Divided genomes and intrinsic noise
Segmental genomes (i.e., genomes in which the genetic information is dispersed between two or more discrete molecules) are abundant in RNA viruses, but virtually absent in DNA viruses. It has been suggested that the division of information in RNA viruses expands the pool of variation available to natural selection by providing for the reassortment of modular RNAs from different genetic sources. This explanation is based on the apparent inability of related RNA molecules to undergo the kinds of physical recombination that generate variation among related DNA molecules. In this paper we propose a radically different hypothesis. Self-replicating RNA genomes have an error rate of about 10−3–10−4 substitutions per base per generation, whereas for DNA genomes the corresponding figure is 10−9–10−11. Thus the level of noise in the RNA copier process is five to eight orders of magnitude higher than that in the DNA process. Since a small module of information has a higher chance of passing undamaged through a noisy channel than does a large one, the division of RNA viral information among separate small units increases its overall chances of survival. The selective advantage of genome segmentation is most easily modelled for modular RNAs wrapped up in separate viral coats. If modular RNAs are brought together in a common viral coat, segmentation is advantageous only when interactions among the modular RNAs are selective enought to provide some degree of discrimination against miscopied sequences. This requirement is most clearly met by the reoviruses.
Key wordsRNA viruses Divided genomes Copying fidelity Intrinsic selection pressure
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- Bancroft JB (1972) A virus made from parts of the genomes of brome mosaic and cowpea chlorotic mottle viruses. J Gen Virol 14:223–228Google Scholar
- Drake JW (1974) The role of mutation in microbial evolution. Soc Gen Microbiol Symp (Cambridge) 24:41–58Google Scholar
- Holland J, Spindler K, Horodyski F, Grabau, E, Nichol S, Vande Pol S (1982) Rapid evolution of RNA genomes. Science 215:1577–1585Google Scholar
- Joklik W (1974) Evolution in viruses. Soc Gen Microbiol (Cambridge) 42:293–320Google Scholar
- Kornberg A (1980) DNA replication. WH Freeman and Co, San Francisco, p 724Google Scholar
- Lane LC (1979) The RNAs of multipartite and satellite viruses of plants. In: Hall TC, Davies JW (eds) Nucleic acids in plants, vol 2. CRC Press, Boca Raton, pp 65–110Google Scholar
- Maynard-Smith J (1978) The evolution of sex. Cambridge University Press. Cambridge, England, chapter 1Google Scholar
- Reanney DC, Pressing J (1983) Heat as a determinative factor in the evolution of genetic systems. J Mol Evol, submittedGoogle Scholar
- Reanney DC (1984) The molecular evolution of RNA viruses. Soc Gen Microbiol Symp (Cambridge) 35:175–196Google Scholar
- Rose M, Doolittle WF (1983) Parasitic DNA—the origin of species and sex. New Scientist 16:787–789Google Scholar
- Shannon CE (1949) The mathematical theory of communication. In: Shannon CE, Weaver W (eds) The mathematical theory of communication. University of Illinois Press, Urbana, IllinoisGoogle Scholar
- Webster RB, Granoff A (1974) The evolution of orthomyxoviruses. In: Kurstak E, Maramorosch K (eds) Viruses, evolution and cancer. Academic Press, New York, pp 625–647Google Scholar