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. 1990 Mar;124(3):717–733. doi: 10.1093/genetics/124.3.717

Geographic Variation in Human Mitochondrial DNA from Papua New Guinea

M Stoneking 1, L B Jorde 1, K Bhatia 1, A C Wilson 1
PMCID: PMC1203963  PMID: 1968873

Abstract

High resolution mitochondrial DNA (mtDNA) restriction maps, consisting of an average of 370 sites per mtDNA map, were constructed for 119 people from 25 localities in Papua New Guinea (PNG). Comparison of these PNG restriction maps to published maps from Australian, Caucasian, Asian and African mtDNAs reveals that PNG has the lowest amount of mtDNA variation, and that PNG mtDNA lineages originated from Southeast Asia. The statistical significance of geographic structuring of populations with respect to mtDNA was assessed by comparing observed G(ST) values to a distribution of G(ST) values generated by random resampling of the data. These analyses show that there is significant structuring of mtDNA variation among worldwide populations, between highland and coastal PNG populations, and even between two highland PNG populations located approximately 200 km apart. However, coastal PNG populations are essentially panmictic, despite being spread over several hundred kilometers. Highland PNG populations also have more mtDNA variability and more mtDNA types represented per founding lineage than coastal PNG populations. All of these observations are consistent with a more ancient, restricted origin of highland PNG populations, internal isolation of highland PNG populations from one another and from coastal populations, and more recent and extensive population movements through coastal PNG. An apparent linguistic effect on PNG mtDNA variation disappeared when geography was taken into account. The high resolution technique for examining mtDNA variation, coupled with extensive geographic sampling within a single defined area, leads to an enhanced understanding of the influence of geography on mtDNA variation in human populations.

