Genetics underlying inbreeding depression in Mimulus with contrasting mating systems


The importance of inbreeding depression in theoretical considerations of mating-system evolution1,2,3,4,5 and its potential impact on the persistence of small populations6 has renewed interest in the genetic basis of this phenomenon. Inbreeding increases homozygosity. This can produce inbreeding depression for two different reasons: first, deleterious recessive or partially recessive alleles that are masked at heterozygous loci by dominant alleles become fully expressed in homozygotes; and second, alleles may interact in an overdominant manner, such that the fitness of either type of homozygote is lower than that of heterozygotes. These two mechanisms produce different long-term effects in populations experiencing increased levels of inbreeding. Inbreeding depression resulting from deleterious alleles can be removed by selection, but inbreeding depression produced by overdominance cannot be removed without lowering the mean fitness of the population1,2,3,4,5. Using a North Carolina 3 breeding programme7, the most powerful quantitative genetics technique available8,9,10, we show here that deleterious recessive alleles are mainly responsible for inbreeding depression in two closely related annual plants, the primarily selfing Mimulus micranthus and the mixed-mating M. guttatus. Estimates indicate that deleterious alleles in M. micranthus are more nearly additive than they are in M. guttatus.

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Figure 1: The North Carolina 3 breeding design.


  1. 1

    Charlesworth, D. & Charlesworth, B. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237–268 (1987).

    Article  Google Scholar 

  2. 2

    Charlesworth, D., Morgan, M. T. & Charlesworth, B. Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Evolution 44, 1469–1489 (1990).

    CAS  Article  Google Scholar 

  3. 3

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

    Article  Google Scholar 

  4. 4

    Holsinger, K. E. Inbreeding depression and the evolution of plant mating systems. Trends Ecol. Evol. 6, 307–308 (1991).

    CAS  Article  Google Scholar 

  5. 5

    Uyenoyama, M. K., Holsinger, K. E. & Waller, D. M. in Oxford Surveys in Evolutionary Biology Vol. 9(eds Futuyma, D. & Antonovics, J.) 327–381 (Oxford Univ. Press, New York, (1993)).

    Google Scholar 

  6. 6

    Fenster, C. B. & Dudash, M. R. in Restoration of Endangered Species (eds Bowles, M. L. & Whelan, C. J.) 34–62 (Cambridge Univ. Press, Cambridge, UK, (1994)).

    Google Scholar 

  7. 7

    Comstock, R. E. & Robinson, H. F. in Heterosis (ed. Gowen, J. W.) 494–516 (Iowa State College Press, Ames, (1952)).

    Google Scholar 

  8. 8

    Jinks, J. L. in Heterosis: Reappraisal of Theory and Practice (ed. Frankel, R.) 1–46 (Springer, Berlin, (1983)).

    Google Scholar 

  9. 9

    Kearsey, M. J. The efficiency of the North Carolina Experiment III and the selfing backcrossing series for estimating additive and dominance variation. Heredity 45, 73–82 (1980).

    Article  Google Scholar 

  10. 10

    Bulmer, M. G. The Mathematical Theory of Quantitative Genetics (Clarendon, Oxford, (1985)).

    Google Scholar 

  11. 11

    El-Nahrawy, M. A. & Bingham, E. T. Performance of S1 alfalfa lines from original and improved populations. Crop Sci. 29, 920–923 (1989).

    Article  Google Scholar 

  12. 12

    Moll, R. H., Lindsey, M. F. & Robinson, H. F. Estimates of genetic variances and level of dominance in maize. Genetics 49, 411–423 (1964).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Hallauer, A. R. & Miranda, J. B. Quantitative Genetics in Maize Breeding (Iowa State Univ. Press, Ames, (1985)).

    Google Scholar 

  14. 14

    Apirion, D. & Zohary, D. Chlorophyll lethal in natural populations of the orchard grass (Dactylis glomerata L.). A case of balanced polymorphism in plants. Genetics 46, 393–399 (1961).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Williams, W. & Brown, A. G. Genetic response to selection in cultivated plants: gene frequencies in Prunus avium. Heredity 10, 237–245 (1956).

    Article  Google Scholar 

  16. 16

    Gustafsson, A. The coorperation of genotypes in barley. Hereditas 39, 1–18 (1950).

    Article  Google Scholar 

  17. 17

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

    ADS  CAS  Article  Google Scholar 

  18. 18

    Johnston, M. O. & Schoen, D. J. Mutation rates and dominance levels of genes affecting total fitness in two angiosperm species. Science 267, 226–229 (1995).

    ADS  CAS  Article  Google Scholar 

  19. 19

    Willis, J. H. Effects of different levels of inbreeding on fitness components in Mimulus guttatus. Evolution 47, 864–876 (1993).

    Article  Google Scholar 

  20. 20

    Fenster, C. B. & Ritland, K. Chloroplast DNA and isozyme diversity in two Mimulus species (Scrophulariaceae) with contrasting mating systems. Am. J. Bot. 79, 1440–1447 (1992).

    CAS  Article  Google Scholar 

  21. 21

    Fu, Y.-B. & Ritland, K. Evidence for the partial dominance of viability genes contributing to inbreeding depression in Mimulus guttatus. Genetics 136, 323–331 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Latta, R. & Ritland, K. The relationship between inbreeding depression and prior inbreeding among populations of four Mimulus taxa. Evolution 48, 806–817 (1994).

    Article  Google Scholar 

  23. 23

    Carr, D. E. & Fenster, C. B. Levels of genetic variation and covaration for Mimulus (Scrophulariaceae) floral traits. Heredity 72, 606–618 (1994).

    Article  Google Scholar 

  24. 24

    Carr, D. E. & Dudash, M. R. Inbreeding depression in two species of Mimulus (Scrophulariaceae) with contrasting mating systems. Am. J. Bot. 83, 586–593 (1996).

    Article  Google Scholar 

  25. 25

    Dudash, M. R. & Ritland, K. Multiple paternity and self-fertilization in relation to floral age in Mimulus guttatus (Scrophulariaceae). Am. J. Bot. 78, 1746–1753 (1991).

    Article  Google Scholar 

  26. 26

    Comstock, R. E. & Robinson, H. F. The components of genetic variation in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics 2, 254–266 (1948).

    Article  Google Scholar 

  27. 27

    Husband, B. C. & Schemske, D. W. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50, 54–70 (1996).

    Article  Google Scholar 

  28. 28

    Dudash, M. R., Carr, D. E. & Fenster, C. B. Five generations of enforced selfing and outcrossing in Mimulus guttatus: inbreeding depression variation at the population and family level. Evolution 51, 54–65 (1997).

    PubMed  Google Scholar 

  29. 29

    Melchinger, A. E., Geiger, H. H. & Schnell, F. W. Epistasis in maize (Zea mays L.) 2. Genetic effects in crosses among early flint and dent inbred lines determined by three methods. Theor. Appl. Genet. 72, 231–239 (1986).

    CAS  Article  Google Scholar 

  30. 30

    Pray, L. A. & Goodnight, C. J. Genetic variation in inbreeding depression in the red flour beetle Tribolium castaneum. Evolution 49, 176–188 (1995).

    Article  Google Scholar 

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We thank M. Lawrence and J. Crow for encouragement, J. Coors for statistical advice, and M. Bowers, L. Chao, D. Charlesworth, C. Cole, L. Delph, J. Dooley, C. Fenster and D.McCauley for comments on earlier versions of the manuscript. This research was supported by the NSF and Maryland Agricultural Experiment Station.

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Correspondence to Michele R. Dudash.

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Dudash, M., Carr, D. Genetics underlying inbreeding depression in Mimulus with contrasting mating systems. Nature 393, 682–684 (1998).

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