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. 1989 Mar;121(3):551–569. doi: 10.1093/genetics/121.3.551

Molecular Population Genetics of Mtdna Size Variation in Crickets

D M Rand 1, R G Harrison 1
PMCID: PMC1203640  PMID: 2565855

Abstract

Nucleotide sequence analysis of a region of cricket (Gryllus firmus) mtDNA showing discrete length variation revealed tandemly repeated sequences 220 base pairs (bp) in length. The repeats consist of 206 bp sequences bounded by the dyad symmetric sequence 5'GGGGGCATGCCCCC3'. The sequence data showed that mtDNA size variation in this species is due to variation in the number of copies of tandem repeats. Southern blot analysis was used to document the frequency of crickets heteroplasmic for two or more different-sized mtDNAs. In New England populations of G. firmus and a close relative Gryllus pennsylvanicus approximately 60% of the former and 45% of the latter were heteroplasmic. From densitometry of autoradiographs the frequencies of mtDNA size classes were determined for the population samples and are shown to be very different in the two species. However, in populations where hybridization between the two species has occurred, the frequencies of size classes and cytoplasmic genotypes in each species' distinct mtDNA lineage were shifted in a manner suggesting nuclear-cytoplasmic interactions. The data were applied to reported diversity indices and hierarchical statistics. The hierarchical statistics indicated that the greatest proportion of variation for mtDNA size was due to variation among individuals in their cytoplasmic genotypes (heteroplasmic or homoplasmic state). The diversity indices were used to estimate a per-generation mutation rate for size variants of 10(-4). The data are discussed in light of the relationship between genetic drift and mutation in maintaining variation for mtDNA size.

