Print version ISSN 1415-4757
Genet. Mol. Biol. vol.31 no.1 São Paulo 2008
HUMAN AND MEDICAL GENETICS
Bruno Maia CarvalhoI; Maria Cátira BortoliniII; Sidney Emanuel Batista dos SantosI; Ândrea Kely Campos Ribeiro-dos-SantosI
ILaboratório de Genética Humana e Médica, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pa, Brazil
IIDepartamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
The formation of the Brazilian Amazonian population has historically involved three main ethnic groups, Amerindian, African and European. This has resulted in genetic investigations having been carried out using classical polymorphisms and molecular markers. To better understand the genetic variability and the micro-evolutionary processes acting in human groups in the Brazilian Amazon region we used mitochondrial DNA to investigate 159 maternally unrelated individuals from five Amazonian African-descendant communities. The mitochondrial lineage distribution indicated a contribution of 50.2% from Africans (L0, L1, L2, and L3), 46.6% from Amerindians (haplogroups A, B, C and D) and a small European contribution of 1.3%. These results indicated high genetic diversity in the Amerindian and African lineage groups, suggesting that the Brazilian Amazonian African-descendant populations reflect a possible population amalgamation of Amerindian women from different Amazonian indigenous tribes and African women from different geographic regions of Africa who had been brought to Brazil as slaves. The present study partially mapped the historical biological and social interactions that had occurred during the formation and expansion of Amazonian African-descendant communities.
Key words: African mtDNA, Amazon population, Amerindian mtDNA, HVS-I.
The Portuguese settled in the Amazon region between the sixteenth and eighteenth centuries and carried out economic activities targeted at the European market. Extractivism based on Amerindian slave labor initially prevailed but later agriculture and cattle raising was supported by the intense Sub-Sahara African slave trade (Porto, 1938; Bezerra-Neto, 2001). Historical records indicate that about three and a half million captives were brought to Brazil, mainly from western and central Africa (Curtin, 1969; Salzano and Freire-Maia, 1970; Ribeiro, 1995). African slaves were brought to the Brazilian Amazon principally in the second half of the eighteenth century and became the main work force in the region (Conrad, 1985; Salles, 1988; Ribeiro, 1995). Approximately 53,000 slaves disembarked in this area, and by the middle of the nineteenth century the slave population in the Brazilian state of Pará in the Amazon region was almost 34,000, of which 49% were women and 51% men (Salles, 1988).
Slaves faced precarious living and working conditions in Brazil and their life expectancy was only 10 years after arrival. The most usual response to bad treatment was escaping, with many fugitive slaves founding independent communities called quilombos or mocambos in isolated areas, which are now known as African-descendant or African-derived communities (Ribeiro, 1995; Acevedo and Castro, 1998; Bezerra-Neto, 2001). Over last 20 years, these populations have been investigated by several groups of researchers such as anthropologists, linguists and geneticists, among others, in order to better understand the socio-biological formation and increment of such populations. Genetic studies based on classical genetic polymorphisms helped to reconstruct part of the history of these populations and also provided the first estimates concerning parental contributions, which demonstrated that these groups preserve a predominantly African genetic pool, notwithstanding the European and Amerindian contributions (Schneider et al., 1987; Bortolini et al., 1995, 1998; Guerreiro et al., 1999).
During the last decade many studies have used lineage markers such as mitochondrial DNA (mtDNA) to describe the genetic variability and evolutionary processes of different world populations. Phylogenetic analyses of mtDNA lineages (matrilineages) have also been published and many geographic-specific haplogroups have been identified (Vigilant et al. 1991; Torroni et al., 1993, 1996; Chen et al., 1995, 2000; Santos et al., 1996; Watson et al., 1996, 1997; Bortolini et al., 1997, 1999; Rando et al., 1998; Bandelt et al., 2001; Pereira et al., 2001; Salas et al., 2002, 2004; Yao et al., 2002; Mishmar et al., 2003; Rosa et al., 2004; Shen et al., 2004).
In this paper we provide information on the mtDNA haplogroup distribution of five African-descendant populations and evaluate the specific social mechanisms active in such communities, the aim being to better understand the genetic variability and the micro-evolutionary processes acting in human groups in the Brazilian Amazon. Additionally, our data were analyzed together with others recently published to determine the phylogeographic composition of the mtDNA lineages of African-descendant populations. We also discuss some aspects of the nature of the Atlantic slave trade to the Brazilian Amazon region.