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Selected References

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  1. Avise J. C. Mitochondrial DNA and the evolutionary genetics of higher animals. Philos Trans R Soc Lond B Biol Sci. 1986 Jan 29;312(1154):325–342. doi: 10.1098/rstb.1986.0011. [DOI] [PubMed] [Google Scholar]
  2. Avise J. C., Neigel J. E., Arnold J. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol. 1984;20(2):99–105. doi: 10.1007/BF02257369. [DOI] [PubMed] [Google Scholar]
  3. Bhatia K. K., Blake N. M., Serjeantson S. W., Kirk R. L. Frequency of private electrophoretic variants and indirect estimates of mutation rate in Papua New Guinea. Am J Hum Genet. 1981 Jan;33(1):112–122. [PMC free article] [PubMed] [Google Scholar]
  4. Bhatia K., Gorogo M., Koki G. HLA-A,B,C and DR antigens in Asaro speakers of Papua New Guinea. Hum Immunol. 1984 Apr;9(4):189–200. doi: 10.1016/0198-8859(84)90024-7. [DOI] [PubMed] [Google Scholar]
  5. Bhatia K., Jenkins C., Prasad M., Koki G., Lombange J. Immunogenetic studies of two recently contacted populations from Papua New Guinea. Hum Biol. 1989 Feb;61(1):45–64. [PubMed] [Google Scholar]
  6. Bhatia K., Prasad M. L., Barnish G., Koki G. Antigen and haplotype frequencies at three human leucocyte antigen loci (HLA-A, -B, -C) in the Pawaia of Papua New Guinea. Am J Phys Anthropol. 1988 Mar;75(3):329–340. doi: 10.1002/ajpa.1330750304. [DOI] [PubMed] [Google Scholar]
  7. Birky C. W., Jr, Maruyama T., Fuerst P. An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics. 1983 Mar;103(3):513–527. doi: 10.1093/genetics/103.3.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Booth P. B. Genetic distances between certain New Guinea population studied under the International Biological Programme. Philos Trans R Soc Lond B Biol Sci. 1974 Aug 1;268(893):257–267. doi: 10.1098/rstb.1974.0029. [DOI] [PubMed] [Google Scholar]
  9. Brown W. M., George M., Jr, Wilson A. C. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. doi: 10.1073/pnas.76.4.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brown W. M. Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3605–3609. doi: 10.1073/pnas.77.6.3605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brown W. M., Prager E. M., Wang A., Wilson A. C. Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol. 1982;18(4):225–239. doi: 10.1007/BF01734101. [DOI] [PubMed] [Google Scholar]
  12. Cann R. L., Brown W. M., Wilson A. C. Polymorphic sites and the mechanism of evolution in human mitochondrial DNA. Genetics. 1984 Mar;106(3):479–499. doi: 10.1093/genetics/106.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cann R. L., Stoneking M., Wilson A. C. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. doi: 10.1038/325031a0. [DOI] [PubMed] [Google Scholar]
  14. Cavalli-Sforza L. L., Piazza A., Menozzi P., Mountain J. Reconstruction of human evolution: bringing together genetic, archaeological, and linguistic data. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6002–6006. doi: 10.1073/pnas.85.16.6002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Crane G., Bhatia K., Honeyman M., Doran T., Messel N., Hakos G., Tarlinton D., Amos D. B., Bashir H. HLA studies of Highland and Coastal New Guineans. Hum Immunol. 1985 Apr;12(4):247–260. doi: 10.1016/0198-8859(85)90340-4. [DOI] [PubMed] [Google Scholar]
  16. Crow J. F., Aoki K. Group selection for a polygenic behavioral trait: estimating the degree of population subdivision. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6073–6077. doi: 10.1073/pnas.81.19.6073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Giles E., Ogan E., Steinberg A. G. Gammaglobulin factors (Gm and Inv) in New Guinea: anthropological significance. Science. 1965 Nov 26;150(3700):1158–1160. doi: 10.1126/science.150.3700.1158. [DOI] [PubMed] [Google Scholar]
  18. Giles R. E., Blanc H., Cann H. M., Wallace D. C. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6715–6719. doi: 10.1073/pnas.77.11.6715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Groube L., Chappell J., Muke J., Price D. A 40,000 year-old human occupation site at Huon Peninsula, Papua New Guinea. Nature. 1986 Dec 4;324(6096):453–455. doi: 10.1038/324453a0. [DOI] [PubMed] [Google Scholar]
  20. Hertzberg M., Mickleson K. N., Serjeantson S. W., Prior J. F., Trent R. J. An Asian-specific 9-bp deletion of mitochondrial DNA is frequently found in Polynesians. Am J Hum Genet. 1989 Apr;44(4):504–510. [PMC free article] [PubMed] [Google Scholar]
  21. Hill A. V. The population genetics of alpha-thalassemia and the malaria hypothesis. Cold Spring Harb Symp Quant Biol. 1986;51(Pt 1):489–498. doi: 10.1101/sqb.1986.051.01.060. [DOI] [PubMed] [Google Scholar]
