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Genetic mechanisms of floral trait correlations in a natural population

Nature volume 420, pages 407–410 (2002)Cite this article

Abstract

Genetic correlations among traits are important in evolution, as they can constrain evolutionary change or reflect past selection for combinations of traits1,2. Constraints and integration depend on whether the correlations are caused by pleiotropy or linkage disequilibrium3, but these genetic mechanisms underlying correlations remain largely unknown in natural populations4. Quantitative trait locus (QTL) mapping studies do not adequately address the mechanisms of within-population genetic correlations because they rely on crosses between distinct species, inbred lines or selected lines (see ref. 5), and they cannot distinguish moderate linkage disequilibrium from pleiotropy because they commonly rely on only one or two episodes of recombination6. Here I report that after nine generations of enforced random mating (nine episodes of recombination), correlations between six floral traits in wild radish plants are unchanged, showing that pleiotropy generates the correlations. There is no evidence for linkage disequilibrium despite previous correlational selection acting on one functionally integrated pair of traits7. This study provides direct evidence of the genetic mechanisms underlying correlations between quantitative traits in a natural population and suggests that there may be constraints on the independent evolution of pairs of highly correlated traits.

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Figure 1: Floral trait correlations with 95% confidence intervals.
Figure 2: Theoretical declines in correlations caused by a reduction in linkage disequilibrium during nine generations of random mating.

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References

  1. Maynard Smith, J. et al. Developmental constraints and evolution. Quart. Rev. Biol. 60, 265–287 (1985)

    Article  Google Scholar 

  2. Deng, H.-W., Haynatzka, V., Spitze, K. & Haynatzki, G. The determination of genetic covariances and prediction of evolutionary trajectories based on a genetic correlation matrix. Evolution 53, 1592–1599 (1999)

    Article  Google Scholar 

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

    Google Scholar 

  4. Clark, A. G. in Genetic Constraints on Adaptive Evolution (ed. Loeschcke, V.) 25–45 (Springer, Berlin, 1987)

    Book  Google Scholar 

  5. 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  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  7. Morgan, M. T. & Conner, J. K. Using genetic markers to directly estimate male selection gradients. Evolution 55, 272–281 (2001)

    Article  CAS  Google Scholar 

  8. Futuyma, D. J. Evolutionary Biology (Sinauer Associates, Sunderland, Massachusetts, 1998)

    Google Scholar 

  9. Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Longman, Harlow, 1996)

    Google Scholar 

  10. Mitchell-Olds, T. Pleiotropy causes long-term genetic constraints on life-history evolution in Brassica rapa. Evolution 50, 1849–1858 (1996)

    Article  Google Scholar 

  11. Lande, R. The genetic correlation between characters maintained by selection, linkage and inbreeding. Genet. Res. 44, 309–320 (1984)

    Article  ADS  CAS  Google Scholar 

  12. Wright, S. Evolution and the Genetics of Populations. Vol. 2. The Theory of Gene Frequencies (Univ. Chicago Press, Chicago, 1969)

    Google Scholar 

  13. Lande, R. The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94, 203–215 (1980)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Nuzhdin, S. V., Dilda, C. & Mackay, F. C. The genetic architecture of selection response: Inferences from fine-scale mapping of bristle number quantitative trait loci in Drosophila melanogaster. Genetics 153, 1317–1331 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Conner, J. K. & Via, S. Patterns of phenotypic and genetic correlations among morphological and life-history traits in wild radish, Raphanus raphanistrum. Evolution 47, 704–711 (1993)

    Article  Google Scholar 

  16. Conner, J. K. Floral evolution in wild radish: the roles of pollinators, natural selection, and genetic correlations among traits. Int. J. Plant Sci. 158, S108–S120 (1997)

    Article  Google Scholar 

  17. Hill, J. P. & Lord, E. M. Floral development in Arabidopsis thaliana: a comparison of the wild type and the homeotic pistillata mutant. Can. J. Bot. 67, 2922–2936 (1989)

    Article  Google Scholar 

  18. Shabalina, S. A., Yampolsky, L. Y. & Kondrashov, A. S. Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proc. Natl Acad. Sci. USA 94, 13034–13039 (1997)

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  20. Shaw, R. G. The comparison of quantitative genetic parameters between populations. Evolution 45, 143–151 (1991)

    Article  Google Scholar 

  21. Houle, D., Mezey, J. & Galpern, P. Interpretation of the results of common principal components analysis. Evolution 56, 433–440 (2002)

    Article  Google Scholar 

  22. Shaw, F. H., Shaw, R. G., Wilkinson, G. S. & Turelli, M. Changes in genetic variances and covariances: G whiz! Evolution 49, 1260–1267 (1995)

    Article  Google Scholar 

  23. Bulmer, M. G. Linkage disequilibrium and genetic variability. Genet. Res. 23, 281–289 (1974)

    Article  CAS  Google Scholar 

  24. Roff, D. A. & Mousseau, T. A. Does natural selection alter genetic architecture? An evaluation of quantitative genetic variation among populations of Allonemobius socius and A. fasciatus. J. Evol. Biol. 12, 361–369 (1999)

    Article  Google Scholar 

  25. Whitlock, M. C., Phillips, P. C., Moore, F. B. G. & Tonsor, S. J. Multiple fitness peaks and epistasis. Annu. Rev. Ecol. System. 26, 601 (1995)

    Article  Google Scholar 

  26. Crow, J. F. & Kimura, M. An Introduction to Population Genetics Theory (Harper and Row, New York, 1970)

    MATH  Google Scholar 

  27. SAS Institute SAS/STAT User's Guide, Version 8 (SAS Institute, Cary, North Carolina, 1999)

    Google Scholar 

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

    Article  Google Scholar 

  29. Snedecor, G. W. & Cochran, W. G. Statistical Methods (Iowa State Univ. Press, Ames, Iowa, 1989)

    MATH  Google Scholar 

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

    MATH  Google Scholar 

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Acknowledgements

I thank C. Haun, T. Hickox, S. Kercher, J. Mudd, C. Stewart and many undergraduates for help in the greenhouse; P. Phillips for help with the CPC analysis and for programs; F. Shaw for analyses with Quercus; E. Brodie, B. Charlesworth, J. Fry, D. Houle, R. Lande, M. Lynch, D. Schluter, M. Turelli, S. Via and M. Whitlock for discussion; and A. Agrawal, M. Duffy, J. Fant, J. Kelly, M. Morgan, P. Phillips, H. Sahli, C. Stewart and S. Via for comments on the manuscript. This work was supported by the US National Science Foundation, the University of Illinois and Michigan State University.

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  1. Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Corners, Michigan, 49060, Hickory, USA

    Jeffrey K. Conner

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Correspondence to Jeffrey K. Conner.

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Conner, J. Genetic mechanisms of floral trait correlations in a natural population. Nature 420, 407–410 (2002). https://doi.org/10.1038/nature01105

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