Skip to main content
SpringerLink
Log in

Possible consequences of genes of major effect: transient changes in the G-matrix

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Understanding the process of evolutionary divergence requires knowledge of the strength, form, and targets of selection, as well as the genetic architecture of the divergent traits. Quantitative genetic approaches to understanding multivariate selection and genetic response to selection have proven to be powerful tools in this endeavor, particularly with respect to short-term evolution. However, the application of quantitative genetic theory over periods of substantial phenotypic change is controversial because it requires that the requisite genetic parameters remain constant over the period of time in question. We show herein how attempts to determine the stability of key genetic parameters may be misled by the ‘many genes of small effect’ type of genetic architecture generally assumed in quantitative genetics. The presence of genes of major effect (GOMEs) can alter the genetic variance-covariance matrix dramatically for brief periods of time, significantly alter the rate and trajectory of multivariate evolution, and thereby mislead attempts to reconstruct or predict long term evolution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arnold, S.J., 1994. Multivariate inheritance and evolution: a review of concepts, pp. 17–48 in Quantitative Genetic Studies of Behavioral Evolution, edited by C.R.B. Boake. Chicago Press, Chicago.

    Google Scholar 

  • Barton, N.H. & M. Turelli, 1987. Adaptive landscapes, genetic distance and the evolution of quantitative characters. Gen. Res. Camb. 49: 157–173.

    Google Scholar 

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

    Google Scholar 

  • Barton, N.H. & M. Turelli, 1991. Natural and sexual selection on many loci. Genetics 127: 229–255.

    Google Scholar 

  • Bradshaw, H.D., K.G. Otto, B.E. Frewen, J.K. McKay & D.W. Schemske, 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 367–382.

  • Carriére, Y. & D.A. Roff, 1995. Change in genetic architecture resulting from the evolution of insecticide resistance: a theoretical and empirical analysis. Heredity 75: 618–629.

    Google Scholar 

  • Carriére, Y., J.P. Deland, D.A. Roff & C. Vincent, 1994. Life history costs associated with the evolution of insecticide resistance. Proc. R. Soc. Lond. B 258: 35–40.

    Google Scholar 

  • Cheverud, J.M., 1988. A comparison of genetic and phenotypic correlations. Evolution 42: 958–968.

    Google Scholar 

  • de Vicente, M.C. & S.D. Tanksley, 1993. QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134: 585–596.

    Google Scholar 

  • Doebley, J., A. Stec & C. Gustus, 1995. Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141: 333–346.

    Google Scholar 

  • Endler, J.A., 1986. Natural Selection in the Wild. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Falconer, D.S. & T. Mackay, 1996. Introduction to Quantitative Genetics. Longman, New York.

    Google Scholar 

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

    Google Scholar 

  • Grant, P.R. & B.R. Grant, 1995. Predicting microevolutionary responses to directional selection on heritable variation. Evolution 49: 241–251.

    Google Scholar 

  • Kingsolver, J.G., H.E. Hoekstra, J.M. Hoekstra, D. Berrigan, S.N. Vignieri, C.E. Hill, A. Hoang, P. Gibert & P. Beerli, 2001. The strength of phenotypic selection in natural populations. Am. Nat.

  • Lai, C., R.F. Lyman, A.D. Long, C.H. Langley & T.F.C. Mackay, 1994. Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster. Science 266: 1697–1702.

    Google Scholar 

  • Lande, R., 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30: 314–334.

    Google Scholar 

  • Lande, R., 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33: 402–416.

    Google Scholar 

  • Lande, R., 1980. The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94: 203–215.

    Google Scholar 

  • Lande, R., 1983. The response to selection on major and minor mutations affecting a metrical trait. Heredity 50: 47–65.

    Google Scholar 

  • Lande, R. & S.J. Arnold, 1983. The measurement of selection on correlated characters. Evolution 37: 1210–1226.

    Google Scholar 

  • Lofsvold, D., 1988. Quantitative genetics of morphological differentiation in Peromyscus. II. Analysis of selection and drift. Evolution 42: 54–67.