  22. Horai S., Matsunaga E. Mitochondrial DNA polymorphism in Japanese. II. Analysis with restriction enzymes of four or five base pair recognition. Hum Genet. 1986 Feb;72(2):105–117. doi: 10.1007/BF00283927. [DOI] [PubMed] [Google Scholar]
  23. Kamboh M. I., Kirk R. L. Distribution of transferrin (Tf) subtypes in Asian, Pacific and Australian Aboriginal populations: evidence for the existence of a new subtype TfC6. Hum Hered. 1983;33(4):237–243. doi: 10.1159/000153384. [DOI] [PubMed] [Google Scholar]
  24. Kamboh M. I., Kirk R. L. Genetic studies of PGM1 subtypes: population data from the Asian-Pacific area. Ann Hum Biol. 1984 May-Jun;11(3):211–219. doi: 10.1080/03014468400007081. [DOI] [PubMed] [Google Scholar]
  25. Kamboh M. I., Kirwood C. Genetic polymorphism of thyroxin-binding globulin (TBG) in the Pacific area. Am J Hum Genet. 1984 May;36(3):646–654. [PMC free article] [PubMed] [Google Scholar]
  26. Kamboh M. I., Ranford P. R., Kirk R. L. Population genetics of the vitamin D binding protein (GC) subtypes in the Asian-Pacific area: description of new alleles at the GC locus. Hum Genet. 1984;67(4):378–384. doi: 10.1007/BF00291395. [DOI] [PubMed] [Google Scholar]
  27. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res. 1967 Feb;27(2):209–220. [PubMed] [Google Scholar]
  28. Mourant A. E., Tills D., Kopeć A. C., Warlow A., Teesdale P., Booth P. B., Hornabrook R. W. Red cell antigen, serum protein and red cell enzyme polymorphisms in Eastern Highlanders of New Guinea. Hum Hered. 1982;32(6):374–384. doi: 10.1159/000153327. [DOI] [PubMed] [Google Scholar]
  29. Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3321–3323. doi: 10.1073/pnas.70.12.3321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nei M., Tajima F. Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics. 1983 Sep;105(1):207–217. doi: 10.1093/genetics/105.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ohtsuka R., Kawabe T., Inaoka T., Akimichi T., Suzuki T. Inter- and intra-population migration of the Gidra in lowland Papua: a population-ecological analysis. Hum Biol. 1985 Feb;57(1):33–45. [PubMed] [Google Scholar]
  32. Serjeantson S. W., Ryan D. P., Thompson A. R. The colonization of the Pacific: the story according to human leukocyte antigens. Am J Hum Genet. 1982 Nov;34(6):904–918. [PMC free article] [PubMed] [Google Scholar]
  33. Singh G., Neckelmann N., Wallace D. C. Conformational mutations in human mitochondrial DNA. Nature. 1987 Sep 17;329(6136):270–272. doi: 10.1038/329270a0. [DOI] [PubMed] [Google Scholar]
  34. Stoneking M., Bhatia K., Wilson A. C. Rate of sequence divergence estimated from restriction maps of mitochondrial DNAs from Papua New Guinea. Cold Spring Harb Symp Quant Biol. 1986;51(Pt 1):433–439. doi: 10.1101/sqb.1986.051.01.052. [DOI] [PubMed] [Google Scholar]
  35. Takahata N., Nei M. Gene genealogy and variance of interpopulational nucleotide differences. Genetics. 1985 Jun;110(2):325–344. doi: 10.1093/genetics/110.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Takahata N., Palumbi S. R. Extranuclear differentiation and gene flow in the finite island model. Genetics. 1985 Feb;109(2):441–457. doi: 10.1093/genetics/109.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vigilant L., Pennington R., Harpending H., Kocher T. D., Wilson A. C. Mitochondrial DNA sequences in single hairs from a southern African population. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9350–9354. doi: 10.1073/pnas.86.23.9350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vigilant L., Stoneking M., Wilson A. C. Conformational mutation in human mtDNA detected by direct sequencing of enzymatically amplified DNA. Nucleic Acids Res. 1988 Jul 11;16(13):5945–5955. doi: 10.1093/nar/16.13.5945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Whittam T. S., Clark A. G., Stoneking M., Cann R. L., Wilson A. C. Allelic variation in human mitochondrial genes based on patterns of restriction site polymorphism. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9611–9615. doi: 10.1073/pnas.83.24.9611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wood J. W., Johnson P. L., Kirk R. L., McLoughlin K., Blake N. M., Matheson F. A. The genetic demography of the Gainj of Papua New Guinea. I. Local differentiation of blood group, red cell enzyme, and serum protein allele frequencies. Am J Phys Anthropol. 1982 Jan;57(1):15–25. doi: 10.1002/ajpa.1330570105. [DOI] [PubMed] [Google Scholar]
  41. Wrischnik L. A., Higuchi R. G., Stoneking M., Erlich H. A., Arnheim N., Wilson A. C. Length mutations in human mitochondrial DNA: direct sequencing of enzymatically amplified DNA. Nucleic Acids Res. 1987 Jan 26;15(2):529–542. doi: 10.1093/nar/15.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]

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