Phylogeographic studies have described a reduced genetic diversity in Native American populations, indicative of one or more bottleneck events during the peopling and prehistory of the Americas. Classical sequencing approaches targeting the mitochondrial diversity have reported the presence of five major haplogroups, namely A, B, C, D and X, whereas the advent of complete mitochondrial genome sequencing has recently refined the number of founder lineages within the given diversity to 15 sub-haplogroups. We developed and optimized a SNaPshot assay to study the mitochondrial diversity in pre-Columbian Native American populations by simultaneous typing of 26 single nucleotide polymorphisms (SNPs) characterising Native American sub-haplogroups. Our assay proved to be highly sensitive with respect to starting concentrations of target DNA and could be applied successfully to a range of ancient human skeletal material from South America from various time periods. The AmericaPlex26 is a powerful assay with enhanced phylogenetic resolution that allows time- and cost-efficient mitochondrial DNA sub-typing from valuable ancient specimens. It can be applied in addition or alternative to standard sequencing of the D-loop region in forensics, ancestry testing, and population studies, or where full-resolution mitochondrial genome sequencing is not feasible.
References
[1]
Torroni A, Schurr TG, Yang CC, Szathmary EJ, Williams RC, et al. (1992) Native American mitochondrial DNA analysis indicates that the Amerind and the Nadene populations were founded by two independent migrations. Genetics 130: 153–162.
[2]
Wallace DC, Torroni A (1992) American Indian prehistory as written in the mitochondrial DNA: a review. Human Biology 64: 403–416. doi: 10.3378/027.081.0602
[3]
Forster P, Harding R, Torroni A, Bandelt HJ (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. American Journal of Human Genetics 59: 935–945.
[4]
Tamm E, Kivisild T, Reidla M, Metspalu M, Smith DG, et al. (2007) Beringian standstill and spread of Native American founders. PLoS ONE 2: e829. doi: 10.1371/journal.pone.0000829
[5]
Schurr TG (2000) Mitochondrial DNA and the Peopling of the New World: Genetic variations among Native Americans provide further clues to who first populated the Americas and when they arrived. American Scientist 88: 246–253.
[6]
Perego UA, Achilli A, Angerhofer N, Accetturo M, Pala M, et al. (2009) Distinctive Paleo-Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Current Biology 19: 1–8. doi: 10.1016/j.cub.2008.11.058
[7]
Wang S, Lewis CM, Jakobsson M, Ramachandran S, Ray N, et al. (2007) Genetic variation and population structure in native Americans. PLoS Genetics 3: e185. doi: 10.1371/journal.pgen.0030185
[8]
O'Rourke DH, Raff JA (2010) The human genetic history of the Americas: the final frontier. Current Biology 20: R202–207. doi: 10.1016/j.cub.2009.11.051
[9]
Kemp BM, Schurr TG (2010) Human Variation in the Americas: The Integration of Archaeology and Biological Anthropology; Auerbach BM, editor: Center for Archaeological Investigations, Southern Illinois University Carbondale.
[10]
Fehren-Schmitz L, Reindel M, Cagigao ET, Hummel S, Herrmann B (2010) Pre-Columbian population dynamics in coastal southern Peru: A diachronic investigation of mtDNA patterns in the Palpa region by ancient DNA analysis. American journal of physical anthropology 141: 208–221. doi: 10.1002/ajpa.21135
[11]
Kaestle FA, Horsburgh KA (2002) Ancient DNA in Anthropology: Methods, Applications and Ethics. Yearbook of Physical Anthropology 45: 92–130. doi: 10.1002/ajpa.10179
[12]
de Saint Pierre M, Bravi CM, Motti JMB, Fuku N, Tanaka M, et al. (2012) An Alternative Model for the Early Peopling of Southern South America Revealed by Analyses of Three Mitochondrial DNA Haplogroups. PLoS ONE 7: e43486. doi: 10.1371/journal.pone.0043486
[13]
álvarez-Iglesias V, Jaime JC, Carracedo á, Salas A (2007) Coding region mitochondrial DNA SNPs: Targeting East Asian and Native American haplogroups. Forensic Science International: Genetics 1: 44–55. doi: 10.1016/j.fsigen.2006.09.001
[14]
Bandelt HJ, Herrnstadt C, Yao YG, Kong QP, Kivisild T, et al. (2003) Identification of Native American founder mtDNAs through the analysis of complete mtDNA sequences: some caveats. Annals of Human Genetics 67: 512–524. doi: 10.1046/j.1469-1809.2003.00049.x
[15]
Quintáns B, álvarez-Iglesias V, Salas A, Phillips C, Lareu MV, et al. (2005) Typing of mitochondrial DNA coding region SNPs of forensic and anthropological interest using SNaPshot minisequencing. Forensic science international 140: 251–257. doi: 10.1016/j.forsciint.2003.12.005
[16]
Bouakaze C, Keyser C, Amory S, Crubézy E, Ludes B (2007) First successful assay of Y-SNP typing by SNaPshot minisequencing on ancient DNA. International Journal of Legal Medicine 121: 493–499. doi: 10.1007/s00414-007-0177-3
[17]
Ballantyne KN, van Oven M, Ralf A, Stoneking M, Mitchell RJ, et al. (2012) MtDNA SNP multiplexes for efficient inference of matrilineal genetic ancestry within Oceania. Forensic Science International: Genetics 6: 425–436. doi: 10.1016/j.fsigen.2011.08.010
[18]
Argac D, Bulbul O, Shahzad MS, Acar E, Altuncul H, et al. (2009) Optimization and validation of 10 mitochondrial DNA SNPs using SNaPshot Kit. Forensic Science International: Genetics Supplement Series 2: 99–101. doi: 10.1016/j.fsigss.2009.08.194
[19]
Paneto GG, K？hnemann S, Martins JA, Cicarelli RMB, Pfeiffer H (2011) A single multiplex SNaPshot reaction of 42 SNPs to classify admixture populations into mitochondrial DNA haplogroups. Forensic Science International: Genetics Supplement Series 3: e198–e199. doi: 10.1016/j.fsigss.2011.08.099
[20]
Geppert M, Roewer L (2012) SNaPshot(R) minisequencing analysis of multiple ancestry-informative Y-SNPs using capillary electrophoresis. Methods in Molecular Biology 830: 127–140. doi: 10.1007/978-1-61779-461-2_9
[21]
Grignani P, Peloso G, Alù M, Ricci U, Robino C, et al. (2006) Subtyping mtDNA haplogroup H by SNaPshot minisequencing. International Congress Series 1288: 124–126. doi: 10.1016/j.ics.2005.12.029
[22]
Perego UA, Angerhofer N, Pala M, Olivieri A, Lancioni H, et al. (2010) The initial peopling of the Americas: A growing number of founding mitochondrial genomes from Beringia. Genome Research 20: 1174–1179. doi: 10.1101/gr.109231.110
[23]
van Oven M, Vermeulen M, Kayser M (2011) Multiplex genotyping system for efficient inference of matrilineal genetic ancestry with continental resolution. Investigative genetics 2: 6. doi: 10.1186/2041-2223-2-6
[24]
Haak W, Balanovsky O, Sanchez JJ, Koshel S, Zaporozhchenko V, et al. (2010) Ancient DNA from European early Neolithic farmers reveals their near eastern affinities. PLoS Biology 8: e1000536. doi: 10.1371/journal.pbio.1000536
[25]
Maricic T, Whitten M, P？？bo S (2010) Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS ONE 5: e14004. doi: 10.1371/journal.pone.0014004
[26]
Brotherton P, Haak W, Templeton J, Brandt G, Soubrier J, et al. (2013) Neolithic mitochondrial haplogroup H genomes and the genetic origins of Europeans. Nature communications 4: 1764. doi: 10.1038/ncomms2656
[27]
Knapp M, Horsburgh KA, Prost S, Stanton JA, Buckley HR, et al. (2012) Complete mitochondrial DNA genome sequences from the first New Zealanders. Proceedings of the National Academy of Sciences USA 109: 18350–18354. doi: 10.1073/pnas.1209896109
[28]
Tamm E, Kivisild T, Reidla M, Metspalu M, Smith DG, et al. (2007) Beringian standstill and spread of Native American founders. PLoS ONE 2: e829. doi: 10.1371/journal.pone.0000829
[29]
Achilli A, Perego UA, Bravi CM, Coble MD, Kong Q-P, et al. (2008) The Phylogeny of the Four Pan-American MtDNA Haplogroups: Implications for Evolutionary and Disease Studies. PLoS ONE 3: e1764. doi: 10.1371/journal.pone.0001764
[30]
Achilli A, Perego UA, Lancioni H, Olivieri A, Gandini F, et al. (2013) Reconciling migration models to the Americas with the variation of North American native mitogenomes. Proceedings of the National Academy of Sciences USA 110: 14308–14313. doi: 10.1073/pnas.1306290110
[31]
Gilbert MT, Kivisild T, Gronnow B, Andersen PK, Metspalu E, et al. (2008) Paleo-Eskimo mtDNA genome reveals matrilineal discontinuity in Greenland. Science 320: 1787–1789. doi: 10.1126/science.1159750
[32]
Kumar S, Bellis C, Zlojutro M, Melton PE, Blangero J, et al. (2011) Large scale mitochondrial sequencing in Mexican Americans suggests a reappraisal of Native American origins. BMC Evolutionary Biology 11: 293. doi: 10.1186/1471-2148-11-293
[33]
Malhi RS, Cybulski JS, Tito RY, Johnson J, Harry H, et al. (2010) Brief communication: Mitochondrial haplotype C4c confirmed as a founding genome in the Americas. American Journal of Physical Anthropology 141: 494–497. doi: 10.1002/ajpa.21238
[34]
Kashani BH, Perego UA, Olivieri A, Angerhofer N, Gandini F, et al. (2012) Mitochondrial haplogroup C4c: A rare lineage entering America through the ice-free corridor? American Journal of Physical Anthropology 147: 35–39. doi: 10.1002/ajpa.21614
[35]
Bodner M, Perego UA, Huber G, Fendt L, R？ck AW, et al. (2012) Rapid coastal spread of First Americans: Novel insights from South America's Southern Cone mitochondrial genomes. Genome research 22: 811–820. doi: 10.1101/gr.131722.111
[36]
Derbeneva OA, Sukernik RI, Volodko NV, Hosseini SH, Lott MT, et al. (2002) Analysis of mitochondrial DNA diversity in the aleuts of the commander islands and its implications for the genetic history of beringia. American Journal of Human Genetics 71: 415–421. doi: 10.1086/341720
[37]
Starikovskaya YB, Sukernik RI, Schurr TG, Kogelnik AM, Wallace DC (1998) mtDNA diversity in Chukchi and Siberian Eskimos: implications for the genetic history of Ancient Beringia and the peopling of the New World. American Journal of Human Genetics 63: 1473–1491. doi: 10.1086/302087
[38]
You FM, Huo N, Gu YQ, Luo M, Ma Y, et al. (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC bioinformatics 9: 253. doi: 10.1186/1471-2105-9-253
[39]
Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. Bioinformatics methods and protocols: Springer. pp. 365–386.
[40]
Sanchez JJ, Endicott P (2006) Developing multiplexed SNP assays with special reference to degraded DNA templates. Nature Protocols 1: 1370–1378. doi: 10.1038/nprot.2006.247
[41]
Vallone PM, Just RS, Coble MD, Butler JM, Parsons TJ (2004) A multiplex allele-specific primer extension assay for forensically informative SNPs distributed throughout the mitochondrial genome. International Journal of Legal Medicine 118: 147–157. doi: 10.1007/s00414-004-0428-5
[42]
Haak W, Forster P, Bramanti B, Matsumura S, Brandt G, et al. (2005) Ancient DNA from the first European farmers in 7500-year-old Neolithic sites. Science 310: 1016–1018. doi: 10.1126/science.1123936
[43]
Der Sarkissian C, Balanovsky O, Brandt G, Khartanovich V, Buzhilova A, et al. (2013) Ancient DNA Reveals Prehistoric Gene-Flow From Siberia in the Complex Human Population History of North East Europe. PLoS Genetics 9: e1003296. doi: 10.1371/journal.pgen.1003296
[44]
Haak W, Brandt G, de Jong HN, Meyer C, Ganslmeier R, et al. (2008) Ancient DNA, Strontium isotopes, and osteological analyses shed light on social and kinship organization of the Later Stone Age. Proceedings of the National Academy of Sciences USA 105: 18226–18231. doi: 10.1073/pnas.0807592105
[45]
Adler CJ, Haak W, Donlon D, Cooper A (2011) Survival and recovery of DNA from ancient teeth and bones. Journal of Archaeological Science 38: 956–964. doi: 10.1016/j.jas.2010.11.010
[46]
Sanchez JJ, Phillips C, B？rsting C, Balogh K, Bogus M, et al. (2006) A multiplex assay with 52 single nucleotide polymorphisms for human identification. Electrophoresis 27: 1713–1724. doi: 10.1002/elps.200500671
[47]
Lanning EP, Pollard G (1967) Peru before the Incas: Prentice-Hall Englewood Cliffs, NJ.
[48]
Butler JM (2011) Advanced Topics in Forensic DNA Typing: Methodology: Academic Press.
[49]
Butler JM (2009) Fundamentals of forensic DNA typing: Academic Press.
[50]
Sobrino B, Carracedo A (2005) SNP Typing in Forensic Genetics; Carracedo á, editor. Totowa, NJ: Humana Press.
[51]
Dario P, Bom J, Ribeiro T, Geada H (2009) MtSNP typing before mtDNA sequencing: Why do it? Forensic Science International: Genetics Supplement Series 2: 187–188. doi: 10.1016/j.fsigss.2009.08.137
[52]
Behar DM, van Oven M, Rosset S, Metspalu M, Loogvali EL, et al. (2012) A “Copernican” Reassessment of the Human Mitochondrial DNA Tree from its Root. American Journal of Human Genetics 90: 675–684. doi: 10.1016/j.ajhg.2012.03.002
[53]
Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, et al. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nature Genetics 23: 147. doi: 10.1038/13779
[54]
Handt O, Krings M, Ward RH, Paabo S (1996) The retrieval of ancient human DNA sequences. American Journal of Human Genetics 59: 368–376.
[55]
Stone AC, Stoneking M (1998) mtDNA analysis of a prehistoric Oneota population: implications for the peopling of the New World 20. American Journal of Human Genetics 62: 1153–1170. doi: 10.1086/301838
