Floral odour and reproductive isolation in two species of Silene

Journal of Evolutionary Biology

Volumn 21, Issue 1, 2008, Pages 111-121

  Waelti, M O ^a   Muhlemann, J K ^a,b   Widmer, A ^a   Schiestl, F P ^a,c  

^a ETH ZURICH   (Switzerland)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Floral odour; Phenylacetaldehyde; Pollen transfer; Reproductive isolation; Scent; Silene dioica; Silene latifolia; Species boundaries

Indexed keywords

ACETALDEHYDE; DRUG DERIVATIVE; PHENYLACETALDEHYDE; UNCLASSIFIED DRUG;

ACETALDEHYDE; AROMATIC HYDROCARBON; DICOTYLEDON; EXPERIMENTAL STUDY; FLOWER; ODOR; POLLINATION; REPRODUCTIVE ISOLATION;

ARTICLE; CHEMISTRY; CIRCADIAN RHYTHM; COMPARATIVE STUDY; FLOWER; ODOR; PHYSIOLOGY; POLLINATION; SILENE; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ACETALDEHYDE; CIRCADIAN RHYTHM; FLOWERS; GENETIC SPECIATION; ODORS; POLLINATION; SILENE; SPECIES SPECIFICITY;

SILENE; SILENE DIOICA; SILENE LATIFOLIA;

EID: 37149033665     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2007.01461.x     Document Type: Article

References (89)

