Demographic and Evolutionary Trajectories of the Guarani and Kaingang Natives of Brazil Andrea R

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 132:301–310 (2007) Demographic and Evolutionary Trajectories of the Guarani and Kaingang Natives of Brazil Andrea R. Marrero,1 Wilson A. Silva-Junior,2 Cla´ udio M. Bravi,3 Mara H. Hutz,1 Maria L. Petzl-Erler,4 Andres Ruiz-Linares,5 Francisco M. Salzano,1 and Maria C. Bortolini1* 1Departamento de Gene´tica, Instituto de Biocieˆncias, Universidade Federal do Rio Grande do Sul, 91501-970 Porto Alegre, Rio Grande do Sul, Brazil 2Departamento de Gene´tica e Centro de Terapia Celular, Universidade de Saõ Paulo, 14049-900 Ribeiraõ Preto, Saõ Paulo, Brazil 3Laboratorio de Gene´tica Molecular Poblacional, Instituto Multidisciplinario de Biologıá Celular (IMBICE), La Plata, Argentina 4Departamento de Gene´tica, Universidade Federal do Parana´, 81531-990 Curitiba, Parana´, Brazil 5The Galton Laboratory, University College, London, UK KEY WORDS mtDNA; Y-chromosome markers; Amerindians; asymmetrical interethnic matings ABSTRACT A total of 278 individuals from two Brazil- gesting a higher level of differentiation between the three ian Indian tribes (Guarani and Kaingang) living in five dif- Guarani partialities than between the two Kaingang ferent localities had their mitochondrial DNA sequenced villages. Non-Amerindian admixture varied with sex and for the first hypervariable segment (HVS-I), and a fraction in the Guarani was only observed through the paternal of them was also studied for seven biallelic Y-chromosome line. Using these data and those of other Tupian and polymorphisms. Nineteen HVS-I lineages were detected, Jeân tribes, it was possible to make inferences about past which showed distinct distributions in the two tribes. The migratory movements and the genetic differentiation of GST value obtained with the mtDNA data is about 5 times these populations. Am J Phys Anthropol 132:301–310, higher for the Guarani as compared to the Kaingang, sug- 2007. VC 2006 Wiley-Liss, Inc. Genetic studies have been used as powerful tools to Using microsatellite loci, Tarazona-Santos et al. (2001) characterize Native American populations. Schurr and showed that the Andean Native populations exhibit signif- Sherry (2004) showed that the mitochondrial DNA icantly higher within-population variability than the east- (mtDNA) and the nonrecombining portion of the Y-chro- ern groups (Amazonian region, Brazilian plateau, and the mosome (NRY) are at present the two genetic systems Chaco region). These authors proposed a model for the most commonly used in studies with these population evolution of the South Amerindian male lineages that groups. Investigations using mtDNA in Amerindians involved differential patterns of genetic drift and gene revealed the presence of five different haplogroups, desig- flow. nated A–D (Schurr et al., 1990; Torroni et al., 1992, 1993) The origin of the Tupian linguistic family is controver- and X (Brown et al., 1998), and the highest level of differ- sial (Noelli, 1998; Rodrigues, 2000). However, most of entiation between populations considering the human the authors report regions at the southern margin of the major geographical groups (Bortolini and Salzano, 1996; Amazon River (Rodrigues, 1964; Migliazza, 1982; Urban, Bortolini et al., 1997). These and other studies have also 1996, 1998; Heckenberger et al., 1998). For example, shown distinct haplogroup distributions in South America: Migliazza (1982) suggested that the probable place of ori- Haplogroup A generally occurs at higher frequencies in gin of the Tupian linguistic family was situated between northern regions, while haplogroups C and D are frequent the Jiparana´ and Aripuana˜ rivers, and that the postu- in several parts of South America. Haplogroup B is only lated parental group was living there about 5,000 years abundant in southern Peru, Andean Bolivia, northern Chile, and Argentina. Haplogroup X is not found in South America (Dornelles et al., 2005). Grant sponsors: Institutos do Mileˆnio; Programa de Apoio a Nu´ cleos Initial analyses with NRY markers, on the other hand, de Exceleˆncia; Conselho Nacional de Desenvolvimento Cientı´fico e found just one haplotype at high frequencies in native Tecnolo´gico; Fundaçaõ de Amparo a` Pesquisa do Estado do Rio ˆ populations in North and South America of all linguistic Grande do Sul; Academia Brasileira de Ciencias; The Royal Society. groups (Pena et al., 1995). This most common Y-chromo- ? *Correspondence to: Maria C. Bortolini, Departamento de Gene´tica, some was afterward characterized by a C T mutation at Instituto de Biocieˆncias, Universidade Federal do Rio Grande do Sul, marker M3 (Underhill et al., 1996), which defines hap- Caixa Postal 15053, 91501-970 Porto Alegre, Rio Grande do Sul, logroup Q3* (The Y Chromosome Consortium, 2002; Brazil. E-mail: [email protected] Jobling and Tyler-Smith, 2003). More recently, other Asian or Native American autochthonous haplogroups Received 14 February 2006; accepted 8 August 2006 have been identified (C*, Q*, Q3a), but with different distributions among populations. For example, C* (which is DOI 10.1002/ajpa.20515 present in high frequencies in Asia) is only found in Published online 28 November 2006 in Wiley InterScience North, and Q3a in South America (Bortolini et al., 2003). (www.interscience.wiley.com). VC 2006 WILEY-LISS, INC. 302 A.R. MARRERO ET AL. 2,000 ybp, whereas that in direction to the Amazonian region was more recent (2,000–1,000 ybp; Urban, 1998). The Kaingang have been recognized as descendents of the native inhabitants of the Brazilian Central-South plateau, who lived in rustic subterraneous houses (Schmitz and Becker, 1997). Their number was drastically dimin- ished after contact with the European colonizers, but those who survived and their descendents live now in reservations in the Brazilian states of Rio Grande do Sul, Santa Catarina, Parana´, and Saõ Paulo. Their contact with non-Indians during the colonization process was less marked than that which occurred with the Guarani, but presently the situation changed, both showing variable local interaction with the surrounding populations. Although Guarani and Kaingang have lived next to each other since the 17th century, they are culturally distinct (Carneiro da Cunha, 1998). Genetic differences have also been reported, with blood group and protein polymorphisms (Salzano et al., 1997; Callegari-Jacques and Salzano, 1999) and different DNA data sets: Y-SNP/STR (Bortolini et al., 2003), AAB-auto-antibody (Utiyama et al., 2000), Alu insertions (Battilana et al., 2002), nuclear STRs (Kohlrausch et al., 2005), HLA, and other MHC (major his- tocompatibility complex) loci (Petzl-Erler et al., 1993; Sotomaior et al., 1998; Faucz et al., 2000; Tsuneto et al., 2003), CYP-cytochrome P-450, GST-glutathione S-trans- ferase, and the TP53 tumor-suppressor gene (Gaspar et al., 2002), and TCR-T-cell receptor and CCR5-chemokine re- Fig. 1. Probable routes of dispersion of the Tupian and Jeân ceptor genes (Hu¨ nemeier et al., 2005). speakers. Arrows indicate possible routes and the estimated dates when they may have occurred in years before present. The present work furnishes data related to the varia- Dots show the main archeological sites of the Tupi-Guarani cul- tion of mtDNA first hypervariable segment (HVS-I) and ture (modified from Schmitz, 1997), while the circle represents of markers located in the NRY-chromosome in Guarani the probable region of origin of the Jeân linguistic family and Kaingang, which represent the southern extremes of (Urban, 1998). the population distribution of members of the Tupian and Jeân linguistic families in Brazil. Questions asked were as follows: (a) what genetic differences can be before present (ybp). The diversification of this major found among them, and how are they distributed among Amerindian linguistic family occurred, due to community local groups? Are their levels of diversity similar or dis- isolation, concomitantly with the extraordinary and suc- tinct? (b) how do they correlate with independent evalua- cessful dispersion of the agriculturalist Tupian speakers tions of their history? and (c) what insights concerning (Fig. 1). The Guarani speak a language classified in the the interethnic exchange which occurred along this his- Tupi-Guarani branch (Campbell, 1997). Their split from torical process can be obtained using parentally diverse the other Tupi probably occurred around 1,800 ybp (Fig. 1; genetic markers? Carneiro da Cunha, 1998). In colonial times, the Gua- rani who lived in the high Parana´ and Uruguay River SUBJECTS AND METHODS basins were attracted to Jesuit missions, where they remained for almost two centuries, while other groups Populations stayed isolated, hidden in the forests. Today, in Brazil, Samples of 200 Guarani and 78 Kaingang living in they generally live in reservations and can be subdivided in reservations (Rio das Cobras, Amambaı´, Limaõ Verde, three partialities, in agreement with several aspects of Porto Lindo, Ivaı´, Nonoai) located in central and south- their culture: Guarani N˜ andeva, Guarani Kaiowa´,and ern states of Brazil (Mato Grosso do Sul, Parana´ and Rio Guarani M’bya´ (Vietta, 1992). Because they have been in Grande do Sul; Fig. 2) were obtained. More details about contact with non-Indians since colonial times (Kern, 1997), these populations can be found in Petzl-Erler et al. (1993), they should also have contributed to the formation of the Bortolini et al. (2002, 2003), Tsuneto et al. (2003), and South Brazilian admixed populations in a significant way Kohlrausch et al. (2005). (Marrero et al., 2005). The term Kaingang (or Caingang) was introduced in 1882 to designate all non-Guarani indigenous people living Y-chromosome markers in South Brazil (Becker and Laroque, 1999), but at the time of the first contact with Europeans they were known Thirty Guarani M’bya´ and 36 Kaingang from Parana´ as Guaiana´s (16th and 17th centuries) or Coroados (19th were studied for seven biallelic polymorphisms (M242, century). The Kaingang are Jeân speakers (Southern M3, M19, 92R7, M9, YAP, and M2), located in the NRY- branch; Campbell, 1997).

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