Skip to main content
Genetics logoLink to Genetics
. 1989 Mar;121(3):613–627. doi: 10.1093/genetics/121.3.613

Organelle Gene Diversity under Migration, Mutation, and Drift: Equilibrium Expectations, Approach to Equilibrium, Effects of Heteroplasmic Cells, and Comparison to Nuclear Genes

C W Birky-Jr 1, P Fuerst 1, T Maruyama 1
PMCID: PMC1203645  PMID: 2714640

Abstract

We developed stochastic population genetic theory for mitochondrial and chloroplast genes, using an infinite alleles model appropriate for molecular genetic data. We considered the effects of mutation, random drift, and migration in a finite island model on selectively neutral alleles. Recurrence equations were obtained for the expectation of gene diversities within zygotes, within colonies, and between colonies. The variables are number and sizes of colonies, migration rates, sex ratios, degree of paternal transmission, number of germ line cell divisions, effective number of segregating organelle genomes, and mutation rate. Computer solutions of the recurrence equations were used to study the approach to equilibrium. Gene diversities equilibrate slowly, while G(ST), used to measure population subdivision, equilibrates rapidly. Approximate equilibrium equations for gene diversities and G(ST) can be obtained by substituting N(eo) and m(e), simple functions of the numbers of breeding or migrating males and females and of the degree of paternal transmission, for the effective numbers of genes and migration rates in the corresponding equations for nuclear genes. The approximate equations are not valid when the diversity within individuals is large compared to that between individuals, as is often true for the D-loop of animal mtDNA. We used the exact equations to verify that organelle genes often show more subdivision than nuclear genes; however, we also identified the range of breeding and migrating sex ratios for which population subdivision is greater for nuclear genes. Finally, we show that gene diversities are higher for nuclei than for organelles over a larger range of sex ratios in a subdivided population than in a panmictic population.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Backer J. S., Birky C. W., Jr The origin of mutant cells: mechanisms by which Saccharomyces cerevisiae produces cells homoplasmic for new mitochondrial mutations. Curr Genet. 1985;9(8):627–640. doi: 10.1007/BF00449815. [DOI] [PubMed] [Google Scholar]
  2. Bermingham E., Lamb T., Avise J. C. Size polymorphism and heteroplasmy in the mitochondrial DNA of lower vertebrates. J Hered. 1986 Jul-Aug;77(4):249–252. doi: 10.1093/oxfordjournals.jhered.a110230. [DOI] [PubMed] [Google Scholar]
  3. Birky C. W., Jr Relaxed cellular controls and organelle heredity. Science. 1983 Nov 4;222(4623):468–475. doi: 10.1126/science.6353578. [DOI] [PubMed] [Google Scholar]
  4. Boursot P., Yonekawa H., Bonhomme F. Heteroplasmy in mice with deletion of a large coding region of mitochondrial DNA. Mol Biol Evol. 1987 Jan;4(1):46–55. doi: 10.1093/oxfordjournals.molbev.a040421. [DOI] [PubMed] [Google Scholar]
  5. Brown G. G., DesRosiers L. J. Rat mitochondrial DNA polymorphism: sequence analysis of a hypervariable site for insertions/deletions. Nucleic Acids Res. 1983 Oct 11;11(19):6699–6708. doi: 10.1093/nar/11.19.6699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown G. G., Simpson M. V. Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci U S A. 1982 May;79(10):3246–3250. doi: 10.1073/pnas.79.10.3246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chapman R. W., Stephens J. C., Lansman R. A., Avise J. C. Models of mitochondrial DNA transmission genetics and evolution in higher eucaryotes. Genet Res. 1982 Aug;40(1):41–57. doi: 10.1017/s0016672300018899. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Densmore L. D., Wright J. W., Brown W. M. Length variation and heteroplasmy are frequent in mitochondrial DNA from parthenogenetic and bisexual lizards (genus Cnemidophorus). Genetics. 1985 Aug;110(4):689–707. doi: 10.1093/genetics/110.4.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hale L. R., Singh R. S. Extensive variation and heteroplasmy in size of mitochondrial DNA among geographic populations of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8813–8817. doi: 10.1073/pnas.83.22.8813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. KIMURA M., CROW J. F. THE NUMBER OF ALLELES THAT CAN BE MAINTAINED IN A FINITE POPULATION. Genetics. 1964 Apr;49:725–738. doi: 10.1093/genetics/49.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Maruyama T. Effective number of alleles in a subdivided population. Theor Popul Biol. 1970 Nov;1(3):273–306. doi: 10.1016/0040-5809(70)90047-x. [DOI] [PubMed] [Google Scholar]
  13. Miyata T., Hayashida H., Kikuno R., Hasegawa M., Kobayashi M., Koike K. Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol. 1982;19(1):28–35. doi: 10.1007/BF02100221. [DOI] [PubMed] [Google Scholar]
  14. Monnerot M., Mounolou J. C., Solignac M. Intra-individual length heterogeneity of Rana esculenta mitochondrial DNA. Biol Cell. 1984;52(3):213–218. doi: 10.1111/j.1768-322x.1985.tb00339.x. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Rand D. M., Harrison R. G. Mitochondrial DNA transmission genetics in crickets. Genetics. 1986 Nov;114(3):955–970. doi: 10.1093/genetics/114.3.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Slatkin M. Gene flow and the geographic structure of natural populations. Science. 1987 May 15;236(4803):787–792. doi: 10.1126/science.3576198. [DOI] [PubMed] [Google Scholar]
  18. Solignac M., Monnerot M., Mounolou J. C. Mitochondrial DNA heteroplasmy in Drosophila mauritiana. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6942–6946. doi: 10.1073/pnas.80.22.6942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Varvio S. L., Chakraborty R., Nei M. Genetic variation in subdivided populations and conservation genetics. Heredity (Edinb) 1986 Oct;57(Pt 2):189–198. doi: 10.1038/hdy.1986.109. [DOI] [PubMed] [Google Scholar]
  21. Wallis G. P. Mitochondrial DNA insertion polymorphism and germ line heteroplasmy in the Triturus cristatus complex. Heredity (Edinb) 1987 Apr;58(Pt 2):229–238. doi: 10.1038/hdy.1987.37. [DOI] [PubMed] [Google Scholar]
  22. Wolfe K. H., Li W. H., Sharp P. M. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9054–9058. doi: 10.1073/pnas.84.24.9054. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES