Abstract
It is well established on theoretical grounds that the accumulation of mildly deleterious mutations in nonrecombining genomes is a major extinction risk in obligately asexual populations. Sexual populations can also incur mutational deterioration in genomic regions that experience little or no recombination, i.e., autosomal regions near centromeres, Y chromosomes, and organelle genomes. Our results suggest, for a wide array of genes (transfer RNAs, ribosomal RNAs, and proteins) in a diverse collection of species (animals, plants, and fungi), an almost universal increase in the fixation probabilities of mildly deleterious mutations arising in mitochondrial and chloroplast genomes relative to those arising in the recombining nuclear genome. This enhanced width of the selective sieve in organelle genomes does not appear to be a consequence of relaxed selection, but can be explained by the decline in the efficiency of selection that results from the reduction of effective population size induced by uniparental inheritance. Because of the very low mutation rates of organelle genomes (on the order of 10−4 per genome per year), the reduction in fitness resulting from mutation accumulation in such genomes is a very long-term process, not likely to imperil many species on time scales of less than a million years, but perhaps playing some role in phylogenetic lineage sorting on time scales of 10 to 100 million years.
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References
Ballard, J.W.O. & M. Kreitman, 1994. Unraveling selection in the mitochondrial genome of Drosophila. Genetics 138: 757–772.
Birky, C.W., Jr., 1995. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl. Acad. Sci. USA 92: 11331–11338.
Birky, C.W., Jr. & J.B. Walsh, 1988. Effects of linkage on rates of molecular evolution. Proc. Natl. Acad. Sci. USA 85: 6414–6418.
Brown, W.M., E.M. Prager, A. Wang & A.C. Wilson, 1982. Mito chondrial DNA sequences of primates: tempo and mode of evolution. J. Mol. Evol. 18: 225–239.
Chao, L., 1990. Fitness of RNA virus decreased by Muller’s ratchet. Nature 348: 454–455.
Charlesworth, D., M.T. Morgan & B. Charlesworth., 1993. Mutation accumulation in finite outbreeding and inbreeding populations. Genet. Res. 61: 39–56.
Comeron, J.M., 1995. A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J. Mol. Evol. 41: 1152–1159.
Crow, J.F. & M. Kimura, 1970. An Introduction to Population Genetics Theory. Harper and Row, New York.
De Rijk, P., Y. Van de Peer & R. De Wachter, 1997. Database on the structure of large ribosomal subunit RNA. Nucl. Acids Res. 25: 117–122.
De Rijk, P. & R. De Wachter, 1993. DCSE, an interactive tool for sequence alignment and secondary structure research. Comput. Appl. Biosci. 9: 735–740.
Duarte, E.A., I.S. Novella, S. Ledesma, D.K. Clarke, A. Moya, S.F. Elena, E. Domingo & J.J. Holland, 1994. Subclonal components of consensus fitness in an RNA virus clone. J. Virol. 68: 4295–4301.
Easteal, S. & C. Collet, 1994. Consistent variation in amino-acid substitution rate, despite uniformity of mutation rate: protein evolution in mammals is not neutral. Mol. Biol. Evol. 11: 643–647.
Escarmis, C.M. Davila, N. Charpentier, A. Bracho, A. Moya & E. Domingo, 1996. Genetic lesions associated with Muller’s ratchet in an RNA virus. J. Mol. Biol. 264: 255–267.
Felsenstein, J., 1974. The evolutionary advantage of recombination. Genetics 78: 737–756.
Gabriel, W., M. Lynch & R. Bürger, 1993. Muller’s ratchet and mutational meltdowns. Evolution 47: 1744–1757.
Gessler, D.D.G., 1996. The constraints of finite size in asexual pop ulations and the rate of the ratchet. Genet. Res. 66: 241–253.
Gillham, N.W., 1995. Organelle Genes and Genomes. Oxford Univ. Press, New York.
Haigh, J., 1978. The accumulation of deleterious genes in a popula tion. Theor. Pop. Biol. 14: 251–267.
Hastings, I.M., 1992. Population genetic aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual repro duction. Genet. Res. 59: 215–225.
Higgins, D.E. & P.M. Sharp, 1989. Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5: 151–153.
Higgs, P.G., 1994. Error thresholds and stationary mutant distrib utions in multi-locus diploid genetics models. Genet. Res. 63: 63–78.
Hill, W.G. & A. Robertson, 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8: 269–294.
Holland, P.W.H., J. Garcia-Fernandez, N.A. Williams & A. Sidow, 1994. Gene duplications and the origins of vertebrate development. Devel. Suppl. 125–133.
Keightley, P.D., 1994. The distribution of mutation effects on viability in D. melanogaster. Genetics 138: 1315–1322.
Keightley, P.D. & A. Caballero, 1997. Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 94: 3823–3827.
Kibota, T.T. & M. Lynch, 1996. Estimate of the genomic mutation rate deleterious to overall fitness in Escherichia coli. Nature 381: 694–696.
Kumar, S., K. Tamura & M. Nei, 1993. MEGA: Molecular evolutionary Genetics Analysis, Version 1.01. Penn. State Univ., University Park, PA.
