Unraveling Selection in the Mitochondrial Genome of Drosophila

INVESTIGATIONS

Unraveling Selection in the Mitochondrial Genome of Drosophila

JWO. Ballard and M. Kreitman
Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, and CSIRO Division of Entomology, Canberra, ACT 2601, Australia

We examine mitochondrial DNA variation at the cytochrome b locus within and between three species of Drosophila to determine whether patterns of variation conform to the predictions of neutral molecular evolution. The entire 1137-bp cytochrome b locus was sequenced in 16 lines of Drosophila melanogaster, 18 lines of Drosophila simulans and 13 lines of Drosophila yakuba. Patterns of variation depart from neutrality by several test criteria. Analysis of the evolutionary clock hypothesis shows unequal rates of change along D. simulans lineages. A comparison within and between species of the ratio of amino acid replacement change to synonymous change reveals a relative excess of amino acid replacement polymorphism compared to the neutral prediction, suggestive of slightly deleterious or diversifying selection. There is evidence for excess homozygosity in our world wide sample of D. melanogaster and D. simulans alleles, as well as a reduction in the number of segregating sites in D. simulans, indicative of selective sweeps. Furthermore, a test of neutrality for codon usage shows the direction of mutations at third positions differs among different topological regions of the gene tree. The analyses indicate that molecular variation and evolution of mtDNA are governed by many of the same selective forces that have been shown to govern nuclear genome evolution and suggest caution be taken in the use of mtDNA as a ``neutral'' molecular marker.

This article has been cited by other articles:

R. E. Broughton and P. C. Reneau
Spatial Covariation of Mutation and Nonsynonymous Substitution Rates in Vertebrate Mitochondrial Genomes
Mol. Biol. Evol., August 1, 2006; 23(8): 1516 - 1524.
[Abstract] [Full Text] [PDF]

B. C. Verrelli, S. A. Tishkoff, A. C. Stone, and J. W. Touchman
Contrasting Histories of G6PD Molecular Evolution and Malarial Resistance in Humans and Chimpanzees
Mol. Biol. Evol., August 1, 2006; 23(8): 1592 - 1601.
[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]

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]

E. Arnason
Mitochondrial Cytochrome b DNA Variation in the High-Fecundity Atlantic Cod: Trans-Atlantic Clines and Shallow Gene Genealogy
Genetics, April 1, 2004; 166(4): 1871 - 1885.
[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]

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]

Y.-w. Zhang, O. A. Ryder, and Y.-p. Zhang
Intra- and Interspecific Variation of the CCR5 Gene in Higher Primates
Mol. Biol. Evol., October 1, 2003; 20(10): 1722 - 1729.
[Abstract] [Full Text]

Y.-C. Chiang, B. A. Schaal, C.-H. Chou, S. Huang, and T.-Y. Chiang
Contrasting selection modes at the Adh1 locus in outcrossing Miscanthus sinensis vs. inbreeding Miscanthus condensatus (Poaceae)
Am. J. Botany, April 1, 2003; 90(4): 561 - 570.
[Abstract] [Full Text] [PDF]

D. R. Denver, K. Morris, and W. K. Thomas
Phylogenetics in Caenorhabditis elegans: An Analysis of Divergence and Outcrossing
Mol. Biol. Evol., March 1, 2003; 20(3): 393 - 400.
[Abstract] [Full Text] [PDF]

S. Doiron, L. Bernatchez, and P. U. Blier
A Comparative Mitogenomic Analysis of the Potential Adaptive Value of Arctic Charr mtDNA Introgression in Brook Charr Populations (Salvelinus fontinalis Mitchill)
Mol. Biol. Evol., November 1, 2002; 19(11): 1902 - 1909.
[Abstract] [Full Text] [PDF]

J. F. Baines, Y. Chen, A. Das, and W. Stephan
DNA Sequence Variation at a Duplicated Gene: Excess of Replacement Polymorphism and Extensive Haplotype Structure in the Drosophila melanogasterbicoid Region
Mol. Biol. Evol., July 1, 2002; 19(7): 989 - 998.
[Abstract] [Full Text] [PDF]

D. Posada
Evaluation of Methods for Detecting Recombination from DNA Sequences: Empirical Data
Mol. Biol. Evol., May 1, 2002; 19(5): 708 - 717.
[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
Clinal Variation for Amino Acid Polymorphisms at the Pgm Locus in Drosophila melanogaster
Genetics, April 1, 2001; 157(4): 1649 - 1663.
[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. Llopart and M. Aguadé
Nucleotide Polymorphism at the RpII215 Gene in Drosophila subobscura: Weak Selection on Synonymous Mutations
Genetics, July 1, 2000; 155(3): 1245 - 1252.
[Abstract] [Full Text]

G. A. T. McVean and B. Charlesworth
The Effects of Hill-Robertson Interference Between Weakly Selected Mutations on Patterns of Molecular Evolution and Variation
Genetics, June 1, 2000; 155(2): 929 - 944.
[Abstract] [Full Text]

M. Zurovcova and W. F. Eanes
Lack of Nucleotide Polymorphism in the Y-Linked Sperm Flagellar Dynein Gene Dhc-Yh3 of Drosophila melanogaster and D. simulans
Genetics, December 1, 1999; 153(4): 1709 - 1715.
[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]

A. Eyre-Walker
Evidence of Selection on Silent Site Base Composition in Mammals: Potential Implications for the Evolution of Isochores and Junk DNA
Genetics, June 1, 1999; 152(2): 675 - 683.
[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]

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]

M. D. Purugganan and J. I. Suddith
Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: Nonneutral evolution and naturally occurring variation in floral homeotic function
PNAS, July 7, 1998; 95(14): 8130 - 8134.
[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.

				B. C. Verrelli, S. A. Tishkoff, A. C. Stone, and J. W. Touchman Contrasting Histories of G6PD Molecular Evolution and Malarial Resistance in Humans and Chimpanzees Mol. Biol. Evol., August 1, 2006; 23(8): 1592 - 1601. [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]

				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]

				E. Arnason Mitochondrial Cytochrome b DNA Variation in the High-Fecundity Atlantic Cod: Trans-Atlantic Clines and Shallow Gene Genealogy Genetics, April 1, 2004; 166(4): 1871 - 1885. [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]

				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]

				Y.-w. Zhang, O. A. Ryder, and Y.-p. Zhang Intra- and Interspecific Variation of the CCR5 Gene in Higher Primates Mol. Biol. Evol., October 1, 2003; 20(10): 1722 - 1729. [Abstract] [Full Text]

				Y.-C. Chiang, B. A. Schaal, C.-H. Chou, S. Huang, and T.-Y. Chiang Contrasting selection modes at the Adh1 locus in outcrossing Miscanthus sinensis vs. inbreeding Miscanthus condensatus (Poaceae) Am. J. Botany, April 1, 2003; 90(4): 561 - 570. [Abstract] [Full Text] [PDF]

				D. R. Denver, K. Morris, and W. K. Thomas Phylogenetics in Caenorhabditis elegans: An Analysis of Divergence and Outcrossing Mol. Biol. Evol., March 1, 2003; 20(3): 393 - 400. [Abstract] [Full Text] [PDF]

				S. Doiron, L. Bernatchez, and P. U. Blier A Comparative Mitogenomic Analysis of the Potential Adaptive Value of Arctic Charr mtDNA Introgression in Brook Charr Populations (Salvelinus fontinalis Mitchill) Mol. Biol. Evol., November 1, 2002; 19(11): 1902 - 1909. [Abstract] [Full Text] [PDF]

				J. F. Baines, Y. Chen, A. Das, and W. Stephan DNA Sequence Variation at a Duplicated Gene: Excess of Replacement Polymorphism and Extensive Haplotype Structure in the Drosophila melanogasterbicoid Region Mol. Biol. Evol., July 1, 2002; 19(7): 989 - 998. [Abstract] [Full Text] [PDF]

				D. Posada Evaluation of Methods for Detecting Recombination from DNA Sequences: Empirical Data Mol. Biol. Evol., May 1, 2002; 19(5): 708 - 717. [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 Clinal Variation for Amino Acid Polymorphisms at the Pgm Locus in Drosophila melanogaster Genetics, April 1, 2001; 157(4): 1649 - 1663. [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. Llopart and M. Aguadé Nucleotide Polymorphism at the RpII215 Gene in Drosophila subobscura: Weak Selection on Synonymous Mutations Genetics, July 1, 2000; 155(3): 1245 - 1252. [Abstract] [Full Text]

				G. A. T. McVean and B. Charlesworth The Effects of Hill-Robertson Interference Between Weakly Selected Mutations on Patterns of Molecular Evolution and Variation Genetics, June 1, 2000; 155(2): 929 - 944. [Abstract] [Full Text]

				M. Zurovcova and W. F. Eanes Lack of Nucleotide Polymorphism in the Y-Linked Sperm Flagellar Dynein Gene Dhc-Yh3 of Drosophila melanogaster and D. simulans Genetics, December 1, 1999; 153(4): 1709 - 1715. [Abstract] [Full Text]

				A. Eyre-Walker Evidence of Selection on Silent Site Base Composition in Mammals: Potential Implications for the Evolution of Isochores and Junk DNA Genetics, June 1, 1999; 152(2): 675 - 683. [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]

				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]

				M. D. Purugganan and J. I. Suddith Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: Nonneutral evolution and naturally occurring variation in floral homeotic function PNAS, July 7, 1998; 95(14): 8130 - 8134. [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.