Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating

Nature volume 430, pages 884–887 (2004)Cite this article

Abstract

The evolution of self-fertilization in hermaphrodites is opposed by costs that decrease the value of self progeny relative to that of outcross progeny1,2,3. However, self-fertilization is common in plants4; 20% are highly selfing and 33% are intermediate between selfing and outcrossing5. Darwin6 proposed an adaptive benefit of self-pollination in providing reproductive assurance when outcrossing is impossible6,7,8,9. Moreover, if outcross pollen receipt is inconsistent within or between years, these conditions likewise favour self-pollination10, and this can result in a mixture of self and outcross seed production (mixed mating). Despite wide acceptance, the reproductive assurance hypothesis has lacked the support of complete empirical evidence to show that variable pollination can create both the ecological and genetic conditions favouring self-pollination. We recently showed in Collinsia verna that during periods of infrequent pollinator visits, autonomous self-pollination boosted seed output per flower11, the key ecological condition. Here we show low inbreeding depression and marker-based estimates of selfing, demonstrating that when the pollination environment in wild populations necessitates reproductive assurance, selfing rates increase. We provide a complete demonstration of reproductive assurance under variable pollination environments and mechanistically link reproductive assurance to intermediate selfing rates through mixed mating.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Populations of the annual species, C. verna, have low values of inbreeding depression, δ.
Figure 2: Annual variation in selfing rates in C. verna populations results from an increase in autonomous self pollination when pollinators fail to visit flowers.

References

  1. 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 

  2. Lande, R. & Schemske, D. W. I. Genetic models. Evolution 39, 24–40 (1985)

    Article  Google Scholar 

  3. Holsinger, K. E. Mass action models of plant mating systems: the evolutionary stability of mixed mating systems. Am. Nat. 138, 606–622 (1991)

    Article  Google Scholar 

  4. Barrett, S. C. H. The evolution of plant sexual diversity. Nature Rev. Genet. 3, 274–284 (2002)

    Article  CAS  Google Scholar 

  5. Vogler, D. W. & Kalisz, S. Sex among the flowers: the distribution of plant mating systems. Evolution 55, 202–204 (2001)

    Article  CAS  Google Scholar 

  6. Darwin, C. R. The Effects of Cross and Self-Fertilization in the Vegetable Kingdom Ch. 9 (John Murray, London, 1876)

    Book  Google Scholar 

  7. Stebbins, G. L. Flowering Plants: Evolution Above the Species Level 52 (Belknap, Cambridge, Massachusetts, 1974)

    Book  Google Scholar 

  8. Lloyd, D. G. II. The selection of self-fertilization. Int. J. Plant Sci. 153, 370–380 (1992)

    Article  Google Scholar 

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

    Google Scholar 

  10. 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 

  11. Kalisz, S. & Vogler, D. W. Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84, 2928–2942 (2003)

    Article  Google Scholar 

  12. Cruden, R. W. & Lyon, D. L. in The Evolutionary Ecology of Plants (eds Bock, J. H. & Linhart, Y. B.) 171–207 (Westview, Boulder, Colorado, 1989)

    Google Scholar 

  13. Fausto, J. A. J., Eckhart, E. V. & Geber, M. A. Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana (Onagraceae). Am. J. Bot. 88, 1794–1800 (2001)

    Article  Google Scholar 

  14. Barrett, S. C. H. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Phil. Trans. R. Soc. Lond. B 358, 991–1004 (2003)

    Article  Google Scholar 

  15. Lloyd, D. G. & Schoen, D. J. I. Functional dimensions. Int. J. Plant Sci. 153, 358–369 (1992)

    Article  Google Scholar 

  16. 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)

    Article  ADS  Google Scholar 

  17. Holsinger, K. Reproductive systems and evolution in vascular plants. Proc. Natl Acad. Sci. USA 97, 7037–7042 (2000)

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  19. Herlihy, C. R. & Eckert, C. G. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416, 320–323 (2002)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  22. Kalisz, S. Fitness consequences of mating system, seed weight and emergence date in a winter annual. Evolution 43, 1263–1272 (2002 1989)

    Article  Google Scholar 

  23. Ritland, K. Multilocus mating system program MLTR 2.2. 〈http://genetics.forestry.ubc.ca/ritland/programs.html〉

  24. Harder, L. D. & Barrett, S. C. H. Mating cost of large floral displays in hermaphrodite plants. Nature 373, 512–515 (1995)

    Article  ADS  CAS  Google Scholar 

  25. 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 

  26. Burd, M. Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot. Rev. 60, 83–139 (1994)

    Article  MathSciNet  Google Scholar 

  27. Byers, D. L. & Waller, D. M. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu. Rev. Ecol. Syst. 30, 479–513 (1999)

    Article  Google Scholar 

  28. Johnston, M. O. Evolution of intermediate selfing rates in plants: pollination ecology versus deleterious mutations. Genetica 102/103, 267–278 (1998)

    Article  Google Scholar 

  29. 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)

    Article  ADS  Google Scholar 

  30. Kalisz, S. et al. The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am. J. Bot. 86, 1239–1247 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Dunn for technical assistance and J. Dunn, P. Zemrowski, A. Richter, C. Jarzab, H. Lang, R. Brown and A. Mergenthaler for field assistance. D.W. Schemske and S. J. Tonsor provided valuable comments on the manuscript. This work was supported by research grants from the National Science Foundation (USA) and the Research Development Fund of The University of Pittsburgh (S.K.).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, 15260, USA

    Susan Kalisz, Donna W. Vogler & Kristen M. Hanley

  2. Biology Department, State University of New York, College at Oneonta, Oneonta, New York, 13820, USA

    Donna W. Vogler

Authors
  1. Susan Kalisz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donna W. Vogler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kristen M. Hanley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susan Kalisz.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kalisz, S., Vogler, D. & Hanley, K. Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430, 884–887 (2004). https://doi.org/10.1038/nature02776

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02776

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing