Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1648, 2008, Pages 2241-2249

  Gómez, José M ^a   Bosch, Jordi ^b   Perfectti, Francisco ^a   Fernandez J D ^a   Abdelaziz, Mohamed ^a   Camacho, J P M ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Corolla shape evolution; Geometric morphometrics; Nectar; Pollen; Pollinator preference; Spatial variation

Indexed keywords

ADAPTATION; DICOTYLEDON; FLOWER VISITING; GENERALIST; GEOGRAPHICAL VARIATION; HOST PREFERENCE; MORPHOLOGY; MORPHOMETRY; NATURAL SELECTION; NECTAR; PHENOTYPIC PLASTICITY; PLANT-POLLINATOR INTERACTION;

ARTICLE; BEE; BRASSICACEAE; FLOWER; GEOGRAPHY; PETAL; PHENOTYPE; PLANT DEVELOPMENT; POLLEN; POLLINATION; PRIORITY JOURNAL;

APOIDEA; BOMBYLIIDAE; BRASSICACEAE; ERYSIMUM MEDIOHISPANICUM;

EID: 49749148454     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0512     Document Type: Article

References (77)

1. Abdi, H. 2007 Partial least square regression. In Encyclopedia of measurements and statistics (ed. N. Salkind), pp. 1-13. Thousand Oaks, CA: Sage.
2. Adams, D. C. & Rosenberg, M. S. 1998 Partial warps, phylogeny, and ontogeny: a comment on Fink and Zelditch (1995). Syst. Biol. 47, 168-173. (doi:10.1080/106351598261111)
3. Adams, D. C., Rohlf, F. J. & Slice, D. E. 2004 Geometric morphometrics: ten years of progress following the 'revolution'. Ital. J. Zool. 71, 5-16.
4. Aigner, P. A. 2006 The evolution of specialized floral phenotypes in a fine-grained environment. In Plant-pollinator interactions, from specialization to generalization (eds N. M. Waser & J. Ollerton), pp. 23-46. Chicago, IL: University of Chicago Press.
5. Armbruster, W. S., Antonsen, L. & Pelabon, C. 2005 Phenotypic selection on Delachampia blossoms: honest signaling affects pollination success. Ecology 86, 3323-3333. (doi:10.1890/04-1873)
6. Ashman, T. L. & Stanton, M. 1991 Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana spp. spicata (Malvaceae). Ecology 72, 993-1003. (doi:10.2307/1940599)
7. Biernaskie, J. M. & Gegear, R. J. 2007 Habitat assessment ability of bumble-bees implies frequency-dependent selection on floral rewards and display size. Proc. R. Soc. B 274, 2595-2601. (doi:10.1098/rspb.2007.0705)
8. Blarer, A., Keasar, T. & Shmida, A. 2002 Possible mechanisms for the formation of flower size preferences by foraging bumblebees. Ethology 108, 341-351. (doi:10.1046/j.1439-0310.2002.00778.x)
9. Boisvert, M. J., Veal, A. J. & Sherry, D. F. 2007 Floral reward production is timed by an insect pollinator. Proc. R. Soc. B 274, 1831-1837. (doi:10.1098/rspb.2007.0445)
10. Campbell, D. R., Waser, N. M., Price, M. V., Lynch, E. A. & Mitchell, R. J. 1991 Components of phenotypic selection: pollen export and flower corollawidth in Ipomopsis aggregata. Evolution 45, 1458-1467. (doi:10.2307/2409892)
11. Campbell, D. R., Waser, N. M. & Price, M. V. 1996 Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77, 1463-1472. (doi:10.2307/2265543)
12. Castellanos, M. C., Wilson, P. & Thomson, J. D. 2004 "Antibee" and "pro-bird" changes during the evolution of hummingbird pollination in Penstemon flowers. J. Evol. Biol. 17, 876-885. (doi:10.1111/j.1420-9101.2004.00729.x)
13. Coen, E. S., Nugent, J. M., Luo, D., Bradley, D., Cubas, P., Chadwick, M., Copsey, L. & Carpenter, R. 1995 Evolution of floral symmetry. Phil. Trans. R. Soc. B 350, 35-38. (doi:10.1098/rstb.1995.0134)
14. Cohen, D. & Shmida, A. 1993 The evolution of flower display and reward. Evol. Biol. 27, 197-243.
15. Cronk, Q. C. B., Bateman, R. M. & Hawkins, J. A. 2005 Developmental genetics and plant evolution. London, UK: Taylor and Francis.
16. Cubas, P. E., Vincent, C. & Coen, E. 1999 An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161. (doi:10.1038/43657)
17. Cunningham, J. P., West, S. A. & Wright, D. J. 1998 Learning in the nectar foraging behaviour of Helicoverpa armigera. Ecol. Entomol. 23, 363-369. (doi:10.1046/j.1365-2311. 1998.00149.x)
18. Dafni, A. & Kevan, P. G. 1997 Flower size and shape: implications in pollination. Isr. J. Plant Sci. 45, 201-211.
19. Dilcher, D. 2000 Toward a new synthesis: major evolutionary trends in the angiosperm fossil record. Proc. Natl Acad. Sci. USA 97, 7030-7036. (doi:10.1073/pnas.97.13.7030)
20. Dilley, J. D., Wilson, P. & Mesler, M. R. 2000 The radiation of Calochortus: generalist flowers moving through a mosaic of potential pollinators. Oikos 89, 209-222. (doi:10.1034/j.1600-0706.2000. 890201.x)
21. Donoghue, M. J., Ree, R. & Baum, D. A. 1998 Phylogeny and the evolution of flower symmetry in Asteridae. Trends Plant Sci. 3, 311-317. (doi:10.1016/S1360-1385(98)01278-3)
22. Endress, P. K. 1999 Symmetry in flowers: diversity and evolution. Int. J. Plant Sci. 160, S3-S23. (doi:10.1086/314211)
23. Endress, P. K. 2001 Evolution of floral symmetry. Curr. Opin. Plant Biol. 4, 86-91. (doi:10.1016/S1369-5266(00)00140-0)
24. Fenster, C. B., Armbruster, W. S., Wilson, P. M., Dudash, R. & Thompson, J. D. 2004 Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35, 375-404. (doi:10.1146/annurev.ecolsys.34. 011802.132347)
25. Fenster, C. B., Cheely, G., Dudash, M. R. & Reynolds, R. J. 2006 Nectar reward and advertisement in hummingbird-pollinated Silene virginica (Caryophyllaceae). Am. J. Bot. 93, 1800-1807. (doi:10.3732/ajb.93.12.1800)
26. Galen, C. & Newport, M. E. A. 1987 Bumble bee behavior and selection on flower size in the sky pilot, Polemonium viscosum. Oecologia 74, 20-23. (doi:10.1007/BF00377340)
27. Galen, C. & Cuba, J. 2001 Down the tube: pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55, 1963-1971. (doi:10.1111/j.0014-3820.2001.tb01313.x)
28. Giurfa, M. & Lehrer, M. 2001 Honeybee vision and floral displays: from detection to close-up recognition. In Cognitive ecology of pollination (eds L. Chittka & J. D. Thomson), pp. 61-82. Cambridge, UK: Cambridge University Press.
29. Gómez, J. M. 2003 Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. Am. Nat. 162, 242-256. (doi:10.1086/376574)
30. Gómez, J. M. 2005 Non-additivity effect of herbivores and pollinators on Erysimum mediohispanicum (Cruciferae) fitness. Oecologia 143, 412-418. (doi:10.1007/s00442-004-1809-7)
31. Gómez, J. M. & Zamora, R. 1999 Generalization vs. specialization in the pollination system of Hormathophylla spinosa (Cruciferae). Ecology 80, 796-805.
32. Gómez, J. M. & Zamora, R. 2000 Spatial variation in the selective scenarios of Hormathophylla spinosa (Cruciferae). Am. Nat. 155, 657-668. (doi:10.1086/303353)
33. Gómez, J. M. & Zamora, R. 2006 Ecological factors that promote the evolution of generalization in pollination systems. In Plant-pollinator interactions, from specialization to generalization (eds N. M. Waser & J. Ollerton), pp. 145-165. Chicago, IL: University of Chicago Press.
34. Gómez, J. M., Perfectti, F. & Camacho, J. P. M. 2006 Natural selection on Erysimum mediohispanicum flower shape. Insights into the evolution of zygomorphy. Am. Nat. 168, 531-545. (doi:10.1086/507048)
35. Gómez, J. M., Bosch, J., Perfectti, F., Fernández, J. D., Abdelaziz, M. & Camacho, J. P. M. 2008 Association between floral traits and reward in Erysimum mediohispanicum (Brassicaceae). Ann. Bot 101, 1413-1420. (doi:10.1093/aob/mcn053)
36. Gould, J. L. 1985 How bees remember flower shapes. Science 227, 1492-1494. (doi:10.1126/science.227.4693.1492)
