Understanding differences between phylogenetic and pedigree-derived mtDNA mutation rate: A model using families from the Azores Islands (Portugal)

Molecular Biology and Evolution

Volumn 22, Issue 6, 2005, Pages 1490-1505

  Santos, Cristina ^a,b   Montiel, Rafael ^c   Sierra, Blanca ^a   Bettencourt, Conceição ^c   Fernandez, Elisabet ^a   Alvarez, Luis ^a   Lima, Manuela ^c   Abade, Augusto ^b   Aluja, M Pilar ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF THE AZORES   (Portugal)

Author keywords

Azores (Portugal); Heteroplasmy; mtDNA mutation rate; Paternal mtDNA; Recombination

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; DNA RECOMBINATION; FAMILY; FEMALE; GENDER; GENE SEGREGATION; GENETIC DRIFT; HETEROPLASMY; HUMAN; MALE; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MUTATION RATE; NUCLEOTIDE SEQUENCE; PEDIGREE; PORTUGAL; PROBABILITY; SOMATIC MUTATION; TIME;

AZORES; CLONING, MOLECULAR; DNA MUTATIONAL ANALYSIS; DNA, MITOCHONDRIAL; EVOLUTION; EVOLUTION, MOLECULAR; FEMALE; GENETIC DRIFT; HUMANS; MALE; MODELS, GENETIC; MODELS, STATISTICAL; MUTATION; PEDIGREE; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 19544384572     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi141     Document Type: Article

References (81)

