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Inferring the major genomic mode of dominance and overdominance

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Abstract

The mode of within-locus gene action in most genomic regions is termed as the major genomic mode, i.e., it is the within-locus allelic effects in most regions of the genome. Determining whether dominance or overdominance is the major genomic mode is important for two long-standing evolutionary genetics issues: 1. How is the genetic variation in most genomic regions maintained? 2. What is the major mechanism for heterosis? Many efforts have been made, but almost all of them suffer some explanational difficulties. Here we propose an alternative inference approach. It is based on the existent theoretical results on the correlation of the recombination rate and the level of neutral variation in different genomic regions. Positive and negative correlations suggest dominance and overdominance, respectively, as the major genomic mode. Zero correlations imply either few selected sites or about equal composition and distribution of dominant and overdominant regions in the genome, depending on the data distribution. This approach not only avoids all the problems associated with earlier approaches, but it is also particularly useful in organisms where controlled breeding is difficult. Well-corroborated data in Drosophila and recently emerging data in mice and humans all suggest dominance as the major genomic mode.

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References

  • Aguade, M. & C. Langley, 1994. Polymorphism and divergence in regions of low recombination in Drosophila, pp. 67-76 in Non-neutral Evolution, edited by B. Golding, Chapman & Hall, New York.

    Google Scholar 

  • Aquadro, C.F., D.J. Begun & E.C. Kindahl, 1994. Selection, recombination, and DNA polymorphism in Drosophila, pp. 47-70 in Non-neutral Evolution, edited by B. Golding, Chapman & Hall, New York.

    Google Scholar 

  • Barrett, S.C.H. & D. Charlesworth, 1991. Effects of a change in the level of inbreeding on the genetic load. Nature 352: 522-524.

    Article  PubMed  CAS  Google Scholar 

  • Begun, D. & C.F. Aquadro, 1992. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356: 519-520.

    Article  PubMed  CAS  Google Scholar 

  • Cavalli-Sforza, L. L. & W. F. Bodmer, 1971. The Genetics of Human Populations. W.H. Freeman, New York.

    Google Scholar 

  • Charlesworth, B., M. T. Morgan & D. Charlesworth, 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.

    PubMed  CAS  Google Scholar 

  • Charlesworth, D. & B. Charlesworth, 1987. Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecolo. Syst. 18: 237-268.

    Article  Google Scholar 

  • Charlesworth, D., B. Charlesworth & M. T. Morgan, 1995. The pattern of neutral variation under the background selection model. Genetics 141: 1618-1632.

    Google Scholar 

  • Charlesworth, B. & K. A. Hughes, 1997. The maintenance of genetic variation in life-history traits, in Evolutionary Genetics from Molecules to Morphology, edited by R.S. Singh & C.B. Krimbas. Cambridge University Press, Cambridge, UK, in press.

    Google Scholar 

  • Crow, J. F., 1952. Dominance and Overdominance, pp. 282-297 in Heterosis, edited by J. W. Gowen. Iowa State College Press, Ames, Iowa.

    Google Scholar 

  • Crow, J. F., 1993. Mutation, mean fitness, and genetic load, in Oxford Surveys in Evolutionary Biology, Vol. 9., Oxford.

  • Crow, J. & M. Kimura, 1970. An Introduction to Population Genetics Theory. Happer & Row, New York.

    Google Scholar 

  • Davenport, C. B., 1908. Degeneration, albinism and inbreeding. Science 28: 454-455.

    PubMed  Google Scholar 

  • Deng, H.W., 1998. Estimating (over)dominance coefficient and discriminating dominance vs. overdominance as the genetic cause of heterosis. Genetics 148: in press.

  • East, E. M., 1908. Inbreeding in corn. Rept. Conn. Agrc. Exp. Stn. (1907) 419-428.

  • Falconer, D. S., 1989. Introduction to Quantitative Genetics. Longman, New York.

    Google Scholar 

  • Fu, Y.-B. & K. Ritland 1996. Marker-based inference about epistasis for gene influencing inbreeding depression. Genetics 144: 339- 348.

    Google Scholar 

  • Fu, Y.-X. & W.-H. Li 1993. Statistical test of neutrality of mutations. Genetics 133: 693-709.

    PubMed  CAS  Google Scholar 

  • Gregory, W. C., 1965. Mutation frequency, magnitude of change and the probability of improvement in adaptation. Radiation Botany 5 (Suppl.): 429-441.

