest proportion of
registered foreigners (predominantly Italians) was in
1900, when they constituted 4% of Minas Gerais inhabitants (Imprensa Oficial, 1925; Monteiro, 1973).
Both mtDNA (Alves-Silva et al., 2000) and Y-chromosome (Carvalho-Silva et al., 2001) studies were conducted on ‘‘white" individuals in Minas Gerais. Also,
autosomal ancestry informative markers (AIMs) were
analyzed for ‘‘white" individuals and for residents of a
rural community (Parra et al., 2003). These studies
found a highly admixed population. Almost all Y-chromosome lineages were of European origin, and similar proportions of mtDNA lineages were of African (0.28),
Amerindian (0.33), and European (0.39) origin. The proportion of African ancestry obtained with AIMs was 32%
for the ‘‘white" group and 44% for the rural community.
This study focused on two populations in Minas Gerais: Belo Horizonte and Marinhos. Belo Horizonte is the
capital of Minas Gerais, founded in 1897 and currently
containing 2,238,526 inhabitants (http://www.ibge.
gov.br). Its population growth was primarily due to massive immigration from the state’s hinterlands, part of the
larger process of urbanization in Brazil. Thus, to understand the population history of Belo Horizonte, we must
understand that of Minas Gerais. Marinhos is a small
village (70 houses) in the countryside of Brumadinho, a
city in the Belo Horizonte metropolitan area, where most
inhabitants are black. It was formed in the 19th century,
probably by liberated slaves of the region. Other villages,
such as Mançangano, Martins, Ribeirão, São José do
Paraopeba, and Sapé, lie in the vicinity of Marinhos and
are characterized by similar African heritage. Many
inhabitants within Marinhos and among the villages
(principally Marinhos and Sapé) are related, suggesting
a small founding population. Farms and churches constructed in the 18th century by slaves can still be found
in the area, including the farm on which the inhabitants
believe their forefathers lived (Martins Farm). In 1919, a
railway line was inaugurated and for its construction
individuals from other cities migrated to Marinhos. This
seems the most important marker of when immigration
to Marinhos began, probably significantly altering the
population structure.
In this study, we used forensic microsatellites that
have been useful in human population genetics research
(Agrawal and Khan, 2005; Pimenta et al., 2006), including admixture analysis (Cerda-Flores et al., 2002; Callegari-Jacques et al., 2003; Barnholtz-Sloan et al., 2005).
American Journal of Physical Anthropology
One advantage of these markers is the growing database
of world populations that they encompass, therefore minimizing the costs of sampling and genotyping. We analyzed 13 microsatellites in the Belo Horizonte population
and 14 in the Marinhos population and estimated the
African, Amerindian, and European genetic contributions to both populations to understand their ongoing
evolution.
MATERIALS AND METHODS
Population sample
The Belo Horizonte (BH) sample was built from a
database of paternity tests in the privately owned
Geneticenter laboratory and included data from 234
parents who were born in Belo Horizonte and lived there
at the time of testing.
The Marinhos (M) sample consisted of 60 individuals,
aged 20–89 years. These individuals were asked to provide age and birthplace information about themselves,
their parents, and grandparents. We built two datasets
excluding first degree relatives: CURRENT (CURR; N 5
44) and ORIGINAL (ORIG; N 5 19). The CURR dataset
represents the population currently living in Marinhos.
The ORIG dataset was composed of 18 individuals from
the CURR dataset plus one individual excluded from the
CURR dataset because of the relationship criterion and
represents families who have lived in the region (Marinhos and nearly villages) since the onset of the 20th
century. Individuals included in the ORIG dataset fit one
of three criteria as follows: 1) more than 88 years old
and born in the region; 2) more than 52 years old and
parents born in the region; or 3) more than 20 years old
and all grandparents born in the region.
Informed consent was obtained from all participants in
the study. This research was approved by the Research
Ethics Committee of the Federal University of Minas
Gerais.
DNA and statistical analyses
DNA was extracted following standard procedures.
Thirteen forensic microsatellites were analyzed in both
populations as follows: CSF1PO, TPOX, TH01, vWA,
D16S539, D7S820, D13S317, D3S1358, F13A01, F13B,
LPL, D8S1179, and D5S818. Also, the D12S391 locus
was analyzed only in the M population. A polymerase
chain reaction (PCR) composed of three quadriplex and
one duplex was performed. PCR products were separated
by electrophoresis in a 6% polyacrilamide denaturating
gel and visualized by silver staining. Allele identification
was achieved by comparison of the amplified fragments
with those of allelic ladders (in units of repeat sizes of
alleles).
We estimated allele frequencies and observed/expected
heterozygosity, verified the Hardy-Weinberg equilibrium,
and observed any significant excesses or deficiencies of
heterozygotes. To test differentiation between the Belo
Horizonte and Marinhos populations, we used the exact
test for genic and genotypic differentiation and also estimates of FST. GENEPOP software (Raymond and Rousset, 1995) was used for these analyses except for the FST
that were calculated with the Fstat program (Goudet,
1995).
Admixture estimates were obtained by two methods as
follows: weighted least squares (Long, 1991) with
ADMIX.PAS software and gene identity (Chakraborty,
593
ADMIXTURE IN BELO HORIZONTE AND MARINHOS
TABLE 1. Genic and genotypic differentiation tests
(significant P-value: P < 0.05) and FST estimates between
BH—CURR and BH—ORIG
BH-CURR
Genic
Genotypic
FST
0.00001
0.00001
0.011 SE 5 0.003
TABLE 2. Genetic contributions of European,
African, and Amerindian populations to Belo Horizonte
population estimated with two methods
Admixture estimates and standard errors
BH-ORIG
6.01006e-013
1.08823e-012
0.041 SE 5 0.010
Method 1
Method 2
European
African
Amerindian
0.66 6 0.03
0.65 6 0.02
0.32 6 0.03
0.34 6 0.02
0.02 6 0.01
0.01 6 0.01
Method 1: Long, 1991. Method 2: Chakraborty, 1985. Both based
on 11 microsatellite.
1985) with ADMIX95 software (www.genetica.fmed.edu.
uy). We used pooled allele frequencies from the following
populations to represent African, Amerindian, and European parental populations: seven African countries
(Angola, Cabinda, Cabo Verde, Guinea-Bissau, Mozambique, Nigeria, and São Tomé); seven Amerindian
populations (Caingang, Guarani, Gavião, Suruı́, Wai
Wai, Xavante, and Zoró); and Portugal (http://www.
uni-duesseldorf.de/WWW/MedFak/Serology/dna.html; Hutz
et al., 2002; Beleza et al., 2004; Kohlrausch et al., 2005).
The origins and sizes of these parental populations are
described in the supporting information.
We also conducted an individual admixture analysis
on the M population using the Structure program
(Pritchard et al., 2000). For this, we used the same set of
Amerindian populations, Guinea Bissau for the African
parental population, and Spain for the European parental population (Gonçalves et al., 2002; Pereira et al.,
2005; Camacho et al., 2007). This analysis included all
sampled individuals (N 5 60) and we constructed the
datasets so that first degree relatives were not included
in the same analysis.
RESULTS AND DISCUSSION
Allele frequencies, statistical parameters, and
population differentiation
The allele frequencies and some statistical parameters
for the microsatellites studied in the BH and M populations (CURR and ORIG datasets) are presented in the
supporting information. In both populations, all loci
were in Hardy-Weinberg equilibrium (P [ 0.05) after the
correction for multiple tests.
For the genic and genotypic differentiation tests
between the two datasets of M, we withdrew from CURR
the 18 individuals that also belong to ORIG. We obtained
significant values of total genic and genotypic differentiation (P 5 0.0015 and P 5 0.0065, respectively), and
the FST estimate confirmed these results (FST 5 0.024;
SE 5 0.009).
We also obtained significant values of differentiation
between BH and each of the M datasets (Table 1) and
observed a higher FST value between BH and ORIG
than between BH and CURR. These results corroborate
the differentiation found between ORIG and CURR and
suggest that a change occurred in Marinhos that made it
more similar to Belo Horizonte, probably a consequence
of the migration into the village.
Admixture analyses
A significantly greater European contribution to the
BH population was found in comparison to the African
contribution. A minimal Amerindian contribution was
identified (Table 2). These results may be explained by
the structure of the Minas Gerais population that
migrated to Belo Horizonte, which was predominantly
admixed with a large degree of European ancestry.
Minas Gerais historical data provide support for this
argument. In 1786, about half of the Minas Gerais population was made up of slaves, and 34% of the free population was black (12%) or brown (22%) (Resende and Villalta, 2007). Nearly a century later, in 1872, the color
distribution of Minas Gerais had altered: whites were
the majority, representing 41% of the population, followed by browns (36%) and blacks (23%) (Imprensa Oficial, 1925). Note that color is a complex trait that flows
in accordance with cultural and social movements, but it
is a useful measure here of the population’s general
make-up. We suggest that this alteration in color distribution was a product of the unequal admixture process,
which leads to two consequences. First, it causes the progressive and drastic decrease of the three original populations in Minas Gerais—African, Amerindian, and European. The increased number of brown individuals is
the most obvious characteristic of this process, but
admixture is also present in black and white individuals
(Alves-Silva et al., 2000; Parra et al., 2003). The second
consequence is the increase of European and decrease of
African and Amerindian contributions. The decimation
of Amerindians since the beginning of the colonization
period occurred at the same time as increases in African
slaves and Portuguese settlers, resulting in the progressive dilution of the Amerindian contribution. This historical process is consistent with our results. It could be
argued that the frequencies of Amerindians making up
the parental sample do not reflect the actual frequencies
of those Amerindians that contributed to the admixture
process, obscuring the identification of their contribution. However, Callegari-Jacques et al. (2003) in an analysis with 12 microsatellites—nine of them the same as
in this study—in five Brazilian populations identified
higher-Amerindian contributions than found in this
study. Thus, we also tested the same Amerindian parental frequencies used by Callegari-Jacques et al. (2003),
and the resultant estimate of the Amerindian contribution was not changed significantly when these frequencies were used (data not shown). Nevertheless, our interpretation of the Amerindian contribution should consider
the fact that the history of the Amerindians and their
interactions with society in Minas Gerais are not wellknown (Resende and Villalta, 2007).
The second wave of European immigration, simultaneous with the foundation of Belo Horizonte, was an important factor in the increase of European ancestry in
the population. The 1920 Belo Horizonte census shows
that 8.6% of the total population (55,527 individuals)
was foreign, mostly Italians (Dep. Estatı́stica, 1953;
Monteiro, 1973).
An additional explanation for our estimates is that our
sample, taken from paternity tests, could have a socioeconomic bias, in that it is formed mainly by people who
American Journal of Physical Anthropology
594
M.O. SCLIAR ET AL.
TABLE 3. Genetic contributions of European, African, and Amerindian populations to the two
datasets of Marinhos population (ORIGINAL and CURRENT) estimated with two methods
Admixture estimates and standard errors
European
Method 1
Method 2
0.27 6 0.15
0.26 6 0.13
0.08 6 0.11
ORIGINAL
African
0.81 6 0.13
1.11 6 0.12
0.92 6 0.11
CURRENT
African
Amerindian
European
20.08 6 0.06
20.37 6 0.05
0.37 6 0.10
0.42 6 0.17
0.33 6 0.15
0.59 6 0.10
0.74 6 0.16
0.67 6 0.15
Amerindian
0.04 6 0.05
20.16 6 0.07
In bold estimates done with two parental populations—European and African.
Method 1: Long, 1991. Method 2: Chakraborty, 1985. Both based on 11 microsatellites.
TABLE 4. Birth place distribution of sampled individuals of Marinhos and of their parents and grandparents
SUBJECTS
THEIR PARENTS
THEIR GRANDPARENTS
Birth place
N 5 60
N 5 102
N 5 151
Marinhos
MAÇ, MAR, RB, SAP, SJPa
Cities of the regionb
MG state
Another states
55%
20%
14%
8%
3%
29%
27%
29%
12%
3%
25%
30%
34%
7%
4%
a
b
MAÇ, Mançangano; MAR, Martins; RB, Ribeirão; SAP, Sapé; SJP, São José do Paraopeba.
Belo Vale, Bonfim, Brumadinho, Moeda.
could pay for the test. In Brazil, there is a positive correlation between individuals of the upper class and white
persons (http://www.ibge.gov.br), and these white individuals could be over-represented in our Belo Horizonte
sample. This would increase the European contribution
and decrease the African contribution in our results. An
approach to control this bias would be to construct samples including and controlling for socioeconomic data.
The estimates for M showed a higher-African than European contribution in the two datasets, CURR and
ORIG, and a higher-African contribution to ORIG than
to CURR. No Amerindian contribution was identified in
either dataset (Table 3).
With the familial birthplace data for the Marinhos
sample, we constructed a demographic picture of
Marinhos and verified that immigration into the village
continued during the last two generations (Table 4). Our
estimates indicate that these immigrants had a higherproportion of European ancestry, explaining the higherEuropean contribution to the CURR dataset than the
ORIG. We expected that this growing migration also
resulted in increased admixture over time, and we
sought to clarify this question with the individual admixture analysis.
Although our small sample size and small number of
loci lead to a high-individual admixture standard error,
and the parental populations were changed, the result of
the individual admixture analysis was concordant with
the population analyses. To visualize admixture, we isolated the African component of the individuals and separated them according to the length of time they have
been in Marinhos. Our division point was 1955, dividing
the period covered here in half. The separation of the
individuals revealed that ORIG individuals are concentrated before 1955 (67%) and 69% of CURRENT WITHOUT ORIG (CURRW/ORIG—we withdrew individuals
from CURR that also belong to ORIG) after 1955. We
observed that persons classified as CURRW/ORIG that
had been in Marinhos previous to 1955 have a highEuropean ancestry (46% with an African admixture
between 0 and 25%). After 1955, this percentage
American Journal of Physical Anthropology
Fig. 1. Distribution of African admixture percentage in
ORIG and CURRW/ORIG individuals separated according to the
length of time they have been in Marinhos, before or after 1955.
Before 1955: ORIG N 5 16, CURRW/ORIG N 5 11. After 1955:
ORIG N 5 8, CURRW/ORIG N 5 25.
decreases to 32% of individuals, and 52% present more
than 50% African admixture (Fig. 1). Figure 1 also shows
a decrease of ORIG individuals with more than 50% African ancestry, from 81% before 1955 to 72% after 1955.
These results, together with genealogical information, confirm that marriages between local people (ORIG) and
migrants have occurred over time and have been an important force in the evolution of this population.
Despite this change, in comparing our results with
other studies of Brazilian African descendants (ArpiniSampaio et al., 1999; Bortolini et al., 1999; Vallinoto
et al., 2003), we found that Marinhos and Sı́tio Velho
(Piauı́ state) are the communities sampled to date with
the largest African ancestry (0.68 and 0.72, respectively).
These communities therefore represent good samples for
further research on the African component of Brazilians.
CONCLUSIONS
Our admixture analysis using forensic microsatellites,
together with historical investigation, allowed us to trace
ADMIXTURE IN BELO HORIZONTE AND MARINHOS
the different evolutions that the urban population of
Belo Horizonte and the rural population of Marinhos
have undergone. Belo Horizonte has been populated by
an admixed population since its formation and Marinhos, originally a population with predominant African
ancestry, has shifted to a more admixed population due
to the continued arrival of immigrants with a highdegree of European ancestry.
Minas Gerais is an advantageous location to study
Brazilian admixture, as it was ‘‘the tie that knotted Brazil and made it a single thing’’ (Ribeiro, 1995). Corroborating this view, previous mtDNA research (Alves-Silva
et al., 2000) and compilation of the color distribution of
Brazilian populations (IBGE, 2006) shows that Minas
Gerais is the state most representative of the whole of
Brazil. More research on the Minas Gerais population
would therefore be welcome.
ACKNOWLEDGMENTS
The authors especially thank the Marinhos population
for their collaboration in this study. They thank E. Tarazona-Santos for helpful discussion and suggestions, J.
Long for made available the ADMIX.PAS program, and
J. Pereira, M. Hutz, S. Callegari-Jacques, and R. Gonçalves for the samples necessary to conduct the individual analysis.
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