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. 1998 Oct;150(2):523–532. doi: 10.1093/genetics/150.2.523

Sex and the evolution of intrahost competition in RNA virus phi6.

P E Turner 1, L Chao 1
PMCID: PMC1460345  PMID: 9755186

Abstract

Sex allows beneficial mutations that occur in separate lineages to be fixed in the same genome. For this reason, the Fisher-Muller model predicts that adaptation to the environment is more rapid in a large sexual population than in an equally large asexual population. Sexual reproduction occurs in populations of the RNA virus phi6 when multiple bacteriophages coinfect the same host cell. Here, we tested the model's predictions by determining whether sex favors more rapid adaptation of phi6 to a bacterial host, Pseudomonas phaseolicola. Replicate populations of phi6 were allowed to evolve in either the presence or absence of sex for 250 generations. All experimental populations showed a significant increase in fitness relative to the ancestor, but sex did not increase the rate of adaptation. Rather, we found that the sexual and asexual treatments also differ because intense intrahost competition between viruses occurs during coinfection. Results showed that the derived sexual viruses were selectively favored only when coinfection is common, indicating that within-host competition detracts from the ability of viruses to exploit the host. Thus, sex was not advantageous because the cost created by intrahost competition was too strong. Our findings indicate that high levels of coinfection exceed an optimum where sex may be beneficial to populations of phi6, and suggest that genetic conflicts can evolve in RNA viruses.

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Selected References

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  1. Birdsell J., Wills C. Significant competitive advantage conferred by meiosis and syngamy in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):908–912. doi: 10.1073/pnas.93.2.908. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chao L. Evolution of sex in RNA viruses. J Theor Biol. 1988 Jul 8;133(1):99–112. doi: 10.1016/s0022-5193(88)80027-4. [DOI] [PubMed] [Google Scholar]
  3. Chao L. Fitness of RNA virus decreased by Muller's ratchet. Nature. 1990 Nov 29;348(6300):454–455. doi: 10.1038/348454a0. [DOI] [PubMed] [Google Scholar]
  4. Chao L., Tran T. T., Tran T. T. The advantage of sex in the RNA virus phi6. Genetics. 1997 Nov;147(3):953–959. doi: 10.1093/genetics/147.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cole C. N., Baltimore D. Defective interfering particles of poliovirus. 3. Interference and enrichment. J Mol Biol. 1973 May 25;76(3):345–361. doi: 10.1016/0022-2836(73)90509-3. [DOI] [PubMed] [Google Scholar]
  6. Day L. A., Mindich L. The molecular weight of bacteriophage phi 6 and its nucleocapsid. Virology. 1980 Jun;103(2):376–385. doi: 10.1016/0042-6822(80)90196-8. [DOI] [PubMed] [Google Scholar]
  7. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. doi: 10.1093/genetics/78.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gerrish P. J., Lenski R. E. The fate of competing beneficial mutations in an asexual population. Genetica. 1998;102-103(1-6):127–144. [PubMed] [Google Scholar]
  9. Gottlieb P., Metzger S., Romantschuk M., Carton J., Strassman J., Bamford D. H., Kalkkinen N., Mindich L. Nucleotide sequence of the middle dsRNA segment of bacteriophage phi 6: placement of the genes of membrane-associated proteins. Virology. 1988 Mar;163(1):183–190. doi: 10.1016/0042-6822(88)90245-0. [DOI] [PubMed] [Google Scholar]
  10. Henle W., Henle G. INTERFERENCE OF INACTIVE VIRUS WITH THE PROPAGATION OF VIRUS OF INFLUENZA. Science. 1943 Jul 23;98(2534):87–89. doi: 10.1126/science.98.2534.87. [DOI] [PubMed] [Google Scholar]
  11. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. doi: 10.1126/science.7041255. [DOI] [PubMed] [Google Scholar]
  12. Huang A. S., Baltimore D. Defective viral particles and viral disease processes. Nature. 1970 Apr 25;226(5243):325–327. doi: 10.1038/226325a0. [DOI] [PubMed] [Google Scholar]
  13. Hurst L. D., Atlan A., Bengtsson B. O. Genetic conflicts. Q Rev Biol. 1996 Sep;71(3):317–364. doi: 10.1086/419442. [DOI] [PubMed] [Google Scholar]
  14. Jarvis T. C., Kirkegaard K. The polymerase in its labyrinth: mechanisms and implications of RNA recombination. Trends Genet. 1991 Jun;7(6):186–191. doi: 10.1016/0168-9525(91)90434-R. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lyttle T. W. Cheaters sometimes prosper: distortion of mendelian segregation by meiotic drive. Trends Genet. 1993 Jun;9(6):205–210. doi: 10.1016/0168-9525(93)90120-7. [DOI] [PubMed] [Google Scholar]
  16. McGraw T., Mindich L., Frangione B. Nucleotide sequence of the small double-stranded RNA segment of bacteriophage phi 6: novel mechanism of natural translational control. J Virol. 1986 Apr;58(1):142–151. doi: 10.1128/jvi.58.1.142-151.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mindich L., Nemhauser I., Gottlieb P., Romantschuk M., Carton J., Frucht S., Strassman J., Bamford D. H., Kalkkinen N. Nucleotide sequence of the large double-stranded RNA segment of bacteriophage phi 6: genes specifying the viral replicase and transcriptase. J Virol. 1988 Apr;62(4):1180–1185. doi: 10.1128/jvi.62.4.1180-1185.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mindich L., Sinclair J. F., Levine D., Cohen J. Genetic studies of temperature-sensitive and nonsense mutants of bacteriophage phi6. Virology. 1976 Nov;75(1):218–223. doi: 10.1016/0042-6822(76)90020-9. [DOI] [PubMed] [Google Scholar]
  19. Paquin C. E., Adams J. Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature. 1983 Nov 24;306(5941):368–370. doi: 10.1038/306368a0. [DOI] [PubMed] [Google Scholar]
  20. Perrault J., Semler B. L. Internal genome deletions in two distinct classes of defective interfering particles of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6191–6195. doi: 10.1073/pnas.76.12.6191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pressing J., Reanney D. C. Divided genomes and intrinsic noise. J Mol Evol. 1984;20(2):135–146. doi: 10.1007/BF02257374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Re G. G., Gupta K. C., Kingsbury D. W. Genomic and copy-back 3' termini in Sendai virus defective interfering RNA species. J Virol. 1983 Feb;45(2):659–664. doi: 10.1128/jvi.45.2.659-664.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Semancik J. S., Vidaver A. K., Van Etten J. L. Characterization of segmented double-helical RNA from bacteriophage phi6. J Mol Biol. 1973 Aug 25;78(4):617–625. doi: 10.1016/0022-2836(73)90283-0. [DOI] [PubMed] [Google Scholar]
  24. Silver L. M. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 1993 Jul;9(7):250–254. doi: 10.1016/0168-9525(93)90090-5. [DOI] [PubMed] [Google Scholar]
  25. Vidaver A. K., Koski R. K., Van Etten J. L. Bacteriophage phi6: a Lipid-Containing Virus of Pseudomonas phaseolicola. J Virol. 1973 May;11(5):799–805. doi: 10.1128/jvi.11.5.799-805.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zeyl C., Bell G. The advantage of sex in evolving yeast populations. Nature. 1997 Jul 31;388(6641):465–468. doi: 10.1038/41312. [DOI] [PubMed] [Google Scholar]

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