Genetics, Vol 138, 741-756, Copyright © 1994

INVESTIGATIONS

Neutral and Non-Neutral Evolution of Drosophila Mitochondrial DNA

D. M. Rand, M. Dorfsman and L. M. Kann
Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912

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.

This article has been cited by other articles:

				T. K. Johnson, S. W. McKechnie, and D. J. Clancy Water balance and cation levels in Drosophila: can early physiological decline predict aging and longevity? J. Gerontol. A Biol. Sci. Med. Sci., February 1, 2006; 61(2): 146 - 152. [Abstract] [Full Text] [PDF]

				S. Breton, G. Burger, D. T. Stewart, and P. U. Blier Comparative Analysis of Gender-Associated Complete Mitochondrial Genomes in Marine Mussels (Mytilus spp.) Genetics, February 1, 2006; 172(2): 1107 - 1119. [Abstract] [Full Text] [PDF]

				D. M. Rand, A. Fry, and L. Sheldahl Nuclear-Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds Genetics, January 1, 2006; 172(1): 329 - 341. [Abstract] [Full Text] [PDF]

				A. Llopart, D. Lachaise, and J. A. Coyne Multilocus Analysis of Introgression Between Two Sympatric Sister Species of Drosophila: Drosophila yakuba and D. santomea Genetics, September 1, 2005; 171(1): 197 - 210. [Abstract] [Full Text] [PDF]

				Z. Gu, L. David, D. Petrov, T. Jones, R. W. Davis, and L. M. Steinmetz Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae PNAS, January 25, 2005; 102(4): 1092 - 1097. [Abstract] [Full Text] [PDF]

				J. W. O. Ballard Sequential Evolution of a Symbiont Inferred From the Host: Wolbachia and Drosophila simulans Mol. Biol. Evol., March 1, 2004; 21(3): 428 - 442. [Abstract] [Full Text] [PDF]

				J. T. Herbeck, D. J. Funk, P. H. Degnan, and J. J. Wernegreen A Conservative Test of Genetic Drift in the Endosymbiotic Bacterium Buchnera: Slightly Deleterious Mutations in the Chaperonin groEL Genetics, December 1, 2003; 165(4): 1651 - 1660. [Abstract] [Full Text] [PDF]

				M. D. Dean, K. J. Ballard, A. Glass, and J. W. O. Ballard Influence of Two Wolbachia Strains on Population Structure of East African Drosophila simulans Genetics, December 1, 2003; 165(4): 1959 - 1969. [Abstract] [Full Text] [PDF]

				A. Navarro-Sabate, M. Aguade, and C. Segarra Excess of Nonsynonymous Polymorphism at Acph-1 in Different Gene Arrangements of Drosophila subobscura Mol. Biol. Evol., November 1, 2003; 20(11): 1833 - 1843. [Abstract] [Full Text] [PDF]

				P. D. Gavino and W. E. Fry Diversity in and evidence for selection on the mitochondrial genome of Phytophthora infestans Mycologia, September 1, 2002; 94(5): 781 - 793. [Abstract] [Full Text] [PDF]

				D. M. Rand, A. G. Clark, and L. M. Kann Sexually Antagonistic Cytonuclear Fitness Interactions in Drosophila melanogaster Genetics, September 1, 2001; 159(1): 173 - 187. [Abstract] [Full Text] [PDF]

				A. Munte, M. Aguade, and C. Segarra Changes in the Recombinational Environment Affect Divergence in the yellow Gene of Drosophila Mol. Biol. Evol., June 1, 2001; 18(6): 1045 - 1056. [Abstract] [Full Text]

				B. C. Verrelli and W. F. Eanes Extensive Amino Acid Polymorphism at the Pgm Locus Is Consistent With Adaptive Protein Evolution in Drosophila melanogaster Genetics, December 1, 2000; 156(4): 1737 - 1752. [Abstract] [Full Text]

				D. M. Weinreich and D. M. Rand Contrasting Patterns of Nonneutral Evolution in Proteins Encoded in Nuclear and Mitochondrial Genomes Genetics, September 1, 2000; 156(1): 385 - 399. [Abstract] [Full Text]

				A. Navarro-Sabate, M. Aguade, and C. Segarra The Relationship Between Allozyme and Chromosomal Polymorphism Inferred From Nucleotide Variation at the Acph-1 Gene Region of Drosophila subobscura Genetics, October 1, 1999; 153(2): 871 - 889. [Abstract] [Full Text] [PDF]

				M. T. Hamblin and M. Veuille Population Structure Among African and Derived Populations of Drosophila simulans: Evidence for Ancient Subdivision and Recent Admixture Genetics, September 1, 1999; 153(1): 305 - 317. [Abstract] [Full Text]

				R. Nielsen and D. M. Weinreich The Age of Nonsynonymous and Synonymous Mutations in Animal mtDNA and Implications for the Mildly Deleterious Theory Genetics, September 1, 1999; 153(1): 497 - 506. [Abstract] [Full Text]

				H. Akashi Inferring the Fitness Effects of DNA Mutations From Polymorphism and Divergence Data: Statistical Power to Detect Directional Selection Under Stationarity and Free Recombination Genetics, January 1, 1999; 151(1): 221 - 238. [Abstract] [Full Text]

				S. D. Irvin, K. A. Wetterstrand, C. M. Hutter, and C. F. Aquadro Genetic Variation and Differentiation at Microsatellite Loci in Drosophila simulans: Evidence for Founder Effects in New World Populations Genetics, October 1, 1998; 150(2): 777 - 790. [Abstract] [Full Text]

				P. Kennedy and M. W. Nachman Deleterious Mutations at the Mitochondrial ND3 Gene in South American Marsh Rats (Holochilus) Genetics, September 1, 1998; 150(1): 359 - 368. [Abstract] [Full Text] [PDF]

				J. Garcia-Martinez, J. A. Castro, M. Ramon, A. Latorre, and A. Moya Mitochondrial DNA Haplotype Frequencies in Natural and Experimental Populations of Drosophila subobscura Genetics, July 1, 1998; 149(3): 1377 - 1382. [Abstract] [Full Text] [PDF]

				H. Quesada, M. Warren, and D. O. F. Skibinski Nonneutral Evolution and Differential Mutation Rate of Gender-Associated Mitochondrial DNA Lineages in the Marine Mussel Mytilus Genetics, July 1, 1998; 149(3): 1511 - 1526. [Abstract] [Full Text] [PDF]

				Departure from Neutrality at the Mitochondrial NADH Dehydrogenase Subunit 2 Gene in Humans, but Not in Chimpanzees Genetics, January 1, 1998; 148(1): 409 - 422.