Kumazawa, Y. & M. Nishida, 1993. Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J. Mol. Evol. 37: 380–398.
Lande, R., 1994. Risk of population extinction from new deleterious mutations. Evolution 48: 1460–1469.
Li, W.-H. & D. Graur, 1991. Fundamentals of Molecular Evolution. Sinauer Assocs., Sunderland, MA.
Lunt, D.H. & B.C. Hyman, 1997. Animal mitochondrial DNA recombination. Nature 387: 247.
Lynch, M., 1996. Mutation accumulation in transfer RNAs: molecu lar evidence for Muller’s ratchet in mitochondrial genomes. Mol. Biol. Evol. 13: 209–220.
Lynch, M., 1997. Mutation accumulation in nuclear, organelle, and prokaryotic transfer RNA genes. Mol. Biol. Evol. 14: 914–925.
Lynch, M., R. Bürger, D. Butcher & W. Gabriel, 1993. The muta tional meltdown in asexual populations. J. Heredity 84: 339–344.
Lynch, M., J. Conery & R. Bürger, 1995a. Mutational meltdowns in sexual populations. Evolution 49: 1067–1080.
Lynch, M., J. Conery & R. Bürger, 1995b. Mutation accumulation and the extinction of small populations. Amer. Nat. 146: 489–518.
Lynch, M. & W. Gabriel, 1990. Mutation load and the survival of small populations. Evolution 44: 1725–1737.
Lynch, M. & J.B. Walsh, 1998. Genetics and Analysis of Quantitative Traits. Sinauer Assocs., Inc., Sunderland, MA.
Moran, N.A., 1996. Accelerated evolution and Muller’s ratchet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 96: 2873–2878.
Muller, H.J., 1964. The relation of recombination to mutational advance. Mut. Res. 1: 2–9.
Nachman, M.W., S.N. Boyer & C.F. Aquadro, 1994. Non-neutral evolution at the mitochondrial ND3 gene in mice. Proc. Natl. Acad. Sci. USA 91: 6364–6368.
Nachman, M.W., W.M. Brown, M. Stoneking & C.F. Aquadro, 1996. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142: 953–963.
Nei, M. & T. Gojobori, 1986. Simple methods for estimating the numbers of synonymous and nonsynonomous nucleotide substi tutions. Mol. Biol. Evol. 3: 418–426.
Ohta, T., 1995. Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory. J. Mol. Evol. 40: 56–63.
Pamilo, P., M. Nei & W.-H. Li, 1987. Accumulation of mutations in sexual and asexual populations. Genet. Res. 49: 135–146.
Rand, D.M., M. Dorfsman & L.M. Kann, 1994. Neutral and nonneutral evolution of Drosophila mitochondrial DNA. Genetics 138: 741–756.
Rand, D.M. & L.M. Kann, 1996. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol. Biol. Evol. 13: 735–748.
Rice, W.R., 1994. Degeneration of a nonrecombining chromosome. Science 263: 230–232.
Schultz, S.T. & M. Lynch, 1997. Deleterious mutation and extinc tion: effects of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing. Evolution 51: 1363–1371.
Shoubridge, E.A., 1994. Mitochondrial DNA diseases: histological and cellular studies. J. Bioenerg. Biomem. 26: 301–310.
Simmons, M.J. & J.F. Crow, 1977. Mutations affecting fitness in Drosophila populations. Ann. Rev. Genet. 11: 49–78.
Söll, D. & U.L. RajBhandary, 1995. tRNA: structure, biosynthesis, and function. ASM Press, Washington, D.C
Stephan, W., L. Chao & J.G. Smale, 1993. The advance of Muller’s ratchet in a haploid asexual population: approximate solutions based on diffusion theory. Genet. Res. 61: 225–231.
Tajima, F., 1993. Unbiased estimation of evolutionary distance between nucleotide sequences. Mol. Biol. Evol. 10: 677–688.
Takahata, N. & M. Slatkin, 1983. Evolutionary dynamics of extranuclear genes. Genet. Res. 42: 257–265.
Thompson, J.D., D.G. Higgins & T.J. Gibson, 1994. Clustal-W: improving the sensitivity of practical multiple sequence align ment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.
Van de Peer, Y, J. Jansen, P. De Rijk & R. De Wachter, 1997. Database on the structure of small ribosomal subunit RNA. Nucl. Acids Res. 25: 111–116.
Wallace, D.C., 1992. Diseases of the mitochondrial DNA. Annu. Rev. Biochem. 61: 1175–1212.
Wallace, D.C., 1994. Mitochondrial DNA mutations in diseases of energy metabolism. J. Bioenerg. Biomem. 26: 241–1250.
Wolstenholme, D.R. & K.W. Jeon (eds.), 1992. Mitochondrial Genomes. Academic Press, New York.
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Lynch, M., Blanchard, J.L. (1998). Deleterious mutation accumulation in organelle genomes. In: Woodruff, R.C., Thompson, J.N. (eds) Mutation and Evolution. Contemporary Issues in Genetics and Evolution, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5210-5_3
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DOI: https://doi.org/10.1007/978-94-011-5210-5_3
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