    Google Scholar 

  • Hilliker, A. J., G. Harauz, A. G. Reaume, M. Gray, S. H. Clark & A. Chovnick, 1994. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics 137: 1019-1026.

    PubMed  CAS  Google Scholar 

  • Houle, D., 1989. Allozyme-associated heterosis in Drosophila melanogaster. Genetics 123: 789-801.

    PubMed  CAS  Google Scholar 

  • Houle, D., 1994. Adaptive distance and the genetic basis of heterosis. Evolution 48: 1410-1417.

    Article  Google Scholar 

  • Houle, D., B. Morikawa & M. Lynch, 1996. Comparing mutational variabilities. Genetics 143: 1467-1483.

    PubMed  CAS  Google Scholar 

  • Hudson, R.R., 1983. Properties of a neutral allele model with intragenic recombination. Theor. Popul. Biol. 23: 1183-201.

    Google Scholar 

  • Hudson, R.R., 1990. Gene genealogies and coalescent process. pp 1-44 in Oxford Surveys in Evolutionary Biology, edited by D. Futuyma & J. Antonovics. Oxford University Press, Oxford.

    Google Scholar 

  • Hudson, R.R. & N.L. Kaplan, 1988. The coalescent process in models with selection and recombination. Genetics 120: 831-40.

    PubMed  CAS  Google Scholar 

  • Hudson, R.R. & N.L. Kaplan, 1994. Gene trees with background selection. pp. 140-153 in Non-Neutral Evolution, edited by B. Golding. Chapman & Hall, New York.

    Google Scholar 

  • Hudson, R.R. & N.L. Kaplan, 1995. Deleterious background selection with recombination. Genetics 141: 1605-1617.

    PubMed  CAS  Google Scholar 

  • Hudson, R.R., M. Kreitman & M. Aquade, 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153- 159.

    PubMed  CAS  Google Scholar 

  • Kaplan, N.L., T. Darden & R.R. Hudson, 1988. The coalescent process in models with selection. Genetics 120: 819-29.

    PubMed  CAS  Google Scholar 

  • Kaplan, N.L.. R.R. Hudson & C.H. Langley, 1989. The ‘hitchhiking effect’ revisited. Genetics 123: 887-899.

    PubMed  CAS  Google Scholar 

  • Kimura, M., 1968. Evolutionary rate at the molecular level. Nature 217: 624-626.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, M., 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge.

    Google Scholar 

  • King, J.L. & T.H. Jukes, 1969. Non-Darwinian evolution. Science 164: 788-798.

    PubMed  CAS  Google Scholar 

  • Kreitman, M. & M. Aquade, 1986. Excess polymorphism at the ADH locus in Drosophila melanogaster. Genetics 114: 93-110.

    PubMed  CAS  Google Scholar 

  • Lande, R. & D.W. Schemske, 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24-40.

    Google Scholar 

  • Lewontin, R.C., 1974. The Genetic Basis of York.

  • Li, C.C., 1967. Genetic equilibrium under selection. Biometrics 23: 397-484.

    Article  PubMed  CAS  Google Scholar 

  • Lynch, M. & B. Walsh. 1997. Principles of Evolutionary Quantitative Genetics. in press. Sinauer, Sunderland, MA.

    Google Scholar 

  • Mandel, S.P.H. 1959. The stability of a multiallelic system. Heredity 13: 289-302.

    Google Scholar 

  • Maynard Smith, J. & J. Haigh, 1974. The hitchhiking effect of a favorable gene. Genet. Res. 231: 1114-1116.

    Google Scholar 

  • McDonald, J. & M. Kreitman, 1991. Adaptive protein evolution at Adh locus in Drosophila. Nature 351: 652-654.

    Article  PubMed  CAS  Google Scholar 

  • Minvielle, F., 1987. Dominance is not necessary for heterosis: a two-locus model. Genetical Research 49: 245-247.

    Article  Google Scholar 

  • Mitton, J.B., 1993. Theory & data pertinent to the relationship between heterozygosity and fitness, pp. 17-41 in The History of Inbreeding and Outbreeding, edited by N.D. Thornhill. The University of Chicago Press, Chicago.

    Google Scholar 

  • Nachman, M.W., in review for Genetics. DNA variability, selection, and recombination at four X-linked loci in Mus domesticus.

  • Nei, M., 1987. Molecular Evolutionary Genetics. Columbia Univ. Press. New York.

