Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1672, 2009, Pages 3447-3455

  Balloux, François ^a   Lawson Handley, Lori Jayne ^b   Jombart, Thibaut ^a   Liu, Hua ^c   Manica, Andrea ^c  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b UNIVERSITY OF HULL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Climate; Human evolution; mtDNA; Selection; Single nucleotide polymorphisms; Temperature

Indexed keywords

CALCIUM; MITOCHONDRIAL DNA;

ARCTIC ENVIRONMENT; CALCIUM; CLIMATE EFFECT; DATA SET; EVOLUTIONARY BIOLOGY; GENETIC DIFFERENTIATION; GENETIC MARKER; HOMINID; MITOCHONDRIAL DNA; MUTATION; NATURAL SELECTION; PH; POLYMORPHISM; SPATIAL DISTRIBUTION;

ALTITUDE; ARTICLE; ATP6 GENE; CELL PH; CLIMATE; COLD; DNA SEQUENCE; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC SELECTION; GENETIC VARIABILITY; GEOGRAPHY; HUMAN; HUMAN GENETICS; MITOCHONDRION; ND3 GENE; POINT MUTATION; POPULATION GENETIC PARAMETERS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TEMPERATURE DEPENDENCE;

BIOLOGICAL EVOLUTION; CLIMATE; DEMOGRAPHY; DNA, MITOCHONDRIAL; GENETIC VARIATION; HUMANS;

EID: 70349611306     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0752     Document Type: Article

References (53)

1. Amo, T. & Brand, M. D. 2007 Were inefficient mitochondrial haplogroups selected during migrations of modern humans? A test using modular kinetic analysis of coupling in mitochondria from cybrid cell lines. Biochem. J. 404, 345-351. (doi:10.1042/BJ20061609) (Pubitemid 46849606)
2. Ballard, J. W. O. & Whitlock, M. C. 2004 The incomplete natural history of mitochondria. Mol. Ecol. 13, 729-744. (doi:10.1046/j.1365-294X.2003. 02063.x)
3. Betti, L., Balloux, F., Amos, W., Hanihara, T. & Manica, A. 2009 Distance from Africa, not climate, explains within-population phenotypic diversity in humans. Proc. R. Soc. B 276, 809-814. (doi:10.1098/rspb.2008.1563)
4. Brand, M. D. 1990 The proton leak across the mitochondrial inner membrane. Biochim. Biophys. Acta 1018, 128-133. (doi:10.1016/0005-2728(90)90232- S)
5. Canter, J. A., Kallianpur, A. R., Parl, F. F. & Millikan, R. C. 2005 Mitochondrial DNA G10398A polymorphism and invasive breast cancer in African-American women. Cancer Res. 65, 8028-8033.
6. Deshpande, O., Batzoglou, S., Feldman, M. W. & Cavalli-Sforza, L. L. 2009 A serial founder effect model for human settlement out of Africa. Proc. R. Soc. B 276, 291-300. (doi:10.1098/rspb.2008.0750)
7. Elson, J. L., Turnbull, D. M. & Howell, N. 2004 Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am. J. Hum. Genet. 74, 229-238. (doi:10.1086/381505)
8. Excoffier, L. & Yang, Z. 1999 Substitution rate variation among sites in mitochondrial hypervariable region I of humans and chimpanzees. Mol. Biol. Evol. 16, 1357-1368.
9. Excoffier, L., Laval, G. & Schneider, S. 2005 ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinformatics Online 1, 47-50.
10. Fagundes,N. J. R., Ray, N., Beaumont, M., Neuenschwander, S., Salzano, F. M., Bonatto, S. L. & Excoffier, L. 2007 Statistical evaluation of alternative models of human evolution. Proc. Natl Acad. Sci. 104, 17614-17619. (doi:10.1073/pnas.0708280104)
11. Fay, J. C. & Wu, C. I. 1999 A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol. Biol. Evol. 16, 1003-1005.
12. Goudet, J. 1995 FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered. 86, 485-486.
13. Hancock, A. M., Witonsky, D. B., Gordon, A. S., Eshel, G., Pritchard, J. K., Coop, G. Di Rienzo, A. 2008 Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet. 4, e32. (doi:10.1371/journal.pgen. 0040032) (Pubitemid 351328537)
14. Handley, L. J., Manica, A., Goudet, J. & Balloux, F. 2007 Going the distance: human population genetics in a clinal world. Trends Genet. 23, 432-439. (doi:10.1016/j.tig.2007.07.002) (Pubitemid 47259574)
15. Hellenthal, G., Auton, A. & Falush, D. 2008 Inferring human colonization history using a copying model. PLoS Genet. 4, e1000078. (doi:10.1371/journal.pgen.1000078) (Pubitemid 351811497)
16. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. 2005 Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965-1978. (doi:10.1002/joc.1276)
17. Hill, W. G. & Robertson, A. 1966 The effect of linkage on limits to artificial selection. Genet. Res. 8, 269-294.
18. Ingman, M. & Gyllensten, U. 2006 mtDB: Human Mitochondrial Genome Database, a resource for population genetics and medical sciences. Nucleic Acids Res. 34, D749-D751. (doi:10.1093/nar/gkj010)
19. Ingman, M. & Gyllensten, U. 2007 Rate variation between mitochondrial domains and adaptive evolution in humans. Hum. Mol. Genet. 16, 2281-2287. (doi:10.1093/hmg/ddm180)
20. Kato, T., Kunugi, H., Nanko, S. & Kato, N. 2001 Mitochondrial DNA polymorphisms in bipolar disorder. J. Affect Disord. 62, 151-164. (doi:10.1016/S0165-0327(99)00173-1) (Pubitemid 32167082)
21. Kazuno, A.-A., Munakata, K., Nagai, T., Shimozono, S., Tanaka, M., Yoneda, M., Kato, N., Miyawaki, A. & Kato, T. 2006 Identification of mitochondrial DNA polymorphisms that alter mitochondrial matrix pH and intracellular calcium dynamics. PLoS Genet. 2, e128. (doi:10.1371/journal.pgen. 0020128) (Pubitemid 44298491)
22. Kivisild, T. et al. 2006 The role of selection in the evolution of human mitochondrial genomes. Genetics 172, 373-387. (doi:10.1534/genetics.105.043901) (Pubitemid 43345499)
23. Kohl, J., Paulsen, I., Laubach, T., Radtke, A. & von Haeseler, A. 2006 HvrBase++: a phylogenetic database for primate species. Nucleic Acids Res. 34, D700-D704. (doi:10.1093/nar/gkj030)
24. Kryazhimskiy, S. & Plotkin, J. B. 2008 The population genetics of dN/dS. PLoS Genet. 4, e1000304. (doi:10.1371/journal.pgen.1000304)
25. Li, J. Z. et al. 2008 Worldwide human relationships inferred from genome-wide patterns of variation. Science 319, 1100-1104. (doi:10.1126/science. 1153717)
26. Liu, H., Prugnolle, F., Manica, A. & Balloux, F. 2006 A geographically explicit genetic model of worldwide human-settlement history. Am. J. Hum. Genet. 79, 230-237. (doi:10.1086/505436)
27. Macaulay, V. et al. 2005 Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308, 1034-1036. (doi:10.1126/science.1109792) (Pubitemid 40664416)