1. Anderson, S., A. Bankier, M. Barrell et al. (14 co-authors). 1981. Sequence and organization of the human mitochondrial genome. Nature 290:457-464.
2. Baasner A., and B. Madea. 2000. Sequence polymorphisms of the mitochondrial DNA control region in 100 German Caucasians. J. Forensic. Sci. 45:1343-1348.
3. Baasner, A., C. Schafer, A. Junge, and B. Madea. 1998. Polymorphic sites in human mitochondrial DNA control region sequences: population data and maternal inheritance. Forensic Sci. Int. 98:169-178.
4. Bandelt, H. J., P. Forster, B. C. Sykes, and M. B. Richards. 1995. Mitochondrial portraits of human populations using median networks. Genetics 141:743-753.
5. Bendall, K. E., V. A. Macaulay, J. R. Baker, and B. C. Sykes. 1996. Heteroplasmic point mutations in the human mtDNA control region. Am. J. Hum. Genet. 59:1276-1287.
6. Bendall, K. E., and B. C. Sykes. 1995. Length heteroplasmy in the first hypervariable segment of the human mtDNA control region. Am. J. Hum. Genet. 57:248-256.
7. Brandstätter, A., H. Niederstatter, and W. Parson. 2004. Monitoring the inheritance of heteroplasmy by computer-assisted detection of mixed basecalls in the entire human mitochondrial DNA control region. Int. J. Legal Med. 118:47-54.
8. Brehm, A., L. Pereira, T. Kivisild, and A. Amorim. 2003. Mitochondrial portraits of the Madeira and Acores archipelagos witness different genetic pools of its settlers. Hum. Genet. 114:77-86.
9. Brown, M. D., S. H. Hosseini, A. Torroni, H. J. Bandelt, J. C. Allen, T. G. Schurr, R. Scozzari, F. Cruciani, and D. C. Wallace. 1998. mtDNA haplogroup X: an ancient link between Europe/Western Asia and North America? Am. J. Hum. Genet. 63:1852-1861.
10. Calafell, F., P. Underhill, A. Tolun, D. Angelicheva, and L. Kalaydjieva. 1996. From Asia to Europe: mitochondrial DNA sequence variability in Bulgarians and Turks. Ann. Hum. Genet. 60(Pt 1):35-49.
11. Cann, R., M. Stoneking, and A. Wilson. 1987. Mitochondrial DNA and human evolution. Nature 325:31-36.
12. Cavalli-Sforza, L. L., and W. F. Bodmer. 1971. The genetics of human populations. W. H. Freeman and Company, San Francisco, Calif.
13. Chen, Y. S., A. Torroni, L. Excoffier, A. S. Santachiara-Benerecetti, and D. C. Wallace. 1995. Analysis of mtDNA variation in African populations reveals the most ancient of all human continent-specific haplogroups. Am. J. Hum. Genet. 57:133-149.
14. Delghandi, M., E. Utsi, and S. Krauss. 1998. Saami mitochondrial DNA reveals deep maternal lineage clusters. Hum. Hered. 48:108-114.
15. Denver, D. R., K. Morris, M. Lynch, L. L. Vassilieva, and W. K. Thomas. 2000. High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science 289:2342-2344.
16. Elson, J. L., D. M. Turnbull, and N. Howell. 2004. Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am. J. Hum. Genet. 74: 229-238.
17. Fisher, R. A. 1930. The genetical theory of natural selection. Clarendon, Oxford.
18. Forster, P., R. Harding, A. Torroni, and H. J. Bandelt. 1996. Origin and evolution of Native American mtDNA variation: a reappraisal. Am. J. Hum. Genet. 59:935-945.
19. Francalacci, P., J. Bertranpetit, F. Calafell, and P. A. Underhill. 1996. Sequence diversity of the control region of mitochondrial DNA in Tuscany and its implications for the peopling of Europe. Am. J. Phys. Anthropol. 100:443-460.
20. Graven, L., G. Passarino, O. Semino, P. Boursot, S. Santachiara- Benerecetti, A. Langaney, and L. Excoffier. 1995. Evolutionary correlation between control region sequence and restriction polymorphisms in the mitochondrial genome of a large Senegalese Mandenka sample. Mol. Biol. Evol. 12:334-345.
21. Grzybowski, T., B. A. Malyarchuk, J. Czarny, D. Miscicka-Sliwka, and R. Kotzbach. 2003. High levels of mitochondrial DNA heteroplasmy in single hair roots: reanalysis and revision. Electrophoresis 24:1159-1165.
22. Hagelberg, E. 2003. Recombination or mutation rate heterogeneity? Implications for mitochondrial Eve. Trends Genet. 19:84-90.
23. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41:95-98.
24. Handt, O., S. Meyer, and A. Haeseler. 1998. Compilation of human mtDNA control region sequences. Nucleic Acids Res. 26:126-129.
25. Hartl, D., and A. Clark. 1997. Principles of population genetics. 3rd edition. Sinauer Associates, Inc., Publishers, Sunderland, Mass.
26. Hasegawa, M., and S. Horai. 1991. Time of the deepest root for polymorphism in human mitochondrial DNA. J. Mol. Evol. 32:37-42.
27. Hauswirth, W. W., and D. A. Clayton. 1985. Length heterogeneity of a conserved displacement loop sequence in human mitochondrial DNA. Nucleic Acids Res. 13:8093-8104.
28. Helgason, A., S. Siguroardóttir, J. Gulcher, R. Ward, and K. Stefánsson. 2000. mtDNA and the origin of the Icelanders: deciphering signals of recent population history. Am. J. Hum. Genet. 66:999-1016.
29. Heyer, E., E. Zietkiewicz, A. Rochowski, V. Yotova, J. Puymirat, and D. Labuda. 2001. Phylogenetic and familial estimates of mitochondrial substitution rates: study of control region mutations in deep-rooting pedigrees. Am. J. Hum. Genet. 69: 1113-1126.
30. Hofmann, S., M. Jaksch, R. Bezold, S. Mertens, S. Aholt, A. Paprotta, and K. D. Gerbitz. 1997. Population genetics and disease susceptibility: characterization of central European haplogroups by mtDNA gene mutations, correlation with D loop variants and association with disease. Hum. Mol. Genet. 6:1835-1846.
31. Horai, S., K. Hayasaka, R. Kondo, K. Tsugane, and N. Takahata. 1995. Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc. Natl. Acad. Sci. USA 92:532-536.
32. Howell, N., J. L. Elson, D. M. Turnbull, and C. Herrnstadt. 2004. African haplogroup L mtDNA sequences show violations of clock-like evolution. Mol. Biol. Evol. 21:1843-1854.
33. Howell, N., S. Halvorson, I. Kubacka, D. A. McCullough, L. A. Bindoff, and D. M. Turnbull. 1992. Mitochondrial gene segregation in mammals: is the bottleneck always narrow? Hum. Genet. 90:117-120.
34. Howell, N., I. Kubacka, and D. A. Mackey. 1996. How rapidly does the human mitochondrial genome evolve? Am. J. Hum. Genet. 59:501-509.
35. Howell, N., C. B. Smejkal, D. A. Mackey, P. F. Chinnery, D. M. Turnbull, and C. Herrnstadt. 2003. The pedigree rate of sequence divergence in the human mitochondrial genome: there is a difference between phylogenetic and pedigree rates. Am. J. Hum. Genet. 72:659-670.
36. INE (Institute Nacional de Estatística). 2003. Anuário Estatístico de Portugal. Instituto Nacional de Estatística, Lisboa Portugal.
37. Ingman, M., H. Kaessmann, S. Pääbo, and U. Gyllensten. 2000. Mitochondrial genome variation and the origin of modern humans. Nature 408:708-713.
38. Jenuth, J. P., A. C. Peterson, K. Fu, and E. A. Shoubridge. 1996. Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat. Genet. 14:146-151.
39. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge.
40. Kraytsberg, Y., M. Schwartz, T. A. Brown, K. Ebralidse, W. S. Kunz, D. A. Clayton, J. Vissing, and K. Khrapko. 2004. Recombination of human mitochondrial DNA. Science 304:981.
41. Lambert, D. M., P. A. Ritchie, C. D. Millar, B. Holland, A. J. Drummond, and C. Baroni. 2002. Rates of evolution in ancient DNA from Adélie penguins. Science 295:2270-2273.
42. Lee, H. Y., U. Chung, J. E. Yoo, M. J. Park, and K. J. Shin. 2004. Quantitative and qualitative profiling of mitochondrial DNA length heteroplasmy. Electrophoresis 25:28-34.
43. Lima, M. M. 1996. Doença de Machado-Joseph nos Açores: Estudo epidemiológico, biodemográfico e genético. PhD thesis, University of the Azores, Ponta Delgada, Azores, Portugal.
44. Lundstrom, R., S. Tavare, and R. H. Ward. 1992. Estimating substitution rates from molecular data using the coalescent. Proc. Natl. Acad. Sci. USA 89:5961-5965.
45. Lutz, S., H. J. Weisser, J. Heizmann, and S. Pollak. 1998. Location and frequency of polymorphic positions in the mtDNA control region of individuals from Germany. Int. J. Legal. Med. 111:67-77.
46. -. 2000. Mitochondrial heteroplasmy among maternally related individuals. Int. J. Legal. Med. 113:155-161.
47. Macaulay, V. A., M. B. Richards, P. Forster, K. E. Bendall, E. Watson, B. Sykes, and H. J. Bandelt. 1997. mtDNA mutation rates-no need to panic. Am. J. Hum. Genet. 61:983-990.
48. Marchington, D. R., V. Macaulay, G. M. Hartshorne, D. Barlow, and J. Poulton. 1998. Evidence from human oocytes for a genetic bottleneck in an mtDNA disease. Am. J. Hum. Genet. 63:769-775.
49. Meyer, S., and A. von Haeseler. 2003. Identifying site-specific substitution rates. Mol. Biol. Evol. 20:182-189.
50. Meyer, S., G. Weiss, and A. von Haeseler. 1999. Pattern of nucleotide substitution and rate heterogeneity in the hypervariable regions I and II of human mtDNA. Genetics 152:1103-1110.
51. Miller, W. G. 2003. OpenStat2 (OS2). Version 1.4.4. West DeMoines, Iowa.
52. Mishmar, D., E. Ruiz-Pesini, P. Golik et al. (13 co-authors). 2003. Natural selection shaped regional mtDNA variation in humans. Proc. Natl. Acad. Sci. USA 100:171-176.
53. Montiel, R. 2001. Estudio diacrónico de la variabilidad del DNA mitocondrial en población Catalana. Ph.D. dissertation. Autonomous University of Barcelona, Barcelona, Spain. (http://www.tdcat.cesca.es/TDCat- 0726101-095837).