37. Harder, L. D. & Barrett, S. C. H. 2006 Ecology and evolution of flowers. Oxford, UK: Oxford University Press.
38. Heinrich, B. 1993 The hot-blooded insects. New York, NY: Harvard University Press.
39. Herrera, C. M. 1993 Selection on floral morphology and environmental determinants of fecundity in a hawk moth-pollinated violet. Ecol. Monogr. 63, 251-275. (doi:10.2307/2937101)
40. Herrera, C. M., Castellanos, M. C. & Medrano, M. 2006 Geographical context of floral evolution: towards an improved research programme in floral diversification. In Ecology and evolution of flowers (eds L. D. Harder & S. C. H. Barrett), pp. 278-294. Oxford, UK: Oxford University Press.
41. Internicola, A. I., Page, P. A., Bernasconi, G. & Gigord, L. D. B. 2007 Competition for pollinator visitation between deceptive and rewarding artificial inflorescences: an experimental test of the effects of floral colour similarity and spatial mingling. Funct. Ecol. 21, 864-872. (doi:10.1111/j.1365-2435.2007.01303.x)
42. Johnson, S. D. & Dafni, A. 1998 Response of bee-flies to the shape and pattern of model flowers: implications for floral evolution in a Mediterranean herb. Funct. Ecol. 12, 289-297. (doi:10.1046/j.1365- 2435.1998.00175.x)
43. Johnson, S. D. & Steiner, K. E. 2000 Generalization vs. specialization in plant pollination systems. Trends Ecol. Evol. 15, 140-143. (doi:10.1016/S0169-5347(99)01811-X)
44. Kalisz, S., Ree, R. H. & Sargent, R. D. 2006 Linking floral symmetry genes to breeding system evolution. Trends Plant Sci. 11, 568-573. (doi:10.1016/j.tplants.2006.10.005)
45. Kearns, C. A. & Inouye, D. W. 1993 Techniques for pollination biologists. Colorado, CO: University Press of Colorado.
46. Klingenberg, C. P. & Leamy, L. J. 2001 Quantitative genetics of geometric shape in the mouse mandible. Evolution 55, 2342-2352. (doi:10.1111/j.0014-3820.2001.tb00747.x)
47. Klingenberg, C. P. & Monteiro, L. R. 2005 Distances and directions in multidimensional shape spaces: implications for morphometric applications. Syst. Biol. 54, 678-688. (doi:10.1080/10635150590947258)
48. Lande, R. & Arnold, S. J. 1983 The measurement of selection on correlated characters. Evolution 37, 1210-1226. (doi:10.2307/2408842)
49. Lloyd, D. G. & Barrett, C. H. 1996 Floral biology, studies on floral evolution in animal-pollinated plants. New York, NY: Chapman and Hall.
50. Luo, D., Carpenter, R., Vincent, C., Copsey, L. & Coen, E. 1995 Origin of floral asymmetry in Antirrhinum. Nature 383, 794-799. (doi:10.1038/383794a0)
51. Makino, T. T. & Sakai, S. 2007 Experience changes pollinator responses to floral display size: from size-based to reward-based foraging. Funct. Ecol. 21, 854-863. (doi:10.1111/j.1365-2435.2007.01293.x)
52. Moellar, D. A. 2005 Pollinator community structure and sources of spatial variation in plant-pollinator interaction in Clarkia xantiana spp. xantiana. Oecologia 142, 28-37. (doi:10.1007/s00442-004-1693-1)
53. Moellar, D. A. 2006 Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. Ecology 87, 1510-1522. (doi:10.1890/0012-9658(2006)87[1510:GSOPCR]2.0.CO;2)
54. Möller, A. P. 1995 Bumblebee preference for symmetrical flowers. Proc. Natl Acad. Sci. USA 92, 2288-2292. (doi:10.1073/pnas.92.6. 2288)
55. Möller, A. P. & Sorci, G. 1998 Insect preference for symmetrical artificial flowers. Oecologia 114, 37-42. (doi:10.1007/ s004420050417)
56. Muchhala, N. 2007 Adaptive trade-off in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds. Am. Nat. 169, 494-504. (doi:10.1086/512047)
57. Neal, P. R., Dafni, A. & Giurfa, M. 1998 Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annu. Rev. Ecol. Syst. 29, 345-373. (doi:10.1146/annurev.ecolsys. 29.1.345)
