Skip to main content
Log in

Forging links between population and quantitative genetics

  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Summary

An initially rare allele with a large effect on a quantitative character is expected to exhibit the following behaviour in artificial selection lines:

  1. 1.

    It should change in frequency, or be lost by chance, at rates predictable from the effects of the allele on the quantitative character and the selection regime imposed.

  2. 2.

    At the phenotypic level the behaviour of the allele should cause (a) asymmetrical responses to bidirectional selection, (b) variation among replicate lines in response to selection corresponding to the behaviour of the allele in individual lines, (c) changes in heritability in lines in which the allele increases in frequency and (d) selection response compatible with the effects of the allele.

This paper reports an experimental evaluation of these predictions utilizing a rare allele of large effect (sm lab) detected in a sample of the Canberra outbred population of Drosophila melanogaster at a frequency of 1/120. Homosygosity for this allele reduced abdominal bristle number by more than 50%, altered the abdominal bristle pattern and reversed the sexual dimorphism for abdominal bristle number. Experiments were done to characterise sm lab and all evidence indicates that it is a single allele with a very large effect.

Bidirectional selection for abdominal bristle number was carried out in three high and three low lines from this sample of the Canberra population. The sm lab allele rose in frequency and went to fixation in two of the low lines (in 10 generations) but was lost from the third. These times to fixation were slower than the expectations derived from computer simulations of the behaviour of such an allele but this can be attributed to the lower fitness of sm lab homozygotes. The proportions of lines with the allele fixed or lost were compatible with expectations. At the phenotypic level, the behavior of sm lab had the expected consequences, namely, (i) asymmetrical responses to bidirectional selection, (ii) variation in response among replicate low lines corresponding to the behaviour of sm lab, (iii) changes in heritabilities in the lines in which sm lab went to fixation, and (iv) selection responses compatible with the effects of the allele.

A test for rare alleles of large effect was proposed, based on the expected pattern of change in heritability under artificial selection. This test was applied to the high selection lines but no evidence was found for important effects due to rare alleles of large effect increasing abdominal bristle number, a conclusion consistent with other independent evidence.

This work provides experimental corroboration of the links between population genetics and quantitative genetics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature

  • Avery, P.J.; Hill, W.G. (1977): Variability in genetic parameters among small populations. Genet. Res. 29, 193–213

    Google Scholar 

  • Beardmore, J.A.; Lints, F.; Al-Baldawi, A.T.F. (1975): Parental age and heritability of sternopleural chaeta number in Drosophila melanogaster. Heredity 34, 71–82

    Google Scholar 

  • Beardmore, J.A.; Shami, S.A. 1976: Parental age, genetic variation and selection. In: Population genetics and ecology (eds.: Karlin, S.; Nevo, E.), pp. 3–22. London: Acad. Press

    Google Scholar 

  • Bulmer, M.G. (1976): The effect of selection on genetic variability: A simulation study. Genet. Res. 28, 101–117

    Google Scholar 

  • Claxton, J.H. (1974): Some quantitative features of Drosophila sternite bristle patterns. Austr. J. Biol. Sci. 27, 533–543

    Google Scholar 

  • Constantino, R.F.; Bell, A.E.; Rogler, J.C. (1967): Genetic analysis of a population of Tribolium. 1: Corn oil sensitivity and selection response. Heredity 22, 529–539

    Google Scholar 

  • Crow, J.F.; Kimura, M. 1970: An Introduction to Population Genetics Theory. New York: Harper and Row

    Google Scholar 

  • Durrant, A. (1974): The association of induced changes in flax. Heredity 32, 133–143

    Google Scholar 

  • East, E.M. (1916): Studies on size inheritance in Nicotiana. Genetics 1, 164–176

    Google Scholar 

  • Falconer, D.S. (1960): Introduction to Quantitative Genetics. Edinburgh: Oliver and Boyd

    Google Scholar 

  • Falconer, D.S. (1977): Some results of the Edinburgh selection experiments with mice. In: Proc. Int. Conf. Quant. Genetics (Eds.: Pollak, E.; Kempthorne, O.; Bailey, T.B.Jr.), pp. 101–115. Ames: Iowa State Univ.

    Google Scholar 

  • Felsenstein, J. (1965): The effect of linkage on directional selection. Genetics 52, 349–363

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Fowler, R.E.; Edwards, R.G. (1961): ‘Midget’, a new dwarfing gene in the house mouse dependent on a genetic background of small body size for its expression. Genet. Res. 2, 272–282

    Google Scholar 

  • Frankham, R. (1974): The nature of quantitative genetic variation in Drosophila. 2: Average dominance of abdominal bristle polygenes. Austr. J. Biol. Sci. 27, 683–686

    Google Scholar 

  • Frankham, R. (1977): The nature of quantitative genetic variation in Drosophila. 3: Mechanism of dosage compensation for sex-linked abdominal bristle polygenes. Genetics 85, 185–191

    Google Scholar 

  • Frankham, R. (1980): The founder effect and response to artificial selection in Drosophila. In: Proc. Int. Sym. on Selection Experiments on Laboratory and Domestic Animals (ed.: Robertson, A.)

  • Frankham, R.; Briscoe, D.A.; Nurthen, R.K. (1978): Unequal crossing over at the rRNA locus as a source of quantitative genetic variation. Nature 272, 80–81

    Google Scholar 

  • Frankham, R.; Briscoe, D.A.; Nurthen, R.K. (1980): Unequal crossing over at the rRNA tandon as a source of quantitative genetic variation in Drosophila. Genetics 95, 121–142

    Google Scholar 

  • Frankham, R.; Jones, L.P.; Barker, J.S.F. (1968a): The effects of population size and selection intensity in selection for a quantitative character in Drosophila. 1: Short-term response to selection. Genet. Res. 12, 237–248

    Google Scholar 

  • Frankham, R.; Jones, L.P.; Barker, J.S.F. (1968b): The effects of population size and selection intensity in selection for a quantitative character in Drosophila. 3: Analyses of the lines. Genet. Res. 12, 267–283

    Google Scholar 

  • Fraser, A.; Miller, D.; Burnell, D. (1965): Polygenic balance. Nature 206, 114

    Google Scholar 

  • Haldane, J.B.S. 1932: The Causes of Evolution. London: Longmans Green

    Google Scholar 

  • Hollingdale, B. (1971): Analyses of some genes from abdominal bristle number selection lines in Drosophila melanogaster. Theor. Appl. Genet 41, 292–301

    Google Scholar 

  • Langley, C.H.; Smith, D.B.; Johnson, F.M. (1978): Analysis of linkage disequilibria between allozyme loci in natural populations of Drosophila melanogaster. Genet. Res. 32, 215–229

    Google Scholar 

  • Latter, B.D.H. (1964): Selection for a threshold character in Drosophila. 1: An analysis of the phenotypic variance on the underlying scale. Genet. Res. 5, 198–210

    Google Scholar 

  • Latter, B.D.H. (1965): The response to artificial selection due to autosomal genes of large effect. 1: Changes in gene frequency at an additive locus. Austr. J. Biol. Sci. 18, 585–598

    Google Scholar 

  • Latter, B.D.H. (1966): The response to artificial selection due to autosomal genes of large effect. 3: The effects of linkage on the rate of advance and approach to fixation in finite populations. Austr. J. Biol. Sci. 19, 131–146

    Google Scholar 

  • Lindsley, D.L.; Grell, E.H. (1968): Genetic variations of Drosophila melanogaster. Carnegie Inst. Wash. Publn. No. 627

  • Lindsley, D.L.; Sandler, L.; Baker, B.S.; Carpenter, A.T.C.; Denell, R.E.; Hall, J.C.; Jacobs, P.A.; Miklos, G.L.G.; Davis, B.K.; Gethmann, R.C.; Hardy, R.W.; Hessler, A.; Miller, S.M.; Nozawa, H.; Parry, D.M.; Gould-Somero, M. (1972): Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71, 157–184

    Google Scholar 

  • Marlowe, T.J. (1964): Evidence of selection for the Snorter dwarf gene in cattle. J. Anim. Sci. 23, 454–460

