Hostname: page-component-84b7d79bbc-g78kv Total loading time: 0 Render date: 2024-07-30T17:19:27.329Z Has data issue: false hasContentIssue false
  • English
  • Français

Population genetic aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction

Published online by Cambridge University Press:  14 April 2009

Ian M. Hastings
Ian M. Hastings
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, Scotland

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A conflict of interest may arise between intra-cellular genomes and their host cell. The example explicitly investigated is that of a ‘selfish’ mitochondrion which increases its own rate of replication at the cost of reduced metabolic activity which is deleterious to the host cell. The results apply to deleterious cytoplasmic agents in general, such as intracellular parasites. Numerical simulation suggests that selfish mitochondria are able to invade an isogamous sexual population and are capable of reducing its fitness to below “5 % of that prior to their invasion. Their spread is enhanced by decreasing the number of mitotic divisions between meioses, and this may constitute a significant constraint on the evolution of lifecycles. The presence of such deleterious cytoplasmic agents favours a nuclear mutation whose expression prevents cytoplasm from the other gamete entering the zygote at fertilization, resulting in uniparental inheritance of cytoplasm. Such a mutation appears physiologically plausible and can increase in frequency despite its deleterious effect in halving the amount of cytoplasm in the zygote. It is suggested that these were the conditions under which anisogamy evolved. These results have implications for the evolution of sexual reproduction. Standard theory suggests there is no immediate cost of sex, a twofold cost being incurred later as anisogamy evolves. The analysis described here predicts a large, rapid reduction in fitness associated with isogamous sexual reproduction, due to the spread of deleterious cytoplasmic agents with fitness only subsequently rising to a maximum twofold cost as uniparental inheritance of cytoplasm and anisogamy evolve.

Type
Research Article
Information
Genetics Research , Volume 59 , Issue 3 , June 1992 , pp. 215 - 225
Copyright
Copyright © Cambridge University Press 1992