Material and Methods
Our population sample consisted of unrelated African-descendants (n = 159) living in five communities located in three states in the Brazilian Amazon region: Trombetas (n = 32), Marajó island (n = 34) and Pitimandeua (n = 29) in Pará state; ii) Tamauari (n = 31) in Maranhão state; and iii) Mazagão (n = 33) in Amapá state. The geographic locations of these communities, self-reported as being based on African-descendants, are shown in Figure 1. All individuals provided their prior informed consent and this research was approved by the Ethical Committee of the Universidade Federal do Pará.
Mitochondrial DNA polymorphisms
The phenol-chloroform and ethanol methods (Sambrook et al., 1989) were used to extract DNA from whole peripheral blood. After extraction the DNA was quantified in a Gene Quant RNA/DNA spectrophotometer (Amersham Biosciences, UK) and diluted to a working concentration of 100 ng mL-1.
We Initially investigated the 9 bp deletion in region V of the CoII/tRNAlys intergenic region as well as the 663/Hae III, 13,259/Hinc II and 5,176/Alu I restriction fragment length polymorphisms (RFLP) which define Amerindian haplogroups (A-D) (Hertzberg et al., 1989; Torroni et al., 1992, 1993) along with the association of the 9 bp deletion with the 3,592/Hpa I RFLP which defines the African L0a2b sub-clade (Chen et al., 2000). Next, we used the L15997 and H16401 primers (Pereira et al., 2000) to amplify the first mitochondrial DNA hypervariable region (HVS-I) of samples from all five populations. The targets and the polymerase chain reaction (PCR) amplified segments were purified with a PureLink kit (Invitrogen, USA). The forward and reverse sequencing reactions were performed with the Big DyeÔ Terminator Cycle Sequence kit (Applied Biosystems, USA). Vertical electrophoresis was performed on 5% (w/v) denaturing polyacrylamide gels using ABI prism 377 DNA Sequencer (Applied Biosystems, USA). To better classify some sequences that did not present informative HVS-I mutations for the geographically-specific haplogroups and Europeans lineages we also used a further 19 RFLP markers belonging to the L0a, L1b, L1c, L3b, L3d, L3e, K, H, W, T, X, U, V, I and J haplogroups (Torroni et al., 1996; Alves-Silva et al., 2000; Chen et al., 2000).
The classification of each mtDNA lineage followed the nomenclature suggested for defining the African, Amerindian and European mitochondrial haplogroups (Torroni et al., 1993, 1996; Pereira et al., 2001; Salas et al., 2002, 2004; Mishmar et al., 2003). African mitochondrial haplogroups were characterized as L0a (pro L1a), L1b, L2a; L2b and other L3 haplogroups. Mutations at nucleotide positions (np) 16124, 16278 and 16362 were characterized as haplogroup L3b, and mutations at np 16124 and 16223 were characterized as haplogroup L3d. According to Bandelt et al. (2001), haplogroup L3e subdivides into L3e1 (16223 and 16327), L3e2 (16223 and 16320) and L3e3 (16223 and 16265T). Haplogroup L3f is characterized by transversions at np 16209 and 16311 (Salas et al., 2002). Sub-clade L3f1 is characterized by mutations at 16209, 16218, 16256, 16292, and 16311. We classified as haplogroup L3h (Kivisild et al., 2004; Rosa et al., 2004) the haplotype characterized by mutations at np 16129, 16256 and 16362. Mutations at np 16224 and 16311 characterize European haplogroup K (Torroni et al., 1996; Pereira et al., 2000).
Global analysis was performed with the 159 samples. We carried out Network analysis separately for the Amerindian and African lineage groups (Figure 2) using the median joining algorithm (Bandelt et al. 1999). Pairwise differences were obtained considering HVS-I for the same lineage groups according to the assumptions of Aris-Brosou and Excoffier (1996) using the DNAsp V 4.10 program (Rozas et al., 2003). Haplotype and nucleotide diversities were estimated using ARLEQUIN 2.0 (Schneider et al., 2000). Since the mtDNA haplogroups are geographically specific, the parental contributions for each population were obtained by direct counting.
Results and Discussion
Table 1 presents the 85 mtDNA haplotypes identified in the 159 samples from African-descendants defined by 78 variable nucleotides evaluated by network analysis (Figure 2). These HVS-I haplotypes have previously been reported by Ribeiro-dos-Santos et al. (2007) but we have reanalyzed all the haplotypes to better understand the genetic variability and the micro-evolutionary processes in the human groups in the Brazilian Amazon.
The five African-descendant populations investigated showed large genetic diversity and variability. The four main Amerindian haplogroups (A-D) and the African L1, L2, and L3 haplogroups were observed at different frequencies in these populations. The African L0 haplogroup was the least frequent and was observed only in the Trombetas and Curiaú populations, the latter having been previously studied by Ribeiro-dos-Santos et al. (2002).
Similar genetic diversity values were observed when the average nucleotide differences (k) and the haplotype diversity results (Hd) of Amazonian African-descendant Brazilians were compared with those of African groups from different regions of Africa (Mateu et al., 1997; Salas et al. 2004) (Table 2). The same occurred when the genetic diversity values of the Amerindian stock identified in the African-descendant populations were compared with those of isolated indigenous communities of the Brazilian Amazon. Since these African-descendant populations have resulted from the miscegenation of Africans and Amerindians our results indicate that the remaining quilombo communities of the Amazon region are possibly an important reservoir of African and Amazonian indigenous mtDNA variability.
Pairwise difference and genetic diversity
Pairwise analyses of nucleotidic differences relative to HVS-I of the samples obtained from the 159 African-descendants of the Amazon region and the Amerindian (74 samples) and African (80 samples) lineage groups were performed separately. The charts showed a normal distribution curves, although the Tajima test results were non-significant (p > 0.1). The average numbers of nucleotide differences for the Amerindian and African lineage groups (see Table 2) were similar to those reported for other Brazilian Amazonian Amerindian populations (Ward et al., 1991; Santos et al., 1996) and native sub-Saharan African populations (Salas et al. 2002, 2004) as well as to haplotype and nucleotide diversity results.
Mitochondrial DNA variability and parental contribution estimates African fraction
Approximately half of the samples (80/159, 50.3%) were from African maternal lineages, which had the widest geographical contribution of the samples studied. The African lineage haplogroups detected by us were as follows: L0, the least frequent (2/80, 2.5%) and containing sub-clades (also called variants) L0a1 and L0a2; L1, moderately frequent (18/80, 22.5%) and containing haplogroups L1b and L1c; L2, the second most frequent (27/80, 33.8%) and containing haplogroups L2a, L2b, and L2c; and L3, the most frequent (33/80, 41.2%) and containing sub-clades L3b, L3d, L3e, L3f and L3h.
The L0a1 sub-clade observed in our study is apparently absent from the northern region of the Brazilian Amazon (Silva-Junior et al., 2006) but was previously identified in the African-descendant Curiaú population in the Brazilian Amazon (Ribeiro-dos-Santos et al., 2002) and has also been described in populations from southeastern and southwestern Africa (Plaza et al., 2004; Salas et al., 2004; Beleza et al., 2005). The L0a2 sub-clade HVS-I mutations detected by us, also identified by the 9 bp deletion in region V, have been reported at a low frequency of ~4.5% in Brazil (Silva-Junior et al., 2006) but at ~19% in Mozambique in southeastern Africa (Salas et al., 2002).
In our study, 10 of the African-descendants belonged to sub-clade L1b, the third most frequent haplogroup (10/80, 12.5%), which has been reported to be almost restricted to West Africa (Salas et al., 2002, 2004). However, we found only eight lineages belonging to haplogroup L1c, which is a marker from western central Africa (Salas et al., 2004; Beleza et al., 2005). None of the HVS-I haplotypes belonging to the L1c haplogroup have been observed in Angola (Plaza et al., 2004) but some have been found in Cabinda in western central Africa and in Mozambique. The L1c haplogroup, and more specifically L1c2, L0a1, L3e1 and L3e2, are known to be frequent in African descendants from different regions of Brazil (Alves-Silva et al., 2000; Silva-Junior et al., 2006). However, we found that the most frequent mtDNA lineages of African descendant in the Brazilian Amazon belonged to haplogroups L3e (19/80, 23.7%), L2a (18/80, 22.5%) and L1b (10/80, 12.5%), these three haplogroups together being found in a total of 47 individuals of the 80 individuals of African maternal lineage (58.7%). These results suggest the existence of dissimilarities in the geographical distribution of African lineages in Brazil, which may be directly associated with slave trade practices adopted in the eighteenth and nineteenth centuries.
We also found that of the two sub-clade L1c2 lineages detected, both with the same haplotype, one (AFR 48a) presented the Hae III restriction site at position 663, which is the marker for Amerindian lineages in haplogroup A. The isolated occurrence of this Amerindian mutation in a lineage of African background might indicate recurrent mutation events, as described for Amerindian lineages by various authors (Bailliet et al., 1994; Santos et al., 1996; Torres et al., 2006). Because this lineage was of certain African origin and was the only one to exhibit a marker of a different geographic group (i.e., an Amerindian marker) we classified it as a complex haplotype.
In our study, there were low frequencies of some other haplogroups and sub-clades, such as L1c2, L2b, L3f1 and L3h. Sub-clade L3f1 only matches the lineages described in the central African Cabinda population (Beleza et al., 2005). The haplotype that represented haplogroup L3h (AFR 80) matched lineages described in the western African region of Guinea-Bissau where it was first described (Rosa et al., 2004). The L1b, L1c2, L3e1, L3f1 and L3h sub-clades have not previously been reported in the Brazilian Amazon (Alves-Silva et al., 2000; Silva-Junior et al., 2006). It is important to emphasize that this is the first report of the L3h haplogroup in Brazil, although it has been reported in Guinea-Bissau in western Africa and Ethiopia in eastern Africa (Kivisild et al., 2004; Rosa et al., 2004) (Figure 1).
Regarding slave trade practices, historical data suggests that 30% of the Africans brought to the Brazilian Amazon came from western Africa (Klein, 2002). Although most of the mtDNA haplogroups and sub-clades are geographically nonspecific, some groups have different distributions in Sub-Saharan Africa. For example, if we consider haplogroups L1b, L2c and L3d as markers from western Africa (Bandelt et al., 2001; Salas et al., 2004) it is possible to estimate that the contribution made by this region to the formation of contemporary Brazilian Amazonian African-descendant populations is about 25%. On the other hand, other haplogroups or sub-clades are more frequent in western, central and southeastern Africa, regions related to the major Bantu linguistic branch. Studies of hemoglobin S related polymorphisms in Brazilian Amazonian African-descendant populations suggest a Bantu contribution of approximately 45% (Pante-de-Souza et al., 1998). Adopting L0a, L2a, L1c, L3e1, and L3e2 as representative Bantu markers (Bandelt et al., 1995; Watson et al., 1997; Alves-Silva et al., 2000) leads to an estimate of 50%. Therefore, the data obtained by us are in agreement with the historical sources and other previously published biological data.
The second most important contribution to the mtDNA lineages of African-descendant populations were Amerindian-descendant (74/159, 46.6%). The four major Amerindian haplogroups (A, B, C and D) were well characterized by RFLP and the HVS-I region. Haplogroups A and C were the most frequent and presented similar distributions, followed by haplogroups B and D (Figure 2).
Haplogroup A lineages were defined by the 663/Hae III marker in association with the transitions at np 16111, 16290, and 16319 in the HVS-I region (Torroni et al. 1993). The mutation at np 16111, identified in Amerindian lineages, was not detected in two of the haplotypes (see Table 1). Similarly, Santos et al. (1996) also reported the absence of this transition in five Brazilian Amazonian Amerindian samples belonging to the same haplogroup. The 9 bp deletion and the absence of the 3592/Hpa I restriction site occurred in all the 17 sequences identified for haplogroup B (Hertzberg et al. 1989; Torroni et al. 1993). Curiously, we found that in haplogroup C (present in 20 of our samples) the 13259/Hinc II site occurred in one sequence (AFR 28a), this also having been reported in other southern Amazonian Brazilian Amerindian populations by Santos et al. (1996) and Bailliet et al. (1994). A recent study of Colombian Amerindians (Torres et al. 2006) reported a haplogroup C revertant lineage (recurrent mutation recreated +13259 Hinc II) with the same HVS-I haplotype as that identified by us in lineage AFR 28a. Own genetic structure analyses are consistent with reverse mutation at an early stage during the tribalization process.
We found that haplogroup D was the least frequent haplogroup in African descendants from the Brazilian Amazon. All 16 samples classified in this group were marked by the absence of the 5176/Alu I site. The T ® C transition at site 16325 of HVS-I identified in Amerindian lineages of haplogroup D in Native Americans was observed in all haplotypes (Ward et al., 1991; Torroni et al., 1993; Santos et al. 1996).
Amerindian lineage groups have been detected in Brazilian Amazon African-descendant communities by classical genetic analysis, which detected 14.7% Amerindian lineage groups, and molecular genetic analysis, which detected 19.1% Amerindian lineage groups (Table 3). However, the mtDNA data revealed an average Amerindian contribution of 50% in nine African-descendant populations located in former slave settlements the Brazilian Amazon. Different genetic markers (e.g., nuclear DNA and Y-DNA) may have underestimated the assimilation of the indigenous element in the formation of African-descendant communities. Alternatively, the Amerindian contribution may have occurred through a larger introgression from Amerindian women than from Amerindian men.
The high mtDNA estimate of Amerindian lineages in the composition of these communities was unexpected because there are no historical data on significant sexual interaction between African slaves and other ethnic groups in quilombo communities. However, the settlement of South America, and the Brazilian Amazon in particular, has involved complex ethnic-social interactions, especially when it comes to pre-existing Amerindian societies. Settlement has resulted in the formation of genetically mixed urban populations, with Alves-Silva et al. (2000) having demonstrated that 54% of the mtDNA lineages of individuals from northern Brazil who considered themselves white have an Amerindian descent. Furthermore, Santos et al. (1999) investigated the urban populations of Belém, the capital of the Brazilian state of Pará, and observed a high Amerindian matrilineal contribution of 57%.
The presence of Amerindian lineages in trihybrid urban populations in the Brazilian Amazon has resulted from Portuguese policy in the sixteenth and seventeenth centuries that encouraged marriages between Portuguese settlers and Amerindian women (Cruz, 1973, Salles, 1988). Since historical records concerning Amerindian miscegenation with African-descendant populations are scarce, we suggest that the "Amerindian-African" union results from a survival and social resistance strategy against the slavery policy adopted in Brazil until the mid nineteenth century.
European and other fractions
European lineages represented the smallest contribution, being detected in only two samples (1.3%). Haplogroup K occurred in Mazagão in Amapá state and Marajó island in Pará state and was defined after the analyses of 23 RFLP (9 bp deletion) and the sequencing of the first hypervariable region (Table 4). The participation of European groups in the formation of African-descendant communities has not been reported in historical records. Therefore, such lineages may have resulted from recent interethnic miscegenation.
Even though the techniques used by us were sophisticated, the classification of three Tamauari and Mazagão lineages (AFR 83, 84, and 85) representing 1.9% of the total sample, remained inconclusive (Table 1).
According to the results observed, the present study partially mapped the social-biological interactions that had occurred during the formation and expansion of Amazonian African-descendant communities. The mtDNA approach reveals that these populations congregate two main genetic backgrounds: African and Native American lineages. Our results also indicate that these communities are an important reservoir of mtDNA variability and diversity for these human geographic groups.
The authors thank the Afro-descendants who donated samples and enabled this study to be carried out. This study was supported by the Brazilian agencies Financiadora de Estudos e Projetos (FINEP), Projeto Milênio de Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Universidade Federal do Pará (UFPA). The authors would like to thank Ana Cecília Feio dos Santos for her contribution.
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Send correspondence to:
Ândrea K.C. Ribeiro-dos-Santos
Laboratório de Genética Humana e Médica, Instituto de Ciências Biológicas
Universidade Federal do Pará
Caixa Postal 8615, Rua Augusto Corrêa 01, Guamá
66075-970 Belém, Pa, Brazil
Received: January 5, 2007; Accepted: June 11, 2007.
Associate Editor: Francisco Mauro Salzano