Identification of Polynesian mtDNA haplogroups in remains of Botocudo Amerindians from Brazil
Edited by Francisco Mauro Salzano, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil, and approved March 4, 2013 (received for review October 15, 2012)
Abstract
There is a consensus that modern humans arrived in the Americas 15,000–20,000 y ago during the Late Pleistocene, most probably from northeast Asia through Beringia. However, there is still debate about the time of entry and number of migratory waves, including apparent inconsistencies between genetic and morphological data on Paleoamericans. Here we report the identification of mitochondrial sequences belonging to haplogroups characteristic of Polynesians in DNA extracted from ancient skulls of the now extinct Botocudo Indians from Brazil. The identification of these two Polynesian haplogroups was confirmed in independent replications in Brazil and Denmark, ensuring reliability of the data. Parallel analysis of 12 other Botocudo individuals yielded only the well-known Amerindian mtDNA haplogroup C1. Potential scenarios to try to help understand these results are presented and discussed. The findings of this study may be relevant for the understanding of the pre-Columbian and/or post-Columbian peopling of the Americas.
Acknowledgments
We thank Dr. Marcel Giovanni Costa França and Dr. Queila Souza Garcia (Departamento de Botânica of Universidade Federal de Minas Gerais) for kindly providing access to their physical facilities; Neuza A. Rodrigues, Kátia Barroso, and Tom Gilbert for providing expert technical assistance; and Dr. James Kennedy (University of Toronto) for all of his support. This work was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico of Brazil and the Danish National Research Foundation.
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References
1
P Rivet, La race de Lagoa-Santa chez le population precolombiennes de L'Equateur. Bull Mem Soc Anthropol Paris 9, 209–268 (1908).
2
A Hrdlicka Early Man in South America (Smithsonian Institution, Washington, 1912).
3
MM Lahr The Evolution of Modern Human Diversity: A Study of Cranial Variatio (Cambridge Univ Press, Cambridge, 1996).
4
WA Neves, A Prous, R González-José, R Kipnis, J Powell, Early Holocene human skeletal remains from Santana do Riacho, Brazil: Implications for the settlement of the New World. J Hum Evol 45, 19–42 (2003).
5
WA Neves, HM Pucciarelli, Morphological affinities of the first Americans: An exploratory analysis based on Early South American human remains. J Hum Evol 21, 261–273 (1991).
6
M Hubbe, WA Neves, JPV Atui, C Cartelle, MP Silva, A new early human skeleton from Brazil: Further support to the “two main biological components model” for the settlement of the Americas. Current Research in the Pleistocene 21, 77–81 (2004).
7
WA Neves, M Hubbe, Cranial morphology of early Americans from Lagoa Santa, Brazil: Implications for the settlement of the New World. Proc Natl Acad Sci USA 102, 18309–18314 (2005).
8
M Hubbe, WA Neves, K Harvati, Testing evolutionary and dispersion scenarios for the settlement of the new world. PLoS ONE 5, e11105 (2010).
9
M Hubbe, K Harvati, W Neves, Paleoamerican morphology in the context of European and East Asian late Pleistocene variation: Implications for human dispersion into the New World. Am J Phys Anthropol 144, 442–453 (2011).
10
D Reich, et al., Reconstructing Native American population history. Nature 488, 370–374 (2012).
11
E Tamm, et al., Beringian standstill and spread of Native American founders. PLoS ONE 2, e829 (2007).
12
UA Perego, et al., Distinctive Paleo-Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Curr Biol 19, 1–8 (2009).
13
UA Perego, et al., The initial peopling of the Americas: A growing number of founding mitochondrial genomes from Beringia. Genome Res 20, 1174–1179 (2010).
14
M Bodner, et al., Rapid coastal spread of First Americans: Novel insights from South America’s Southern Cone mitochondrial genomes. Genome Res 22, 811–820 (2012).
15
M de Saint Pierre, et al., An alternative model for the early peopling of southern South America revealed by analyses of three mitochondrial DNA haplogroups. PLoS ONE 7, e43486 (2012).
16
NJ Fagundes, R Kanitz, SL Bonatto, A reevaluation of the Native American mtDNA genome diversity and its bearing on the models of early colonization of Beringia. PLoS ONE 3, e3157 (2008).
