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The Evolutionary Reduction Principle for Linear Variation in Genetic Transmission

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Abstract

The evolution of genetic systems has been analyzed through the use of modifier gene models, in which a neutral gene is posited to control the transmission of other genes under selection. Analysis of modifier gene models has found the manifestations of an “evolutionary reduction principle”: in a population near equilibrium, a new modifier allele that scales equally all transition probabilities between different genotypes under selection can invade if and only if it reduces the transition probabilities. Analytical results on the reduction principle have always required some set of constraints for tractability: limitations to one or two selected loci, two alleles per locus, specific selection regimes or weak selection, specific genetic processes being modified, extreme or infinitesimal effects of the modifier allele, or tight linkage between modifier and selected loci. Here, I prove the reduction principle in the absence of any of these constraints, confirming a twenty-year-old conjecture. The proof is obtained by a wider application of Karlin’s Theorem 5.2 (Karlin in Evolutionary biology, vol. 14, pp. 61–204, Plenum, New York, 1982) and its extension to ML-matrices, substochastic matrices, and reducible matrices.

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References

  • Altenberg, L., 1984. A generalization of theory on the evolution of modifier genes. Ph.D. thesis, Stanford University. Searchable online and available from University Microfilms, Ann Arbor, MI.

  • Altenberg, L., Feldman, M.W., 1987. Selection, generalized transmission, and the evolution of modifier genes. I. The reduction principle. Genetics 117, 559–572.

    Google Scholar 

  • Balkau, B., Feldman, M.W., 1973. Selection for migration modification. Genetics 74, 171–174.

    MathSciNet  Google Scholar 

  • Barton, N.H., 1995. A general model for the evolution of recombination. Genet. Res. (Camb.) 65, 123–144.

    Google Scholar 

  • Cavalli-Sforza, L.L., Feldman, M.W., 1973. Models for cultural inheritance. I. Group mean and within group variation. Theor. Popul. Biol. 4, 42–55.

    Article  Google Scholar 

  • Charlesworth, B., 1976. Recombination modification in a fluctuating environment. Genetics 83, 181–195.

    MathSciNet  Google Scholar 

  • Charlesworth, B., 1993. Directional selection and the evolution of sex and recombination. Genet. Res. (Camb.) 61, 205–224.

    Google Scholar 

  • Cohen, J.E., 1978. Derivatives of the spectral radius as a function of non-negative matrix elements. Math. Proc. Camb. Philos. Soc. 83, 183–190.

    Article  MATH  Google Scholar 

  • Cohen, J.E., 1979. Random evolutions and the spectral radius of a non-negative matrix. Math. Proc. Camb. Philos. Soc. 86, 345–350.

    Article  MATH  Google Scholar 

  • Cohen, J.E., 1981. Convexity of the dominant eigenvalue of an essentially nonnegative matrix. Proc. Am. Math. Soc. 81, 657–658.

    Article  MATH  Google Scholar 

  • Deutsch, E., Neumann, M., 1984. Derivatives of the Perron root at an essentially nonnegative matrix and the group inverse of an M-matrix. J. Math. Anal. Appl. 102, 1–29.

    Article  MATH  MathSciNet  Google Scholar 

  • Deutsch, E., Neumann, M., 1985. On the first and second order derivatives of the Perron vector. Linear Algebra Appl. 71, 57–76.

    Article  MATH  MathSciNet  Google Scholar 

  • Feldman, M.W., 1972. Selection for linkage modification: I. Random mating populations. Theor. Popul. Biol. 3, 324–346.

    Article  Google Scholar 

  • Feldman, M.W., Balkau, B., 1973. Selection for linkage modification: II. A recombination balance for neutral modifiers. Genetics 74, 713–726.

    MathSciNet  Google Scholar 

  • Feldman, M.W., Krakauer, J., 1976. Genetic modification and modifier polymorphisms. In: Karlin, S., Nevo, E. (Eds.), Population Genetics and Ecology, pp. 547–583. Academic Press, New York.

    Google Scholar 

  • Feldman, M.W., Liberman, U., 1986. An evolutionary reduction principle for genetic modifiers. Proc. Natl. Acad. Sci. USA 83, 4824–4827.

    Article  MATH  MathSciNet  Google Scholar 

  • Feldman, M.W., Otto, S.P., 1991. A comparative approach to the population genetic theory of segregation distortion. Am. Nat. 137, 443–456.

    Article  Google Scholar 

  • Feldman, M.W., Christiansen, F.B., Brooks, L.D., 1980. Evolution of recombination in a constant environment. Proc. Natl. Acad. Sci. USA 77, 4838–4841.

    Article  MathSciNet  Google Scholar 

  • Feldman, M.W., Otto, S.P., Christiansen, F.B., 1997. Population genetic perspectives on the evolution of recombination. Annu. Rev. Genet. 20, 261–295.

