Abstract
Despite considerable investigation, two main questions on the origin of Native Americans remain the topic of intense debate-namely, the number and time of the migration(s) into the Americas. Using the 720 available Amerindian mtDNA control-region sequences, we reanalyzed the nucleotide diversity found within each of the four major mtDNA haplogroups (A-D) thought to have been present in the colonization of the New World. We first verified whether the within-haplogroup sequence diversity could be used as a measure of the haplogroup's age. The pattern of shared polymorphism, the mismatch distribution, the phylogenetic trees, the value of Tajima's D, and the computer simulations all suggested that the four haplogroups underwent a bottleneck followed by a large population expansion. The four haplogroup diversities were very similar to each other, offering a strong support for their single origin. They suggested that the beginning of the Native Americans' ancestral-population differentiation occurred approximately 30,000-40,000 years before the present (ybp), with a 95%-confidence-interval lower bound of approximately 25,000 ybp. These values are in good agreement with the New World-settlement model that we have presented elsewhere, extending the results initially found for haplogroup A to the three other major groups of mtDNA sequences found in the Americas. These results put the peopling of the Americas clearly in an early, pre-Clovis time frame.
Full text
PDF










Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
- Aris-Brosou S., Excoffier L. The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol. 1996 Mar;13(3):494–504. doi: 10.1093/oxfordjournals.molbev.a025610. [DOI] [PubMed] [Google Scholar]
- Bailliet G., Rothhammer F., Carnese F. R., Bravi C. M., Bianchi N. O. Founder mitochondrial haplotypes in Amerindian populations. Am J Hum Genet. 1994 Jul;55(1):27–33. [PMC free article] [PubMed] [Google Scholar]
- Batista O., Kolman C. J., Bermingham E. Mitochondrial DNA diversity in the Kuna Amerinds of Panamá. Hum Mol Genet. 1995 May;4(5):921–929. doi: 10.1093/hmg/4.5.921. [DOI] [PubMed] [Google Scholar]
- Bonatto S. L., Redd A. J., Salzano F. M., Stoneking M. Lack of ancient Polynesian-Amerindian contact. Am J Hum Genet. 1996 Jul;59(1):253–258. [PMC free article] [PubMed] [Google Scholar]
- Bonatto S. L., Salzano F. M. A single and early migration for the peopling of the Americas supported by mitochondrial DNA sequence data. Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1866–1871. doi: 10.1073/pnas.94.5.1866. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donnelly P., Tavaré S. Coalescents and genealogical structure under neutrality. Annu Rev Genet. 1995;29:401–421. doi: 10.1146/annurev.ge.29.120195.002153. [DOI] [PubMed] [Google Scholar]
- Easton R. D., Merriwether D. A., Crews D. E., Ferrell R. E. mtDNA variation in the Yanomami: evidence for additional New World founding lineages. Am J Hum Genet. 1996 Jul;59(1):213–225. [PMC free article] [PubMed] [Google Scholar]
- Excoffier L., Smouse P. E., Quattro J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992 Jun;131(2):479–491. doi: 10.1093/genetics/131.2.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Forster P., Harding R., Torroni A., Bandelt H. J. Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet. 1996 Oct;59(4):935–945. [PMC free article] [PubMed] [Google Scholar]
- Ginther C., Corach D., Penacino G. A., Rey J. A., Carnese F. R., Hutz M. H., Anderson A., Just J., Salzano F. M., King M. C. Genetic variation among the Mapuche Indians from the Patagonian region of Argentina: mitochondrial DNA sequence variation and allele frequencies of several nuclear genes. EXS. 1993;67:211–219. doi: 10.1007/978-3-0348-8583-6_17. [DOI] [PubMed] [Google Scholar]
- Harpending H. C. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol. 1994 Aug;66(4):591–600. [PubMed] [Google Scholar]
- Hoffecker J. F., Powers W. R., Goebel T. The colonization of beringia and the peopling of the new world. Science. 1993 Jan 1;259(5091):46–53. doi: 10.1126/science.259.5091.46. [DOI] [PubMed] [Google Scholar]
- Horai S., Hayasaka K., Kondo R., Tsugane K., Takahata N. Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):532–536. doi: 10.1073/pnas.92.2.532. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horai S., Kondo R., Nakagawa-Hattori Y., Hayashi S., Sonoda S., Tajima K. Peopling of the Americas, founded by four major lineages of mitochondrial DNA. Mol Biol Evol. 1993 Jan;10(1):23–47. doi: 10.1093/oxfordjournals.molbev.a039987. [DOI] [PubMed] [Google Scholar]
- Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
- Kolman C. J., Bermingham E., Cooke R., Ward R. H., Arias T. D., Guionneau-Sinclair F. Reduced mtDNA diversity in the Ngöbé Amerinds of Panamá. Genetics. 1995 May;140(1):275–283. doi: 10.1093/genetics/140.1.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kolman C. J., Sambuughin N., Bermingham E. Mitochondrial DNA analysis of Mongolian populations and implications for the origin of New World founders. Genetics. 1996 Apr;142(4):1321–1334. doi: 10.1093/genetics/142.4.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Merriwether D. A., Ferrell R. E. The four founding lineage hypothesis for the New World: a critical reevaluation. Mol Phylogenet Evol. 1996 Feb;5(1):241–246. doi: 10.1006/mpev.1996.0017. [DOI] [PubMed] [Google Scholar]