    Google Scholar 

  • Lynch, M. & B. Walsh, 1998. Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA.

    Google Scholar 

  • Mackay, T.F.C., 1995. The genetic basis of quantitative variation: numbers of sensory bristles of Drosophila melanogaster as a model system. Trends Genet. 11: 464–470.

    Google Scholar 

  • Mackay, T.F.C., 1996. The nature of quantitative genetic variation revisited: lessons from Drosophila bristles. BioEssays 18: 113–121.

    Google Scholar 

  • Orr, H.A., 1998. The population genetic of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935–949.

    Google Scholar 

  • Orr, H.A. & J.A. Coyne, 1992. The genetics of adaptation revisited. Am. Nat. 140: 725–742.

    Google Scholar 

  • Phillips, P.C. & S.J. Arnold, 1989. Visualizing multivariate selection. Evolution 43: 1209–1222.

    Google Scholar 

  • Phillips, P.C. & S.J. Arnold, 1999. Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution 53: 1506–1515.

    Google Scholar 

  • Price, T., M. Turelli & M. Slatkin, 1993. Peak shifts produced by correlated response to selection. Evolution 47: 280–290.

    Google Scholar 

  • Reznick, D.N., F.H. Shaw, F.H. Rodd & R.G. Shaw, 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275: 1934–1937.

    Google Scholar 

  • Roff, D.A., 2000. The evolution of the G-matrix: selection or drift. Heredity 84: 135–142.

    Google Scholar 

  • Schluter, D., 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50: 1766–1774.

    Google Scholar 

  • Tanksley, S.D., 1993. Mapping polygenes. Annu. Rev. Genet. 27: 205–233.

    Google Scholar 

  • True, J.R., J. Liu, L.F. Stam, Z.-B. Zeng & C.C. Laurie, 1997. Quantitative genetic analysis of divergence in male secondary sexual traits between Drosophila simulans and Drosophila mauritiana. Evolution 51: 816–832.

    Google Scholar 

  • Turelli, M., 1988. Phenotypic evolution, constant covariances, and the maintanence of additive variance. Evolution 42: 1342–1347.

    Google Scholar 

  • Turelli, M., 1990. Dynamics of polygenic characters under selection. Theor. Pop. Biol. 38: 1–57.

    Google Scholar 

  • Turelli, M. & N.H. Barton, 1994. Genetic and statistical analyses of strong selection on polygenic traits: what, me normal? Genetics 138: 913–941.

    Google Scholar 

  • Whitlock, M.C., P.C. Phillips, F.B.-G. Moore & S.J. Tonsor, 1995. Multiple fitness peaks and epistasis. Annu. Rev. Ecol. Syst. 26: 601–629.

    Google Scholar 

  • Willis, J.H., J.A. Coyne & M. Kirkpatrick, 1991. Can one predict the evolution of quantitative characters without genetics? Evolution 45: 441–444.

    Google Scholar 

  • Zeng, Z.-B., 1988. Long-term correlated response, interpopulation covariation, and interspecific allometry. Evolution 42: 363–374.

    Google Scholar 

  • Zeng, Z.-B., J. Liu, L.F. Stam, C.-H. Kao, J.M. Mercer & C.C. Laurie, 2000. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics 154: 299–310.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Indiana University, 1001 E. 3rd street, Bloomington, IN, 47405-3700, USA

    Aneil F. Agrawal, Edmund D. Brodie III & Loren H. Rieseberg

  2. Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN, 47405-3700, USA

    Aneil F. Agrawal & Edmund D. Brodie III

Authors
  1. Aneil F. Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edmund D. Brodie III
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Loren H. Rieseberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Agrawal, A.F., Brodie, E.D. & Rieseberg, L.H. Possible consequences of genes of major effect: transient changes in the G-matrix. Genetica 112, 33–43 (2001). https://doi.org/10.1023/A:1013370423638

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1013370423638

Search

Navigation