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Waiting for a compensatory mutation: phase zero of the shifting-balance process

Published online by Cambridge University Press:  14 April 2009

Patrick C. Phillips
Patrick C. Phillips*
Affiliation:
Biology Department, University of Texas at Arlington, Arlington, Texas, USA
*
†All correspondence should be addressed to: Patrick Phillips. Biology Department, Box 19498, University of Texas at Arlington, Arlington, TX 76019-0498, USA. Telephone: + 1(817)272-2409, Fax: +1(817)272-2855, e-mail: pphillips@uta.edu.
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In highly integrated genetic systems, changes in any one component may have a deleterious effect on fitness, but coordinated, or compensatory, change in these components could lead to an overall increase in fitness compared with the current state. Wright designed his shifting-balance theory to account for evolutionary change in such systems, since natural selection alone can not lead to the new optimal state. A largely untreated aspect of the shifting-balance theory, that of the limiting impact of waiting for the production of new mutations, is analysed here. It is shown that the average time to double fixation of compensatory mutations is extremely long (of the order of tens or hundreds of thousands of generations), because selection is too effective in large populations, and mutations are too rare in small populations. Further, the probability that a new mutant will arise and undergo fixation quickly is extremely small. Tight linkage can reduce the time to fixation somewhat, but only in models in which the double heterozygote does not have reduced fitness. It is argued that the only reasonable way for compensatory mutations to become fixed in a population is if the new mutants are first allowed to achieve a moderate frequency through the relaxation of selection. Under these conditions, the time required to reach fixation is reasonably low, althoug the probability of being fixed is still small when the initial allele frequencies are low. It is likely that the waiting time for fixation of new mutants, which is here called phase zero, is the major limiting factor for the success of the shifting-balance process

Information

Type
Research Article
Information
Genetics Research , Volume 67 , Issue 3 , June 1996, pp. 271 - 283
Copyright
Copyright © Cambridge University Press 1996

References

Barton, N. H., (1992). On the spread of a new gene combination in the third phase of Wright's shiftingbalance. Evolution 46, 551–557.Google ScholarPubMed
Barton, N. H., & Rouhani, S., (1993). Adaptation and the ‘shifting-balance’. Genetical Research, Cambridge 125, 57–74.CrossRefGoogle Scholar
Brimacombe, R., (1984). Conservation of structure in ribosomal RNA. Tends in Biochemical Sciences 9, 273–277.CrossRefGoogle Scholar
Carson, H. L., & Templeton, A. R., (1984). Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics 15, 97–131.CrossRefGoogle Scholar
Charlesworth, B., & Smith, D. B., (1982). A computer model of speciation by founder effects. Genetical Research, Cambridge 39, 227–236.CrossRefGoogle Scholar
Crow, J. F., & Kimura, M., (1956). Some genetic problems in natural populations. In Proceedings of the Third Berkeley Symposium on Mathematical Statistics and Probability, vol. 4, pp. 1–2. Berkeley: University of California Press.Google Scholar
Crow, J. F., & Kimura, M., (1970). An Introduction to Population Genetics Theory. Minneapolis, Minnesota: Burgess.Google Scholar
Crow, J. F., Engels, W. R., & Denniston, C., (1990). Phase three of Wright's shifting-balance theory. Evolution 44, 233–247.CrossRefGoogle ScholarPubMed
Fisher, R. A., (1930). The Genetical Theory of Natural Selection. Oxford: Clarendon Press.CrossRefGoogle Scholar
Fitch, W. M., & Markowitz, E., (1970). An improved method for determining codon variability in a gene and its application to the rate of fixation of mutations in evolution. Biochemical Genetics 4, 579–593.CrossRefGoogle Scholar
Fu, Y.-X., & Arnold, J., (1992). Dynamics of cytonuclear disequilibria in finite populations and comparison with a two-locus nuclear system. Theoretical Population Biology 41, 1–25.CrossRefGoogle ScholarPubMed
Gillespie, J. H., (1984). Molecular evolution over the mutational landscape. Evolution 38; 1116–129.CrossRefGoogle ScholarPubMed
Haldane, J. B. S., (1931). A mathematical theory of natural selection. VI. Isolation. Transactions of the Cambridge Philosophical Society 26, 220–230.CrossRefGoogle Scholar
Karlin, S., & McGregor, J., (1968). Rates and probabilities of fixation for two locus random mating finite populations without selection. Genetics 58, 141–159.CrossRefGoogle ScholarPubMed
Kimura, M., (1955). Stochastic processes and distribution of gene frequencies under natural selection. Cold Spring Harbor Symposium on Quantitative Biology 20, 33–53.CrossRefGoogle ScholarPubMed
Kimura, M., (1964). Diffusion models in population genetics. Journal of Applied Probability 1, 177–232.CrossRefGoogle Scholar
Kimura, M., (1980). Average time until fixation of a mutant allele in a finite population under continued mutation pressure: studies by analytical, numerical, and pseudosampling methods. Proceedings of the National Academy of Sciences, USA 77, 522–526.CrossRefGoogle Scholar
Kimura, M., (1985 a). Diffusion models in population genetics with special reference to fixation time of molecular mutants under mutational pressure. In Population Genetics and Molecular Evolution (ed. Ohta, T. and Aoki, K.), pp. 19–39. Tokyo/Berlin: Japan Scientific Societies Press/Springer.Google Scholar
Kimura, M., (1985 b). The role of compensatory neutral mutation in molecular evolution. Journal of Genetics 64, 7–19.CrossRefGoogle Scholar
Kimura, M., (1990). Some models of neutral evolution, compensatory evolution, and the shifting balance process. Theoretical Population Biology 37, 150–158.CrossRefGoogle ScholarPubMed
Kimura, M., & Ohta, T., (1971). Theoretical Aspects of Population Genetics. Princeton N.J.: Princeton University Press.Google ScholarPubMed
Kimura, M., & Takahata, N., (1983). Selective constraint in protein polymorphism: study of the effectively neutral mutation model by using an improved pseudosampling method. Proceedings of the National Academy of Sciences, USA 80, 1048–1052.CrossRefGoogle ScholarPubMed
Kondrashov, A. S., (1992). The third phase of Wright's shifting-balance: a simple analysis of the extreme case. Evolution 46, 1972–1975.CrossRefGoogle ScholarPubMed
Lande, R., (1985). The fixation of chromosomal rearrangements in a subdivided population with local extinction and recolonisation. Heredity 54, 323–332.CrossRefGoogle Scholar
Lande, R., (1986). The dynamics of peak shifts and the pattern of morphological evolution. Paleobiology 12, 343–354.CrossRefGoogle Scholar
Lande, R., (1988). Genetics and demography in biological conservation. Science 241, 1455–146.CrossRefGoogle ScholarPubMed
Littler, R. A., (1973). Linkage disequilibrium in finite populations. Theoretical Population Biology 4, 259–275.CrossRefGoogle Scholar
Michalakis, Y., & Slatkin, M., (1996). Interaction of selection and recombination in the fixation of negative-epistatic genes. Genetical Research, Cambridge (in press).CrossRefGoogle ScholarPubMed
Moore, F. B.-G., & Tonsor, S. J., (1994). A simulation of Wright's shifting-balancing process: migration and the three phases. Evolution 48, 69–80.Google ScholarPubMed
Newman, C. M., Cohen, J. E., & Kipnis, C., (1985). Neo-Darwinian evolution implies punctuated equilibria. Nature 315, 400–402.CrossRefGoogle Scholar
Ohta, T., (1988). Evolution by gene duplication and compensatory advantageous mutations. Genetics 120, 841–847.CrossRefGoogle ScholarPubMed
Ohta, T., & Kimura, M., (1969). Linage disequilibrium due to random genetic drift. Genetical Research, Cambridge 13, 47–55.CrossRefGoogle Scholar
Orr, H. A., (1995). The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139, 1805–1813.CrossRefGoogle ScholarPubMed
Phillips, P. C., (1993). Peaks shifts and polymorphism during phase three of Wright's shifting-balance process. Evolution 47, 1733–1743.Google Scholar
Provine, W. B., (1989). Foundereffectsandgeneticrevolutions in microevolution and speciation: a historical perspective. In Genetics, Speciation, and the Founder Principle (ed. Giddings, L. V., Kaneshiro, K. Y. and Anderson, W. W.), pp. 43–76. New York: Oxford University Press.Google Scholar
Rouhani, S., & Barton, N. H., (1987). Speciation and the ‘shifting balance’ in a continuous population. Theoretical Population Biology 31, 465–492.CrossRefGoogle Scholar
Rouhani, S., & Barton, N. H., (1993). Group selection and the ‘shifting balance’. Genetical Research, Cambridge 61, 127–135.CrossRefGoogle Scholar
Rutledge, R. A., (1970). The survival of epistatic gene complexes in subdivided populations. Unpublished PhD dissertation, Columbia University.Google Scholar
Stephan, W., & Kirby, D. A., (1993). RNA folding in Drosophila.shows a distance effect of compensatory fitness interactions. Genetics 135, 97–103.CrossRefGoogle Scholar
Takahata, N., (1982). Sexual recombination under the joint effects of mutation, selection, and random sampling drift. Theoretical Population Biology 22, 258–277.CrossRefGoogle ScholarPubMed
Tjian, R., (1995). Molecular machines that control genes. Scientific American 272, 54–61.CrossRefGoogle ScholarPubMed
Tsukihara, T., Kobayashi, M., Nakamura, M., Katsube, Y., Fukuyama, K., Hase, T., Wada, K., & Matsubara, H., (1982). Structure-function relationship of [2Fe-2S] ferre doxins and design of a model molecule. Biosystems 15, 243–257.CrossRefGoogle Scholar
Whitlock, M. C., Phillips, P. C., Moore, F. B.-G., & Tonsor, S. J., (1995). Multiple fitness peaks and epistasis. Annual Review of Ecology and Systematics 26, 601–629.CrossRefGoogle Scholar
Wright, S., (1931). Evolution in Mendelian populations. Genetics 16, 97–159.CrossRefGoogle ScholarPubMed
Wright, S., (1932). The roles of mutation, inbreeding, crossbreeding and selection in evolution. In Proceedings of the 6th International Congress on Genetics, vol. 1, pp. 356–366.Google Scholar
Wright, S., (1977). Evolution and the Genetics of Populations, vol. 3, Experimental Results and Evolutionary Deductions. Chicago: University of Chicago Press.Google Scholar