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4 - Nucleo-cytoplasmic conflict and the evolution of gamete dimorphism

Published online by Cambridge University Press:  19 May 2011

Rolf F. Hoekstra
Affiliation:
Wageningen University, Netherlands
Tatsuya Togashi
Affiliation:
Chiba University, Japan
Paul Alan Cox
Affiliation:
Institute for Ethnomedicine
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Summary

CYTOPLASMIC SELECTION MAY CAUSE NUCLEO-CYTOPLASMIC CONFLICT

Several authors have noted that the mixing of cytoplasm following gamete fusion may increase the potential for spread of deleterious cytoplasmic variants through a sexual population (Grun, 1976; Eberhard, 1980; Cosmides and Tooby, 1981). This argument assumes a lack of precise control of intracellular replication and subsequent lack of segregation of the cytoplasmic DNA at gametogenesis. The replication and transmission of nuclear genes is tightly regulated, ensuring no segregation of alleles at mitosis and a fair meiotic segregation in heterozygotes. Thus, in the words of Birky (1983), the nuclear genome is “stringent.” In contrast, cytoplasmic genomes are “relaxed”: multiple cytoplasmic genomes populate each cell; they can be replicated different numbers of times during a cell cycle (Clayton, 1982) and can be differently transmitted to daughter cells. Throughout this chapter I focus primarily on mitochondria as examples of obligate cytoplasmic organelles, but similar reasoning applies to other cytoplasmic entities like plastids in plants and vertically transmitted endosymbiontic bacteria. The relaxed regulation of mitochondrial replication and segregation increases the scope for within-individual selection among mitochondrial genomes. This may possibly result in the evolution of selfish mitochondrial variants that are able to acquire a within-individual transmission advantage while being harmful to the host organism. A transmission advantage of a selfish mitochondrial mutant could result from superior competitiveness in heteroplasmic cells, for example due to a higher replication rate resulting in numerical over-representation in zygotes.

Type
Chapter
Information
The Evolution of Anisogamy
A Fundamental Phenomenon Underlying Sexual Selection
, pp. 111 - 130
Publisher: Cambridge University Press
Print publication year: 2011