References

Alberts, B.Bray, D.Lewis, J.Raff, M.Roberts, K. & Watson, J. D. (1983). Molecular Biology of the Cell. New York: Garland Publishing.Google Scholar
Anderson, R. M. & May, R. M. (1979). Population biology of infectious diseases: Part 1. Nature 190, 361–367.CrossRefGoogle Scholar
Beale, G. & Knowles, J. (1978). Extranuclear Genetics. London: Edward Arnold.Google Scholar
Beatty, R. A. (1972). The Genetics of the Spermatozoan (ed Beatty, R. A. and Gluecksohn-Waelsch, S.). Congress Proceedings, distributed by the Dept. of Genetics, Edinburgh University, Scotland.Google Scholar
Bell, G. (1978). The evolution of anisogamy. Journal of Theoretical Biology 73, 247–270.CrossRefGoogle ScholarPubMed
Bennoun, P.Delosme, M. & Kuck, U. (1991). Mitochondrial genetics of Chlamydomonas reinhardtii: resistance mutations marking the cytochrome b gene. Genetics 127, 335–343.CrossRefGoogle ScholarPubMed
Birky, C. W. (1991). Evolution and population genetics of organelle genes: mechanisms and models. In Evolution at the Molecular Level (ed. Selander, R.K., Clark, A. G. & Whittam, T. S.). Massachusetts USA: Sinauer Associates.Google Scholar
Birky, C. W.Fuerst, P. & Maruyama, T. (1989). Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparisons to nuclear genes. Genetics 121, 613–627.CrossRefGoogle ScholarPubMed
Birky, C. W.Maruyama, T. & Fuerst, P. (1983). An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103, 513–527.CrossRefGoogle ScholarPubMed
Birky, C. W. & Skavaril, R. S. (1976). Maintenance of genetic homogeneity in systems with multiple genomes. Genetical Research 27, 249–265.CrossRefGoogle ScholarPubMed
Chapman, R. W.Stephens, J.C.Lansman, R. A. & Avise, J. A. (1982). Models of mitochondrial DNA transmission genetics and evolution in higher eucaryotes. Genetical Research 40, 41–57.CrossRefGoogle ScholarPubMed
Cosmides, L. M. & Tooby, J. (1981). Cytoplasmic inheritance and intragenomic conflict. Journal of Theoretical Biology 89, 83–129.CrossRefGoogle ScholarPubMed
Dujon, B. (1981). Mitochondrial genetics and function. In The Molecular Biology of the Yeast Saccharomyces. Lifecycle and Inheritance (ed. Strathern, J. N., Jones, E. W. & Broach, J. B.). Cold Spring Harbor Laboratory, USA.Google Scholar
Eberhard, W. G. (1980). Evolutionary consequences of intracellular organelle competition. Quarterly Review of Biology 55, 231–249.CrossRefGoogle ScholarPubMed
Fisher, C. & Skibinski, D. O. F. (1990). Sex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus. Proceedings of the Royal Society of London, B242, 149–156.Google Scholar
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford, UK: Clarendon Press.CrossRefGoogle Scholar
Gyllensten, U.Wharton, D.Josefsson, A. & Wilson, A. C. (1991). Paternal inheritance of mitochondrial DNA in mice. Nature 352, 255–257.CrossRefGoogle ScholarPubMed
Grun, P. (1976). Cytoplasmic Genetics and Evolution. New York: Columbia University Press.Google Scholar
Harrison, R. G. & Doyle, J. J. (1990). Redwoods break the rules. Nature 344, 295–296.CrossRefGoogle Scholar
Hastings, I. M. (1991). Germline selection: population genetic aspects of the sexual/asexual lifecycle. Genetics 129, 1167–1176.CrossRefGoogle Scholar
Hoekstra, R. F. (1987). The evolution of sexes. In The Evolution of Sex and its Consequences (ed. Stearns, S. C.). Basel: Birkhauser Verlag.Google Scholar
Hoekstra, R. F. (1990 a). Evolution of uniparental inheritance of cytoplasmic DNA. In Organisational Constraints on the Dynamics of Evolution (ed. Maynard-Smith, J. & Vida, G.). Manchester University Press.Google Scholar
Hoekstra, R. F. (1990 b). The evolution of male-female dimorphism: older than sex? Journal of Genetics 69, 11–15.Google Scholar
Hoeizer, M. A. & Michod, R. E. (1991). DNA repair and the evolution of transformation in Bacillus subtilis. IN. Sex with damaged DNA. Genetics 128, 215–223.CrossRefGoogle Scholar
Hurst, L. D. (1990). Parasite diversity and the evolution of diploidy, multicellularity and anisogamy. Journal of Theoretical Biology 144, 429–443.CrossRefGoogle ScholarPubMed
Hurst, L. D.Godfray, H. C. J. & Harvey, P. H. (1990). Antibiotics cure asexuality. Nature 346, 510–511.CrossRefGoogle Scholar
Hurst, L. D. & Hamilton, W. D. (1992). Cytoplasmic fusion and the nature of sexes. Proceedings of the Royal Society of London, B (in the press).Google Scholar
Kondo, R.Satto, Y.Matsuura, E. T.Ishiwa, H.Takahata, N. & Chigusa, S. I. (1990). Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126, 657–663.Google Scholar
Kuroiwa, T.Kawano, S. & Nishibayashi, S. (1982). Epiflourescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298, 481–483.CrossRefGoogle Scholar
Lavitrano, M.Camaioni, A.Fazio, V. M.Dolci, S.Farace, M. G. & Spadafora, C. (1989). Sperm cells as vectors for introducing foreign DNA into eggs: genetic transformation of mice. Cell 57, 717–723.CrossRefGoogle ScholarPubMed
Law, R. & Hutson, V. (1992). Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance (submitted).Google Scholar
May, R. M. & Anderson, R. M. (1979). Population biology of infectious diseases: Part 2. Nature 190, 455–161.Google Scholar
Maynard-Smith, J. (1978). The Evolution of Sex. Cambridge, UK: Cambridge University Press.Google Scholar
Maynard-Smith, J. (1989). Evolutionary Genetics. Oxford, UK: Oxford University Press.Google Scholar
Meland, S.Johansen, S.Johansen, T.Haugli, K. & Haugli, F. (1991). Rapid disappearance of one parental mitochondrial genotype after isogamous mating in the myxomycete Physarum polycephalum. Current Genetics 19, 55–59.CrossRefGoogle ScholarPubMed
Neale, D. B.Marshall, K. A. & Sederoff, R. R. (1989). Chloroplast and mitochondria DNA are paternally inherited in Sequoia sempervirens. Proceedings of the National Academy of Science, USA 86, 9347–9349.CrossRefGoogle ScholarPubMed
Parker, G. A.Baker, R. R. & Smith, V. G. F. (1972). The origin and evolution of gamete dimorphism and the malefemale phenomenon. Journal of Theoretical Biology 36, 529–553.CrossRefGoogle ScholarPubMed
Rand, D. M. & Harrison, R. G. (1986). Mitochondrial DNA transmission in crickets. Genetics 114, 955–970.CrossRefGoogle ScholarPubMed
Rousset, F. & Raymond, M. (1991). Cytoplasmic incompatibility in insects: why sterilize females. Trends in Ecology and Evolution 6, 54–57.CrossRefGoogle ScholarPubMed
Stouthamer, R.Luck, R. F. & Hamilton, W. D. (1990). Antibiotics cause parthenogenic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proceedings of the National Academy of Science, USA 87, 2424–2427.CrossRefGoogle Scholar
Takahata, N. (1984). A model of extranuclear genomes and the substitution rate under within-generation selection. Genetical Research 44, 109–116.CrossRefGoogle Scholar
Takahata, N. & Maruyama, T. (1981). A mathematical model of extranuclear genes and the genetic variability maintained in a finite population. Genetical Research 37, 291–302.CrossRefGoogle Scholar
Takahata, N. & Palumbi, S. R. (1985). Extranuclear differentiation and gene flow in the finite island model. Genetics 109, 441–457.CrossRefGoogle ScholarPubMed
Takahata, N. & Slatkin, M. (1983). Evolutionary dynamics of extranuclear genes. Genetical Research 42, 257–265.CrossRefGoogle Scholar
Wigler, M.Sweet, R.Sim, G. K.Wold, B.Angel, P.Lacy, E.Maniatis, T.Silverstein, S. & Axel, R. (1979). Transformation of mammalian cells with genes from prokaryotes and eukaryotes. Cell 16, 777–785.CrossRefGoogle Scholar