    Google Scholar 

  • Oakeshott, J.G., J.B. Gibson, P.R. Anderson, W.R. Knibb, D.G. Anderson & G.K. Chambers, 1982. Alcohol dehydrogenase and glyceral-3-phosphate dehydrogenase clines in Drosohpila melanogaster on three continents. Evolution 36: 86-96.

    Article  Google Scholar 

  • Richey, F.D., 1942. Mock-dominance and hybrid vigor. Science 96: 280-281.

    PubMed  Google Scholar 

  • Robertson, A., 1962. Selection for heterozygotes in small populations. Genetics 47: 1291-1230.

    PubMed  CAS  Google Scholar 

  • Schemske, D.W. & R. Lande, 1985. The evolution of self-fertilization and inbreeding depression in plants. II Empirical observations. Evolution 39: 41-52.

    Article  Google Scholar 

  • Schnell, F.W. & C.C. Cockerham, 1992. Multiplicative vs. arbitrary gene action in heterosis. Genetics 131: 461-469.

    PubMed  CAS  Google Scholar 

  • Shields, W.M., 1982. Philotary, Inbreeding, and the Evolution of Sex. SUNY press, Albany, New York.

    Google Scholar 

  • Shull, G.H., 1908. The composition of a field of maize. Rpt. Am, Breed. Assoc. 4: 296-301.

    Google Scholar 

  • Simmons, M.J. & J.F. Crow, 1977. Mutations affecting fitness in Drosophila populations. Ann. Rev. Genet. 11: 49-78.

    Article  PubMed  CAS  Google Scholar 

  • Soule, M., 1986. Conservation Biology. Sinauer Association, Sunderland, Mass.

    Google Scholar 

  • Sprague, G.F., 1983. Heterosis in maize: Theory and practice, pp. 47-70 in Heterosis: Reappraisal of Theory and Practice, edited by R. Frankel, Springer-Verlag, Berlin.

    Google Scholar 

  • Stearns, S.C., 1992. The Evolution of Life-Histories. Oxford Univ. Press. New York.

    Google Scholar 

  • Stephan, W., 1994. Effects of genetic recombination and population subdivision on nucleotide sequence variation in Drosophila ananassae, pp. 57-66 in Non-neutral Evolution, edited by B. Golding, Chapman & Hall, New York.

    Google Scholar 

  • Stephan, W., T.H.E. Wiehe & M.W. Lenz, 1992. The effect of strongly selected substitutions on neutral polymorphism: analytical results based on diffusion theory. Theor. Popul. Biol. 41: 1039-1045.

    Google Scholar 

  • Stuber, C.W., S.E. Lincoln, D.W. Wolff, T. Helentijaris & E.S. Lander, 1992. Identification of genetic factors in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132: 823-839.

    PubMed  CAS  Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.

    PubMed  CAS  Google Scholar 

  • Tajima, F., 1990. Relationship between DNA polymorphism and fixation time. Genetics 125: 447-454.

    PubMed  CAS  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimating the number of nucleotide substitutions in the control region of mitochondrial DNA in human and chimpanzees. Mol. Biol. Evol. 10: 512-526.

    PubMed  CAS  Google Scholar 

  • Thomson, G., 1977. The effect of a selected locus on a linked neutral locus. Genetics 85: 752-778.

    Google Scholar 

  • Vigilant L., M. Stoneking, H. Harpending, K. Hawkes, & A. C. Wilson, 1991. African populations and the evolution of human mitochondrial DNA. Science 253: 1503-1507.

    PubMed  CAS  Google Scholar 

  • Wallace, B., 1989. One selectionist's perspective. Quart. Rev. Biol. 64: 127-145.

    Article  PubMed  CAS  Google Scholar 

  • Wiehe, T.H.E. & W. Stephan, 1993. Analysis of a genetic hitchhiking model and its application to DNA polymorphism data from Drosophila melanogaster. Mol. Biol. Evol. 10: 824-854.

    Google Scholar 

  • Wright, S. 1977. Evolution and the Genetics of Populations. Vol. 3. Experimental results and evolutionary deductions. The University of Chicago Press, Chicago.

    Google Scholar 

  • Zukerkandl, E., 1976. Gene control in eukaryotes and the C-value paradox: ‘Excess’ DNA as an impediment to transcription of coding sequences. J. Mol. Evol. 9: 73-104.

    Article  Google Scholar 

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Deng, HW., Fu, YX. & Lynch, M. Inferring the major genomic mode of dominance and overdominance. Genetica 102, 559–567 (1998). https://doi.org/10.1023/A:1017084220186

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