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Selected References

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

  1. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  2. Asmussen M. A., Arnold J., Avise J. C. Definition and properties of disequilibrium statistics for associations between nuclear and cytoplasmic genotypes. Genetics. 1987 Apr;115(4):755–768. doi: 10.1093/genetics/115.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Birky C. W., Jr, Fuerst P., Maruyama T. Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics. 1989 Mar;121(3):613–627. doi: 10.1093/genetics/121.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Birky C. W., Jr Transmission genetics of mitochondria and chloroplasts. Annu Rev Genet. 1978;12:471–512. doi: 10.1146/annurev.ge.12.120178.002351. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. Caccone A., Amato G. D., Powell J. R. Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics. 1988 Apr;118(4):671–683. doi: 10.1093/genetics/118.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cann R. L., Wilson A. C. Length mutations in human mitochondrial DNA. Genetics. 1983 Aug;104(4):699–711. doi: 10.1093/genetics/104.4.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chang D. D., Clayton D. A. Identification of primary transcriptional start sites of mouse mitochondrial DNA: accurate in vitro initiation of both heavy- and light-strand transcripts. Mol Cell Biol. 1986 May;6(5):1446–1453. doi: 10.1128/mcb.6.5.1446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chang D. D., Clayton D. A. Precise identification of individual promoters for transcription of each strand of human mitochondrial DNA. Cell. 1984 Mar;36(3):635–643. doi: 10.1016/0092-8674(84)90343-x. [DOI] [PubMed] [Google Scholar]
  16. Clary D. O., Wolstenholme D. R. Drosophila mitochondrial DNA: conserved sequences in the A + T-rich region and supporting evidence for a secondary structure model of the small ribosomal RNA. J Mol Evol. 1987;25(2):116–125. doi: 10.1007/BF02101753. [DOI] [PubMed] [Google Scholar]
  17. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  18. Clayton D. A., Davis R. W., Vinograd J. Homology and structural relationships between the dimeric and monomeric circular forms of mitochondrial DNA from human leukemic leukocytes. J Mol Biol. 1970 Jan 28;47(2):137–153. doi: 10.1016/0022-2836(70)90335-9. [DOI] [PubMed] [Google Scholar]
  19. Clayton D. A. Replication of animal mitochondrial DNA. Cell. 1982 Apr;28(4):693–705. doi: 10.1016/0092-8674(82)90049-6. [DOI] [PubMed] [Google Scholar]
  20. Clayton D. A., Vinograd J. Circular dimer and catenate forms of mitochondrial DNA in human leukaemic leucocytes. Nature. 1967 Nov 18;216(5116):652–657. doi: 10.1038/216652a0. [DOI] [PubMed] [Google Scholar]
  21. DeSalle R., Giddings L. V., Kaneshiro K. Y. Mitochondrial DNA variability in natural populations of Hawaiian Drosophila. II. Genetic and phylogenetic relationships of natural populations of D. silvestris and D. heteroneura. Heredity (Edinb) 1986 Feb;56(Pt 1):87–96. doi: 10.1038/hdy.1986.12. [DOI] [PubMed] [Google Scholar]
  22. DeSalle R., Giddings L. V., Templeton A. R. Mitochondrial DNA variability in natural populations of Hawaiian Drosophila. I. Methods and levels of variability in D. silvestris and D. heteroneura populations. Heredity (Edinb) 1986 Feb;56(Pt 1):75–85. doi: 10.1038/hdy.1986.11. [DOI] [PubMed] [Google Scholar]
  23. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  24. Ferris S. D., Sage R. D., Prager E. M., Ritte U., Wilson A. C. Mitochondrial DNA evolution in mice. Genetics. 1983 Nov;105(3):681–721. doi: 10.1093/genetics/105.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gregorius H. R., Ross M. D. Selection with gene-cytoplasm interactions. I. Maintenance of cytoplasm polymorphisms. Genetics. 1984 May;107(1):165–178. doi: 10.1093/genetics/107.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Harrison R. G., Rand D. M., Wheeler W. C. Mitochondrial DNA size variation within individual crickets. Science. 1985 Jun 21;228(4706):1446–1448. doi: 10.1126/science.228.4706.1446. [DOI] [PubMed] [Google Scholar]
  27. Hauswirth W. W., Laipis P. J. Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4686–4690. doi: 10.1073/pnas.79.15.4686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hauswirth W. W., Van de Walle M. J., Laipis P. J., Olivo P. D. Heterogeneous mitochondrial DNA D-loop sequences in bovine tissue. Cell. 1984 Jul;37(3):1001–1007. doi: 10.1016/0092-8674(84)90434-3. [DOI] [PubMed] [Google Scholar]
  29. Keith T. P., Brooks L. D., Lewontin R. C., Martinez-Cruzado J. C., Rigby D. L. Nearly identical allelic distributions of xanthine dehydrogenase in two populations of Drosophila pseudoobscura. Mol Biol Evol. 1985 May;2(3):206–216. doi: 10.1093/oxfordjournals.molbev.a040348. [DOI] [PubMed] [Google Scholar]
  30. Lansman R. A., Avise J. C., Huettel M. D. Critical experimental test of the possibility of "paternal leakage" of mitochondrial DNA. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1969–1971. doi: 10.1073/pnas.80.7.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. MacRae A. F., Anderson W. W. Evidence for non-neutrality of mitochondrial DNA haplotypes in Drosophila pseudoobscura. Genetics. 1988 Oct;120(2):485–494. doi: 10.1093/genetics/120.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Merten S. H., Pardue M. L. Mitochondrial DNA in Drosophila. An analysis of genome organization and transcription in Drosophila melanogaster and Drosophila virilis. J Mol Biol. 1981 Nov 25;153(1):1–21. doi: 10.1016/0022-2836(81)90523-4. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Moritz C., Brown W. M. Tandem duplication of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science. 1986 Sep 26;233(4771):1425–1427. doi: 10.1126/science.3018925. [DOI] [PubMed] [Google Scholar]
  35. Moritz C., Brown W. M. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7183–7187. doi: 10.1073/pnas.84.20.7183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Osinga K. A., Tabak H. F. Initiation of transcription of genes for mitochondrial ribosomal RNA in yeast: comparison of the nucleotide sequence around the 5'-ends of both genes reveals a homologous stretch of 17 nucleotides. Nucleic Acids Res. 1982 Jun 25;10(12):3617–3626. doi: 10.1093/nar/10.12.3617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Snyder M., Fraser A. R., Laroche J., Gartner-Kepkay K. E., Zouros E. Atypical mitochondrial DNA from the deep-sea scallop Placopecten magellanicus. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7595–7599. doi: 10.1073/pnas.84.21.7595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Solignac M., Génermont J., Monnerot M., Mounolou J. C. Drosophila Mitochondrial Genetics: Evolution of Heteroplasmy through Germ Line Cell Divisions. Genetics. 1987 Dec;117(4):687–696. doi: 10.1093/genetics/117.4.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thrailkill K. M., Birky C. W., Jr Intracellular population genetics: evidence for random drift of mitochondrial allele frequencies in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Genetics. 1980 Sep;96(1):237–262. doi: 10.1093/genetics/96.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Upholt W. B., Dawid I. B. Mapping of mitochondrial DNA of individual sheep and goats: rapid evolution in the D loop region. Cell. 1977 Jul;11(3):571–583. doi: 10.1016/0092-8674(77)90075-7. [DOI] [PubMed] [Google Scholar]
  44. Vawter L., Brown W. M. Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science. 1986 Oct 10;234(4773):194–196. doi: 10.1126/science.3018931. [DOI] [PubMed] [Google Scholar]
  45. Wallace D. C. Structure and evolution of organelle genomes. Microbiol Rev. 1982 Jun;46(2):208–240. doi: 10.1128/mr.46.2.208-240.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. Wolstenholme D. R., Macfarlane J. L., Okimoto R., Clary D. O., Wahleithner J. A. Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1324–1328. doi: 10.1073/pnas.84.5.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wong J. F., Ma D. P., Wilson R. K., Roe B. A. DNA sequence of the Xenopus laevis mitochondrial heavy and light strand replication origins and flanking tRNA genes. Nucleic Acids Res. 1983 Jul 25;11(14):4977–4995. doi: 10.1093/nar/11.14.4977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zannis-Hadjopoulos M., Frappier L., Khoury M., Price G. B. Effect of anti-cruciform DNA monoclonal antibodies on DNA replication. EMBO J. 1988 Jun;7(6):1837–1844. doi: 10.1002/j.1460-2075.1988.tb03016.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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