    Google Scholar 

  • Felsenstein, J., 1974. The evolutionary advantage of recombination. Genetics 78, 737–756.

    Google Scholar 

  • Felsenstein, J., Yokoyama, S., 1976. The evolutionary advantage of recombination. II. Individual selection for recombination. Genetics 83, 845–859.

    Google Scholar 

  • Fisher, R.A., 1922. On the dominance ratio. Proc. R. Soc. Edinb. 42, 321–341.

    Google Scholar 

  • Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Clarendon Press, Oxford.

    MATH  Google Scholar 

  • Friedland, S., 1981. Convex spectral functions. Linear Multilinear Algebra 9, 299–316.

    Article  MATH  MathSciNet  Google Scholar 

  • Friedland, S., Karlin, S., 1975. Some inequalities for the spectral radius of non-negative matrices and applications. Duke Math. J. 42, 459–490.

    Article  MATH  MathSciNet  Google Scholar 

  • Gantmacher, F.R., 1959. The Theory of Matrices, vol. 2. Chelsea, New York.

    MATH  Google Scholar 

  • Haldane, J.B.S., 1924. A mathematical theory of natural and artificial selection. Part I. Trans. Camb. Philos. Soc. 23, 19–41.

    Google Scholar 

  • Hamilton, W.D., 1980. Sex versus non-sex versus parasite. Oikos 35, 282–290.

    Article  Google Scholar 

  • Karlin, S., 1982. Classification of selection-migration structures and conditions for a protected polymorphism. In: Hecht, M.K., Wallace, B., Prance, G.T. (Eds.), Evolutionary Biology, vol. 14, pp. 61–204. Plenum, New York.

    Google Scholar 

  • Karlin, S., McGregor, J., 1972. The evolutionary development of modifier genes. Proc. Natl. Acad. Sci. USA 69, 3611–3614.

    Article  Google Scholar 

  • Karlin, S., McGregor, J., 1974. Towards a theory of the evolution of modifier genes. Theor. Popul. Biol. 5, 59–103.

    Article  MathSciNet  Google Scholar 

  • Kimura, M., 1956. A model of a genetic system which leads to closer linkage by natural selection. Evolution 10, 278–287.

    Article  Google Scholar 

  • Liberman, U., Feldman, M.W., 1986a. Modifiers of mutation rate: A general reduction principle. Theor. Popul. Biol. 30, 125–142.

    Article  MATH  MathSciNet  Google Scholar 

  • Liberman, U., Feldman, M.W., 1986b. A general reduction principle for genetic modifiers of recombination. Theor. Popul. Biol. 30, 341–371.

    Article  MATH  MathSciNet  Google Scholar 

  • Liberman, U., Feldman, M.W., 1989. The reduction principle for genetic modifiers of the migration rate. In: Feldman, M.W. (Ed.), Mathematical Evolutionary Theory, pp. 111–137. Princeton University Press, Princeton.

    Google Scholar 

  • Maynard Smith, J., 1988. Selection for recombination in a polygenic model—the mechanism. Genet. Res. (Camb.) 51, 59–63.

    Article  Google Scholar 

  • Nei, M., 1967. Modification of linkage intensity by natural selection. Genetics 57, 625–641.

    MathSciNet  Google Scholar 

  • Odling-Smee, J., 2007. Niche inheritance: A possible basis for classifying multiple inheritance systems in evolution. Biol. Theory 2, 276–289.

    Article  Google Scholar 

  • Schauber, E., Goodwin, B., Jones, C., Ostfeld, R., 2007. Spatial selection and inheritance: applying evolutionary concepts to population dynamics in heterogeneous space. Ecology 88, 1112–1118.

    Article  Google Scholar 

  • Seneta, E., 1981. Non-negative Matrices and Markov Chains. Springer, New York.

    MATH  Google Scholar 

  • Wright, S., 1931. Evolution in Mendelian populations. Genetics 16, 97–159.

    Google Scholar 

  • Zhivotovsky, L.A., Feldman, M.W., Christiansen, F.B., 1994. Evolution of recombination among multiple selected loci: A generalized reduction principle. Proc. Natl. Acad. Sci. USA 91, 1079–1083.

    Article  Google Scholar 

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Correspondence to Lee Altenberg.

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Dedicated to my doctoral advisor Marc Feldman on his 65th birthday, and to the memory of Marc’s doctoral advisor, Sam Karlin, who each laid the foundations necessary for these results; and to my mother Elizabeth Lee and to the memory of my father Roger Altenberg, who together laid the foundation necessary for me.

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Altenberg, L. The Evolutionary Reduction Principle for Linear Variation in Genetic Transmission. Bull. Math. Biol. 71, 1264–1284 (2009). https://doi.org/10.1007/s11538-009-9401-2

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