Aspects of Ancient Mitochondrial DNA Analysis in Different Populations for Understanding Human Evolution

Open access


The evolution of modern humans is a long and difficult process which started from their first appearance and continues to the present day. The study of the genetic origin of populations can help to determine population kinship and to better understand the gradual changes of the gene pool in space and time. Mitochondrial DNA (mtDNA) is a proper tool for the determination of the origin of populations due to its high evolutionary importance. Ancient mitochondrial DNA retrieved from museum specimens, archaeological finds and fossil remains can provide direct evidence for population origins and migration processes. Despite the problems with contaminations and authenticity of ancient mitochondrial DNA, there is a developed set of criteria and platforms for obtaining authentic ancient DNA. During the last two decades, the application of different methods and techniques for analysis of ancient mitochondrial DNA gave promising results. Still, the literature is relatively poor with information for the origin of human populations. Using comprehensive phylogeographic and population analyses we can observe the development and formation of the contemporary populations. The aim of this study was to shed light on human migratory processes and the formation of populations based on available ancient mtDNA data.

1. Shriver MD, Kittles RA. Genetic ancestry and the search for personalized genetic histories. Nat Rev Genet. 2004; 5(8): 611-618.

2. Suissa S, Wang Z, Poole J, Wittkopp S, Feder, Shutt TE, et al. Ancient mtDNA genetic variants modulate mtDNA transcription and replication. PLoS Genet. 2009; 5(5): e1000474.

3. Moreno-Loshuertos R, Acin-Perez R, Fernandez- Silva P, Movilla N, Perez-Martoz A, Rodriguez de Cordoba S, et al. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat Genet. 2006; 38(11): 1261-1268.

4. Kazuno AA, Manukata K, Nagai T, Shimozono S, Tanaka M, Yoneda M, et al. Identification of mitochondrial DNA polymorphisms that alter mitochondrial matrix pH and intracellular calcium dynamics. PLoS Genet. 2006; 2(8): e128.

5. Anderson S, Bankier AT, Barrell BG, de Bruin MH, Coulson AR, Drouin J, et al. Sequence and organization of the human mitochondrial genome. Nature. 1981; 290(5806): 457-465.

6. Pakendorf B, Stoneking M. Mitochondrial DNA and human evolution. Annu Rev Genomics Hum Genet. 2005; 6: 165-183.

7. 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 USA. 1995; 92(2): 532-536.

8. Tully LA, Parsons TJ, Steighner RJ, Holland MM, Marino MA, Prenger VL. A sensitive denaturing gradient-gel electrophoresis assay reveals a high frequency of het-eroplasmy in hypervariable region 1 of the human mtDNA control region. Am J Hum Genet. 2000; 67(2): 432-443.

9. Vigilant L, Stone king M, Harpending H, Hawkes K, Wilson AC. African populations and the evolution of human mitochondrial DNA. Science. 1991; 253(5027): 1503-1507.

10. Forster P, Matsumura S. Evolution. Did early humans go north or south? Science. 2005; 308(5724): 965-966.

11. Salas A, Richards M, de la Fe T, Lares MV, Sobrino B, Sanchez-Diz P, et al. The making of the African mtDNA landscape. Am J Hum Genet. 2002; 71(5): 1082-1111.

12. Comas D, Calafell F, Mateu E, Perez-Sezaun A, Bosch E, Bertranpetit J. Mitochondrial DNA variation and the origin of the Europeans. Hum Genet. 1997; 99(4): 443-449.

13. Calafell F, Underhill P, Tolu A, Angelicheva D, Kalaydjieva L. From Asia to Europe: Mitochondrial DNA sequence variability in Bulgarians and Turks. Ann Hum Genet. 1996; 60(Pt 1): 35-49.

14. Andrews RM, Kubacka I, Chinnery PF, Lightow- lers RN, Turnbull, Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet. 1999; 23(2): 147.

15. Yonggang Y, Yaping Z. Pitfalls in the analysis of ancient human mtDNA. Chinese Sci Bull. 2003; 48(8): 826-830.

16. Yao YG, Zhang YP. Mitochondrial DNA and human evolution (in Chinese). Zool Res. 2000; 21(4): 392-406.

17. Higuchi R, Bowman B, Freiberger M, Ryder OA, Wilson AC. DNA sequences from the quagga, an extinct member of the horse family. Nature. 1984; 312(5991): 282-284.

18. Paabo S. Molecular cloning of ancient Egyptian mummy DNA. Nature. 1985; 314(6012): 644-645.

19. Krings M, Stone A, Schlitz RW, Krainitzki H, Stone king M, Paabo S. Neanderthal DNA sequences and the origin of modern humans. Cell. 1997; 90(1): 19-30.

20. Adachi N, Umetsu K, Takigawa W, Sakauea K. Phylogenetic analysis of the human ancient mitochondrial DNA. J Archaeol Sci. 2004; 31(10): 1339-1348.

21. Forster P. Ice Ages and the mitochondrial DNA chronology of human dispersals: A review. Philos Trans R Soc Lond B Biol Sci. 2004; 359(1442): 255-264 (discussion: 264).

22. Cooper A, Poinar HN. Ancient DNA: Do it right or not at all. Science. 2000; 289(5482): 1139.

23. Kolman CJ, Tuross N. Ancient DNA analysis of human populations. Am J Phys Anthropol. 2000; 111(1): 5-23.

24. Bandelt HJ. Mosaics of ancient mitochondrial DNA: positive indicators of nonauthenticity. Eur J Hum Genet. 2005; 13(10): 1106-1112.

25. Garcia-Garcera M, Gigli E, Sanchez-Quinto F, Ramirez O, Calafell F, Civit S, et al. Fragmentation of contaminant and endogenous DNA in ancient samples determined by shotgun sequencing; prospects for human palaeogenomics. PLoS One. 2011; 6(8): e24161.

26. Wall JD, Kim SK. Inconsistencies in Neanderthal genomic DNA sequences. PLoS Genet. 2007; 3(10): 1862-1866.

27. Pilli E, Modi A, Serpico C Chilli A, Lancioni H, Lippi B, et al. Monitoring DNA contamination in handled vs. directly excavated ancient human skeletal remains. PLoS One. 2013; 8(1): e52524.

28. Richards M, Smalley K, Sykes B, Hedges R. Archaeology and genetics: Analyzing DNA from skeletal remains. World Archaeol. 1993; 25(1): 18-28.

29. Caramelli D, Milani L, Vai S, Modi A, Pecchioli E, Girard M, et al. A 28,000 years old Cro-Magnon mtDNA sequence differs from all potentially contaminating modern sequences. PLoS One. 2008; 3(7): e2700.

30. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA. 1977; 74(12): 5463-5467.

31. Knapp M, Hofreiter M. Next generation sequencing of ancient DNA: Requirements, strategies and perspectives. Genes (Basel). 2010; 1(2): 227-243.

32. Wolpoff MH, Caspari R. Race and Human Evolution: A Fatal Attraction. New York, NY: Westview Press, Simon & Schuster. 1997: 11-18.

33. Caramelli D, Laluela-Fox C, Vernesi C, Lari M, Caroli A, Mallegni F, et al. Evidence for a genetic discontinuity between Neanderthals and 24,000-year-old anatomically modern Europeans. Proc Natl Acad Sci USA. 2003; 100(11): 6593-6597.

34. Lalueza-Fox C, Sampietro ML, Caramelli D, Puder Y, Lari M, Calafell F, et al. Neanderthal evolutionary genetics: mitochondrial DNA data from the Iberian Peninsula. Mol Biol Evol. 2005; 22(4): 1077-1081

35. Condemi S, Mounier A, Giunti P, Lari M, Caramelli D, Longo L. Possible interbreeding in late Italian Neanderthals? New data from the Mezzena jaw (Monti Lessini, Verona, Italy). PLoS One. 2013; 8(3): e59781.

36. Smith FH, Falsetto AB, Donnelly SM. Modern human origins. Yearbook Phys Anthropol. 1989; 32: 35-68.

37. Frayer D. Evolution at the European edge: Neanderthal and Upper Paleolithic relationships. Préhistoire Européenne. 1992; 2: 9-69.

38. Eriksson A, Manica A. Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Proc Natl Acad Sci USA. 2012; 109(35): 13956-13960.

39. Bertranpetit J, Sala J, Calafell F, Underhill PA, Moral P, Comas D. Human mitochondrial DNA variation and the origin of Basques. Ann Hum Genet. 1995; 59(Pt 1): 63-81.

40. Cavalli-Sforza LL, Menozzi P, Piazza A. Demic expansions and human evolution. Science. 1993; 259(5095): 639-646.

41. Bramanti B, Thomas MG, Haak W, Unterlaender M, Jores P, Tambets K, et al. Genetic discontinuity between local hunter-gatherers and central Europe’s first farmers. Science. 2009; 326(5949): 137-140.

42. Balter M. Archaeology. Ancient DNA says Europe’s first farmers came from afar. Science. 2009; 325(5945): 1189.

43. Sampietro ML, Lao O, Caramelli D, Lari M, Pou R, Marti M, et al. Palaeogenetic evidence supports a dual model of Neolithic spreading into Europe. Proc Biol Sci. 2007; 274(1622): 2161-2167.

44. Fu Q, Rudan P, Paabo S, Krause J. Complete mitochondrial genomes reveal neolithic expansion into Europe. PLoS One. 2012; 7(3): e32473.

45. Richards M. The neolithic invasion of Europe. Annu Rev Anthropol. 2003; 32: 135-162.

46. Haak W, Balanovsky O, Sanchez JJ, Kosher S, Zaporoshchenko V, Adler CJ, et al. Ancient DNA from European early neolithic farmers reveals their near eastern affinities. PLoS Biol. 2010; 8(11): e1000536.

47. Hervella M, Izagirre N, Alonso S, Fregel R, Alonso A, Cabrera VM, et al. Ancient DNA from hunter-gatherer and farmer groups from Northern Spain supports a random dispersion model for the Neolithic expansion into Europe. PLoS One. 2012; 7(4): e34417.

48. Melchior L, Lynnerup N, Siegismund HR, Kivisild T, Dissing J. Genetic diversity among ancient Nordic populations. PLoS One, 2010. 5(7): p. e11898.

49. Helgason A, Hrafnkelsson B, Gulcher JR, Ward R, Stefansson K. A populationwide coalescent analysis of Icelandic matrilineal and patrilineal genealogies: Evidence for a faster evolutionary rate of mtDNA lineages than Y chromosomes. Am J Hum Genet. 2003; 72(6): 1370-1388.

50. Helgason A, Lalueza-Fox C, Ghosh S, Sigurethar- dottir S, Sampietro ML, Gigli E, et al. Sequences from first settlers reveal rapid evolution in Icelandic mtDNA pool. PLoS Genet. 2009; 5(1): e1000343.

51. Rando JC, Cabrera VM, Larruga JM, Hernandez M, Gonzalez AM, Pinto F, et al. Phylogeographic patterns of mtDNA reflecting the colonization of the Canary Islands. Ann Hum Genet. 1999; 63(Pt 5): 413-428.

52. Maca-Meyer N, Array M, Rando JC, Flores C, Gonzalez AM, Cabrera VM, et al. Ancient mtDNA analysis and the origin of the Guanches. Eur J Hum Genet. 2004; 12(2): 155-162.

53. Kaestle FA, Smith DG. Ancient mitochondrial DNA evidence for prehistoric population movement: The Numic expansion. Am J Phys Anthropol. 2001; 115(1): 1-12.

54. Jin L, Seielstad M, Xiao C. Genetic, linguistic and archaeological perspectives on human diversity in Southeast Asia. In: Oxnard CE, Ed. Recent Advances in Human Biology. New Jersey, NJ: World Scientific. 2001: 17-34.

55. Lertrit P, Poolsuwan S, Thosarat R, Sanpachudayan T, Boonyarit H, Chinpaisal C, et al. Genetic history of Southeast Asian populations as revealed by ancient and modern human mitochondrial DNA analysis. Am J Phys Anthropol. 2008; 137(4): 425-440.

56. Xu Z, Zhang F, Xu B, Tan J, Li S, Li C, et al. Mitochondrial DNA evidence for a diversified origin of workers building First Emperor of China. PLoS One. 2008; 3(10): e3275.

57. Tomory G, Csany B, Bogacsi-Szabo E, Kalmar T, Czibula A, Csosz A, et al. Comparison of maternal lineage and biogeographic analyses of ancient and modern Hungarian populations. Am J Phys Anthropol. 2007; 134(3): 354-368.

58. Adcock GJ, Dennis ES, Osteal S, Huntley GA, Germain LS, Peacock WJ, et al. Mitochondrial DNA sequences in ancient Australians: implications for modern human origins. Proc Natl Acad Sci USA. 2001; 98(2): 537-542.

59. Crubézy E, Amory S, Geyser C, Bouakaze C, Bodner M, Gilbert M, et al. Human evolution in Siberia: from frozen bodies to ancient DNA. BMC Evol Biol. 2010; 10: 25.

60. Ricaut FX, Geyser-Tracqui C, Bland in P, Crubézy E, Ludes B. Mitochondrial DNA analysis of ancient Yakut skeletons. International Congress Series 1261. 2004: 392-394.

61. Topf AL, Gilbert MT, Fleischer RC, Hoelzel AR. Ancient human mtDNA genotypes from England reveal lost variation over the last millennium. Biol Lett. 2007; 3(5): 550-553.

62. Shinoda K, Adachi N, Guillen S, Shimada I. Mitochondrial DNA analysis of ancient Peruvian highlanders. Am J Phys Anthropol. 2006; 131(1): 98-107.

63. Karachanak S, Carissa V, Nesheva D, Olivieri A, Pala M, Hooshiar Kashani B, et al. Bulgarians vs the other European populations: a mitochondrial DNA perspective. Int J Legal Med. 2012; 126(4): 497-503.

Balkan Journal of Medical Genetics

The Journal of Macedonian Academy of Sciences and Arts

Journal Information

IMPACT FACTOR 2017: 0.306
5-year IMPACT FACTOR: 0.527

CiteScore 2017: 0.51

SCImago Journal Rank (SJR) 2017: 0.199
Source Normalized Impact per Paper (SNIP) 2017: 0.170


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 268 268 26
PDF Downloads 105 105 13