Abstract
To test hypotheses of neutral evolution of mitochondrial DNA (mtDNA), nucleotide sequences were determined for 1515 base pairs of the NADH dehydrogenase subunit 5 (ND5) gene in the mitochondrial DNA of 29 lines of Drosophila melanogaster and 9 lines of its sibling species Drosophila simulans. In contrast to the patterns for nuclear genes, where D. melanogaster generally exhibits much less nucleotide polymorphism, the number of segregating sites was slightly higher in a global sample of nine ND5 sequences in D. melanogaster (s = 8) than in the nine lines of D. simulans (s = 6). When compared to variation at nuclear loci, the mtDNA variation in D. melanogaster does not depart from neutral expectations. The ND5 sequences in D. simulans, however, show fewer than half the number of variable sites expected under neutrality when compared to sequences from the period locus. While this reduction in variation is not significant at the 5% level, HKA tests with published restriction data for mtDNA in D. simulans do show a significant reduction of variation suggesting a selective sweep of variation in the mtDNA in this species. Tests of neutral evolution based on the ratios of synonymous and replacement polymorphism and divergence are generally consistent with neutral expectations, although a significant excess of amino acid polymorphism within both species is localized in one region of the protein. The rate of mtDNA evolution has been faster in D. melanogaster than in D. simulans and the population structure of mtDNA is distinct in these species. The data reveal how different rates of mtDNA evolution between species and different histories of neutral and adaptive evolution within species can compromise historical inferences in population and evolutionary biology.
Full Text
The Full Text of this article is available as a PDF (1.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- ATWOOD K. C., SCHNEIDER L. K., RYAN F. J. Selective mechanisms in bacteria. Cold Spring Harb Symp Quant Biol. 1951;16:345–355. doi: 10.1101/sqb.1951.016.01.026. [DOI] [PubMed] [Google Scholar]
- Aguade M., Miyashita N., Langley C. H. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989 Jul;122(3):607–615. doi: 10.1093/genetics/122.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
- Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
- Begun D. J., Aquadro C. F. Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking of the yellow-achaete region. Genetics. 1991 Dec;129(4):1147–1158. doi: 10.1093/genetics/129.4.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berry A. J., Ajioka J. W., Kreitman M. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics. 1991 Dec;129(4):1111–1117. doi: 10.1093/genetics/129.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cann R. L., Stoneking M., Wilson A. C. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. doi: 10.1038/325031a0. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeSalle R., Freedman T., Prager E. M., Wilson A. C. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol. 1987;26(1-2):157–164. doi: 10.1007/BF02111289. [DOI] [PubMed] [Google Scholar]
- 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]
- Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaneko M., Satta Y., Matsuura E. T., Chigusa S. I. Evolution of the mitochondrial ATPase 6 gene in Drosophila: unusually high level of polymorphism in D. melanogaster. Genet Res. 1993 Jun;61(3):195–204. doi: 10.1017/s0016672300031360. [DOI] [PubMed] [Google Scholar]
- Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kondo R., Satta Y., Matsuura E. T., Ishiwa H., Takahata N., Chigusa S. I. Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics. 1990 Nov;126(3):657–663. doi: 10.1093/genetics/126.3.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kreitman M., Landweber L. F. A strategy for producing single-stranded DNA in the polymerase chain reaction. A direct method for genomic sequencing. Gene Anal Tech. 1989 Jul-Aug;6(4):84–88. doi: 10.1016/0735-0651(89)90021-6. [DOI] [PubMed] [Google Scholar]
- Martín-Campos J. M., Comerón J. M., Miyashita N., Aguadé M. Intraspecific and interspecific variation at the y-ac-sc region of Drosophila simulans and Drosophila melanogaster. Genetics. 1992 Apr;130(4):805–816. doi: 10.1093/genetics/130.4.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
- Rousset F., Vautrin D., Solignac M. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc Biol Sci. 1992 Mar 23;247(1320):163–168. doi: 10.1098/rspb.1992.0023. [DOI] [PubMed] [Google Scholar]
- 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]
- Satta Y., Takahata N. Evolution of Drosophila mitochondrial DNA and the history of the melanogaster subgroup. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9558–9562. doi: 10.1073/pnas.87.24.9558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaeffer S. W., Miller E. L. Molecular population genetics of an electrophoretically monomorphic protein in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics. 1992 Sep;132(1):163–178. doi: 10.1093/genetics/132.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp P. M., Li W. H. On the rate of DNA sequence evolution in Drosophila. J Mol Evol. 1989 May;28(5):398–402. doi: 10.1007/BF02603075. [DOI] [PubMed] [Google Scholar]
- Sheen J. Y., Seed B. Electrolyte gradient gels for DNA sequencing. Biotechniques. 1988 Nov-Dec;6(10):942–944. [PubMed] [Google Scholar]
- Singh R. S., Rhomberg L. R. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. II. Estimates of Heterozygosity and Patterns of Geographic Differentiation. Genetics. 1987 Oct;117(2):255–271. doi: 10.1093/genetics/117.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
- 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]
- Tajima F. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics. 1993 Oct;135(2):599–607. doi: 10.1093/genetics/135.2.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol. 1992 Jul;9(4):678–687. doi: 10.1093/oxfordjournals.molbev.a040752. [DOI] [PubMed] [Google Scholar]
- Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
- 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]