    Google Scholar 

  • Mather, K.; Harrison, B.J. (1949): The manifold effect of selection. I and II. Heredity 3, 1–52; 131–162

    Google Scholar 

  • Mather, K.; Jinks, J.L. 1971: Biometrical Genetics (2nd ed.). London: Chapman and Hall

    Google Scholar 

  • McBride, G.; Robertson, A. (1963): Selection using assortative mating in Drosophila melanogaster. Genet. Res. 4, 356–369

    Google Scholar 

  • McMillan, I.; Robertson, A. (1974): The power of methods for the detection of major genes affecting quantitative characters. Heredity 32, 349–356

    Google Scholar 

  • McPhee, C.P.; Robertson, A. (1970): The effect of suppressing crossing over on the response to selection in Drosophila melanogaster. Genet. Res. 16, 1–16

    Google Scholar 

  • Milkman, R. (1978): Review of Proceedings of the International Conference on Quantitative Genetics. Science 200, 1261–1262

    Google Scholar 

  • Piper, L.R. (1971): The isolation of genes underlying continuous variation. Ph.D. thesis. University of Edinburgh

  • Pollak, E.; Kempthorne, O.; Bailey, T.B. Jr. (eds.) (1977): Proc. Int. Conf. Quant. Genetics. Ames: Iowa State Univ.

    Google Scholar 

  • Popper, K.R. (1972): The Logic of Scientific Discovery. London: Hutchinson

    Google Scholar 

  • Reeve, E.C.R.; Robertson, F.W. (1954): Studies in quantitative inheritance. VI. Sternite chaeta number in Drosophila, a metameric quantitative character. Z. ind. Abst. Vererbungsl. 86, 269–288

    Google Scholar 

  • Robertson, A. (1960): A theory of limits in artificial selection. Proc. Roy. Soc. (Lond.) B 153, 234–249

    Google Scholar 

  • Robertson, A. (1966): Artificial selection in plants and animals. Proc. Roy. Soc. (Lond.) B 164, 341–349

    Google Scholar 

  • Robertson, F.W.; Reeve, E.C.R. (1953): Studies in quantitative inheritance. IV. The effects of substituting chromosomes from different genetic backgrounds of Drosophila melanogaster. J. Genet. 51, 586–610

    Google Scholar 

  • Sax, K. (1923): The association of size differences with seed-coat pattern and pigmentation in Phaseolus vulgaris. Genetics 8, 552–560

    Google Scholar 

  • Sheridan, A.K.; Frankham, R.; Jones, L.P.; Rathie, K.A.; Barker, J.S.F. (1968): Partitioning of variance and estimation of genetic parameters for various bristle number characters of Drosophila melanogaster. Theor. Appl. Genet. 38, 179–187

    Google Scholar 

  • Snedecor, G.W.; Cochran, W.G. 1967: Statistical Methods (6th Ed.). Ames: Iowa State Univ.

    Google Scholar 

  • Thoday, J.M. 1977: Effects of specific genes. In: Proc. Int. Conf. Quant. Genetics pp. 141–159. Ames: Iowa State Univ.

    Google Scholar 

  • Thompson, J.N. Jr.; Thoday, J.M. (1974): A definition and standard nomenclature for ‘polygenic loci’. Heredity 33, 430–437

    Google Scholar 

  • Thompson, J.N. Jr.; Thoday, J.M. (eds.) (1979): Quantitative Genetic Variation. New York; Acad. Press

    Google Scholar 

  • Warwick, E.J.; Lewis, W.L. (1954): Increase in frequency of a deleterious recessive gene in mice. J. Hered. 45, 143–145

    Google Scholar 

  • Wright, S. (1921): Systems of mating. Genetics 6, 111–178

    Google Scholar 

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

    Google Scholar 

  • Wright, S. (1969): The theoretical course of directional selection. Amer. Nat. 103, 561–574

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J.S.F. Barker

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frankham, R., Nurthen, R.K. Forging links between population and quantitative genetics. Theoret. Appl. Genetics 59, 251–263 (1981). https://doi.org/10.1007/BF00265506

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00265506

Key words

Navigation