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Population genetics of extranuclear genomes under the neutral mutation hypothesis*

Published online by Cambridge University Press:  14 April 2009

Naoyuki Takahata
Affiliation:
National Institute of Genetics, Mishima, Shizuoka-ken 411, Japan

Summary

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Population genetics of extranuclear genomes is further developed under the neutral-mutation random-drift hypothesis, and the characteristic evolutionary aspects are summarized. Several formulae derived here are concerned with the variances of genetic variability (gene identity) at a single extranuclear locus and the evolutionary distance between two isolated populations which is estimated from a comparison of homologous linked nucleotide sites. Two types of variance are considered; one is the variance in the entire population (VQ) and the other is the variance within a single germ cell (VH). When compared with a Mendelian genetic system in a panmictic population, an extranuclear genetic system has the following equilibrium properties: (1) the mean genetic variability is low if, despite the high multiplicity of the genome in a cell, the proportion of the cytoplasmic contribution from the male's gamete is small, (2) the effect of recombination is small and a large amount of variance of linkage disequilibrium tends to be maintained, (3) the overall relationship between the mean and variance of genetic variability does not much differ but VQ (VH) is expected to be small if the paternal contribution is small, and (4) the evolutionary distance estimated depends on the extent of intrapopulational variation in a common ancestor population which in turn depends on within-cell variation. I argue that there is an analogy between the model of extranuclear genomes in a finite population and that of nuclear genes in a subdivided population. The analogy helps our understanding of some properties in an extranuclear genetic system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1983