17
SD Pena, et al., A major founder Y-chromosome haplotype in Amerindians. Nat Genet 11, 15–16 (1995).
18
FR Santos, et al., The central Siberian origin for native American Y chromosomes. Am J Hum Genet 64, 619–628 (1999).
19
SL Zegura, TM Karafet, LA Zhivotovsky, MF Hammer, High-resolution SNPs and microsatellite haplotypes point to a single, recent entry of Native American Y chromosomes into the Americas. Mol Biol Evol 21, 164–175 (2004).
20
TM Karafet, et al., New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res 18, 830–838 (2008).
21
R González-José, MC Bortolini, FR Santos, SL Bonatto, The peopling of America: Craniofacial shape variation on a continental scale and its interpretation from an interdisciplinary view. Am J Phys Anthropol 137, 175–187 (2008).
22
MHB Paraiso História dos Índios no Brasil [History of Indians in Brazil] (FAPESP/SMC/Companhia das Letras, São Paulo), pp. 413–430 (1992).
23
MHB Paraiso, O tempo de dor e do trabalho: A conquista dos territórios indígenas nos sertões do leste [The time of pain and labor: The conquest of indigenous territories in eastern inlands]. PhD thesis. (Universidade de São Paulo, Brazil, 1998).
24
H Langfur, Uncertain refuge: Frontier formation and the origins of the Botocudo war in late colonial Brazil. Hisp Am Hist Rev 82, 215–256 (2002).
25
F Lacerda, R Peixoto, Contribuições para o estudo antropológico das raças indígenas do Brazil [Contributions to the anthropological study of indigenous races of Brazil]. Arquivos do Museu Nacional do Rio de Janeiro 1, 47–79 (1876).
26
R Peixoto, Novos estudos craniológicos sobre os Botocudos [New studies on cranial features of the Botocudos]. Arquivos do Museu Nacional do Rio de Janeiro 6, 5–53 (1885).
27
Atui JPV (2005) Morfologia craniana de ameríndios brasileiros recentes e suas implicações para a questão da ocupação do novo mundo: Uma análise exploratória [Cranial morphology of recent Brazilian Amerindians and its implications for the occupation of the New World: An exploratory analysis]. PhD thesis (Universidade de São Paulo, Brazil).
28
J Alves-Silva, et al., The ancestry of Brazilian mtDNA lineages. Am J Hum Genet 67, 444–461 (2000).
29
H Razafindrazaka, et al., Complete mitochondrial DNA sequences provide new insights into the Polynesian motif and the peopling of Madagascar. Eur J Hum Genet 18, 575–581 (2010).
30
VF Gonçalves, et al., Recovering mitochondrial DNA lineages of extinct Amerindian nations in extant homopatric Brazilian populations. Investig Genet 1, 13 (2010).
31
AJ Redd, et al., Evolutionary history of the COII/tRNALys intergenic 9 base pair deletion in human mitochondrial DNAs from the Pacific. Mol Biol Evol 12, 604–615 (1995).
32
JA Trejaut, et al., Traces of archaic mitochondrial lineages persist in Austronesian-speaking Formosan populations. PLoS Biol 3, e247 (2005).
33
P Soares, et al., Ancient voyaging and Polynesian origins. Am J Hum Genet 88, 239–247 (2011).
34
JS Friedlaender, et al., Melanesian mtDNA complexity. PLoS ONE 2, e248 (2007).
35
BA Lie, et al., Molecular genetic studies of natives on Easter Island: Evidence of an early European and Amerindian contribution to the Polynesian gene pool. Tissue Antigens 69, 10–18 (2007).
36
E Thorsby, The Polynesian gene pool: An early contribution by Amerindians to Easter Island. Philos Trans R Soc Lond B Biol Sci 367, 812–819 (2012).
37
WA Neves, M Hubbe, G Correal, Human skeletal remains from Sabana de Bogotá, Colombia: A case of Paleoamerican morphology late survival in South America? Am J Phys Anthropol 133, 1080–1098 (2007).
38
R González-José, et al., Craniometric evidence for Palaeoamerican survival in Baja California. Nature 425, 62–65 (2003).
