Abstract
Why did sex ever arise in the first place? Why it does not disappear in view of the greater efficiency of asexuals? These are clearly two different questions, and we suggest here that the solution for the origin of sex does not necessarily come from theoretical considerations based on currently existing genetic systems. Thus, while we agree with a number of authors in that the emergence of sex (understood as the exchange of genetic material between genomes) is deeply rooted in the origin of life and happened during the very early stages in the transition from individual genes (`replicators') to bacteria-like cells (`reproducers'), we challenge the idea that recombinational repair was the major selective force for the emergence of sex. Taking the stochastic corrector model as a starting point, we provide arguments that question the putative costs of redundancy in primitive protocells. In addition, if genes that cause intragenomic conflict (i.e., parasites) are taken into account, it is certainly wrong to suggest that cellular fusion would be beneficial at the population level (although this strong claim needs some qualifications). However, when a continuous input of deleterious mutations that impair the fitness of the protocell as a whole is considered in the model (in the realistic range in which stable mutant distributions of quasi-species within compartments are established), there are circumstances when sex could be beneficial as a side effect of the dynamic equilibrium between cellular fusion-mutation-selection. The scenario we have explored numerically is fully consistent with the idea that the universal ancestor was not a discrete entity but an ensemble of proto-organisms that exchanged much genetic information.
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Amores, A., Force, A., Yan, Y. L., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Prince, V., Wang, Y. L., Westerfield, M., Ekker, M. and Postlethwait, J. H.: 1998, Zebrafish Hox Clusters and Vertebrate Genome Evolution, Science 282, 1711-1714.
Anderson, R. M. and May, R. M.: 1982, Coevolution of Hosts and Parasites, Parasitology 85, 411–426.
Bernstein, H., Byerly, H. C., Hopf, F. A. and Michod, R. E.: 1984, Origin of Sex, J. Theor. Biol. 110, 323–351.
Bernstein, H., Byerly, H. C., Hopf, F. A. and Michod, R. E.: 1985, Genetic Damage, Mutation, and the Evolution of Sex, Science 229, 1277–1281.
Bresch, C., Niesert, U. and Harnasch, D.: 1980, Hypercycles, Parasites and Packages, J. Theor. Biol. 85, 399–405.
Cavalier-Smith, T.: 1985, The Evolution of Genome Size, Wiley, Chichester.
Cavalier-Smith, T.: 2002, Origins of the Machinery of Recombination and Sex, Heredity 88, 125–141.
Cronn, R. C., Small, R. L. and Wendel, J. F.: 1999, Duplicated Genes Evolve Independently After Polyploid Formation in Cotton, Proc. Natl. Acad. Sci. USA 96, 14406–14411.
De Duve, C.: 1991, Blueprint for a Cell: The Nature and Origin of Life, Neil Patterson, Burlington.
Dyson, F. J.: 1999, Origins of Life, Cambridge University Press, Cambridge.
Eigen, M.: 1971, Self-Organization of Matter and the Evolution of Biological Macromolecules, Naturwissenschaften 58, 465–523.
Eigen, M. and Schuster, P.: 1979, The Hypercycle: A Principle of Natural Self-Organization, Springer-Verlag, Berlin.
Eigen, M., Schuster, P., Gardiner, W. and Winkler-Oswatitsch, R.: 1981, The Origin of Genetic Information, Sci. Am. 244, 78–94.
Ewald, P. W.: 1983, Host-Parasite Relations, Vectors, and the Evolution of Disease Severity, Ann. Rev. Ecol. Syst. 14, 465–485.
Frank, S. A.: 1995, Mutual Policing and Repression of Competition in the Evolution of Cooperative groups, Nature 377, 520–522.
Friedberg, E. C., Walker, G. C. and Siede, W.: 1995, DNA Repair and Mutagenesis, ASM Press, Washington.
Gánti, T.: 1987, The Principle of Life, OMIKK, Budapest.
Gánti, T.: 2003, The Principles of Life, Oxford Univ. Press, Oxford.
Gesteland, R. F., Cech, T. R. and Atkins, J. F. (eds): 1999, The RNA World, 2nd ed., Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press.
Gilbert, W.: 1986, The RNA World, Nature 319, 618.
Grey, D., Hutson, V. and Szathmáry, E.: 1995, A Re-Examination of the Stochastic Corrector Model, Proc. R. Soc. Lond. B 262, 29–35.
Hamilton, W. D., Axelrod, R. and Tanese, R.: 1990, Sexual Reproduction as an Adaptation to Resist Parasites (A Review), Proc. Natl. Acad. Sci. USA 87, 3566–3573.
Hickey, D. A. and Rose, M. R.: 1988, The Role of Gene Transfer in the Evolution of Eukaryotic Sex in Michod, R. E. and Levin, B. R. (eds.), The Evolution of Sex: An Examination of Current Ideas, Sinauer Associates, Sunderland, pp. 161–175.
Hurst, L. and Peck, J. R.: 1996, Recent Advances in Understanding the Evolution and Maintenance of Sex, Trends Ecol. Evol. 11, 46–52.
Johnston, W. K., Unrau, P. J., Lawrence, M. S., Glasner, M. E. and Bartel, D. P.: 2001, RNACatalyzed RNA Polymerization: Accurate and General RNA-Templated Primer Extension, Science 292, 1319–1325.
Joyce, G. F., Schwartz, A.W., Miller, S. L. and Orgel, L. E.: 1987, The Case for an Ancestral Genetic System Involving Simple Analogues of the Nucleotides, Proc. Natl. Acad. Sci. USA 84, 4398–4402.
Keightley, P. D. and Eyre-Walker, A.: 2000, Deleterious Mutations and the Evolution of Sex, Science 290, 331–333.
Knoll, A. H.: 2003, Life on a Young Planet. The First Three Billion Years of Evolution on Earth, Princeton Univ. Press, Princeton.
Koch, A. L.: 1984, Evolution vs the Number of Gene Copies per Primitive Cell. J. Mol. Biol. 20, 71–76.
Kondrashov, A. S. and Crow, J. F.: 1991, Haploid or Diploidy: Which is Better? Nature 351, 314–315.
Kondrashov F. A., Rogozin, I. B., Wolf, Y. I. and Koonin E. V.: 2002, Selection in the Evolution of Gene Duplications, Genome Biol. 3, research0008.1-0008.9 (URL: http: //genomebiology.com/2002/3/2/research/0008).
Lasic, D. D.: 1998, Novel Applications of Liposomes, Trends Biotech. 16, 307–321.
Levin, S. A. and Pimental, D.: 1981, Selection of Intermediate Rates of Increase in Parasite-Host Systems, Am. Nat. 117, 308–315.
Lupski, J. R., Roth, J. R. and Weinstock, G. M.: 1996, Chromosomal Duplications in Bacteria, Fruit Flies, and Humans, Am. J. Hum. Genet. 58, 21–27.
Lynch, M. and Conery, J. S.: 2000, The Evolutionary Fate and Consequences of Duplicate Genes, Science 290, 1151–1155.
MATLAB V.5.3.: 1999, The Language of Technical Computing, The Math Works, Inc. URL: http: //www.mathworks.com.
Maynard Smith, J.: 1978, The Evolution of Sex, Cambridge University Press, Cambridge.
Maynard Smith, J.: 1979, Hypercycles and the Origin of Life, Nature 280, 445–446.
Maynard Smith, J. and Szathmáry, E.: 1993, The Origin of Chromosomes I. Selection for Linkage, J. Theor. Biol. 164, 437–446.
Maynard Smith, J. and Szathmáry, E.: 1995, The Major Transitions in Evolution, W. H. Freeman, Oxford.
McDermid, H. E., and Morrow, B. E.: 2002, Genomic Disorders on 22q11, Am. J. Hum. Genet. 70, 1077–1088.
Mergenthaler, S., Sharp, A., Ranke, M. B., Kalscheuer, V. M., Wollmann, H. A. and Eggermann, T.: 2001, Gene Dosage Analysis in Silver-Russell Syndrome: Use of Quantitative Competitive PCR and Dual-Color FISH to Estimate the Frequency of Duplications in 7p11.2-p13, Genet. Test. 5, 261–266.
Michod, R. E.: 1993, Genetic Error, Sex, and Diploidy, J. Heredity 84, 360–371.
Michod, R. E. and Levin, B. R. (eds): 1988, The Evolution of Sex: An Examination of Current Ideas, Sinauer Associates, Sunderland.
Niesert, U., Harnasch, D. and Bresch, C.: 1981, Origin of Life: Between Scylla and Charybdis, J. Molec. Evol. 17, 348–353.
Otto, S. P. and Whitton, J.: 2000, Polyploid Incidence and Evolution, Annu. Rev. Genet. 34, 401–437.
Otto, S. P. and Yong, P.: 2002, The Evolution of Gene Duplicates, Adv. Genet. 46, 451–483.
Partridge, L. and Hurst, L. D.: 1998, Sex and Conflict, Science 281, 2003–2008.
Perrot, V., Richerd, S. and Valéro, M,: 1991, Transition from Haploidy to Diploidy, Nature 351, 315–317.
Pohorille, A. and Deamer, D.: 2002, Artificial Cells: Prospects for Biotechnology, Trends Biotech. 20, 123–128.
Reanney, D. C.: 1987, Genetic Error and Genome Design, Cold. Spring. Harb. Symp. Quant. Biol. 52, 751–757.
Redfield, R. J.: 2001, Do Bacteria Have Sex? Nat. Rev. Genet. 2, 634–639.
Sagan, D. and Margulis, L.: 1987, Cannibal's Relief: The Origins of Sex, New Sci. 115, 36–40.
Szathmáry, E.: 1989, The Integration of the Earliest Genetic Information, Trends Ecol. Evol. 4, 200–204.
Szathmáry, E. and Demeter, L.: 1987, Group Selection of Early Replicators and the Origin of Life, J. Theor. Biol. 128, 463–486.
Szathmáry, E. and Maynard Smith, J.: 1993, The Evolution of Chromosomes II. Molecular Mechanisms, J. Theor. Biol. 164, 447–454.
Szostak, J. W., Bartel, D. P. and Luisi, P. L.: 2001, Synthesizing Life, Nature 409, 387–390.
Werren, J. H., Nur, U. and Wu, C.-I.: 1988, Selfish Genetic Elements, Trends Ecol. Evol. 3, 297–302.
West, S. A., Lively, C. M. and Read, A. F.: 1999, A Pluralist Approach to Sex and Recombination, J. Evol. Biol. 12, 1003–1012.
Wilke, C. O., Wang, J. L., Ofria, C., Lenski, R. E. and Adami, C.: 2001, Evolution of Digital Organisms at High Mutation Rates Leads to Survival of the Flattest, Nature 412, 331–333.
Williams, G. C.: 1975, Sex and Evolution, Princeton University Press, Princeton.
Woese, C.: 1998, The Universal Ancestor, Proc. Natl. Acad. Sci. USA 95, 6854–6859.
Zintzaras, E., Santos, M. and Szathmáry, E.: 2002, 'Living' under the Challenge of Information Decay: The Stochastic Corrector Model versus Hypercycles. J. Theor. Biol. 217, 167–181.
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Santos, M., Zintzaras, E. & Szathmáry, E. Origin of Sex Revisited. Orig Life Evol Biosph 33, 405–432 (2003). https://doi.org/10.1023/A:1025759024888
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DOI: https://doi.org/10.1023/A:1025759024888