Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae)

Arthropod-Plant Interactions

Volumn 5, Issue 3, 2011, Pages 235-244

  Owen, Christina R ^a   Bradshaw, H D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Color contrast; Floral form; Mimulus; Nectar guides; Petal number; Pollinator choice

Indexed keywords

ANGIOSPERM; BEE; FLORA; FORAGING BEHAVIOR; MUTATION; NECTAR; PERENNIAL PLANT; PHENOTYPE; PLANT-POLLINATOR INTERACTION; POLLINATOR;

ANIMALIA; BOMBUS IMPATIENS; IMPATIENS; MAGNOLIOPHYTA; MIMULUS (ANGIOSPERM); MIMULUS LEWISII; PHRYMACEAE;

EID: 80051671151     PISSN: 18728855     EISSN: 18728847     Source Type: Journal    
DOI: 10.1007/s11829-011-9133-8     Document Type: Article

References (82)

1. Aigner PA (2001) Optimality modeling and fitness trade-offs: when should plants become pollinator specialists? OIKOS 95: 177-184.
2. Ando T, Nomura M, Tsukahara J, Watanabe H, Kokubun H, Tsukamoto T, Hashimoto G, Marchesi E, Kitching IJ (2001) Reproductive isolation in a native poulation of Petunia sensu Jussieu (Solanaceae). Ann Bot 88: 403-413.
3. Armbruster WS (1988) Mulitlevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology 69: 1746-1761.
4. Armbruster WS, Muchhala N (2009) Associations between floral specialization and species diversity: cause, effect, or correlation? Evol Ecol 23: 159-179.
5. Beardsley PM, Yen A, Olmstead RG (2003) AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evolution 57: 1397-1410.
6. Bradshaw HD Jr, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426: 176-178.
7. Campbell DR, Waser NM, Price MV (1996) Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77: 1463-1472.
8. Castellanos MC, Wilson P, Thomson JD (2004) 'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers. J Evol Biol 17: 876-885.
9. Cnaani J, Thomson JD, Papaj DR (2006) Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112: 278-285.
10. Comba L, Corbet SA, Hunt H, Outram S, Parker JS, Glover BJ (2000) The role of genes influencing the corolla in pollination of Antirrhinum majus. Plant Cell Environ 23: 639-647.
11. Coyne J, Orr A (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts, USA.
12. Crepet WL (1984) Advanced (constant) insect pollination mechanisms: pattern of evolution and implications vis-à-vis angiosperm diversity. Ann Mo Bot Gard 71: 607-630.
13. Cunningham JP, Moore CJ, Zalucki MP, West SA (2004) Learning, odour preference and flower foraging in moths. J Exp Biol 20: 87-94.
14. Dafni A, Kevan PG (1996) Floral symmetry and nectar guides: ontogenetic constraints from floral development, colour pattern rules and functional significance. Bot J Linn Soc 120: 371-377.
15. Darwin C (1877) The various contrivances by which orchids are fertilized by insects, 2nd edn. J. Murray, London, UK.
16. Dobson HEM, Danielson EM, van Wesep ID (2008) Pollen odor chemicals as modulator of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Species Biol 14: 153-166.
17. Dodd ME, Silvertown J, Chase MW (1999) Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53: 732-744.
18. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebe perception o Antirrhinum majus flower colour. Arthropod Plant Interact 1: 45-55.
19. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35: 375-403.
20. Fenster CB, Cheely G, Dudash MR, Reynolds RJ (2006) Nectar reward and advertisement in hummingbird-pollinated Silene virginica (Caryophyllaceae). Am J Bot 93: 1800-1807.
21. Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and Aquilegiapubescens. Proc Biol Sci 266: 2247-2252.
22. 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.
23. Gegear RJ, Burns JG (2007) The birds, the bees, and the virtual flowers: can pollinator behavior drive ecological speciation in flowering plants? Am Nat 170: 551-566.
24. Gegear RJ, Laverty TM (2005) Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim Behav 69: 939-949.
25. Glover BJ, Martin C (1998) The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80: 778-784.
26. Gomez JM, Bosch J, Perfectti F, Fernández JD, Abdelaziz M, Camacho JPM (2008) Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc Royal Soc B 275: 2241-2249.
27. Goulson D, Hawson SA, Stout JC (1998) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Anim Behav 55: 199-206.
28. Grant V (1949) Pollination systems as isolating mechanisms in angiosperms. Evolution 3: 82-97.
29. Grant KA (1966) A hypothesis concerning the prevalence of red coloration in California hummingbird flowers. Am Nat 100: 85-97.
30. Grant V (1994) Modes and origins of mechanical and ethological isolation in angiosperms. Proc Natl Acad Sci USA 91: 3-10.
31. Gumbert A (2000) Color choices by bumblebees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48: 36-43.
32. Heuschen B, Gumbert A, Lunau K (2005) A generalized mimicry system involving angiosperm flower colour, pollen, and bumblebees' innate colour preferences. Plant Syst Evol 252: 121-137.
33. Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell'Olivo A, Arnold M, Kuhlemeier C (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19: 779-790.
34. Hodges SA, Whittall JB, Fulton M, Yang JY (2002) Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and Aquilegia pubescens. Am Nat 159: S51-S60.
35. Hodges SA, Fulton M, Yang JY, Whittall JB (2003) Verne Grant and evolutionary studies of Aquilegia. New Phytol 161: 113-120.
36. Ishii HS (2006) Floral display size influences subsequent plant choice by bumble bees. Funct Ecol 20: 233-238.
37. Johnson SD, 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.
38. Johnson SD, Steiner KE (1997) Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution 51: 45-53.
39. Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15: 140-143.
40. Johnson SD, Linder HP, Steiner KE (1998) Phylogeny and radiation of pollination systems in Disa (Orchidaceae). Am J Bot 85: 402-411.
41. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29: 83-112.
42. Kelber A (1997) Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. J Exp Biol 200: 827-836.
43. Kimball S (2008) Links between floral morphology and floral visitors along an elevational gradient in a Penstemon hybrid zone. Oikos 117: 1064-1074.
44. Laverty TM (1994) Bumble bee learning and flower morphology. Anim Behav 47: 531-545.
45. Lunau K (2000) The ecology and evolution of visual pollen signals. Plant Syst Evol 222: 89-111.
46. Lunau K, Wacht S, Chittka L (1996) Colour choices of naive bumblebees and their implications for colour perception. J Comp Physiol [A] 178: 477-489.
47. Makino TT, Sakai S (2007) Experience changes pollinator responses to floral display size: from size-based to reward-based foraging. Funct Ecol 21: 854-863.
48. Manning A (1956) The effects of honey-guides. Behaviour 9: 114-139.
49. Martin NH, Sapir Y, Arnold ML (2008) The genetic architecture of reproductive isolation in Louisiana irises: pollination syndromes and pollinator preferences. Evolution 62: 740-752.
50. Medel R, Botto-Mahan C, Kalin-Arroyo M (2003) Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus. Ecology 84: 1721-1732.
51. Meléndez-Ackerman E, Campbell DR (1998) Adaptive significance of flower color and inter-trait correlations in an Ipomopsis hybrid zone. Evolution 52: 1293-1303.
52. Meléndez-Ackerman E, Campbell DR, Waser NM (1997) Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis. Ecology 78: 2532-2541.
53. Møller AP (1995) Bumblebee preference for symmetrical flowers. Proc Natl Acad Sci USA 92: 2288-2292.
54. Penny JHJ (1983) Nectar guide colour contrast: a possible relationship with pollination strategy. New Phytol 95: 707-721.
55. Petrikin J, Wells H (1995) Honey bee (Apis mellifera) use of flower pigment patterns in making foraging choices. J Kans Entomol Soc 68: 377-387.
56. Pohl M, Watolla T, Lunau K (2008) Anther-mimicking floral guides exploit a conflict between innate preference and learning in bumblebees (Bombus terrestris). Behav Ecol Sociobiol 63: 295-302.
57. Ramsey J, Bradshaw HD Jr, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57: 1520-1534.
58. Ricklefs RE, Renner SS (1994) Richness within families of flowering plants. Evolution 48: 1619-1636.
59. Riffell JA, Alarcón R, Abrell L, Davidowitz G, Bronstein JL, Hildebrand JG (2008) Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions. Proc Natl Acad Sci USA 105: 3404-3409.
60. Rodriguez-Gironez MA, Santamaria L (2007) Resource competition, character displacement, and the evolution of deep corolla tubes. Am Nat 170: 455-464.
61. Sargent RD, Otto SP (2005) The role of local species abundance in the evolution of pollinator attraction in flowering plants. Am Nat 167: 67-80.
62. Schemske DW, Bradshaw HD Jr (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96: 11910-11915.
63. Schemske DW, Horvitz CC (1984) Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225: 519-521.
64. Schemske DW, Horvitz CC (1989) Temporal variation in selection on a floral character. Evolution 43: 461-465.
65. Scora RW (1964) Dependency of pollination on patterns in Monarda (Labiatae). Nature 204: 1011-1012.
66. Shang Y, Venail J, Mackay S, Bailey PC, Schwinn KE, Jameson PE, Martin CR, Davies KM (2011) The molecular basis for venation patterning of pigmentation and its effects on pollinator attration in flowers of Antirrhinum. New Phytol 189: 602-615.
67. Smith SDW, Ané C, Baum DA (2008) The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution 62: 793-806.
68. Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst 1: 307-326.
69. Streisfeld MA, Kohn JR (2006) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20: 122-132.
70. Suárez LH, Gonzáles WL, Gianoli E (2009) Foliar damage modifies floral attractiveness to pollinators in Alstroemeria exerens. Evol Ecol 23: 545-555.
71. Sutherland SD, Vickery RK Jr (1993) On the relative importance of floral color, shape, and nectar rewards in attracting pollinators to Mimulus. Great Basin Nat 53: 107-117.
72. Thomson JD, Wilson P (2008) Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. Int J Plant Sci 169: 23-38.
73. Waser NM (1986) Flower constancy: definition, cause, and measurement. Am Nat 127: 593-603.
74. Waser NM (1998) Angiosperm speciation, and the nature of species boundaries. Oikos 82: 198-201.
75. Waser NM, Price MV (1985) The effect of nectar guides on pollinator preference: experimental studies with a montane herb. Oecologia 67: 121-126.
76. Whibley AC, Langlade NB, Andalo C, Hanna AI, Bangham A, Thébaud C, Coen E (2006) Evolutionary paths underlying flower color variation in Antirrhinum. Science 313: 963-966.
77. Whitney HM, Glover BJ (2007) Morphology and development of floral features recognized by pollinators. Arthropod Plant Interact 1: 147-158.
78. Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447: 706-710.
79. Wilbert SM, Schemske DW, Bradshaw HD Jr (2007) Floral anthocyanins from two monkeyflower species with different pollinators. Biochem Syst Ecol 25: 437-443.
80. Wilson P, Stine M (1996) Floral constancy in bumble bees: handling efficiency or perceptual conditioning. Oecologia 106: 493-499.
81. Wilson P, Castellanos MC, Hogue JN, Thomson JD, Armbruster WS (2004) A multivariate search for pollination syndromes among penstemons. OIKOS 104: 345-361.
82. Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH (2008) Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220-230.