54. Montiel, R., A. Malgosa, and P. Francalacci. 2001. Authenticating ancient human mitochondrial DNA. Hum Biol 73:689-713.
55. Pääbo, S. 1996. Mutational hot spots in the mitochondrial microcosm. Am. J. Hum. Genet. 59:493-496.
56. Parson, W., T. J. Parsons, R. Scheithauer, and M. M. Holland. 1998. Population data for 101 Austrian Caucasian mitochondrial DNA d-loop sequences: application of mtDNA sequence analysis to a forensic case. Int. J. Legal. Med. 111:124-132.
57. Parsons, T. J., D. S. Muniec, K. Sullivan et al. (11 co-authors). 1997. A high observed substitution rate in the human mitochondrial DNA control region. Nat. Genet. 15:363-368.
58. Pereira, L., M. J. Prata, and A. Amorim. 2000. Diversity of mtDNA lineages in Portugal: not a genetic edge of European variation. Ann. Hum. Genet. 64:491-506.
59. Pesole, G., E. Sbisa, G. Preparata, and C. Saccone. 1992. The evolution of the mitochondrial D-loop region and the origin of modern man. Mol. Biol. Evol. 9:587-598.
60. Piercy, R., K. M. Sullivan, N. Benson, and P. Gill. 1993. The application of mitochondrial DNA typing to the study of white Caucasian genetic identification. Int. J. Legal. Med. 106:85-90.
61. Poulton, J., V. Macaulay, and D. R. Marchington. 1998. Mitochondrial genetics '98 is the bottleneck cracked? Am. J. Hum. Genet. 62:752-757.
62. Poulton, J., and D. R. Marchington. 2002. Segregation of mitochondrial DNA (mtDNA) in human oocytes and in animal models of mtDNA disease: clinical implications. Reproduction 123:751-755.
63. Rand, D. M. 2001. The units of selection on mitochondrial DNA. Ann. Rev. Ecol. Syst. 32:415-448.
64. Rannala, B., and G. Bertorelle. 2001. Using linked markers to infer the age of a mutation. Hum. Mutat. 18:87-100.
65. Richards, M., H. Corte-Real, P. Forster, V. Macaulay, H. Wilkinson-Herbots, A. Demaine, S. Papiha, R. Hedges, H. J. Bandelt, and B. Sykes. 1996. Paleolithic and neolithic lineages in the European mitochondrial gene pool. Am. J. Hum. Genet. 59:185-203.
66. Richards, M. B., V. A. Macaulay, H. J. Bandelt, and B. C. Sykes. 1998. Phylogeography of mitochondrial DNA in western Europe. Ann. Hum. Genet. 62(Pt 3):241-260.
67. Richards, M., V. Macaulay, E. Hickey et al. (37 co-authors). 2000. Tracing European founder lineages in the Near Eastern mtDNA pool. Am. J. Hum. Genet. 67:1251-1276.
68. Rousselet, F., and P. Mangin. 1998. Mitochondrial DNA polymorphisms: a study of 50 French Caucasians individuals and application to forensic casework. Int. J. Legal. Med. 111:292-298.
69. Ruiz-Pesini, E., D. Mishmar, M. Brandon, V. Procaccio, and D. C. Wallace. 2004. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303:223-226.
70. Salas, A., M. Richards, M. V. Lareu, R. Scozzari, A. Coppa, A. Torroni, V. Macaulay, and A. Carracedo. 2004. The African diaspora: mitochondrial DNA and the Atlantic slave trade. Am. J. Hum. Genet. 74:454-465.
71. Santos, C., M. Lima, R. Montiel, N. Angles, L. Pires, A. Abade, and M. P. Aluja. 2003. Genetic structure and origin of peopling in the Azores islands (Portugal): the view from mtDNA. Ann. Hum. Genet. 67:433-456.
72. Schwartz, M., and J. Vissing. 2002. Paternal inheritance of mitochondrial DNA. N. Engl. J. Med. 347:576-580.
73. Siguroardóttir, S., A. Helgason, J. R. Gulcher, K. Stefansson, and P. Donnelly. 2000. The mutation rate in the human mtDNA control region. Am. J. Hum. Genet. 66:1599-1609.
74. Soodyall, H., L. Vigilant, A. V. Hill, M. Stoneking, and T. Jenkins. 1996. mtDNA control-region sequence variation suggests multiple independent origins of an "Asian-specific" 9-bp deletion in sub-Saharan Africans. Am. J. Hum. Genet. 58:595-608.
75. SPSS Inc. 1989-2003. SPSS 12.0S for Windows. SPSS Inc., Chicago, Ill.
76. Stoneking, M., S. T. Sherry, A. J. Redd, and L. Vigilant. 1992. New approaches to dating suggest a recent age for the human mtDNA ancestor. Philos. Trans. R. Soc. Lond. B Biol. Sci. 337:167-175.
77. Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
78. Torroni, A., C. Rengo, V. Guida et al. (12 co-authors). 2001. Do the four clades of the mtDNA haplogroup L2 evolve at different rates? Am. J. Hum. Genet. 69:1348-1356.
79. Vigilant, L., M. Stoneking, H. Harpending, K. Hawkes, and A. C. Wilson. 1991. African populations and the evolution of human mitochondrial DNA. Science 253:1503-1507.
80. Wright, S. 1931. Evolution in Mendelian population. Genetics 16:97-159.
81. Wright, S. 1939. Statistical genetics in relation to evolution. Pp. 1-64 in G. Teissier, ed. Exposés de biométrie et de statistique biologique. Vol. 13. Hermann, Paris.