References

REFERENCES

Anderson, S., Bankier, A. T., Barbell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R. & Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature 290, 457465.CrossRefGoogle ScholarPubMed
Avise, J. C., Lansman, R. A. & Shade, R. O. (1979). The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. I. Population structure and evolution in the genus Peromyscus. Genetics 92, 279295.Google ScholarPubMed
Beale, G. H. & Knowles, J. K. C. (1978). Extranuclear Genetics. London: Edward Arnold.Google Scholar
Bibb, M. J., Van Etten, R. A., Wright, C. T., Walberg, M. W. & Clayton, D. A. (1981). Sequence and gene organization of mouse mitochondrial DNA. Cell 26, 167180.CrossRefGoogle ScholarPubMed
Birky, C. W. Jr., (1978). Transmission genetics of mitochondria and chloroplasts. Annual Review of Genetics 12, 417512.Google ScholarPubMed
Birky, C. W. Jr, Maruyama, T. & Fuerst, P. (1983). An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103, 513527.CrossRefGoogle ScholarPubMed
Bogenhagen, D. & Clayton, D. A. (1974). The number of mitochondrial deoxyribonucleic acid genomes in mouse L and human Hela cells. Quantitative isolation of mitochondrial deoxyribonucleic acid. Journal of Biological Chemistry 249, 79917995.CrossRefGoogle ScholarPubMed
Chapman, R. W., Stephens, J. C., Lansman, R. A. & Avise, J. C. (1982). Models of mitochondrial DNA transmission genetics and evolution in higher eucaryotes. Genetical Research 40, 4157.CrossRefGoogle ScholarPubMed
Dawid, I. B. & Blackler, A. W. (1972). Maternal and cytoplasmic inheritance of mitchondrial DNA in Xenopus. Developmental Biology 29, 152161.Google Scholar
Dujon, B., Slonimski, P. P. & Weill, L. (1974). Mitochondrial genetics. IX. A model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78, 415437.CrossRefGoogle Scholar
Engels, W. R. (1981). Estimating genetic divergence and genetic variability with restriction endonucleases. Proceedings of the National Academy of Sciences, U.S.A. 78, 63296333.CrossRefGoogle ScholarPubMed
Giles, R. E., Blanc, H., Cann, H. M. & Wallace, D. C. (1980). Maternal inheritance of human mitochondrial DNA. Proceedings of the National Academy of Sciences, U.S.A. 77, 67156719.CrossRefGoogle ScholarPubMed
Gillham, N. W. (1978). Organelle Heredity. New York: Raven Press.Google Scholar
Golding, G. B. & Strobeck, C. (1982). The distribution of nucleotide site differences between two finite sequences. Theoretical Population Biology 22, 96107.Google ScholarPubMed
Golding, G. B. & Strobeck, C. (1983). Variance and covariance of homozygosity in a structured population. Genetics 104, 513529.CrossRefGoogle Scholar
Griffiths, R. C. (1981). Transient distribution of the number of segregating sites in a neutral infinite-sites model with no recombination. Journal of Applied Probability 18, 4251.CrossRefGoogle Scholar
Gross, N. J., Getz, G. S. & Rabinowitz, M. (1969). Apparent turnover of mitochondrial deoxyribonucleic acid and mitochondrial phospholipids in the tissues of the rat. Journal of Biological Chemistry 244, 15521562.CrossRefGoogle ScholarPubMed
Hauswirth, W. W. & Laipis, P. J. (1982). Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proceedingsof the National Academy of Sciences, U.S.A. 79, 46864690.CrossRefGoogle Scholar
Jukes, T. H. & Cantor, C. H. (1969). Evolution of protein molecules. In Mammalian Protein Metabolism (ed. Munro, H. N.), pp. 21123. New York: Academic Press.Google Scholar
Kimura, M. (1968). Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. Genetical Research 11, 247269.CrossRefGoogle Scholar
Kimura, M. & Ohta, T. (1972). On the stochastic model for estimation of mutational distance between homologous proteins. Journal of Molecular Evolution 2, 8790.Google ScholarPubMed
Kondo, S. (1977). Evolutionary considerations on DNA repair and mutagenesis. In Molecular Evolution and Polymorphism (Proceedings of the Second Taniguchi International Symposium on Biophysics, (ed. Motoo, Kimura)) pp. 313331.Google Scholar
Lansman, R. A., Avise, J. C. & Huettel, M. D. (1983). Critical experimental test of the possibility of ‘paternal leakage’ of mitochondrial DNA. Proceedings of the National Academy of Sciences, U.S.A. 80, 19691971.CrossRefGoogle ScholarPubMed
Nass, M. K. (1969). Mitochondrial DNA: advances, problems, and goals. Science 165, 2535.CrossRefGoogle ScholarPubMed
Nei, M. & Li, W.-H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences, U.S.A. 76, 52695273.Google ScholarPubMed
Ohta, T. (1980). Two-locus problems in transmission genetics of mitochondria and chloroplasts. Genetics 96, 543555.CrossRefGoogle ScholarPubMed
Rabinowitz, M. & Swift, H. (1970). Mitochondrial nucleic acids and their relation to the biogenesis of mitochondria. Physiological Reviews 50, 376427.CrossRefGoogle Scholar
Reilly, J. G. & Thomas, C. A. Jr, (1980). Length polymorphisms, restriction site variation, and maternal inheritance of mitochondrial DNA of Drosophila melanogaster. Plasmid 3, 109115.CrossRefGoogle ScholarPubMed
Stewart, F. M. (1976). Variability in the amount of heterozygosity maintained by neutral mutations. Theoretical Population Biology 9, 188201.CrossRefGoogle ScholarPubMed
Takahata, N. (1982). Linkage disequilibrium, genetic distance and evolutionary distance under a general model of linked genes or a part of the genome. Genetical Research 39, 6377.CrossRefGoogle Scholar
Takahata, N. (1983 a). Linkage disequilibrium of extranuclear genes under neutral mutations and random genetic drift. Theoretical Population Biology 24, 121.CrossRefGoogle Scholar
Takahata, N. (1983 b). Gene identity and genetic differentiation of populations in the finite island model. Genetics 104, 497512.CrossRefGoogle ScholarPubMed
Takahata, N. & Maruyama, T. (1981). A mathematical model of extranuclear genes and the genetic variability maintained in a finite population. Genetical Research 37, 291302.Google Scholar
Takahata, N. & Slatkin, M. (1983). Evolutionary dynamics of extranuclear genes. Genetical Research 42, 257262.Google Scholar
Upholt, W. B. (1977). Estimation of DNA sequence divergence from comparison of restriction endonuclease digests. Nucleic Acids Research 4, 12571265.CrossRefGoogle ScholarPubMed
Wallace, D. C. (1982). Structure and evolution of organelle genomes. Microbiological Reviews 46, 208240.CrossRefGoogle ScholarPubMed