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References

Andersson, M. (1996). Sexual Selection. Princeton, NJ: Princeton University Press.Google ScholarPubMed
Barr, C. M., Neiman, M., and Taylor, D. R. (2005). Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist, 168, 39–50.CrossRefGoogle ScholarPubMed
Bell, G. (1993). The sexual nature of the eukaryote genome. Journal of Heredity, 84, 351–359.CrossRefGoogle ScholarPubMed
Bertrand, H., Chan, B. S. S., and Griffiths, A. J. F. (1985). Insertion of a foreign nucleotide sequence into mitochondrial DNA causes senescence in Neurospora intermedia. Cell, 41, 877–884.CrossRefGoogle ScholarPubMed
Birky, C. W. (1983). Relaxed cellular controls and organelle heredity. Science, 222, 468–475.CrossRefGoogle ScholarPubMed
Birky, C. W. (1995). Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proceedings of the National Academy of Sciences of the United States of America, 92, 11331–11338.CrossRefGoogle ScholarPubMed
Birky, C. W. (2001). The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annual Review of Genetics, 35, 125–148.CrossRefGoogle ScholarPubMed
Blakeslee, A. F. (1904). Sexual reproduction in the Mucorineae. Proceedings of the American Academy of Arts and Sciences, 40, 205–319.CrossRefGoogle Scholar
Bull, J. J. (1983). Evolution of Sex Determining Mechanisms. Menlo Park, CA: Benjamin Cummings.Google Scholar
Burt, A. and Trivers, R. (2006). Genes in Conflict. Cambridge, MA: The Belknap Press.CrossRefGoogle Scholar
Butler, G. (2007). The Evolution of MAT: the Ascomycetes. In Heitman, J., Kronstad, J. W., Taylor, J. W., and Casselton, L. A. (editors), Sex in Fungi. Washington, DC: ASM Press, pp. 3–18.Google Scholar
Casselton, L. A. and Economou, A. (1985). Dikaryon formation. In Moore, D., Casselton, L. A., Wood, D. A., and Frankland, J. C. (editors), Developmental Biology of Higher Fungi. Cambridge: Cambridge University press, pp. 213–229.Google Scholar
Charlesworth, B. (1991). The evolution of sex chromosomes. Science, 251, 1030–1033.CrossRefGoogle ScholarPubMed
Clayton, D. A. (1982). Replication of animal mitochondrial DNA. Cell, 28, 693–705.CrossRefGoogle ScholarPubMed
Coppin, E., Debuchy, R., Arnaise, S., and Picard, M. (1997). Mating types and sexual development in filamentous ascomycetes. Microbiology and Molecular Biology Review, 61, 411–428.Google ScholarPubMed
Cosmides, L. M. and Tooby, J. (1981). Cytoplasmic inheritance and intragenomic conflict. Journal of Theoretical Biology, 89, 83–129.CrossRefGoogle ScholarPubMed
Czárán, T. L. and Hoekstra, R. F. (2004). Evolution of sexual asymmetry. BMC Evolutionary Biology, 4, 34.CrossRefGoogle ScholarPubMed
Damme, J. M. M. and Delden, W. (1984). Gynodioecy in Plantago lanceolata L. IV. Fitness components of sex types in different life cycle stages. Evolution, 38, 1326–1336.CrossRefGoogle ScholarPubMed
Debuchy, R. T. and Turgeon, B. G. (2006). Mating-type structure, evolution and function in euascomycetes. In Kues, U. and Fischer, R. (editors), Growth, Differentiation and Sexuality, I. Berlin: Springer Verlag, pp. 293–323.CrossRefGoogle Scholar
Eberhard, W. G. (1980). Evolutionary consequences of intracellular organelle competition. Quarterly Review of Biology, 55, 231–249.CrossRefGoogle ScholarPubMed
Fraser, J. A., Diezmann, S., Subaran, R. L., et al. (2004). Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biology, 2, 384.CrossRefGoogle ScholarPubMed
Fraser, J. A.Hsueh, Y.-P., Findley, K. M., and Heitman, J. (2007). Evolution of the mating-type locus: the Basidiomycetes. In Heitman, J., Kronstad, J. W., Taylor, J. W., and Casselton, L. A. (editors), Sex in Fungi. Washington, DC: ASM Press, pp. 19–34.Google Scholar
Gillham, N. W. (1994). Organelle Genes and Genomes. New York: Oxford University Press.Google Scholar
Goodenough, U., Lin, H., and Lee, J. H. (2007). Sex determination in Chlamydomonas. Seminars in Cell and Developmental Biology, 18, 350–361.CrossRefGoogle ScholarPubMed
Griffiths, A. J. F. (1992). Fungal senescence. Annual Review of Genetics, 26, 351–372.CrossRefGoogle ScholarPubMed
Grun, P. (1976). Cytoplasmic Genetics and Evolution. New York: Columbia University Press.Google Scholar
Hastings, I. M. (1992). Population genetic aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction. Genetical Research, 59, 215–225.CrossRefGoogle ScholarPubMed
Herskowitz, I. (1988). Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiolgical Reviews, 52, 536–553.Google ScholarPubMed
Hoekstra, R. F. (1982). On the asymmetry of sex: evolution of mating types in isogamous populations. Journal of Theoretical Biology, 98, 427–451.CrossRefGoogle Scholar
Hoekstra, R. F. (1987). The evolution of sexes. In Stearns, S. C. (editor), The Evolution of Sex and its Consequences. Basel: Birkhäuser Verlag, pp. 59–91.CrossRefGoogle Scholar
Hoekstra, R. F. (1990a). The evolution of male-female dimorphism: older than sex? Journal of Genetics, 69, 11–15.CrossRefGoogle Scholar
Hoekstra, R. F. (1990b). Evolution of uniparental inheritance of cytoplasmic DNA. In Smith, J. M. and Vida, G. (editors), Organizational Constraints on the Dynamics of Evolution. Manchestor and New York: Manchester University press, pp. 269–278.Google Scholar
Hoekstra, R. F., Iwasa, Y., and Weissing, F. (1991). The origin of isogamous sexual differentiation. In Selten, R. (editor), Game Equilibrium Models, I. Berlin: Springer Verlag, pp. 155–181.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. (1995). Selfish genetic elements and their role in evolution: the evolution of sex and some of what that entails. Philosophical Transactions of The Royal Society of London Series B Biological Sciences, 349, 321–332.CrossRefGoogle ScholarPubMed
Hurst, L. D. and Hamilton, W. D. (1992). Cytoplasmic fusion and the nature of sexes. Proceedings of The Royal Society of London Series B Biological Sciences, 247, 189–194.CrossRefGoogle Scholar
Hutson, V. and Law, R. (1993). Four steps to two sexes. Proceedings of The Royal Society of London B Biological Science, 253, 43–51.CrossRefGoogle ScholarPubMed
Kaneda, H., Hayashi, J., Takahama, S., et al. (1995). Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proceedings of the National Academy of Sciences of the United States of America, 92, 4542–4546.CrossRefGoogle ScholarPubMed
Kuroiwa, T., Kawano, S., Nishibayashi, S., and Sato, C. (1982). Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature, 298, 481–483.CrossRefGoogle ScholarPubMed
Lane, N. (2005). Power, Sex, Suicide: Mitochondria and the Meaning of Life. Oxford: Oxford University press.Google Scholar
Law, R. and Hutson, V. (1992). Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance. Proceedings. Biologycal Sciences / The Royal Society, 248, 69–77.CrossRefGoogle ScholarPubMed
Lee, S. C., Corradi, N., Brynes, E. J., et al. (2008). Microsporidia evolved from ancestral sexual fungi. Current Biology, 18, 1675–1679.CrossRefGoogle ScholarPubMed
Manicacci, D., Atlan, A., Rossello, J. A. E., and Couvet, D. (1998). Gynodioecy and reproductive trait variation in three Thymus species (Lamiaceae). International Journal of Plant Sciences, 159, 948–957.CrossRefGoogle Scholar
Meusel, M. S. and Moritz, R. F. A. (1993). Transfer of paternal mitochondrial DNA during fertilization of honeybee (Apis mellifera L.) eggs. Current Genetics, 24, 539–543.CrossRefGoogle ScholarPubMed
Miyake, A. (1981). Cell Interaction by Gamones in Blepharisma. New York: Academic Press.CrossRefGoogle Scholar
Miyake, A. (1981). Cell interaction by gamones in Blepharisma. In O'Day, D. H. and Horgen, P. A (editors), Sexual Interactions in Eukaryotic Microbes. New York: Academic Press, pp. 95–129.Google Scholar
Miyake, A. (1996). Fertilization and sexuality in ciliates. In Hausmann, K. and Bradbury, P. (editors), Ciliates – Cells as Organisms. Stuttgart and New York: Gustav Fischer Verlag, pp. 243–290.Google Scholar
Neale, D. B. and Sederoff, R. R. (1989). Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. TAG Theoretical and Applied Genetics, 77, 212–216.CrossRefGoogle ScholarPubMed
Nettancourt, D. (1977). Incompatibility in Angiosperms. Berlin: Springer Verlag.CrossRefGoogle Scholar
Nishimura, Y., Misumi, O., Matsunaga, S., et al. (1999). The active digestion of uniparental chloroplast DNA in a single zygote of Chlamydomonas reinhardtii is revealed by using the optical tweezer. Proceedings of the National Academy of Sciences of the United States of America, 96, 12577–12582.CrossRefGoogle Scholar
Nozaki, H., Mori, T., Misumi, O., Matsunaga, S., and Kuroiwa, T. (2006). Males evolved from the dominant isogametic mating type. Current Biology, 16, R1018–R1020.CrossRefGoogle ScholarPubMed
Parker, G. A., Baker, R. R., and Smith, V. G. F. (1972). The origin and evolution of gamete dimorphism and the male-female phenomenon. Journal of Theoretical Biology, 36, 529–553.CrossRefGoogle ScholarPubMed
Pringsheim, E. G. and Ondracek, K. (1939). Untersuchungen über die Geslechtsvorgaenge bei Polytoma. Beihefte zum Botanischen Centralblatt, I, 118–172.Google Scholar
Rand, D. M. and Harrison, R. G. (1989). Molecular population genetics of mtDNA size variation in crickets. Genetics, 121, 551–569.Google ScholarPubMed
Randerson, J. P. and Hurst, L. D. (1999). Small sperm, uniparental inheritance and selfish cytoplasmic elements: a comparison of two models. Journal of Evolutionary Biology, 12, 1110–1124.CrossRefGoogle Scholar
Randerson, J. P. and Hurst, L. D. (2001). A comparative test of a theory for the evolution of anisogamy. Proceedings of The Royal Society of London B Biological Science, 268, 879–884.CrossRefGoogle ScholarPubMed
Raper, J. R. (1966). Genetics of Sexuality in Higher Fungi. New York: Ronald Press.Google Scholar
Sager, R. (1972). Cytoplasmic Genes and Organelles. New York: Academic Press.Google Scholar
Sprague, G. F. and Thorner, J. (1992). Pheromone response and signal transduction during the mating process of Saccharomyces cerevisiae. In Jones, E. W., Pringle, J. R., and Broach, J. R. (editors), The Molecular and Cellular Biology of the Yeast. New York: Cold Spring Harbor Laboratory Press, pp. 657–744.Google Scholar
Stanton, B. C. and Hull, C. M. (2007). Mating-type locus control of cell identity. In Heitman, J., Kronstad, J. W., Taylor, J. W., and Casselton, L. A. (editors), Sex in Fungi. Washington, DC: ASDM Press, pp. 59–74.Google Scholar
Suda, S., Watanabe, M. M., and Inouye, I. (2004). Electron microscopy of sexual reproduction in Nephroselmis olivacea (Prasinophyceae, Chlorophyta). Phycological Research, 52, 273–283.CrossRefGoogle Scholar
Sutovsky, P., McCauley, T. C., Sutovsky, M., and Day, B. N. (2003). Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biology of Reproduction, 68, 1793–1800.CrossRefGoogle ScholarPubMed
Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., et al. (1999). Ubiquitin tag for sperm mitochondria. Nature, 402, 371–372.CrossRefGoogle ScholarPubMed
Szmidt, A. E., Aldén, T., and Hällgren, J. E. (1987). Paternal inheritance of chloroplast DNA in Larix. Plant Molecular Biology, 9, 59–64.CrossRefGoogle ScholarPubMed
Thompson, W. E., Ramalho-Santos, J., and Sutovsky, P. (2003). Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biology of Reproduction, 69, 254–260.CrossRefGoogle ScholarPubMed
Urushihara, H. (1992). Sexual development of cellular slime molds. Development Growth and Differentiation, 34, 1–7.CrossRefGoogle Scholar
Weismann, A. (1886). Die Bedeutung der Sexuellen Fortpflanzung. Die Selektions – Theorie. Jena: Fischer Verlag.Google Scholar
Williamson, D. (2002). The curious history of yeast mitochondrial DNA. Nature Reviews Genetics, 3, 475–481.CrossRefGoogle ScholarPubMed

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