Abstract
We present a theoretical framework within which to analyze the results of experimental evolution. Rapidly evolving organisms such as viruses, bacteria, and protozoa can be induced to adapt to laboratory conditions on very short human time scales. Artificial adaptive radiation is characterized by a list of common observations; we offer a framework in which many of these repeated questions and patterns can be characterized analytically. We allow for stochasticity by including rare mutations and bottleneck effects, demonstrating how these increase variability in the evolutionary trajectory. When the product Np, the population size times the per locus error rate, is small, the rate of evolution is limited by the chance occurrence of beneficial mutations; when Np is large and selective pressure is strong, the rate-limiting step is the waiting time while existing beneficial mutations sweep through the population. We derive the rate of divergence (substitution rate) and rate of fitness increase for the case when Np is large and illustrate our approach with an application to an experimental data set. A minimal assumption of independent additive fitness contributions provides a good fit to the experimental evolution of the bacteriophage phiX174.
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Selected References
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- Bull J. J., Badgett M. R., Wichman H. A. Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol. 2000 Jun;17(6):942–950. doi: 10.1093/oxfordjournals.molbev.a026375. [DOI] [PubMed] [Google Scholar]
- Bull J. J., Badgett M. R., Wichman H. A., Huelsenbeck J. P., Hillis D. M., Gulati A., Ho C., Molineux I. J. Exceptional convergent evolution in a virus. Genetics. 1997 Dec;147(4):1497–1507. doi: 10.1093/genetics/147.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eigen M., Schuster P. The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. Naturwissenschaften. 1977 Nov;64(11):541–565. doi: 10.1007/BF00450633. [DOI] [PubMed] [Google Scholar]
- Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971 Oct;58(10):465–523. doi: 10.1007/BF00623322. [DOI] [PubMed] [Google Scholar]
- Franklin I., Lewontin R. C. Is the gene the unit of selection? Genetics. 1970 Aug;65(4):707–734. doi: 10.1093/genetics/65.4.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Huynen M. A. Exploring phenotype space through neutral evolution. J Mol Evol. 1996 Sep;43(3):165–169. doi: 10.1007/BF02338823. [DOI] [PubMed] [Google Scholar]
- Huynen M. A., Stadler P. F., Fontana W. Smoothness within ruggedness: the role of neutrality in adaptation. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):397–401. doi: 10.1073/pnas.93.1.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones B. L. Some principles governing selection in self-reproducing macromolecular systems. An analog of Fisher's fundamental theorem. J Math Biol. 1978 Jul 27;6(2):169–175. doi: 10.1007/BF02450787. [DOI] [PubMed] [Google Scholar]
- Lenski R. E., Travisano M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6808–6814. doi: 10.1073/pnas.91.15.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miralles R., Gerrish P. J., Moya A., Elena S. F. Clonal interference and the evolution of RNA viruses. Science. 1999 Sep 10;285(5434):1745–1747. doi: 10.1126/science.285.5434.1745. [DOI] [PubMed] [Google Scholar]
- Miralles R., Moya A., Elena S. F. Diminishing returns of population size in the rate of RNA virus adaptation. J Virol. 2000 Apr;74(8):3566–3571. doi: 10.1128/jvi.74.8.3566-3571.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novella I. S., Quer J., Domingo E., Holland J. J. Exponential fitness gains of RNA virus populations are limited by bottleneck effects. J Virol. 1999 Feb;73(2):1668–1671. doi: 10.1128/jvi.73.2.1668-1671.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Papadopoulos D., Schneider D., Meier-Eiss J., Arber W., Lenski R. E., Blot M. Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3807–3812. doi: 10.1073/pnas.96.7.3807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rainey P. B., Travisano M. Adaptive radiation in a heterogeneous environment. Nature. 1998 Jul 2;394(6688):69–72. doi: 10.1038/27900. [DOI] [PubMed] [Google Scholar]
- Rosenzweig R. F., Sharp R. R., Treves D. S., Adams J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics. 1994 Aug;137(4):903–917. doi: 10.1093/genetics/137.4.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Treves D. S., Manning S., Adams J. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol. 1998 Jul;15(7):789–797. doi: 10.1093/oxfordjournals.molbev.a025984. [DOI] [PubMed] [Google Scholar]
- Tsimring LS, Levine H, Kessler DA. RNA virus evolution via a fitness-space model. Phys Rev Lett. 1996 Jun 3;76(23):4440–4443. doi: 10.1103/PhysRevLett.76.4440. [DOI] [PubMed] [Google Scholar]
- Wichman H. A., Badgett M. R., Scott L. A., Boulianne C. M., Bull J. J. Different trajectories of parallel evolution during viral adaptation. Science. 1999 Jul 16;285(5426):422–424. doi: 10.1126/science.285.5426.422. [DOI] [PubMed] [Google Scholar]