Abstract
Sex (genetic exchange) is a nearly universal phenomenon in biological populations. But this is surprising given the costs associated with sex. For example, sex tends to break apart co-adapted genes, and sex causes a female to inefficiently contribute only half the genes to her offspring. Why then did sex evolve? One famous model poses that sex evolved to combat Muller's ratchet, the mutational load that accrues when harmful mutations drift to high frequencies in populations of small size. In contrast, the Fisher-Muller Hypothesis predicts that sex evolved to promote genetic variation that speeds adaptation in novel environments. Sexual mechanisms occur in viruses, which feature high rates of deleterious mutation and frequent exposure to novel or changing environments. Thus, confirmation of one or both hypotheses would shed light on the selective advantages of virus sex. Experimental evolution has been used to test these ZFS25245ZFS25245classic models in the RNA bacteriophage φ6, a virus that experiences sex via reassortment of its chromosomal segments. Empirical data suggest that sex might have originated in φ6 to assist in purging deleterious mutations from the genome. However, results do not support the idea that sex evolved because it provides beneficial variation in novel environments. Rather, experiments show that too much sex can be bad for φ6; promiscuity allows selfish viruses to evolve and spread their inferior genes to subsequent generations. Here I discuss various explanations for the evolution of segmentation in RNA viruses, and the added cost of sex when large numbers of viruses co-infect the same cell.
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Barton, N. H. and Charlesworth, B.: 1998, 'Why Sex and Recombination?', Science 281, 1986-1990.
Basler, C. F., Reid, A. H., Dybing, J. K., Janczewski, T. A., Fanning, T. G., Zheng, H., Salvatore, M., Perdue, M. L., Swayne, D. E., Garcia-Sastre, A., Palese, P. and Taubenberger, J. K.: 2001, 'Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes', Proc. Natl. Acad. Sci. USA 98, 2746-2751.
Bennett, A. F.: 2002, 'Experimental Evolution: An Overview', in M. Pagel (ed.), Encyclopedia of Evolution, Oxford University Press, Oxford, pp. 339-342.
Brasier, M. D., Green, O. R., Jephcoat, A. P., Kleppe, A. K., Van Kranendonk, M. J., Lindsay, J. F., Steeles, A. and Grassineau, N. V.: 2002, 'Questioning the evidence for Earth's oldest fossils', Nature 416, 76-81.
Burch, C. L. and Chao, L.: 1999, 'Evolution by small steps and rugged landscapes in the RNA virus ö6', Genetics 151, 921-927.
Butcher, S. J., Dokland, T., Ojala, P. M., Bamford, D. H. and Fuller, S. D.: 1997, 'Intermediates in the assembly pathway of the double-stranded RNA virus ö6', EMBO J. 16, 4477-4487.
Chao, L.: 1988, 'Evolution of sex in RNA viruses', J. Theor. Biol. 133, 99-112.
Chao, L.: 1990, 'Fitness of RNA virus decreased by Muller's ratchet', Nature 348, 454-455.
Chao, L.: 1992, 'Evolution of sex in RNA viruses', Trends Ecol. Evol. 7, 147-151.
Chao, L., Tran, T. T. and Tran, T. T.: 1997, 'The advantage of sex in RNA virus phi-6', Genetics 147, 953-959.
Drake, J.W. and Holland, J. J.: 1999, 'Mutation rates among RNA viruses', PNAS 96, 13910-13913.
Felsenstein, J.: 1988, 'Sex and the Evolution of Recombination', in R. E. Michod and B. R. Levin (eds), The Evolution of Sex: An Examination of Current Ideas, Sinauer, Sunderland, MA, pp. 74-86.
Fisher, R. A.: 1930, The Genetical Theory of Natural Selection, Oxford University Press, Oxford.
Gerrish, P. J. and Lenski, R. E.: 1998, 'The Fate of Competing Beneficial Mutations in an Asexual Population', Genetica 100, 127-144.
Hurst, L. and Peck, J. R.: 1996, 'Recent advances in understanding the evolution and maintenance of sex', Trends Ecol. Evol. 11, 46-52.
Iturriza-Gomara, M., Isherwood, B., Desselberger, U. and Gray, J.: 2001, 'Reassortment in vivo: Driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999', J. Virol. 75, 3696-3705.
Kilbourne, E. D.: 1979, 'Molecular epidemiology-influenza as archetype', The Harvey Lectures 73, 225-258.
Kondrashov, A.: 1993, 'Classification of hypotheses on the advantage of amphimixis', J. Heredity 84, 372-387.
Malmberg, R. L.: 1977, 'The evolution of epistasis and the advantage of recombination in populations of bacteriophage T4', Genetics 86, 607-621.
Maynard Smith, J.: 1978, The Evolution of Sex, Cambridge University Press, Cambridge.
Michod, R. E. and Levin, B. R.: 1988, The Evolution of Sex: An Examination of Current Ideas, Sinauer, Sunderland, MA.
Mindich, L.: 1988, 'Bacteriophage ö6: A unique virus having a lipid-containing membrane and a genome composed of three dsRNA segments', Adv. Virus Res. 35, 137-176.
Muller, H. J.: 1932, 'Some Genetic Aspects of Sex', Am. Nat. 66, 118-138.
Muller, H. J.: 1964, 'The relation of recombination to mutational advance', Mut. Res. 1, 2-9.
Nee, S. and Maynard Smith, J.: 1990, 'The evolutionary biology of molecular parasites', Parasitology 100, S5-S18.
Olkkonen, V. M. and Bamford, D. H.: 1989, 'Quantitation of the adsorption and penetration stages of bacteriophage ö6 infection', Virology 171, 229-238.
Onodera, S., Qiao, X., Qiao, J. and Mindich, L.: 1998, 'Directed changes in the number of double-stranded RNA genomic segments in bacteriophage ö6', Proc. Natl. Acad. Sci. USA 95, 3920-3924.
Peck, J. R.: 1994, 'A ruby in the rubbish: Beneficial mutations, deleterious mutations and the evolution of sex', Genetics 137, 597-606.
Peters, A. D. and Lively, C. M.: 2000, 'Epistasis and the Maintenance of Sex', in J. B. Wolf, E. D. Brodie III and M. Wade (eds), Epistasis and the Evolutionary Process, Oxford University Press, Oxford, pp. 99-112.
Pressing, J. and Reanney, D.: 1984, 'Divided genomes and intrinsic noise', J. Mol. Evol. 20, 135-146.
Qiao, X., Qiao, J., Onodera, S. and Mindich, L.: 2000, 'Characterization of ö13, a bacteriophage related to ö6 and containing three dsRNA genomic segments', Virology 275, 218-224.
Semancik, J. S., Vidaver, A. K. and Van Etten, J. L.: 1973, 'Characterization of a segmented doublehelical RNA from bacteriophage ö6', J. Mol. Biol. 76, 617-625.
Sevilla, N., Ruiz-Jarabo, C. M., Gomez-Mariano, G., Baranowski, E. and Domingo, E.: 1998, 'An RNA virus can adapt to the multiplicity of infection', J. Gen. Virol. 79, 2971-2980.
Shields, W. M.: 1988, 'Sex and Adaptation', in R. E. Michod and B. R. Levin (eds), The Evolution of Sex: An Examination of Current Ideas, Sinauer, Sunderland, MA, pp. 253-269.
Sokal, R. R. and Rohlf, F. J.: 1995, Biometry, 3rd ed., Freeman, San Francisco.
Turner, P. E. and Chao, L.: 1998, 'Sex and the evolution of intrahost competition in RNA virus ö6', Genetics 150, 523-532.
Turner, P. E. and Chao, L.: 1999, 'Prisoner's dilemma in an RNA virus', Nature 398, 441-443.
Turner, P. E., Burch, C., Hanley, K. and Chao, L.: 1999, 'Hybrid frequencies confirm limit to coinfection in the RNA bacteriophage ö6', J. Virol. 73, 2420-2424
Tyler, K. and Fields, B.: 1986, 'Reovirus and its Replication', in B. Fields and D. Knipe (eds), Fundamental Virology, Raven Press, New York.
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Turner, P.E. Searching for the Advantages of Virus Sex. Orig Life Evol Biosph 33, 95–108 (2003). https://doi.org/10.1023/A:1023973015054
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DOI: https://doi.org/10.1023/A:1023973015054