Journal of Insect Behavior

, Volume 18, Issue 6, pp 743–756 | Cite as

Insect Choice and Floral Size Dimorphism: Sexual Selection or Natural Selection?

Article

Abstract

In considerations of sexual floral size dimorphism, there is a conflict between sexual selection theory, which predicts that larger floral displays attract more pollinators, and optimality theory—particularly the ideal free distribution—which predict that pollinators' visits should match nutritional rewards. As an alternate explanation of this dimorphism, Müller reported that pollinators tend to visit larger male flowers before visiting smaller female flowers, thereby promoting effective pollination. To investigate optimality predictions, I offered pollinators a choice between smaller, less numerous, but more rewarding flowers; and larger, more numerous, but less rewarding flowers. Foragers initially favored the larger and more numerous flowers, but rapidly shifted preferences to conform with the predictions of the ideal free distribution. To test Müller's hypothesis, I offered pollinators choices between larger and smaller corollas of equal caloric reward. Results showed that although pollinators tended to visit larger corollas first, they did not visit them more often. These experiments highlight the need for further investigation into the tradeoff between natural and sexual selection, and their respective influences in pollination ecology.

Keywords

sexual selection optimality pollination floral dimorphism ideal free distribution 

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References

  1. Abraham, J. N. (1996). La saboteuse: An ecological theory of sexual dimorphism in animals. Acta Biotheor. 46: 23–35.Google Scholar
  2. Agren, J., Elmqvist, T., and Tunlid, A. (1986). Pollination by deceit, floral sex ratios and seed set in dioecious Rubus chamaemorus L. Oecologia 70: 332–338.Google Scholar
  3. Andersson, S. (1991). Floral display and pollination success in Achillea ptarmica (Asteraceae). Hol. Ecol. 14: 186–191.Google Scholar
  4. Anderson, G. J., and Symon, D. E. (1989). Functional dioecy and andromonoecy in Solanum. Evolution 43: 204–219.Google Scholar
  5. Arnold, S. J. (1994). Supplement: Sexual selection in plants and animals, a symposium organized by Stevan J. Arnold. Am. Nat. 144: S1–S149.Google Scholar
  6. Ashman, T. L., and Stanton, M. L. (1991). Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72: 993–1003.Google Scholar
  7. Baker, H. G. (1948). Corolla size in gynodioecious and gynomonoecious species of flowering plants. Proc. Leeds Phil. Lit. Soc. 5: 136–139.Google Scholar
  8. Bawa, K. S. (1980a). Mimicry of male by female flowers and intrasexual competition for pollinators in Jacaratia dolichaula (D. Smith) Woodson (Caricaceae). Evolution 34: 467–474.Google Scholar
  9. Bawa, K. S. (1980b). Evolution of dioecy in flowering plants. Ann. Rev. Ecol. Syst. 11: 15–39.CrossRefGoogle Scholar
  10. Beach, J. H. (1981). Pollinator foraging and the evolution of dioecy. Am. Nat. 118: 572–577.CrossRefGoogle Scholar
  11. Bell, G. (1985). On the function of flowers. Proc. R. Soc. Lond. B 224: 223–265.CrossRefGoogle Scholar
  12. Bell, G., Lefebvre, L., Giraldeau, L.-A., and Weary, D. (1984). Partial preference of insects for the male flowers of an annual herb. Oecologia 65: 287–294.Google Scholar
  13. Broyles, S. B., and Wyatt, R. (1995). A reexamination of the pollen-donation hypothesis in an experimental population of Asclepias exaltata. Evolution 49: 89–99.Google Scholar
  14. Broyles, S. B., and Wyatt, R. (1997). The pollen donation hypothesis revisited: A response to Queller. Am. Nat. 149: 595–599.CrossRefGoogle Scholar
  15. Butler, C. G. (1945). The influence of various physical and biological factors of the environment on honey bee activity. An examination of the relationship between activity and nectar concentration and abundance. J. Exp. Biol. 21: 5–12.Google Scholar
  16. Campbell, D. R. (1989). Inflorescence size: A test of the male function hypothesis. Am. J. Bot. 76: 730–738.Google Scholar
  17. Campbell, D. R., Waser, N. M., Price, M. V., Lynch, E. A., and Mitchell, R. J. (1991). Components of phenotypic selection: Pollen export and flower corolla width in Ipomopsis aggregata. Evolution 45: 1458–1467.Google Scholar
  18. Chaplin, S. J., and Walker, J. L. (1982). Energetic constraints and adaptive significance of the floral display of a forest milkweed. Ecology 63: 1857–1870.Google Scholar
  19. Comba, L., Corbet, S. A., Barron, A., Bird, A., Collinge, S., Miyazaki, N., and Powell, M. (1999). Garden flowers: insect visits and the floral reward of horticulturally-modified variants. Ann. Bot. 83: 73–86.Google Scholar
  20. Conner, J. K., and Rush, S. (1996). Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia 104: 409–516.Google Scholar
  21. Corbet, S. A., Cuthill, I., Fallows, M., Harrison, T., and Hartley, G. (1981). Why do nectar-foraging bees and wasps work upwards on inflorescences? Oecologia 51: 79–83.Google Scholar
  22. Dafni, A. (1984). Mimicry and deception in pollination. Ann. Rev. Ecol. Syst. 15: 359–378.CrossRefGoogle Scholar
  23. Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. J. Murray, London.Google Scholar
  24. Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. J. Murray, London.Google Scholar
  25. Darwin, C. (1888). The Different Forms of Flowers on Plants of the Same Species, University of Chicago Press, Chicago.Google Scholar
  26. Delph, L. F., and Lively, C. M. (1992). Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos 63: 161–170.Google Scholar
  27. Devlin, B., and Stephenson, A. G. (1985). Sex differential floral longevity, nectar secretion, and pollinator foraging in a protandrous species. Am. J. Bot. 72: 303–310.Google Scholar
  28. Dreisig, H. (1995). Ideal free distributions of nectar foraging bumblebees. Oikos 72: 161–172.Google Scholar
  29. Eckhart, V. M. (1991). The effects of floral display on pollinator visitation vary among populations of Phacelia linearis (Hydrophyllaceae). Evol. Ecol. 5: 370–384.CrossRefGoogle Scholar
  30. Emms, S. K., Stratton, D. A., and Snow, A. A. (1997). The effect of inflorescence size on male fitness: experimental tests in the andromonoecious lily, Zigadenus paniculatus. Evolution 51: 1481–1489.Google Scholar
  31. Faegri, K., and van der Pijl, L. (1979). The Principles of Pollination Ecology, 3rd revised ed. Pergamon, Oxford.Google Scholar
  32. Fisher, R. A. (1915). The evolution of sexual preference. Eugen. Rev. 7: 184–192.Google Scholar
  33. Fisher, R. A. (1958). The Genetical Theory of Natural Selection, Dover, New York.Google Scholar
  34. Firmage, D. H., and Cole, F. R. (1988). Reproductive success and inflorescence size of Calopogon tuberosus (Orchidaceae). Am. J. Bot. 75: 1371–1377.Google Scholar
  35. Frankie, G. W., and Haber, W. A. (1983). Why bees move among mass flowering neotropical trees. In Jones, C. E., and Little, R. J. (eds.), Handbook of Experimental Pollination Biology. Scientific and Academic Editions, New York, pp. 360–372.Google Scholar
  36. Free, J. B. (1968). Dandelion as a competitor to fruit trees for bee visits. J. Appl. Ecol. 5: 169–178.Google Scholar
  37. Grant, K. (1966). A hypothesis concerning the prevalence of red coloration in California hummingbird flowers. Am. Nat. 100: 85–97.Google Scholar
  38. Grant, K. (1995). Sexual selection in plants: Pros and cons. Proc. Nat. Acad. Sci. USA 92: 1247–1250.PubMedGoogle Scholar
  39. Harder, L. D., and Cruzan, M. B. (1990). An evaluation of the physiological and evolutionary influences of inflorescence size and flower depth on nectar production. Funct. Ecol. 4: 559–572.Google Scholar
  40. Harder, L. D., Thomson, J. D., Cruzan, M. B., and Unnasch, R. S. (1985). Sexual reproduction and variation in floral morphology in an ephemeral vernal lily, Erythronium americanum. Oecologia 67: 286–291.CrossRefGoogle Scholar
  41. Haynes, J. G., and Mesler, M. (1984). Pollen foraging by bumblebees: Foraging patterns and efficiency of Lupinus polyphyllus. Oecologia 61: 249–253.CrossRefGoogle Scholar
  42. Heinrich, B. (1975). Energetics of pollination. Ann. Rev. Ecol. Syst. 6: 139–170.CrossRefGoogle Scholar
  43. Heinrich, B. (1976). The foraging specializations of individual bumblebees. Ecol. Mon. 46: 105–128.Google Scholar
  44. Heinrich, B. (1983). Insect foraging energetics. In Jones, C. E., and Little, R. J. (eds.), Handbook of Experimental Pollination Biology. Scientific and Academic Editions, New York, pp. 187–214.Google Scholar
  45. Huxley, J. S. (1938). Darwin's theory of sexual selection and the data subsumed by it, in the light of recent research. Am. Nat. 72: 416–433.CrossRefGoogle Scholar
  46. Janzen, D. H. (1971). Euglossine bees as long distance pollinators of tropical plants. Science 171: 203–205.PubMedGoogle Scholar
  47. Janzen, D. H. (1977). A note on optimal mate selection by plants. Am. Nat. 111: 365–371.Google Scholar
  48. Kaplan, S. M., and Mulcahy, D. L. (1971). Mode of pollination and floral sexuality in Thalictrum. Evolution 25: 659–668.Google Scholar
  49. Kay, Q. O. N., Lack, A. J., Bamber, F. C., and Davies, C. R. (1984). Differences between sexes in floral morphology, nectar production and insect visits in a dioecious species. Silene dioica. New Phytol. 98: 515–529.Google Scholar
  50. Krebs, J. R., and Davies, N. B. (1993) An Introduction to Behavioural Ecology, Blackwell Scientific, Oxford.Google Scholar
  51. Lloyd, D. G., and Webb, C. J. (1977). Secondary sex characters in plants. Bot. Rev. 43: 177–216.Google Scholar
  52. Lyons, E. E., Waser, N. M., Price, M. V., Antonovics, J., and Motten, A. F. (1989). Sources of variation in plant reproductive success and implications for concepts of sexual selection. Am. Nat. 134: 409–433.CrossRefGoogle Scholar
  53. Maynard Smith, J. (1991). Theories of sexual selection. Trends Ecol. Evol. 6: 146–151.Google Scholar
  54. McGregor, S. E., Alcorn, S. M., Kurtz, E. G. Jr., and Butler, G. D. Jr. (1959). Bee visitors to saguaro flowers. J. Econ. Entom. 52: 1002–1004.Google Scholar
  55. Mitchell, R. J. (1993). Adaptive significance of Ipomopsis aggregata nectar production: Observation and experiment in the field. Evolution 47: 25–35.Google Scholar
  56. Miyake, T., and Yafuso, M. (2003). Floral scents affect reproductive success in fly-pollinated Alocasia odora (Araceae). Am. J. Botany 90: 370–376.Google Scholar
  57. Müller, H. (1873). Ground ivy. Nature 8: 161–162.Google Scholar
  58. Nakamura, R. R., Stanton, M. L., and Mazer, S. J. (1989). Effects of mate size and mate number on male reproductive success in plants. Ecology 70: 71–76.Google Scholar
  59. Pleasants, J. M. (1981). Bumblebee response to variation in nectar availability. Ecology 62: 1648–1661.Google Scholar
  60. Poldolsky, R. D. (1993). Evolution of a flower dimorphism: How effective is pollen dispersal by “male” flowers? Ecology 74: 2255–2260.Google Scholar
  61. Primack, R. B. (1987). Relationships among flowers, fruits, and seeds. Ann. Rev. Ecol. Syst. 18: 409–430.CrossRefGoogle Scholar
  62. Pyke, G. H. (1978). Optimal foraging: Movement patterns of bumblebees between inflorescences. Theor. Pop. Biol. 13: 72–98.CrossRefGoogle Scholar
  63. Pyke, G. H. (1982). Foraging in bumblebees: Rule of departure from an inflorescence. Canadian J. of Zool. 60: 417–428.Google Scholar
  64. Pyke, G. H., Pulliam, H. R., and Charnov, E. L. (1977). Optimal foraging: A selective review of theory and tests. Q. Rev. Biol. 52: 137–154.CrossRefGoogle Scholar
  65. Queller, D. C. (1983). Sexual selection in a hermaphroditic plant. Nature 305: 706–707.CrossRefGoogle Scholar
  66. Ryan, M. J., and Rand, A. S. (1990). The sensory basis of sexual selection for complex calls in the túngara frog, Physalae mus pustulosus (sexual selection for sensory exploitation). Evolution 44: 305–314.Google Scholar
  67. Spaethe, J., Tautz, J., and Chittka, L. (2001). Visual constraints in foraging bumblebees: Flower size and color affect search time and flight behavior. Proc. Nat. Acad. Sci. 98: 3898–3903.PubMedCrossRefGoogle Scholar
  68. Stanton, M. L., Young, H. J., Ellstrand, N. C., and Clegg, J. M. (1991). Consequences of floral variation for male and female reproduction in experimental populations of wild radish, Raphanus sativus L. Evolution 45: 268–280.Google Scholar
  69. Stanton, M. L., Ashman, T.-L., Galloway, L. F., and Young, H. J. (1992). Estimating male fitness of plants in natural populations. In Wyatt, R. (ed.), Ecology and Evolution of Plant Reproduction, Chapman& Hall, New York, pp. 62–90.Google Scholar
  70. Stephenson, A. G., and Bertin, R. I. (1983). Male competition, female choice, and sexual selection in plants. In Real, L. (ed.), Pollination Biology, Academic Press, New York, pp. 110–149.Google Scholar
  71. Sutherland, S., and Delph, L. F. (1984). On the importance of male fitness in plants: Patterns of fruit set. Ecology 65: 1093–1104.Google Scholar
  72. Thomson, J. D., and Plowright, R. C. (1980). Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46: 68–74.CrossRefGoogle Scholar
  73. Thomson, J. D., Maddison, W. P., and Plowright, R. C. (1982). Behavior of bumble bee pollinators of Aralia hispida Vent. (Araliaceae). Oecologia 54: 326–336.CrossRefGoogle Scholar
  74. Thomson, J. D., McKenna, M. A., and Cruzan, M. B. (1989). Temporal patterns of nectar and pollen production in Aralia hispida: Implications for reproductive success. Ecology 70: 1061–1068.Google Scholar
  75. Waddington, D., and Heinrich, B. (1979). The foraging movements of bumblebees on vertical inflorescences: An experimental analysis. J. Comp. Physiol. 134: 113–117.CrossRefGoogle Scholar
  76. Wainselboim, A. J., Roces, F., and Farina, W. M. (2002). Honeybees assess changes in nectar flow within a single foraging bout. Animal Behav. 63: 1–6.Google Scholar
  77. Willson, M. F. (1979). Sexual selection in plants. Am. Nat. 113: 777–790.CrossRefGoogle Scholar
  78. Willson, M. F. (1990). Sexual selection in plants and animals. Trends Ecol. Evol. 5: 210–214.CrossRefGoogle Scholar
  79. Willson, M. F. (1991). Sexual selection, sexual dimorphism and plant phylogeny. Evol. Ecol. 5: 69–87.Google Scholar
  80. Willson, M. F. (1994). Sexual selection in plants: Perspective and overview. Am. Nat. 144: S13–S39.CrossRefGoogle Scholar
  81. Willson, M. F., and Rathcke, B. J. (1974). Adaptive design of the floral display in Asclepias syriaca L. Am. Mid. Nat. 92: 47–57.Google Scholar
  82. Wilson, P., Thomson, J. D., Stanton, M. L., and Rigney, L. P. (1994). Beyond floral Batemania: Gender biases in selection for pollination success. Am. Nat. 143: 283–296.CrossRefGoogle Scholar
  83. Young, H. J., and Stanton, M. L. (1990). Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71: 536–547.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  1. 1.College of SciencesThe University of LouisianaLafayette
  2. 2.LafayetteUSA

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