58. Olsen, K. M. 1997 Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109, 114-121. (doi:10.1007/PL00008811)
59. Plepys, D., Ibarra, F., Fracnke, W. & Löfstedt, C. 2002 Odour-mediated nectar foraging in the silver Y moth Autographa gamma (Lepidoptera: Noctuidae): behavioural and electrophysiological responses to floral volatiles. Oikos 99, 75-82. (doi:10.1034/j.1600-0706.2002. 990108.x)
60. Ree, R. H. & Donoghue, M. J. 1999 Inferring rates of change in flower symmetry in Asterid angiosperms. Syst. Biol. 48, 633-641. (doi:10.1080/106351599260201)
61. Reeves, P. A. & Olmstead, R. G. 1998 Evolution of novel morphological and reproductive traits in a clade containing Antirrhinum majus (Scrophulariaceae). Am. J. Bot. 85, 1047-1056. (doi:10.2307/2446338)
62. Rohlf, F. J. & Corti, M. 2000 Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740-753. (doi:10.1080/106351500750049806)
63. Rohlf, F. J., Loy, A. & Corti, M. 1996 Morphometric analysis of Old World Talpidae (Mammalia, Insectivora) using partial-warp scores. Syst. Biol. 45, 344-362. (doi:10.2307/2413569)
64. Sargent, R. D. & Otto, S. P. 2006 The role of local species abundance in the evolution of pollinator attraction in flowering plants. Am. Nat. 167, 67-80. (doi:10.1086/498433)
65. Schaefer, H. M., Schaefer, V. & Levey, D. J. 2004 How plant-animal interactions signal new insights in communication. Trends Ecol. Evol. 19, 1-8. (doi:10.1016/j.tree.2003.11.001)
66. Scheiner, R., Erber, J. & Page Jr, R. E. 1999 Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J. Comp. Physiol. A. 185, 1-10. (doi:10.1007/s003590050360)
67. Schemske, D. W. & Bradshaw, H. D. 1999 Pollinator preference and the evolution of floral traits in monkey-flowers (Mimulus). Proc. Natl Acad. Sci. USA 96, 11 910-11 915. (doi:10.1073/pnas.96.21.11910)
68. Smithson, A. & Macnair, M. R. 1997 Negative frequency-dependent selection by pollinators on artificial flowers without rewards. Evolution 51, 715-723. (doi:10.2307/2411148)
69. Stanton, M. L. & Preston, R. E. 1988 Ecological consequences and phenotypic correlates of flower size variation in wild radish, Raphanus sativus L. (Brassicaceae). Am. J. Bot. 75, 528-539. (doi:10.2307/2444218)
70. Stanton, M. & Young, H. J. 1994 Selection for floral character associations in wild radish, Raphanus sativus L. J. Evol. Biol. 7, 271-285. (doi:10.1046/j.1420-9101.1994.7030271.x)
71. Vazquez, D. P., Morris, W. F. & Jordano, P. 2005 Interaction frequency as a surrogate for the total effect of mutualistic animals on plants. Ecol. Lett. 8, 1088-1094. (doi:10.1111/j.1461-0248.2005.00810.x)
72. Waddington, K. D. 2001 Subjective evaluation and choice behavior by nectar- and pollen-collecting bees. In Cognitive ecology of pollination: animal behavior and floral evolution (eds L. Chittka & J. D. Thomson), pp. 41-60. Cambridge, UK: Cambridge University Press.
73. Walker, J. A. 2000 The ability of geometric morphometric methods to estimate a known covariance matrix. Syst. Biol. 49, 686-696. (doi:10.1080/106351500750049770)
74. Wilson, P. & Thomson, J. D. 1996 How do flowers diverge? In Floral biology (eds D. Lloyd & S. C. H. Barrett), pp. 88-111. New York, NY: Chapman & Hall.
75. Yoshioka, Y., Ohashi, K., Konuma, A., Iwata, H., Ohsawa, R. & Ninomiya, S. 2007 Ability of bumblebees to discriminate differences in the shape of artificial flowers of Primula sieboldii (Primulaceae). Ann. Bot. 90, 1175-1182. (doi:10.1093/aob/mcm059)
76. Young, H. J. & Stanton, M. L. 1990 Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71, 536-547. (doi:10.2307/1940307)
77. Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. 2004 Geometric morphometrics for biologists: a primer. San Diego, CA: Elsevier Academic Press.