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Understanding quantitative genetic variation - Nature Reviews Genetics

  • ️Keightley, Peter D.
  • ️Tue Jan 01 2002
  • Provine, W. The Origins of Theoretical Population Genetics (Chicago Univ. Press, Chicago, Illinois, 1971).

    Google Scholar 

  • Barton, N. H. & Turelli, M. Evolutionary quantitative genetics: how little do we know? Annu. Rev. Genet. 23, 337–370 (1989).

    Article  CAS  PubMed  Google Scholar 

  • Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Longman, London, 1995).

    Google Scholar 

  • Roff, D. A. Evolutionary Quantitative Genetics (Chapman & Hall, New York, 1997).

    Book  Google Scholar 

  • Houle, D. Comparing evolvability and variability of quantitative traits. Genetics 130, 195–204 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewontin, R. C. The Genetic Basis of Evolutionary Change (Columbia Univ. Press, New York, 1974).

    Google Scholar 

  • Bodmer, W. F. & Cavalli-Sforza, L. L. Genetics, Evolution and Man (W. H. Freeman, San Francisco, 1976).

    Google Scholar 

  • Kondrashov, A. S. & Turelli, M. Deleterious mutations, apparent stabilising selection and the maintenance of quantitative variation. Genetics 132, 603–618 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).A comprehensive survey of the strength of selection on quantitative traits in natural populations, which implies that stabilizing selection might be less prevalent and is harder to measure accurately than has been previously thought.

    Article  CAS  PubMed  Google Scholar 

  • Fisher, R. A. The correlation between relatives on the supposition of Mendelian inheritance. Proc. R. Soc. Edinb. 52, 399–433 (1918).

    Google Scholar 

  • Hill, W. G. Rates of change in quantitative traits from fixation of new mutations. Proc. Natl Acad. Sci. USA 79, 142–145 (1982).This work quantified the contribution of new mutations to artificial selection response, and predicted that this could be substantial.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch, M. & Walsh, J. B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Sunderland, Massachusetts, 1998).

    Google Scholar 

  • Yoo, B. H. Long-term selection for a quantitative character in large replicate populations of Drosophila melanogaster. II. Lethals and visible mutants with large effects. Genet. Res. 35, 19–31 (1980).

    Article  Google Scholar 

  • Weber, K. E. Large genetic change at small fitness cost in large populations of Drosophila melanogaster selected for wind tunnel flight: rethinking fitness surfaces. Genetics 144, 205–213 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill, W. G. & Keightley, P. D. in Second International Conference on Quantitative Genetics (eds Eisen, E. J., Goodman, M. M., Namkoong, G. & Weir, B. S.) 57–70 (Sinauer Associates, Sunderland, Massachusetts, 1988).

    Google Scholar 

  • Orr, H. A. The genetics of species differences. Trends Ecol. Evol. 16, 343–358 (2001).

    Article  Google Scholar 

  • Kearsey, M. J. & Farquhar, A. G. L. QTL analysis in plants; where are we now? Heredity 80, 137–142 (1998).

    Article  PubMed  Google Scholar 

  • Mackay, T. F. C. Quantitative trait loci in Drosophila. Nature Rev. Genet. 2, 11–20 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Mackay, T. F. C. & Langley, C. H. Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster. Nature 348, 64–66 (1990).This paper shows that naturally occurring large insertions in a candidate gene for bristle number in Drosophila melanogaster are associated with bristle number variation.

    Article  CAS  PubMed  Google Scholar 

  • Long, A. D., Lyman, R. F., Morgan, A. H., Langley, C. H. & Mackay, T. F. C. Both naturally occurring insertions of transposable elements and intermediate frequency polymorphisms at the achaete scute complex are associated with variation in bristle number in Drosophila melanogaster. Genetics 154, 1255–1269 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth, B. & Langley, C. H. The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23, 251–287 (1989).

    Article  CAS  PubMed  Google Scholar 

  • Lyman, R. F., Lai, C. Q. & Mackay, T. F. C. Linkage disequilibrium mapping of molecular polymorphisms at the scabrous locus associated with naturally occurring variation in bristle number in Drosophila melanogaster. Genet. Res. 74, 303–311 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Long, A. D., Lyman, R. F., Langley, C. H. & Mackay, T. F. C. Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster. Genetics 149, 999–1017 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zapata, C. & Alvarez, G. The detection of gametic disequilibrium between allozyme loci in natural populations of Drosophila. Evolution 46, 1900–1917 (1992).

    Article  CAS  PubMed  Google Scholar 

  • Begun, D. J. & Aquadro, C. F. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 353, 548–549 (1993).

    Article  Google Scholar 

  • Przeworski, M., Wall, J. D. & Andolfatto, P. Recombination and the frequency spectrum in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 18, 291–298 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Teeter, K. et al. Haplotype dimorphism in a SNP collection from Drosophila melanogaster. J. Exp. Zool. 88, 63–75 (2000).

    Article  Google Scholar 

  • Stam, L. F. & Laurie, C. C. Molecular dissection of a major gene effect on a quantitative trait: the level of alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 144, 1559–1564 (1996).A beautiful paper that studied replicated transgenic constructs of the Adh gene in Drosophila to dissect the contribution of molecular variation in different parts of the gene to variation in enzyme activity.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurie-Ahlberg, C. C. Genetic variation affecting the expression of enzyme-coding genes in Drosophila: an evolutionary perspective. Curr. Top. Biol. Med. Res. 12, 33–88 (1985).

    CAS  Google Scholar 

  • Risch, N. J. Searching for genetic determinants in the new millennium. Nature 405, 847–856 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Cardon, L. R. & Bell, J. I. Association study designs for complex diseases. Nature Rev. Genet. 2, 91–99 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Weiss, K. M. & Terwilliger, J. D. How many diseases does it take to map a gene with SNPs? Nature Genet. 26, 151–157 (2001).

    Article  CAS  Google Scholar 

  • Graham, G. I., Wolff, D. W. & Stuber, C. W. Characterization of a yield quantitative trait locus on chromosome five of maize by fine mapping. Crop Sci. 37, 1601–1610 (1997).

    Article  CAS  Google Scholar 

  • Iraqi, F. et al. Fine mapping of trypanosomiasis resistance loci in murine advanced intercross lines. Mamm. Genome 11, 645–648 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Legare, M. E., Bartlett, F. S. & Frankel, W. N. A major effect QTL determined by multiple genes in epileptic EL mice. Genome Res. 10, 42–48 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Monforte, A. J. & Tanksley, S. D. Fine mapping of a quantitative trait locus (QTL) from Lycopersicon hirsutum chromosome 1 affecting fruit characteristics and agronomic traits: breaking linkage among QTL affecting different traits and dissection of heterosis for yield. Theor. Appl. Genet. 100, 471–497 (2000).

    Article  CAS  Google Scholar 

  • Podolin, P. L. et al. Localization of two insulin-dependent diabetes (Idd) genes to the Idd10 region on mouse chromosome 3. Mamm. Genome 9, 283–286 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Vladutu, C., McLaughlin, J. & Phillips, R. L. Fine mapping and characterization of linked quantitative trait loci involved in the transition of the maize apical meristem from vegetative to generative structures. Genetics 153, 993–1007 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez, D. E. & Wu, C. I. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics 140, 201–206 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doebley, J., Stec, A. & Hubbard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997).Reports what is generally accepted to be the first map-based cloning of a QTL, teosinte branched1.

    Article  CAS  PubMed  Google Scholar 

  • Frary, A., Nesbitt, T. C. & Frary, A. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Fridman, E., Pleban, T. & Zamir, D. A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc. Natl Acad. Sci. USA 97, 4718–4723 (2000).References 41 and 42 report successful positional cloning experiments for agronomic traits in tomato.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, R. L., Stec, A., Hey, J., Ukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236–239 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Barton, N. H. Pleiotropic models of quantitative variation. Genetics 124, 773–782 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turelli, M. Heritable genetic variation via mutation–selection balance: Lerch's ζ meets the abdominal bristle. Theor. Popul. Biol. 25, 138–193 (1984).

    Article  CAS  PubMed  Google Scholar 

  • Lande, R. The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet. Res. 26, 221–236 (1975).References 45 and 46 provide two mathematical analyses of the stabilizing selection model and come to different conclusions concerning the variation that can be maintained for quantitative traits, depending on the mutation rates at the individual loci involved.

    Article  CAS  PubMed  Google Scholar 

  • Wagner, G. P. Apparent stabilizing selection and the maintenance of neutral genetic variation. Genetics 143, 617–619 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keightley, P. D. & Eyre-Walker, A. Deleterious mutations and the evolution of sex. Science 290, 331–333 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Wagner, G. P. Multivariate mutation–selection balance with constrained pleiotropic effects. Genetics 122, 223–234 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turelli, M. Effects of pleiotropy on predictions concerning mutation–selection balance for polygenic traits. Genetics 111, 165–195 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keightley, P. D. & Hill, W. G. Quantitative genetic variability maintained by mutation/stabilising selection balance in finite populations. Genet. Res. 52, 33–43 (1988).

    Article  CAS  PubMed  Google Scholar 

  • Lyman, R. F., Lawrence, F., Nuzhdin, S. & Mackay, T. F. C. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics 143, 277–292 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hastings, A. & Hom, C. L. Pleiotropic stabilising selection limits the number of polymorphic loci to at most the number of characters. Genetics 122, 459–463 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright, S. Evolution in populations in approximate equilibrium. J. Genet. 30, 257–266 (1935).

    Article  Google Scholar 

  • Lerner, I. M. Genetic Homeostasis (Oliver & Boyd, Edinburgh, 1954).

    Google Scholar 

  • Gillespie, J. H. & Turelli, M. Genotype–environment interactions and the maintenance of polygenic variation. Genetics 137, 129–138 (1989).

    Article  Google Scholar 

  • Zhivotovsky, L. A. & Feldman, M. W. On models of quantitative genetic variation: a stabilizing selection-balance model. Genetics 130, 947–955 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podolsky, R. H. Genetic variation for morphological and allozyme variation in relation to population size in Clarkia dudleyana, an endemic annual. Conserv. Biol. 15, 412–423 (2001).

    Article  Google Scholar 

  • Charlesworth, D. & Mayer, S. Genetic variability of plant characters in the partial inbreeder Collinsia heterophylla (Scrophulariaceae). Am. J. Bot. 82, 112–120 (1995).

    Article  Google Scholar 

  • Smith, T. B. Disruptive selection and the genetic basis of bill size polymorphism in the African finch Pyrenestes. Nature 363, 618–620 (1993).

    Article  Google Scholar 

  • Sasaki, A. & Ellner, S. Quantitative genetic variance maintained by fluctuating selection with overlapping generations: variance components and covariances. Evolution 51, 682–696 (1997).

    Article  PubMed  Google Scholar 

  • Slatkin, M. Frequency- and density-dependent selection on a quantitative character. Genetics 93, 755–771 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulmer, M. G. The Mathematical Theory of Quantitative Genetics (Oxford Univ. Press, Oxford, 1985).

    Google Scholar 

  • Burger, R. Evolution of genetic variability and the advantage of sex and recombination in changing environments. Genetics 153, 1055–1069 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waxman, D. & Peck, J. R. Sex and adaptation in a changing environment. Genetics 153, 1041–1053 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kondrashov, A. S. & Yampolsky, L. Y. High genetic variability under the balance between symmetric mutation and fluctuating stabilizing selection. Genet. Res. 68, 157–164 (1996).

    Article  Google Scholar 

  • Robertson, A. Effect of selection against extreme deviants based on deviation or on homozygosis. J. Genet. 54, 236–248 (1956).

    Article  Google Scholar 

  • Gillespie, J. H. Pleiotropic overdominance and the maintenance of genetic variation in polygenic characters. Genetics 107, 321–330 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watt, W. B., Cassin, R. C. & Swan, M. S. Adaptation at specific loci. III. Field behaviour and survivorship differences among Colias PGI genotypes are predictable from in vitro biochemistry. Genetics 103, 725–729 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreitman, M. & Aguade, M. Excess polymorphism in the Adh region of Drosophila melanogaster. Genetics 114, 93–110 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes, A. L. Adaptive Evolution of Genes and Genomes (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  • Burger, R. The Mathematical Theory of Selection, Recombination and Mutation (Wiley, Chichester, UK, 2000).

    Google Scholar 

  • Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, 1930).

    Book  Google Scholar 

  • Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).

    Book  Google Scholar 

  • Orr, H. A. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935–949 (1998).An analysis of Fisher's model of adaptation, which shows that the distribution of factors fixed during adaptation is expected to be approximately exponential.

    Article  PubMed  Google Scholar 

  • Hayes, B. & Goddard, M. E. The distribution of the effects of genes affecting quantitative traits in livestock. Genet. Select. Evol. 33, 209–230 (2001).

    Article  CAS  Google Scholar 

  • Shrimpton, A. E. & Robertson, A. The isolation of polygenic factors controlling bristle score in Drosophila melanogaster. II. Distribution of third chromosome bristle effects within chromosome sections. Genetics 118, 445–459 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orr, H. A. Adaptation and the cost of complexity. Evolution 54, 13–20 (2000).

    Article  CAS  PubMed  Google Scholar 

  • True, H. L. & Lindquist, S. L. A yeast prion provides a mechanism for genetic variation and genetic diversity. Nature 407, 477–483 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Hirsh, A. E. & Fraser, H. B. Protein dispensability and rate of evolution. Nature 411, 1046–1049 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Smith, V., Chou, K. N., Lashkari, D., Botstein, D. & Borwn, P. O. Functional analysis of the genes of yeast chromosome V by genetic footprinting. Science 274, 2069–2074 (1996).

    Article  CAS  PubMed  Google Scholar 

  • Kauffman, S. Origins of Order (Cambridge Univ. Press, Cambridge, 1992).

    Google Scholar 

  • Kacser, H. in Evolution and Animal Breeding (eds Hill, W. G. & Mackay, T. F. C.) 219–226 (CAB International, Wallingford, UK, 1989).

    Google Scholar 

  • Hasty, J., McMillen, D., Isaacs, F. & Collins, J. J. Computational studies of gene regulatory networks: in numero molecular biology. Nature Rev. Genet. 2, 268–279 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Weber, K. E. et al. An analysis of polygenes affecting wing shape on chromosome 3 in Drosophila melanogaster. Genetics 153, 773–786 (1999).An extremely well-replicated QTL-mapping experiment for wing shape in Drosophila that points to a highly polygenic basis of inheritance.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keightley, P. D. Models of quantitative genetic variation of flux in metabolic pathways. Genetics 121, 869–876 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kacser, H. & Burns, J. A. The molecular basis of dominance. Genetics 97, 639–666 (1981).A classic paper that was one of the first to explicitly model a biochemical system and relate its properties to the properties of quantitative traits, such as dominance and epistasis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keightley, P. D. Metabolic models of selection response. J. Theor. Biol. 182, 311–316 (1996).

    Article  CAS  PubMed  Google Scholar 

  • Gurganus, M. C., Nuzhdin, S. V., Leips, J. W. & Mackay, T. F. C. High-resolution mapping of quantitative trait loci for sternopleural bristle number in Drosophila melanogaster. Genetics 152, 1585–1604 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long, A. D. et al. High resolution genetic mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics 139, 1273–1291 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Routman, E. J. & Cheverud, J. M. Gene effects on a quantitative trait: two-locus epistatic effects measured at microsatellite markers and at estimated QTL. Evolution 51, 1654–1662 (1997).

    PubMed  Google Scholar 

  • Eshed, Y. & Zamir, D. Less-than-additive epistatic interactions of quantitative trait loci in tomato. Genetics 143, 1807–1817 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukens, L. N. & Doebley, J. Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genet. Res. 74, 291–302 (1999).

    Article  CAS  Google Scholar 

  • Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–441 (1988).

    Article  CAS  PubMed  Google Scholar 

  • Lehman, N. & Joyce, G. F. Evolution in vitro: analysis of a lineage of ribozymes. Curr. Biol. 3, 723–734 (1993).

    Article  CAS  PubMed  Google Scholar 

  • McKenzie, J. A. & O'Farrell, K. Modification of developmental instability and fitness — malathion resistance in the Australian sheep blowfly, Lucilia cuprina. Genetica 89, 67–76 (1993).

    Article  Google Scholar 

  • Schrag, S. J., Perrot, V. & Levin, B. R. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. R. Soc. Lond. B 264, 1287–1291 (1997).

    Article  CAS  Google Scholar 

  • Stern, D. L. Evolutionary developmental biology and the problem of variation. Evolution 54, 1079–1091 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Weatherall, D. J. Phenotype–genotype relationships in monogenic disease: lessons from the thalassaemias. Nature Rev. Genet. 2, 245–255 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Dekkers, J. C. M. & Dentine, M. R. Quantitative genetic variance associated with chromosomal markers in segregating populations. Theor. Appl. Genet. 81, 212–220 (1991).

    Article  CAS  PubMed  Google Scholar 

  • Visscher, P. M. & Haley, C. S. Detection of putative quantitative trait loci in line crosses under infinitesimal genetic models. Theor. Appl. Genet. 93, 691–702 (1996).

    Article  CAS  PubMed  Google Scholar 

  • Noor, M. A., Cunningham, A. L. & Larkin, J. C. Consequences of recombination rate variation on quantitative trait locus mapping studies. Simulations based on the Drosophila melanogaster genome. Genetics 159, 581–588 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyne, V. & Kearsey, M. J. QTL analysis — further uses of marker regression. Theor. Appl. Genet. 91, 471–476 (1995).

    Article  CAS  PubMed  Google Scholar 

  • Beavis, W. D. in Proceedings of the Corn and Sorghum Industry Research Conference 250–266 (American Seed Trade Association, Washington DC, 1994).

    Google Scholar 

  • White, S. & Doebley, J. Of genes and genomes and the origin of maize. Trends Genet. 14, 327–332 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Doebley, J. & Stec, A. Genetic analysis of the morphological differences between maize and teosinte. Genetics 129, 285–295 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorweiler, J. et al. Teosinte glume architecture 1: a genetic locus controlling a key step in maize evolution. Science 262, 233–235 (1993).

    Article  CAS  PubMed  Google Scholar 

  • Doebley, J., Stec, A. & Gustus, C. Teosinte branched 1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141, 333–346 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrimpton, A. E. & Robertson, A. The isolation of polygenic factors controlling bristle score in Drosophila melanogaster. I. Allocation of third chromosome sternopleural bristle effect to chromosome sections. Genetics 118, 437–443 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paterson, A. H. et al. Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335, 721–726 (1988).

    Article  CAS  PubMed  Google Scholar 

  • Darvasi, A. Experimental strategies for the genetic dissection of complex traits in animal models. Nature Genet. 18, 19–24 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Breese, E. L. & Mather, K. The organization of polygenic activity within a chromosome in Drosophila. 1. Hair characters. Heredity 11, 373–395 (1957).

    Article  Google Scholar 

  • Adams, M. D., Celniker, S. E. & Holt, R. A. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 (2000).

    Article  PubMed  Google Scholar 

  • Lander, E. S. & Botstein, D. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185–199 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thoday, J. M. Location of polygenes. Nature 191, 368–370 (1961).

    Article  Google Scholar 

  • Yoo, B. H. Long-term selection for a quantitative character in large replicate populations of Drosophila melanogaster. I. Response to selection. Genet. Res. 35, 1–17 (1980).

    Article  Google Scholar 

  • Yoo, B. H. Long-term selection for a quantitative character in large replicate populations of Drosophila melanogaster. III. The nature of residual genetic variability. Theor. Appl. Genet. 57, 25–32 (1980).

    Article  CAS  PubMed  Google Scholar 

  • Barton, N. H. The geometry of adaptation. Nature 395, 751–752 (1998).

    Article  CAS  PubMed  Google Scholar