Skip to main content
Genetics logoLink to Genetics
. 2003 May;164(1):187–194. doi: 10.1093/genetics/164.1.187

Mitochondrial genotype affects fitness in Drosophila simulans.

Avis C James 1, J William O Ballard 1
PMCID: PMC1462568  PMID: 12750331

Abstract

Drosophila simulans is known to harbor three distinct mitochondrial DNA (mtDNA) haplotype groups (siI, -II, and -III) with nearly 3.0% interhaplotypic divergence but <0.06% intrahaplotypic diversity. With the large amount of genetic variation in this system, the potential power to detect intraspecific fitness differences in fly lines that carry distinct haplotypes is great. We test three life-history traits on fly lines with known sequence differences in the mtDNA genome after controlling the nuclear genome by backcrossing. We find that flies with the siI haplotype are fastest developing and have the lowest probability of surviving to three experimental periods (2-6, 12-17, and 34-39 days of age). Wild-type males with siIII mtDNA were more active while disruption of specific coadapted nucleo-mitochondrial complexes caused a significant decrease in activity. These results are discussed in the context of the geographic distribution of each haplotype.

Full Text

The Full Text of this article is available as a PDF (92.3 KB).

Selected References

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

  1. 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]
  2. 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]
  3. 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]
  4. Clark A. G., Lyckegaard E. M. Natural selection with nuclear and cytoplasmic transmission. III. Joint analysis of segregation and mtDNA in Drosophila melanogaster. Genetics. 1988 Mar;118(3):471–481. doi: 10.1093/genetics/118.3.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Dermitzakis E. T., Masly J. P., Waldrip H. M., Clark A. G. Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics. 2000 Feb;154(2):687–694. doi: 10.1093/genetics/154.2.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Frank S. A., Hurst L. D. Mitochondria and male disease. Nature. 1996 Sep 19;383(6597):224–224. doi: 10.1038/383224a0. [DOI] [PubMed] [Google Scholar]
  9. García-Martínez J., Castro J. A., Ramón M., Latorre A., Moya A. Mitochondrial DNA haplotype frequencies in natural and experimental populations of Drosophila subobscura. Genetics. 1998 Jul;149(3):1377–1382. doi: 10.1093/genetics/149.3.1377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hercus M. J., Hoffmann A. A. Maternal and grandmaternal age influence offspring fitness in Drosophila. Proc Biol Sci. 2000 Oct 22;267(1457):2105–2110. doi: 10.1098/rspb.2000.1256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hiraizumi Y. Genetics of factors affecting the life history of Drosophila melanogaster. I. Female productivity. Genetics. 1985 Jul;110(3):452–464. [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. Matsuura E. T., Fukuda H., Chigusa S. I. Mitochondrial DNA heteroplasmy maintained in natural populations of Drosophila simulans in Réunion. Genet Res. 1991 Apr;57(2):123–126. doi: 10.1017/s0016672300029189. [DOI] [PubMed] [Google Scholar]
  18. Matsuura E. T., Niki Y., Chigusa S. I. Temperature-dependent selection in the transmission of mitochondrial DNA in Drosophila. Jpn J Genet. 1993 Apr;68(2):127–135. doi: 10.1266/jjg.68.127. [DOI] [PubMed] [Google Scholar]
  19. Merçot H., Llorente B., Jacques M., Atlan A., Montchamp-Moreau C. Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics. 1995 Nov;141(3):1015–1023. doi: 10.1093/genetics/141.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nagata Y., Matsuura E. T. Temperature-dependency of electron-transport activity in mitochondria with exogenous mitochondrial DNA in Drosophila. Jpn J Genet. 1991 Jun;66(3):255–261. doi: 10.1266/jjg.66.255. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Satta Y., Ishiwa H., Chigusa S. I. Analysis of nucleotide substitutions of mitochondrial DNAs in Drosophila melanogaster and its sibling species. Mol Biol Evol. 1987 Nov;4(6):638–650. doi: 10.1093/oxfordjournals.molbev.a040464. [DOI] [PubMed] [Google Scholar]
  24. Scheffler I. E. A century of mitochondrial research: achievements and perspectives. Mitochondrion. 2001 Jun;1(1):3–31. doi: 10.1016/s1567-7249(00)00002-7. [DOI] [PubMed] [Google Scholar]
  25. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  26. Tsujimoto Y., Niki Y., Matsuura E. T. Further study on selective transmission of mitochondrial DNA in heteroplasmic lines of Drosophila melanogaster. Jpn J Genet. 1991 Oct;66(5):609–616. doi: 10.1266/jjg.66.609. [DOI] [PubMed] [Google Scholar]
  27. de Benedictis G., Carrieri G., Varcasia O., Bonafè M., Franceschi C. Inherited variability of the mitochondrial genome and successful aging in humans. Ann N Y Acad Sci. 2000 Jun;908:208–218. doi: 10.1111/j.1749-6632.2000.tb06648.x. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES