Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1988 Mar;118(3):471–481. doi: 10.1093/genetics/118.3.471

Natural Selection with Nuclear and Cytoplasmic Transmission. III. Joint Analysis of Segregation and Mtdna in Drosophila Melanogaster

A G Clark 1, EMS Lyckegaard 1
PMCID: PMC1203301  PMID: 3130289

Abstract

Despite the widespread use of mitochondrial DNA by evolutionary geneticists, relatively little effort has been spent assessing the magnitude of forces maintaining mtDNA sequence diversity. In this study the influence of cytoplasmic variation on viability in Drosophila was examined by analysis of second chromosome segregation. A factorial experiment with balancer chromosomes permitted the effects of cytoplasm and reciprocal crosses to be individually distinguished. The first test used six lines of diverse geographic origin, testing the segregation of all six second chromosomes in all six cytoplasms. The second and third tests were also factorial designs, but used flies from one population in central Pennsylvania. The fourth test was a large chain cross, using 28 lines from the same Pennsylvania population. Only the first test detected a significant nuclear-cytoplasmic effect. Restriction site variation in the mtDNA of all of these lines was assayed by Southern blotting, and statistical tests were performed in an effort to detect an influence of mtDNA type on fitness components. Posterior linear contrasts revealed an effect of mtDNA on segregation only among lines of diverse geographic origin. Within a population, no such influence was detected, even though the experiment was sufficiently large to have revealed statistical significance of a 0.5% segregation difference with a 57% probability.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

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. Avise J. C., Saunders N. C. Hybridization and introgression among species of sunfish (Lepomis): analysis by mitochondrial DNA and allozyme markers. Genetics. 1984 Sep;108(1):237–255. doi: 10.1093/genetics/108.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bender W., Spierer P., Hogness D. S. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):17–33. doi: 10.1016/s0022-2836(83)80320-9. [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. 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]
  6. 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]
  7. 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]
  8. Carr S. M., Ballinger S. W., Derr J. N., Blankenship L. H., Bickham J. W. Mitochondrial DNA analysis of hybridization between sympatric white-tailed deer and mule deer in west Texas. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9576–9580. doi: 10.1073/pnas.83.24.9576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Clark A. G. Natural selection with nuclear and cytoplasmic transmission. I. A deterministic model. Genetics. 1984 Aug;107(4):679–701. doi: 10.1093/genetics/107.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Clark A. G. Natural selection with nuclear and cytoplasmic transmission. II. Tests with Drosophila from diverse populations. Genetics. 1985 Sep;111(1):97–112. doi: 10.1093/genetics/111.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clark A. G. Neutrality tests of highly polymorphic restriction-fragment-length polymorphisms. Am J Hum Genet. 1987 Nov;41(5):948–956. [PMC free article] [PubMed] [Google Scholar]
  13. Clayton D. A. Transcription of the mammalian mitochondrial genome. Annu Rev Biochem. 1984;53:573–594. doi: 10.1146/annurev.bi.53.070184.003041. [DOI] [PubMed] [Google Scholar]
  14. DeSalle R., Giddings L. V. Discordance of nuclear and mitochondrial DNA phylogenies in Hawaiian Drosophila. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6902–6906. doi: 10.1073/pnas.83.18.6902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. DeSalle R., Templeton A., Mori I., Pletscher S., Johnston J. S. Temporal and spatial heterogeneity of mtDNA polymorphisms in natural populations of Drosophila mercatorum. Genetics. 1987 Jun;116(2):215–223. doi: 10.1093/genetics/116.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Dewey R. E., Levings C. S., 3rd, Timothy D. H. Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell. 1986 Feb 14;44(3):439–449. doi: 10.1016/0092-8674(86)90465-4. [DOI] [PubMed] [Google Scholar]
  19. Dykhuizen D. E., Hartl D. L. Selection in chemostats. Microbiol Rev. 1983 Jun;47(2):150–168. doi: 10.1128/mr.47.2.150-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dykhuizen D. E., de Framond J., Hartl D. L. Selective neutrality of glucose-6-phosphate dehydrogenase allozymes in Escherichia coli. Mol Biol Evol. 1984 Feb;1(2):162–170. doi: 10.1093/oxfordjournals.molbev.a040309. [DOI] [PubMed] [Google Scholar]
  21. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  22. Ferris S. D., Sage R. D., Huang C. M., Nielsen J. T., Ritte U., Wilson A. C. Flow of mitochondrial DNA across a species boundary. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2290–2294. doi: 10.1073/pnas.80.8.2290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Hale L. R., Beckenbach A. T. Mitochondrial DNA variation in Drosophila pseudoobscura and related species in Pacific northwest populations. Can J Genet Cytol. 1985 Jun;27(3):357–364. doi: 10.1139/g85-053. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Latorre A., Moya A., Ayala F. J. Evolution of mitochondrial DNA in Drosophila subobscura. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8649–8653. doi: 10.1073/pnas.83.22.8649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Levings C. S., 3rd The plant mitochondrial genome and its mutants. Cell. 1983 Mar;32(3):659–661. doi: 10.1016/0092-8674(83)90051-x. [DOI] [PubMed] [Google Scholar]
  28. Monnat R. J., Jr, Loeb L. A. Nucleotide sequence preservation of human mitochondrial DNA. Proc Natl Acad Sci U S A. 1985 May;82(9):2895–2899. doi: 10.1073/pnas.82.9.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Powell J. R. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc Natl Acad Sci U S A. 1983 Jan;80(2):492–495. doi: 10.1073/pnas.80.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Reilly J. G., Thomas C. A., Jr Length polymorphisms, restriction site variation, and maternal inheritance of mitochondrial DNA of Drosophila melanogaster. Plasmid. 1980 Mar;3(2):109–115. doi: 10.1016/0147-619x(80)90102-x. [DOI] [PubMed] [Google Scholar]
  33. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  34. Slott E. F., Jr, Shade R. O., Lansman R. A. Sequence analysis of mitochondrial DNA in a mouse cell line resistant to chloramphenicol and oligomycin. Mol Cell Biol. 1983 Oct;3(10):1694–1702. doi: 10.1128/mcb.3.10.1694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Solignac M., Monnerot M., Mounolou J. C. Mitochondrial DNA evolution in the melanogaster species subgroup of Drosophila. J Mol Evol. 1986;23(1):31–40. doi: 10.1007/BF02100996. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  38. Takahata N. Introgression of extranuclear genomes in finite populations: nucleo-cytoplasmic incompatibility. Genet Res. 1985 Apr;45(2):179–194. doi: 10.1017/s0016672300022102. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Takahata N., Slatkin M. Mitochondrial gene flow. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1764–1767. doi: 10.1073/pnas.81.6.1764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Wallace D. C. Assignment of the chloramphenicol resistance gene to mitochondrial deoxyribonucleic acid and analysis of its expression in cultured human cells. Mol Cell Biol. 1981 Aug;1(8):697–710. doi: 10.1128/mcb.1.8.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Wolstenholme D. R., Clary D. O. Sequence evolution of Drosophila mitochondrial DNA. Genetics. 1985 Apr;109(4):725–744. doi: 10.1093/genetics/109.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES