Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Jun 7;271(1544):1197–1201. doi: 10.1098/rspb.2004.2709

Differential fitness of mitochondrial DNA in perturbation cage studies correlates with global abundance and population history in Drosophila simulans.

J William O Ballard 1, Avis C James 1
PMCID: PMC1691713  PMID: 15306370

Abstract

Mitochondria are often referred to as the powerhouse of the cell. However, research linking intraspecific differences in organismal fitness with genotypic mitochondrial DNA (mtDNA) variation has been hampered by the lack of variation in experimentally tractable species. This study examines whether fly lines harbouring three distinct Drosophila simulans mtDNA types (siI, -II and -III) exhibit differential fitness in laboratory perturbation cages. Comparison of the pre-perturbation and post-perturbation data shows that both the mtDNA and mitonuclear interactions have a significant and repeatable effect on the frequency of flies with specific genotypes in population cages (siII > -III > -I) and that coadapted mitonuclear interactions are greatest in the siI type. The rank order of mtDNA frequency correlates with the observed worldwide distribution of the haplogroups while mitonuclear interactions are most significant in the siI haplogroup that is likely to have been subject to repeated population bottlenecks. One possible explanation for the maintenance of the least fit siI haplogroup on Pacific islands is that it is protected from extinction by Wolbachia infection.

Full Text

The Full Text of this article is available as a PDF (147.5 KB).

Selected References

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

  1. Arnason E. Perturbation-reperturbation test of selection vs. hitchhiking of the two major alleles of Esterase-5 in Drosophila pseudoobscura. Genetics. 1991 Sep;129(1):145–168. doi: 10.1093/genetics/129.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. doi: 10.1146/annurev.cb.04.110188.001445. [DOI] [PubMed] [Google Scholar]
  3. Baba-Aïssa F., Solignac M., Dennebouy N., David J. R. Mitochondrial DNA variability in Drosophila simulans: quasi absence of polymorphism within each of the three cytoplasmic races. Heredity (Edinb) 1988 Dec;61(Pt 3):419–426. doi: 10.1038/hdy.1988.133. [DOI] [PubMed] [Google Scholar]
  4. Ballard J. W. Comparative genomics of mitochondrial DNA in Drosophila simulans. J Mol Evol. 2000 Jul;51(1):64–75. doi: 10.1007/s002390010067. [DOI] [PubMed] [Google Scholar]
  5. Ballard J. W., Kreitman M. Unraveling selection in the mitochondrial genome of Drosophila. Genetics. 1994 Nov;138(3):757–772. doi: 10.1093/genetics/138.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ballard J. William O., Chernoff Barry, James Avis C. Divergence of mitochondrial dna is not corroborated by nuclear dna, morphology, or behavior in Drosophila simulans. Evolution. 2002 Mar;56(3):527–545. doi: 10.1111/j.0014-3820.2002.tb01364.x. [DOI] [PubMed] [Google Scholar]
  7. Ballard J. William O. Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol Biol Evol. 2003 Dec 5;21(3):428–442. doi: 10.1093/molbev/msh028. [DOI] [PubMed] [Google Scholar]
  8. Clayton D. A., Teplitz R. L., Nabholz M., Dovey H., Bodmer W. Mitochondrial DNA of human-mouse cell hybrids. Nature. 1971 Dec 31;234(5331):560–562. doi: 10.1038/234560a0. [DOI] [PubMed] [Google Scholar]
  9. De Stordeur E. Nonrandom partition of mitochondria in heteroplasmic Drosophila. Heredity (Edinb) 1997 Dec;79(Pt 6):615–623. doi: 10.1038/hdy.1997.207. [DOI] [PubMed] [Google Scholar]
  10. Dean Matthew D., Ballard Kirrie J., Glass Anne, Ballard J. William O. Influence of two Wolbachia strains on population structure of East African Drosophila simulans. Genetics. 2003 Dec;165(4):1959–1969. doi: 10.1093/genetics/165.4.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936 Mar;21(2):113–135. doi: 10.1093/genetics/21.2.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fos M., Domínguez M. A., Latorre A., Moya A. Mitochondrial DNA evolution in experimental populations of Drosophila subobscura. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4198–4201. doi: 10.1073/pnas.87.11.4198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hutter C. M., Rand D. M. Competition between mitochondrial haplotypes in distinct nuclear genetic environments: Drosophila pseudoobscura vs. D. persimilis. Genetics. 1995 Jun;140(2):537–548. doi: 10.1093/genetics/140.2.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. James A. C., Ballard J. W. Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evolution. 2000 Oct;54(5):1661–1672. doi: 10.1111/j.0014-3820.2000.tb00710.x. [DOI] [PubMed] [Google Scholar]
  15. James Avis C., Ballard J. William O. Mitochondrial genotype affects fitness in Drosophila simulans. Genetics. 2003 May;164(1):187–194. doi: 10.1093/genetics/164.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jenkins T. M., Babcock C. S., Geiser D. M., Anderson W. W. Cytoplasmic incompatibility and mating preference in Colombian Drosophila pseudoobscura. Genetics. 1996 Jan;142(1):189–194. doi: 10.1093/genetics/142.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kilpatrick S. T., Rand D. M. Conditional hitchhiking of mitochondrial DNA: frequency shifts of Drosophila melanogaster mtDNA variants depend on nuclear genetic background. Genetics. 1995 Nov;141(3):1113–1124. doi: 10.1093/genetics/141.3.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. MacRae A. F., Anderson W. W. Can mating preferences explain changes in mtDNA haplotype frequencies? Genetics. 1990 Apr;124(4):999–1001. doi: 10.1093/genetics/124.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Mishmar Dan, Ruiz-Pesini Eduardo, Golik Pawel, Macaulay Vincent, Clark Andrew G., Hosseini Seyed, Brandon Martin, Easley Kirk, Chen Estella, Brown Michael D. Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci U S A. 2002 Dec 30;100(1):171–176. doi: 10.1073/pnas.0136972100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Montchamp-Moreau C., Ferveur J. F., Jacques M. Geographic distribution and inheritance of three cytoplasmic incompatibility types in Drosophila simulans. Genetics. 1991 Oct;129(2):399–407. doi: 10.1093/genetics/129.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nigro L. Nuclear background affects frequency dynamics of mitochondrial DNA variants in Drosophila simulans. Heredity (Edinb) 1994 Jun;72(Pt 6):582–586. doi: 10.1038/hdy.1994.80. [DOI] [PubMed] [Google Scholar]
  24. Rand D. M., Clark A. G., Kann L. M. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics. 2001 Sep;159(1):173–187. doi: 10.1093/genetics/159.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rand D. M., Dorfsman M., Kann L. M. Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics. 1994 Nov;138(3):741–756. doi: 10.1093/genetics/138.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roubertoux Pierre L., Sluyter Frans, Carlier Michèle, Marcet Brice, Maarouf-Veray Fatima, Chérif Chabane, Marican Charlotte, Arrechi Patricia, Godin Fabienne, Jamon Marc. Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nat Genet. 2003 Aug 17;35(1):65–69. doi: 10.1038/ng1230. [DOI] [PubMed] [Google Scholar]
  27. Ruiz-Pesini Eduardo, Mishmar Dan, Brandon Martin, Procaccio Vincent, Wallace Douglas C. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science. 2004 Jan 9;303(5655):223–226. doi: 10.1126/science.1088434. [DOI] [PubMed] [Google Scholar]
  28. Singh R. S., Hale L. R. Are mitochondrial DNA variants selectively non-neutral? Genetics. 1990 Apr;124(4):995–997. doi: 10.1093/genetics/124.4.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tram Uyen, Sullivan William. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science. 2002 May 10;296(5570):1124–1126. doi: 10.1126/science.1070536. [DOI] [PubMed] [Google Scholar]
  30. Turelli M., Hoffmann A. A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics. 1995 Aug;140(4):1319–1338. doi: 10.1093/genetics/140.4.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Willett Christopher S., Burton Ronald S. Environmental influences on epistatic interactions: viabilities of cytochrome c genotypes in interpopulation crosses. Evolution. 2003 Oct;57(10):2286–2292. doi: 10.1111/j.0014-3820.2003.tb00240.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES