Oecologia

, Volume 155, Issue 3, pp 469–477 | Cite as

The reproductive assurance benefit of selfing: importance of flower size and population size

Population Ecology - Original Paper

Abstract

Autonomous selfing can provide reproductive assurance (RA) for flowering plants that are unattractive to pollinators or in environments that are pollen limited. Pollen limitation may result from the breakdown of once-continuous habitat into smaller, more isolated patches (habitat fragmentation) if fragmentation negatively impacts pollinator populations. Here we quantify the levels of pollen limitation and RA among large and small populations of Collinsia parviflora, a wildflower with inter-population variation in flower size. We found that none of the populations were pollen limited, as pollen-supplemented and intact flowers did not differ in seed production. There was a significant effect of flower size on RA; intact flowers (can self) produced significantly more seeds than emasculated flowers (require pollen delivery) in small-flowered plants but not large-flowered plants. Population size nested within flower size did not significantly affect RA, but there was a large difference between our two replicate populations for large-flowered, small populations and small-flowered, large populations that appears related to a more variable pollination environment under these conditions. In fact, levels of RA were strongly negatively correlated with rates of pollinator visitation, whereby infrequent visitation by pollinators yielded high levels of RA via autonomous selfing, but there was no benefit of autonomous selfing when visitation rates were high. These results suggest that autonomous selfing may be adaptive in fragmented habitats or other ecological circumstances that affect pollinator visitation rates.

Keywords

Autonomous selfing Collinsia parviflora Habitat fragmentation Pollen limitation Reproductive assurance 

Notes

Acknowledgements

We thank E. Fairhurst, S. Gillespie, and E. Jones for field assistance; J. Conner, D. Moeller, S. Kalisz, C. Herlihy, M. Hart, D. Green, and an anonymous reviewer for helpful conversations and/or constructive comments on the manuscript; I. Bercovitz and C. Schwarz for statistical advice; and Capital Regional District Parks, The Nature Conservancy of Canada, British Columbia Provincial Parks, District of Saanich Parks, District of Esquimalt Parks, and TimberWest for access to field sites. This research was supported by a Discovery Grant to E. Elle from the Natural Sciences and Engineering Research Council of Canada. All research complied with the current regulations of landowners and the Canadian Government.

References

  1. Aarssen LW (2000) Why are most selfers annuals? A new hypothesis for the fitness benefit of selfing. Oikos 89:606–612CrossRefGoogle Scholar
  2. Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980PubMedCrossRefGoogle Scholar
  3. Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H (2002) Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae S.L.). Am J Bot 89:37–49CrossRefGoogle Scholar
  4. Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DL, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421CrossRefGoogle Scholar
  5. Becerra J, Lloyd D (1992) Competition-dependent abscission of self-pollinated flowers of Phormium tenax (Agavaceae): a second action of self-incompatibility at the whole flower level. Evolution 46:458–469CrossRefGoogle Scholar
  6. Bell G (1985) On the function of flowers. Proc R Soc Lond 224: 223–265CrossRefGoogle Scholar
  7. Celedon-Neghme C, Gonzales WL, Gianoli E (2007) Cost and benefits of attractive floral traits in the annual species Madia sativa (Asteraceae). Evol Ecol 21:247–257CrossRefGoogle Scholar
  8. Cheptou P-O, Avendaño V LG (2006) Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phytol 172:774–783PubMedCrossRefGoogle Scholar
  9. Conner J (1997) Floral evolution in wild radish: the roles of pollinators, natural selection, and genetic correlations among traits. Int J Plant Sci 158:S108–120CrossRefGoogle Scholar
  10. Cruden R, Lyon D (1985) Patterns of biomass allocation to male and female functions in plants with different mating systems. Oecologia 66:299–306Google Scholar
  11. Cruden R, Lyon D (1989) Facultative xenogamy: examination of a mixed mating system. In: Bock J, Linhart Y (eds) The evolutionary ecology of plants. Westview, Boulder, pp 171–207Google Scholar
  12. Culley TM (2002) Reproductive biology and delayed selfing in Viola pubescens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. Int J Plant Sci 163:113–122CrossRefGoogle Scholar
  13. Darwin C (1876) The effects of cross and self-fertilization in the vegetable kingdom. Murray, LondonGoogle Scholar
  14. Day RW, Quinn GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecol Monogr 59:433–463CrossRefGoogle Scholar
  15. Diggle PK (1992) Development and the volution of plant reproductive characters. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman and Hall, New York, pp 326–355Google Scholar
  16. Douglas GW, Meidinger DV, Pojar J (2000) Illustrated Flora of British Columbia, vol 5. Dicotyledons (Salicaceae through Zygophyllaceae) and pteridophytes. British Columbia Ministry of Environment, Lands & Parks, British Columbia Ministry of Forests, VictoriaGoogle Scholar
  17. Eckert CG, Schaefer A (1998) Does self-pollination provide reproductive assurance in Aquilegia Canadensis (Ranunculaceae)? Am J Bot 85:919–924CrossRefGoogle Scholar
  18. Eckhart VM, Geber MA (1999) Character variation and geographic distribution of Clarkia xantiana A. Gray (Onagraceae): flowers and phenology distinguish two subspecies. Madroño 46:117–125Google Scholar
  19. Elle E (2004) Floral adaptations and biotic and abiotic selection pressures. In: Cronk QCB, Whitton J, Ree RH, Taylor IEP (eds) Plant adaptation: molecular genetics and ecology. Proceedings of an International Workshop, 11–13 December 2002, Vancouver, British Columbia. NRC Research Press, Ottawa, pp 111–118Google Scholar
  20. Elle E, Carney R (2003) Reproductive assurance varies with flower size in Collinsia parviflora (Scrophularaceae). Am J Bot 90:888–896CrossRefGoogle Scholar
  21. Fisher RA (1941) Average excess and average effect of a gene substitution. Ann Eugen 11:53–63Google Scholar
  22. Fuchs MA (2001) Towards a recovery strategy for Garry oak and associated ecosystems in Canada: ecological assessment and literature review. Technical report GBEI/EC-00-030. Environment Canada, Canadian Wildlife Service, Pacific and Yukon RegionGoogle Scholar
  23. Ganders FR, Krause GR (1986) Systematics of Collinsia parviflora and C. grandiflora (Scrophulariaceae). Madroño 33:63–70Google Scholar
  24. Ghazoul J (2005) Pollen and seed dispersal and dispersed plants. Biol Rev 80:1–31CrossRefGoogle Scholar
  25. Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst 36:47–79CrossRefGoogle Scholar
  26. Guerrant EOJ (1989) Early maturity, small flowers, and autogamy: a developmental connection? In: Bock J, Linhart Y (eds) The evolutionary ecology of plants. Westview, Boulder, pp 61–84Google Scholar
  27. Herlihy CR, Eckert CG (2002) Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416:320–323PubMedCrossRefGoogle Scholar
  28. Jennersten O (1988) Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366CrossRefGoogle Scholar
  29. Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942CrossRefGoogle Scholar
  30. Kennedy BF, Sabara HA, Haydon D, Husband BC (2006) Pollinator-mediated assortative mating in mixed ploidy populations of Chamerion angustifolium (Onagraceae). Oecologia 150:398–408PubMedCrossRefGoogle Scholar
  31. Kéry M, Matthies D (2004) Reduced fecundity in small populations of the rare plant Gentianopsis ciliate (Gentianaceae). Plant Biol 6:683–688PubMedCrossRefGoogle Scholar
  32. Kimura M (1959) Conflict between self-fertilization and outbreeding in plants. Annu Report Nat Inst Jpn 9:87–88Google Scholar
  33. Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497CrossRefGoogle Scholar
  34. Lande R, Schemske D (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40CrossRefGoogle Scholar
  35. Lea T (2002) Historical Garry oak ecosystems of Greater Victoria and the Saanich Peninsula background information. Terrestrial Information Branch, British Columbia Ministry of Sustainable Resource Management, VictoriaGoogle Scholar
  36. Lloyd DG (1992) Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380CrossRefGoogle Scholar
  37. Moeller DA (2004) Facilitative interactions among plants via shared pollinators. Ecology 85:3289–3301CrossRefGoogle Scholar
  38. Moeller DA, Geber MA (2005) Ecological context of the evolution of self-pollination in Clarkia xantiana: population size, plant communities, and reproductive assurance. Evolution 59:786–799PubMedGoogle Scholar
  39. Moeller DA (2006) Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. Ecology 87:1510–1522PubMedCrossRefGoogle Scholar
  40. Morgan MT, Wilson WG (2005) Self-fertilization and the escape from pollen limitation in variable pollination environments. Evolution 59:1143–1148PubMedGoogle Scholar
  41. Palmer TM, Stanton ML, Young TP (2003) Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am Nat 162:S63–S79PubMedCrossRefGoogle Scholar
  42. Parachnowitsch AL, Elle E (2004) Variation in sex allocation and male-female trade-offs in sex populations of Collinsia parviflora (Scrophulariaceae S.L.). Am J Bot 91: 1200–1207CrossRefGoogle Scholar
  43. Runions CJ, Geber MA (2000) Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae). I. Size and development of floral organs. Am J Bot 87:1439–1451PubMedCrossRefGoogle Scholar
  44. SAS (1996) SAS/STAT software: changes and enhancements for release, version 6.12. SAS Institute, CaryGoogle Scholar
  45. Schoen DJ, Morgan MT, Bataillon T (1996) How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Philos Trans R Soc Lond B Biol Sci 351:1281–1290CrossRefGoogle Scholar
  46. Sih A, Baltus M (1987) Patch size, pollinator behaviour, and pollinator limitation in catnip. Ecology 68:1679–1690CrossRefGoogle Scholar
  47. Stebbins GL (1957) Self-fertilization and population variability in the higher plants. Am Nat 91:337–354CrossRefGoogle Scholar
  48. Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440CrossRefGoogle Scholar
  49. Thompson JD (2001) How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia 126:386–394CrossRefGoogle Scholar
  50. Vogler DW, Kalisz S (2001) Sex among flowers: the distribution of plant mating systems. Evolution 55:202–204PubMedGoogle Scholar
  51. Wagenius S (2006) Scale dependence of reproductive failure in fragmented Echinacea populations. Ecology 87:931–941PubMedCrossRefGoogle Scholar
  52. Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270–276PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada

Personalised recommendations