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Genetic cost of reproductive assurance in a self-fertilizing plant

Abstract

The transition from outcrossing to self-fertilization is one of the most common evolutionary trends in plants1. Reproductive assurance, where self-fertilization ensures seed production when pollinators and/or potential mates are scarce, is the most long-standing and most widely accepted explanation for the evolution of selfing2,3,4,5,6,7,8, but there have been few experimental tests of this hypothesis. Moreover, many apparently adaptive floral mechanisms that ensure the autonomous production of selfed seed might use ovules that would have otherwise been outcrossed. This seed discounting is costly if selfed offspring are less viable than their outcrossed counterparts, as often happens. The fertility benefit of reproductive assurance has never been examined in the light of seed discounting. Here we combine experimental measures of reproductive assurance with marker-gene estimates of self-fertilization, seed discounting and inbreeding depression to show that, during 2 years in 10 Ontario populations of Aquilegia canadensis (Ranunculaceae), reproductive assurance through self-fertilization increases seed production, but this benefit is greatly outweighed by severe seed discounting and inbreeding depression.

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Figure 1: Trade-off between the gain in seed production through autogamous selfing (reproductive assurance, R) and the loss of outcrossed seeds (seed discounting, D).
Figure 2: Cost–benefit analysis of variation in autogamous selfing among populations.

References

  1. Stebbins, G. L. Flowering Plants: Evolution above the Species Level (Belknap, Cambridge, Massachusetts, 1974).

    Book  Google Scholar 

  2. Darwin, C. R. The Effects of Cross and Self-fertilization in the Vegetable Kingdom (John Murray, London, 1876).

    Book  Google Scholar 

  3. Baker, H. G. Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9, 347–348 (1955).

    Google Scholar 

  4. Jain, S. K. The evolution of inbreeding in plants. Annu. Rev. Ecol. Syst. 7, 69–95 (1976).

    Article  Google Scholar 

  5. Lloyd, D. G. in Demography and Evolution in Plant Populations (ed. Solbrig, O. T.) 67–88 (Blackwell, Oxford, 1980).

    Google Scholar 

  6. Yahara, T. Graphical analysis of mating system evolution in plants. Evolution 46, 557–561 (1992).

    Article  Google Scholar 

  7. Jarne, P. & Charlesworth, D. The evolution of the selfing rate in functionally hermaphroditic plants and animals. Annu. Rev. Ecol. Syst. 24, 441–466 (1993).

    Article  Google Scholar 

  8. Holsinger, K. E. Pollination biology and the evolution of mating systems in flowering plants. Evol. Biol. 29, 107–149 (1996).

    Google Scholar 

  9. Fisher, R. A. Average excess and average effect of a gene substitution. Ann. Eugen. 11, 53–63 (1941).

    Article  Google Scholar 

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

    Article  Google Scholar 

  11. Barrett, S. C. H., Harder, L. D. & Worley, A. C. The comparative biology of pollination and mating in flowering plants. Phil. Trans. R. Soc. Lond. B 351, 1271–1280 (1996).

    ADS  Article  Google Scholar 

  12. Lande, R., Schemske, D. W. & Schultz, S. T. High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutations. Evolution 48, 965–978 (1994).

    Article  Google Scholar 

  13. 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 

  14. Lloyd, D. G. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153, 370–380 (1992).

    Article  Google Scholar 

  15. Schoen, D. J., Morgan, M. T. & Bataillon, T. How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Phil. Trans. R. Soc. Lond. B 351, 1281–1290 (1996).

    ADS  Article  Google Scholar 

  16. Schoen, D. J. & Brown, A. H. D. Whole- and part-flower self-pollination in Glycine clandestina and G. argyrea and the evolution of autogamy. Evolution 45, 1665–1674 (1991).

    Article  Google Scholar 

  17. Eckert, C. G. & Schaefer, A. Does self-pollination provide reproductive assurance in wild columbine, Aquilegia canadensis (Ranunculaceae)? Am. J. Bot. 85, 919–924 (1998).

    CAS  Article  Google Scholar 

  18. Cruden, R. W. & Lyon, D. L. in The Evolutionary Ecology of Plants (eds Bock, J. H. & Linhart, Y. B.) 171–208 (Westview Press, Boulder, Colorado, 1989).

    Google Scholar 

  19. Piper, J. G., Charlesworth, B. & Charlesworth, D. A high rate of self-fertilization and increased seed fertility of homostyle primroses. Nature 310, 50–51 (1984).

    ADS  Article  Google Scholar 

  20. Piper, J. G., Charlesworth, B. & Charlesworth, D. Breeding system evolution in Primula vulgaris and the role of reproductive assurance. Heredity 56, 207–217 (1986).

    Article  Google Scholar 

  21. Routley, M. B., Mavraganis, K. & Eckert, C. G. Effect of population size on the mating system in a self-compatible, autogamous plant, Aquilegia canadensis (Ranunculaceae). Heredity 82, 518–528 (1999).

    Article  Google Scholar 

  22. Mavraganis, K. & Eckert, C. G. Effect of population size and isolation on reproductive output of Aquilegia canadensis (Ranunculaceae). Oikos 95, 533–546 (2001).

    Article  Google Scholar 

  23. Macior, L. W. The pollination of vernal angiosperms. Oikos 30, 452–460 (1978).

    Article  Google Scholar 

  24. Lloyd, D. G. & Schoen, D. J. Self- and cross-fertilization in plants. I. Functional dimensions. Int. J. Plant Sci. 153, 358–369 (1992).

    Article  Google Scholar 

  25. Griffin, S. R., Mavraganis, K. & Eckert, C. G. Experimental analysis of protogyny in Aquilegia canadensis. Am. J. Bot. 87, 1246–1256 (2000).

    CAS  Article  Google Scholar 

  26. Morgan, M. T., Schoen, D. J. & Bataillon, T. M. The evolution of self-fertilization in perennials. Am. Nat. 150, 618–638 (1997).

    CAS  Article  Google Scholar 

  27. Morgan, M. T., and Schoen, D. J. The role of theory in an emerging new plant reproductive biology. Trends Ecol. Evol. 12, 231–234 (1997).

    CAS  Article  Google Scholar 

  28. Ritland, K. A series of FORTRAN computer programs for estimating plant mating systems. J. Hered. 81, 235–237 (1990).

    Article  Google Scholar 

  29. Schoen, D. J. & Lloyd, D. G. Self- and cross-fertilization in plants. III. Methods for studying modes and functional aspects of self-fertilization. Int. J. Plant Sci. 153, 381–393 (1992).

    Article  Google Scholar 

  30. Ritland, K. Inferences about inbreeding depression based on changes of the inbreeding coefficient. Evolution 44, 1230–1241 (1990).

    Article  Google Scholar 

Download references

Acknowledgements

We thank M. Bhardwaj, S. Griffin and A. Kliber for help with the field work; C. Muis and M. Bhardwaj for help in the laboratory; and S. Barrett, K. Holsinger, A. Kliber, B. Montgomerie and M. Morgan for comments on the manuscript. This work was supported in the field by the Queen's University Biological Station and by a research grant from the Natural Sciences and Engineering Research Council of Canada to C.G.E.

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Herlihy, C., Eckert, C. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416, 320–323 (2002). https://doi.org/10.1038/416320a

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