39
MM Lahr, The multiregional model of modern human origins: A reassessment of its morphological basis. J Hum Evol 26, 23–56 (1994).
40
MM Lahr, Patterns of modern human diversification: Implications for Amerindian origins. Yearb Phys Anthropol 38, 163–198 (1995).
41
MP Cox, Indonesian mitochondrial DNA and its opposition to a Pleistocene era origin of proto-Polynesians in island southeast Asia. Hum Biol 77, 179–188 (2005).
42
H Soodyall, T Jenkins, M Stoneking, ‘Polynesian’ mtDNA in the Malagasy. Nat Genet 10, 377–378 (1995).
43
RL Cann, mtDNA and Native Americans: A Southern perspective. Am J Hum Genet 55, 7–11 (1994).
44
SL Bonatto, AJ Redd, FM Salzano, M Stoneking, Lack of ancient Polynesian-Amerindian contact. Am J Hum Genet 59, 253–258 (1996).
45
AA Storey, et al., Radiocarbon and DNA evidence for a pre-Columbian introduction of Polynesian chickens to Chile. Proc Natl Acad Sci USA 104, 10335–10339 (2007).
46
D Yen The Sweet Potato in Oceania: An Essay in Ethnobotany (Bishop Museum Press, Honolulu, HI, 1974).
47
RC Green, A range of disciplines support a dual origin for the bottle gourd in the Pacific. J Polyn Soc 109, 191–197 (2000).
48
HE Maude Slavers in Paradise: The Peruvian Slave Trade in Polynesia, 1862–1864 (Stanford Univ Press, Stanford, CA, 1981).
49
ML Moraga, et al., Mitochondrial DNA polymorphisms in Chilean aboriginal populations: Implications for the peopling of the southern cone of the continent. Am J Phys Anthropol 113, 19–29 (2000).
50
S Fuselli, et al., Mitochondrial DNA diversity in South America and the genetic history of Andean highlanders. Mol Biol Evol 20, 1682–1691 (2003).
51
CM Lewis, RY Tito, B Lizárraga, AC Stone, Land, language, and loci: mtDNA in Native Americans and the genetic history of Peru. Am J Phys Anthropol 127, 351–360 (2005).
52
M Baca, K Doan, M Sobczyk, A Stankovic, P Węgleński, Ancient DNA reveals kinship burial patterns of a pre-Columbian Andean community. BMC Genet 13, 30 (2012).
53
PD Curtin The Atlantic Slave Trade: A Census (Univ of Wisconsin Press, Madison, 1969).
54
G Campbell, Madagascar and the Slave Trade, 1810–1895. J Afr Hist 22, 203–227 (1981).
55
VML Moreira, A guerra contra os índios botocudos e a formação de quilombos no Espírito Santo. [The war against the Botocudo Indians and the formation of African communities in Espirito Santo] Afro-Asia 41, 57–83 (2010).
56
N Rohland, M Hofreiter, Ancient DNA extraction from bones and teeth. Nat Protoc 2, 1756–1762 (2007).
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Cover image: Pictured is a gargoyle gecko, Rhacodactylus auriculatus. Previous studies have examined how geckos stick to clean, dry laboratory surfaces, but how the gecko adhesive system functions in wet conditions remains unclear. Alyssa Y. Stark et al. measured gecko adhesion to a variety of surfaces under wet and dry conditions, and found that the animals can stick equally well to wet and dry hydrophobic surfaces, but not to wet hydrophilic surfaces. The findings suggest that water might not impair gecko adhesion to hydrophobic surfaces found in nature, such as plant leaves. See the article by Stark et al. on pages 6340–6345. Image courtesy of Alyssa Y. Stark.
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Published online: April 1, 2013
Published in issue: April 16, 2013
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Acknowledgments
We thank Dr. Marcel Giovanni Costa França and Dr. Queila Souza Garcia (Departamento de Botânica of Universidade Federal de Minas Gerais) for kindly providing access to their physical facilities; Neuza A. Rodrigues, Kátia Barroso, and Tom Gilbert for providing expert technical assistance; and Dr. James Kennedy (University of Toronto) for all of his support. This work was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico of Brazil and the Danish National Research Foundation.
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This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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