Abstract
Mobile genetic elements may be molecular parasites that reduce the fitness of individuals that bear them by causing predominantly deleterious mutations, but increase in frequency when rare because transposition increases their rates of transmission to the progeny of crosses between infected and uninfected individuals. If this is true, then the initial spread of a mobile element requires sex. We tested this prediction using the yeast retrotransposon Ty3 and a strain of Saccharomyces cerevisiae lacking Ty3. We infected replicate isogenic sexual and asexual populations with a galactose-inducible Ty3 element at an initial frequency of 1%. In two of six asexual populations, active Ty3 elements increased in frequency to 38 and 86%, due to the spread in each population of a competitively superior mutant carrying a new Ty3 insertion. Ty3 frequencies increased above 80% in all sexual populations in which transposition was induced in haplophase or in diplophase. Ty3 did not increase in frequency when active during both haplophase and diplophase, apparently because of selective sweeps during adaptation to galactose. Repressed Ty3 elements spread in sexual populations, by increasing sexual fitness. These results indicate that active Ty3 elements are more likely to become established in sexual populations than in asexual populations.
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- Bilanchone V. W., Claypool J. A., Kinsey P. T., Sandmeyer S. B. Positive and negative regulatory elements control expression of the yeast retrotransposon Ty3. Genetics. 1993 Jul;134(3):685–700. doi: 10.1093/genetics/134.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boeke J. D., Eichinger D., Castrillon D., Fink G. R. The Saccharomyces cerevisiae genome contains functional and nonfunctional copies of transposon Ty1. Mol Cell Biol. 1988 Apr;8(4):1432–1442. doi: 10.1128/mcb.8.4.1432. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994 Sep 15;371(6494):215–220. doi: 10.1038/371215a0. [DOI] [PubMed] [Google Scholar]
- Futcher B., Reid E., Hickey D. A. Maintenance of the 2 micron circle plasmid of Saccharomyces cerevisiae by sexual transmission: an example of a selfish DNA. Genetics. 1988 Mar;118(3):411–415. doi: 10.1093/genetics/118.3.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hickey D. A. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics. 1982 Jul-Aug;101(3-4):519–531. doi: 10.1093/genetics/101.3-4.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kidwell M. G., Novy J. B., Feeley S. M. Rapid unidirectional change of hybrid dysgenesis potential in Drosophila. J Hered. 1981 Jan-Feb;72(1):32–38. doi: 10.1093/oxfordjournals.jhered.a109422. [DOI] [PubMed] [Google Scholar]
- Kirchner J., Sandmeyer S. B., Forrest D. B. Transposition of a Ty3 GAG3-POL3 fusion mutant is limited by availability of capsid protein. J Virol. 1992 Oct;66(10):6081–6092. doi: 10.1128/jvi.66.10.6081-6092.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mackay T. F. Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics. 1985 Oct;111(2):351–374. doi: 10.1093/genetics/111.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shah H. C., Carlson G. P. Alteration by phenobarbital and 3-methyl-cholanthrene of functional and structural changes in rat liver due to carbon tetrachloride inhalation. J Pharmacol Exp Ther. 1975 Apr;193(1):281–292. [PubMed] [Google Scholar]
- Torkamanzehi A., Moran C., Nicholas F. W. P element transposition contributes substantial new variation for a quantitative trait in Drosophila melanogaster. Genetics. 1992 May;131(1):73–78. doi: 10.1093/genetics/131.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilke C. M., Adams J. Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics. 1992 May;131(1):31–42. doi: 10.1093/genetics/131.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]