- Merriwether D. A., Rothhammer F., Ferrell R. E. Distribution of the four founding lineage haplotypes in Native Americans suggests a single wave of migration for the New World. Am J Phys Anthropol. 1995 Dec;98(4):411–430. doi: 10.1002/ajpa.1330980404. [DOI] [PubMed] [Google Scholar]
- Monsalve M. V., Cardenas F., Guhl F., Delaney A. D., Devine D. V. Phylogenetic analysis of mtDNA lineages in South American mummies. Ann Hum Genet. 1996 Jul;60(Pt 4):293–303. doi: 10.1111/j.1469-1809.1996.tb01193.x. [DOI] [PubMed] [Google Scholar]
- Redd A. J., Takezaki N., Sherry S. T., McGarvey S. T., Sofro A. S., Stoneking M. Evolutionary history of the COII/tRNALys intergenic 9 base pair deletion in human mitochondrial DNAs from the Pacific. Mol Biol Evol. 1995 Jul;12(4):604–615. doi: 10.1093/oxfordjournals.molbev.a040240. [DOI] [PubMed] [Google Scholar]
- Rogers A. R., Fraley A. E., Bamshad M. J., Watkins W. S., Jorde L. B. Mitochondrial mismatch analysis is insensitive to the mutational process. Mol Biol Evol. 1996 Sep;13(7):895–902. doi: 10.1093/molbev/13.7.895. [DOI] [PubMed] [Google Scholar]
- Rogers A. R., Harpending H. Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol. 1992 May;9(3):552–569. doi: 10.1093/oxfordjournals.molbev.a040727. [DOI] [PubMed] [Google Scholar]
- Rogers A. R., Jorde L. B. Genetic evidence on modern human origins. Hum Biol. 1995 Feb;67(1):1–36. [PubMed] [Google Scholar]
- Santos S. E., Ribeiro-Dos-Santos A. K., Meyer D., Zago M. A. Multiple founder haplotypes of mitochondrial DNA in Amerindians revealed by RFLP and sequencing. Ann Hum Genet. 1996 Jul;60(Pt 4):305–319. doi: 10.1111/j.1469-1809.1996.tb01194.x. [DOI] [PubMed] [Google Scholar]
- Shields G. F., Schmiechen A. M., Frazier B. L., Redd A., Voevoda M. I., Reed J. K., Ward R. H. mtDNA sequences suggest a recent evolutionary divergence for Beringian and northern North American populations. Am J Hum Genet. 1993 Sep;53(3):549–562. [PMC free article] [PubMed] [Google Scholar]
- Slatkin M., Hudson R. R. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics. 1991 Oct;129(2):555–562. doi: 10.1093/genetics/129.2.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stoneking M., Sherry S. T., Redd A. J., Vigilant L. New approaches to dating suggest a recent age for the human mtDNA ancestor. Philos Trans R Soc Lond B Biol Sci. 1992 Aug 29;337(1280):167–175. doi: 10.1098/rstb.1992.0094. [DOI] [PubMed] [Google Scholar]
- Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993 May;10(3):512–526. doi: 10.1093/oxfordjournals.molbev.a040023. [DOI] [PubMed] [Google Scholar]
- Torroni A., Neel J. V., Barrantes R., Schurr T. G., Wallace D. C. Mitochondrial DNA "clock" for the Amerinds and its implications for timing their entry into North America. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1158–1162. doi: 10.1073/pnas.91.3.1158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torroni A., Schurr T. G., Cabell M. F., Brown M. D., Neel J. V., Larsen M., Smith D. G., Vullo C. M., Wallace D. C. Asian affinities and continental radiation of the four founding Native American mtDNAs. Am J Hum Genet. 1993 Sep;53(3):563–590. [PMC free article] [PubMed] [Google Scholar]
- Torroni A., Schurr T. G., Yang C. C., Szathmary E. J., Williams R. C., Schanfield M. S., Troup G. A., Knowler W. C., Lawrence D. N., Weiss K. M. Native American mitochondrial DNA analysis indicates that the Amerind and the Nadene populations were founded by two independent migrations. Genetics. 1992 Jan;130(1):153–162. doi: 10.1093/genetics/130.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wakeley J. Substitution rate variation among sites in hypervariable region 1 of human mitochondrial DNA. J Mol Evol. 1993 Dec;37(6):613–623. doi: 10.1007/BF00182747. [DOI] [PubMed] [Google Scholar]
- Wallace D. C. 1994 William Allan Award Address. Mitochondrial DNA variation in human evolution, degenerative disease, and aging. Am J Hum Genet. 1995 Aug;57(2):201–223. [PMC free article] [PubMed] [Google Scholar]
- Ward R. H., Frazier B. L., Dew-Jager K., Päbo S. Extensive mitochondrial diversity within a single Amerindian tribe. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8720–8724. doi: 10.1073/pnas.88.19.8720. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ward R. H., Redd A., Valencia D., Frazier B., Päbo S. Genetic and linguistic differentiation in the Americas. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10663–10667. doi: 10.1073/pnas.90.22.10663. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang Z., Kumar S. Approximate methods for estimating the pattern of nucleotide substitution and the variation of substitution rates among sites. Mol Biol Evol. 1996 May;13(5):650–659. doi: 10.1093/oxfordjournals.molbev.a025625. [DOI] [PubMed] [Google Scholar]