Selection for mitonuclear co-adaptation could favour the evolution of two sexes

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1734, 2012, Pages 1865-1872

  Hadjivasiliou, Zena ^a   Pomiankowski, Andrew ^a   Seymour, Robert M ^a   Lane, Nick ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Biparental inheritance; Bottleneck; Mitochondria; Mitonuclear; Uniparental inheritance

Indexed keywords

ADAPTATION; BACTERIUM; COEVOLUTION; ECOLOGICAL MODELING; FITNESS; GENE EXPRESSION; GENOME; HERITABILITY; MATHEMATICAL ANALYSIS; MITOCHONDRIAL DNA; OXIDATION; POPULATION BOTTLENECK; SELECTION;

EID: 84858772121     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1871     Document Type: Article

References (34)

1. Keightley, P. D. & Otto, S. P. 2006 Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443, 89-92. (doi:10.1038/nature05049)
2. Parker, G. A., Smith, V. G. F. & Baker, R. R. 1972 Origin and evolution of gamete dimorphism and male-female phenomenon. J. Theor. Biol. 36, 529-553. (doi:10. 1016/0022-5193(72)90007-0)
3. Birky, C. W. 2001 The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu. Rev. Genet. 35, 125-148. (doi:10.1146/annurev. genet.35.102401.090231)
4. Kawano, S., Anderson, R. W., Nanba, T. & Kuroiwa, T. 1987 Polymorphism and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J. Gen. Microbiol. 133, 3175-3182.
5. Raper, J. R. 1966 Genetics of sexuality in higher fungi. New York, NY: Ronald Press Co.
6. Zouros, E., Ball, A. O., Saavedra, C. & Freeman, K. R. 1994 An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc. Natl Acad. Sci. USA 91, 7463-7467. (doi:10.1073/pnas.91.16.7463)
7. Cosmides, L. M. & Tooby, J. 1981 Cytoplasmic inheritance and intragenomic conflict. J. Theor. Biol. 89, 83-129. (doi:10.1016/0022-5193(81)90181-8)
8. Hurst, L. D. & Hamilton, W. D. 1992 Cytoplasmic fusion and the nature of sexes. Proc. R. Soc. Lond. B 247, 189-194. (doi:10.1098/rspb.1992.0027)
9. Hutson, V. & Law, R. 1993 Four steps to two sexes. Proc. R. Soc. Lond. B 253, 43-51. (doi:10.1098/rspb.1993.0080)
10. Hoekstra, R. F. 1982 On the asymmetry of sex: evolution of mating types in isogamous populations. J. Theor. Biol. 98, 427-451. (doi:10.1016/0022-5193(82)90129-1)
11. Birky, C. W. 1995 Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl Acad. Sci. USA 92, 11 331-11 338. (doi:10. 1073/pnas.92.25.11331)
12. Hoekstra, R. F. 2011 Nucleo-cytoplasmic conflict and the evolution of gamete dimorphism. In The evolution of anisogamy (eds T. Togashi & P. A. Cox), pp. 111-130. Cambridge, UK: Cambridge University Press.
13. Gray, M. W., Burger, G. & Lang, B. F. 1999 Mitochondrial evolution. Science 283, 1476-1481. (doi:10.1126/science.283.5407.1476)
14. Esser, C. et al. 2004 A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643-1660. (doi:10.1093/Molbev/Msh160)
15. Blier, P. U., Dufresne, F. & Burton, R. S. 2001 Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17, 400-406. (doi:10.1016/S0168-9525(01)02338-1)
16. Dowling, D. K., Friberg, U. & Lindell, J. 2008 Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol. Evol. 23, 546-554. (doi:10.1016/J.Tree.2008.05.011)
17. Lane, N. 2011 Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations. BioEssays 33, 860-869. (doi:10.1002/bies. 201100051)
18. Lane, N. 2011 Evolution. The costs of breathing. Science 334, 184-185. (doi:10.1126/science.1214012)
19. Lane, N. 2005 Power, sex, suicide: mitochondria and the meaning of life, vol. 8. Oxford, UK: Oxford University Press.
20. Adkins, R. M., Honeycutt, R. L. & Disotell, T. R. 1996 Evolution of eutherian cytochrome c oxidase subunit II: heterogeneous rates of protein evolution and altered interaction with cytochrome c. Mol. Biol. Evol. 13, 1393-1404.
21. Bergstrom, C. T. & Pritchard, J. 1998 Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics 149, 2135-2146.
22. Roze, D., Rousset, F. & Michalakis, Y. 2005 Germline bottlenecks, biparental inheritance and selection on mitochondrial variants: a two-level selection model. Genetics 170, 1385-1399. (doi:10.1534/genetics.104. 039495)
23. Thrailkill, K. M. & Birky, C. W. 1980 Intracellular population genetics: evidence for random drift of mitochondrial allele frequencies in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Genetics 96, 237-262.
24. Hermann, G. J. & Shaw, J. M. 1998 Mitochondrial dynamics in yeast. Annu. Rev. Cell. Dev. Biol. 14, 265-303. (doi:10.1146/annurev.cellbio.14.1.265)
25. Rand, D. M. 2001 The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Syst. 32, 415-448. (doi:10.1146/annurev.ecolsys.32.081501.114109)
26. Jansen, R. P. S. & de Boer, K. 1998 The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol. Cell. Endocrinol. 145, 81-88. (doi:10.1016/S0303-7207(98)00173-7)
27. Hauswirth, W. W. & Laipis, P. J. 1985 Transmission genetics of mammalian mitochondria: a model and experimental evidence. In Achievements and perspectives of mitochondrial research (eds E. Quagliariello, E. C. Slater, F. Palmieri, C. Saccone & A. M. Kroon), pp. 49-59. Amsterdam, The Netherlands: Elsevier Science.
28. Krakauer, D. C. & Mira, A. 1999 Mitochondria and germ-cell death. Nature 400, 125-126. (doi:10.1038/22026)
29. Lane, N. 2008 Low variability on the W chromosome in birds is more likely to indicate selection on mitochondrial genes. Heredity 100, 444-445. (doi:10.1038/Hdy.2008.9)
30. Lynch, M., Koskella, B. & Schaack, S. 2006 Mutation pressure and the evolution of organelle genomic architecture. Science 311, 1727-1730. (doi:10.1126/science. 1118884)
31. Nabholz, B., Glemin, S. & Galtier, N. 2008 Strong variations of mitochondrial mutation rate across mammals-the longevity hypothesis. Mol. Biol. Evol. 25, 120-130. (doi:10.1093/molbev/msm248)
32. Palmer, J. D. & Herbon, L. A. 1988 Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J. Mol. Evol. 28, 87-97. (doi:10.1007/BF02143500)
33. Wolfe, K. H., Li, W. H. & Sharp, P. M. 1987 Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl Acad. Sci. USA 84, 9054-9058. (doi:10.1073/pnas.84.24.9054)
34. Zhang, Q., Liu, Y. & Sodmergen 2003 Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell. Physiol. 44, 941-951. (doi:10.1093/pcp/pcg121)