28. Manica, A., Prugnolle, F. & Balloux, F. 2005 Geography is a better determinant of human genetic differentiation than ethnicity. Hum. Genet. 118, 366-371. (doi:10.1007/s00439-005-0039-3)
29. Manica, A., Amos, W., Balloux, F. & Hanihara, T. 2007 The effect of ancient population bottlenecks on human phenotypic variation. Nature 448, 346-348. (doi:10.1038/nature05951) (Pubitemid 47080340)
30. McDougall, I., Brown, F. H. & Fleagle, J. G. 2005 Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433, 733-736. (doi:10.1038/nature03258) (Pubitemid 40292980)
31. Mims, M. P. et al. 2006 Mitochondrial DNA G10398A polymorphism and invasive breast cancer in African-American women. Cancer Res. 66, 1880-1881. (doi:10.1158/0008-5472.CAN-05-3774)
32. Mishmar, D. et al. 2003 Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100, 171-176. (doi:10.1073/pnas. 0136972100)
33. Niemi,A.K.,Moilanen, J. S.,Tanaka,M.,Hervonen,A.,Hurme, M., Lehtimaki, T., Arai, Y., Hirose, N. & Majamaa, K. 2005 A combination of three common inherited mitochondrial DNA polymorphisms promotes longevity in Finnish and Japanese subjects. Eur. J. Hum. Genet. 13, 166-170. (doi:10.1038/sj.ejhg. 5201308)
34. Paradis, E., Claude, J. & Strimmer, K. 2004 APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. (doi:10.1093/bioinformatics/btg412) (Pubitemid 38195693)
35. Posada, D. & Crandall, K. A. 1998 MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818. (doi:10.1093/bioinformatics/14.9.817) (Pubitemid 28552116)
36. Prugnolle, F., Manica, A. & Balloux, F. 2005a Geography predicts neutral genetic diversity of human populations. Curr. Biol. 15, R159-R160. (doi:10.1016/j.cub.2005.02.038)
37. Prugnolle, F., Manica, A., Charpentier, M., Guegan, J. F., Guernier, V. & Balloux, F. 2005b Pathogen-driven selection and worldwide HLA class I diversity. Curr. Biol. 15, 1022-1027. (doi:10.1016/j.cub.2005.04.050)
38. Rai, E., Sharma, S., Koul, A., Bhat, A., Bhanwer, A. & Bamezai, R. 2007 Interaction between the UCP2- 866G/A, mtDNA 10398G/A and PGC1a p.Thr394Thr and p.Gly482Ser polymorphisms in type 2 diabetes susceptibility in North Indian population. Hum. Genet. 122, 535-540. (doi:10.1007/s00439-007-0421-4)
39. Ramachandran, S., Deshpande, O., Roseman, C. C., Rosenberg, N. A., Feldman, M. W. & Cavalli-Sforza, L. L. 2005 Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc. Natl Acad. Sci. USA 102, 15 942-15 947. (doi:10.1073/pnas.0507611102)
40. Relethford, J. H. 2004 Global patterns of isolation by distance based on genetic and morphological data. Hum. Biol. 76, 499-513. (doi:10.1353/hub.2004. 0060)
41. Romero, I. G., Manica, A., Goudet, J., Handley, L. L. & Balloux, F. 2008 How accurate is the current picture of human genetic variation? Heredity 102, 120-126. (doi:10.1038/hdy.2008.89)
42. Rosenberg, N. A. 2006 Standardized subsets of the HGDPCEPH Human Genome Diversity Cell Line Panel, accounting for atypical and duplicated samples and pairs of close relatives. Ann. Hum. Genet. 70, 841-847. (doi:10.1111/j.1469- 1809.2006.00285.x)
43. Ruiz-Pesini, E., Mishmar, D., Brandon, M., Procaccio, V. & Wallace, D. C. 2004 Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303, 223-226. (doi:10.1126/science.1088434) (Pubitemid 38057570)
44. Ruiz-Pesini, E. et al. 2007 An enhanced MITOMAP with a global mtDNA mutational phylogeny. Nucleic Acids Res. 35, D823-D828. (doi:10.1093/nar/gkl927) (Pubitemid 46056316)
45. Stringer, C. B. & Andrews, P. 1988 Genetic and fossil evidence for the origin of modern humans. Science 239, 1263-1268. (doi:10.1126/science. 3125610) (Pubitemid 18299222)
46. Sun, C., Kong, Q.-P. & Zhang, P. 2007 The role of climate in human mitochondrial DNA evolution: a reappraisal. Genomics 89, 338-342. (doi:10.1016/j.ygeno.2006.11.005) (Pubitemid 46205122)
47. Tamura, K. & Nei, M. 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.
48. Torroni, A. et al. 2001 Do the four clades of the mtDNA haplogroup L2 evolve at different rates. Am. J. Hum. Genet. 69, 1348-1356. (doi:10.1086/324511)
49. van der Walt, J. M. et al. 2003 Mitochondrial polymorphisms significantly reduce the risk of Parkinson disease. Am. J. Hum. Genet. 72, 804-811. (doi:10.1086/373937)
50. van derWalt, J.M. et al. 2004 Analysis of European mitochondrial haplogroups withAlzheimer disease risk. Neurosci. Lett. 365, 28-32. (doi:10.1016/j.neulet.2004.04.051)
51. von Cramon-Taubadel, N. & Lycett, S. J. 2008 Brief communication: human cranial variation fits iterative founder effect model with African origin. Am. J. Phys. Anthropol. 136, 108-113. (doi:10.1002/ajpa.20775)
52. Xu, H., Chakraborty, R. & Fu, X. 2005 Mutation rate variation at human dinucleotide microsatellites. Genetics 170, 305-312. (doi:10.1534/ genetics.104.036855) (Pubitemid 40799992)
53. Young, J. H., Chang, Y.-P. C., Kim, J. D.-O., Chretien, J.-P., Klag, M. J., Levine, M. A., Ruff, C. B., Wang, N.-Y. & Chakravarti, A. 2005 Differential susceptibility to hypertension is due to selection during the out-of-Africa expansion. PLoS Genet. 1, e82. (doi:10.1371/journal.pgen.0010082)