1. Adler, L.S. Irwin, R.E. 2006. Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann. Bot. 97 : 141 150.
2. Altizer, S.M., Thrall, P.H. Antonovics, J. 1998. Vector behavior and the transmission of anther-smut infection in Silene alba. Am. Midl. Nat. 139 : 147 163.
3. Andersson, S. 2003. Antennal responses to floral scents in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae). Chemoecology 13 : 13 20.
4. Andersson, S. Dobson, H.E.M. 2003. Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. J. Chem. Ecol. 29 : 2303 2318.
5. Ashman, T.L., Bradburn, M., Cole, D.H., Blaney, B.H. Raguso, R.A. 2005. The scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86 : 2099 2105.
6. Ayasse, M., Schiestl, F.P., Paulus, H.F., Lofstedt, C., Hansson, B., Ibarra, F. Francke, W. 2000. Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54 : 1995 2006.
7. Baker, H.G. 1947. Infection of species of Melandrium by Ustilago violacea (Pers) Fuckel and the transmission of the resultant disease. Ann. Bot. 11 : 333 348.
8. Baker, H.G. 1948. Stages in invasion and replacement demonstrated by species of Melandrium. J. Ecol. 36 : 96 119.
9. Baldwin, I.T., Preston, C., Euler, M. Gorham, D. 1997. Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plants. J. Chem. Ecol. 23 : 2327 2343.
10. Bradshaw, H.D., Wilbert, S.M., Otto, K.G. Schemske, D.W. 1995. Genetic-mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376 : 762 765.
11. Bradshaw, H.D., Otto, K.G., Frewen, B.E., McKay, J.K. Schemske, D.W. 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149 : 367 382.
12. Brantjes, N.B.M. 1978. Sensory responses to flowers in night-flying moths. In : The Pollination of Flowers by Insects (A. J. Richards, ed pp. 13 19. Academic Press, London, UK.
13. Bruce, T.J. Cork, A. 2001. Electrophysiological and behavioral responses of female Helicoverpa armigera to compounds identified in flowers of African marigold, Tagetes erecta. J. Chem. Ecol. 27 : 1119 1131.
14. Cantelo, W.W. Jacobson, M. 1979. Phenylacetaldehyde attracts moths to bladder flower and to blacklight traps. Environ. Entomol. 8 : 444 447.
15. Carlsson-Graner, U., Elmqvist, T., Agren, J., Gardfjell, H. Ingvarsson, P. 1998. Floral sex ratios, disease and seed set in dioecious Silene dioica. J. Ecol. 86 : 79 91.
16. Charnov, E.L. 1976. Optimal foraging, marginal value theorem. Theor. Popul. Biol. 9 : 129 136.
17. Chittka, L., Thomson, J.D. Waser, N.M. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86 : 361 377.
18. Coyne, J.A. Orr, H.A. 2004. Speciation, 1st edn. Sinauer Associates, Inc., Sunderland, MA, USA.
19. Cunningham, J.P., Moore, C.J., Zalucki, M.P. West, S.A. 2004. Learning, odour preference and flower foraging in moths. J. Exp. Biol. 207 : 87 94.
20. Cunningham, J.P., Moore, C.J., Zalucki, M.P. Cribb, B.W. 2006. Insect odour perception: recognition, of odour components by flower foraging moths. Proc. R. Soc. Lond. B Biol. Sci. 273 : 2035 2040.
21. Dobson, H.E.M. 1991. Analysis of flower and pollen volatiles. In : Modern Methods of Plant Analysis, New Series, Vol. 12 (H. F. Linskens J. F. Jackson, eds pp. 231 251. Springer, Berlin, Heidelberg, New York.
22. Dobson, H.E.M., Arroyo, J., Bergstrom, G. Groth, I. 1997. Interspecific variation in floral fragrances within the genus Narcissus (Amaryllidaceae). Biochem. Syst. Ecol. 25 : 685 706.
23. Dobson, H.E.M., Danielson, M.E. Van Wesep, I.D. 1999. Pollen odor chemicals as modulators of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Species Biol. 14 : 153 166.
24. Dobzhansky, T. 1951. Genetics and the Origin of Species, 3rd edn. Colombia University Press, New York.
25. Dötterl, S., Jürgens, A., Seifert, K., Laube, T., Weissbecker, B. Schütz, S. 2005a. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol. 169 : 707 718.
26. Dötterl, S., Wolfe, L.M. Jürgens, A. 2005b. Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66 : 203 213.
27. Dötterl, S., Burkhardt, D., Weissbecker, B., Jürgens, A., Schütz, S. Mosandl, A. 2006. Linalool and lilac aldehyde/alcohol in flower scents - Electrophysiological detection of lilac aldehyde stereoisomers by a moth. J. Chromatogr. A 1113 : 231 238.
28. Goulson, D. 1994. A model to predict the influence of insect flower constancy on interspecific competition between insect pollinated plants. J. Theor. Biol. 168 : 309 314.
29. Goulson, D. Jerrim, K. 1997. Maintenance of the species boundary between Silene dioica and S. latifolia (red and white campion). Oikos 79 : 115 126.
30. Grant, V. 1981. Plant Speciation, 2nd edn. Columbia University Press, New York.
31. Grant, V. 1992. Floral isolation between ornithophilous and sphingophilous species of Ipomopsis and Aquilegia. Proc Natl Acad Sci USA 89 : 11828 11831.
32. Grant, V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. Proc. Natl. Acad. Sci. USA 91 : 3 10.
33. Gregg, K.B. 1983. Variation in floral fragrances and morphology - incipient speciation in Cycnoches. Bot. Gaz. 144 : 566 576.
34. Greuter, W. 1995. Silene (Caryophyllaceae) in Greece - a subgeneric and sectional classification. Taxon 44 : 543 581.
35. Haynes, K.F., Zhao, J.Z. Latif, A. 1991. Identification of floral compounds from Abelia grandiflora that stimulate upwind flight in cabbage looper moths. J. Chem. Ecol. 17 : 637 646.
36. Heath, R.R., Landolt, P.J., Dueben, B. Lenczewski, B. 1992. Identification of floral compounds of night-blooming Jessamine attractive to cabbage looper moths. Environ. Entomol. 21 : 854 859.
37. Hess, H.E., Landolt, E. Hirzel, R. 1972. Flora der Schweiz. Birkhäuser Verlag, Basel.
38. Honda, K., Omura, H. Hayashi, N. 1998. Identification of floral volatiles from Ligustrum japonicum that stimulate flower-visiting by cabbage butterfly, Pieris rapae. J. Chem. Ecol. 24 : 2167 2180.
39. Hossaert-McKey, M., Gibernau, M. Frey, J.E. 1994. Chemosensory attraction of fig wasps to substances produced by receptive figs. Entomol. Exp. Appl. 70 : 185 191.
40. Huber, F.K., Kaiser, R., Sauter, W. Schiestl, F.P. 2005. Floral scent emission and pollinator attraction in two species of Gymnadenia (Orchidaceae). Oecologia 142 : 564 575.
41. Jürgens, A. 2004. Flower scent composition in diurnal Silene species (Caryophyllaceae): phylogenetic constraints or adaption to flower visitors? Biochem. Syst. Ecol. 32 : 841 859.
42. Jürgens, A., Witt, T. Gottsberger, G. 1996. Reproduction and pollination in central European populations of Silene and Saponaria species. Bot. Acta 109 : 316 324.
43. Jürgens, A., Witt, T. Gottsberger, G. 2002. Flower scent composition in night-flowering Silene species (Caryophyllaceae). Biochem. Syst. Ecol. 30 : 383 397.
44. Jürgens, A., Witt, T. Gottsberger, G. 2003. Flower scent composition in Dianthus and Saponaria species (Caryophyllaceae) and its relevance for pollination biology and taxonomy. Biochem. Syst. Ecol. 31 : 345 357.
45. Kaminaga, Y., Schnepp, J., Peel, G., Kish, C.M., Ben-Nissan, G., Weiss, D., Orlova, I., Lavie, O., Rhodes, D., Wood, K., Porterfield, D.M., Cooper, A.J.L., Schloss, J.V., Pichersky, E., Vainstein, A. Dudareva, N. 2006. Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J. Biol. Chem. 281 : 23357 23366.
46. Knudsen, J.T. 1994. Floral scent variation in the Pyrola rotundifolia complex in Scandinavia and Western Greenland. Nord. J. Bot. 14 : 277 282.
47. Knudsen, J.T. 2002. Variation in floral scent composition within and between populations of Geonoma macrostachys (Arecaceae) in the western Amazon. Am. J. Bot. 89 : 1772 1778.
48. Knudsen, J.T. Gershenzon, J. 2006. The chemical diversity of floral scent. In : Biology of Floral Scent (N. Dudareva E. Pichersky, eds pp. 27 52. Taylor & Francis Group, Boca Raton.
49. Knudsen, J.T. Mori, S.A. 1996. Floral scents and pollination in neotropical Lecythidaceae. Biotropica 28 : 42 60.
50. Knudsen, J.T. Tollsten, L. 1991. Floral scent and intrafloral scent differentiation in Moneses and Pyrola (Pyrolaceae). Plant Syst. Evol. 177 : 81 91.
51. Knudsen, J.T. Tollsten, L. 1993. Trends in floral scent chemistry in pollination syndromes - floral scent composition in moth-pollinated taxa. Bot. J. Linn. Soc. 113 : 263 284.
52. Knudsen, J.T., Tollsten, L. Bergström, L.G. 1993. Floral scents - a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33 : 253 280.
53. Knudsen, J.T., Eriksson, R., Gershenzon, J. Stahl, B. 2006. Diversity and distribution of floral scent. Bot. Rev. 72 : 1 120.
54. Landolt, P.J., Adams, T., Reed, H.C. Zack, R.S. 2001. Trapping alfalfa looper moths (Lepidoptera: Noctuidae) with single and double component floral chemical lures. Environ. Entomol. 30 : 667 672.
55. Levin, R.A., Raguso, R.A. McDade, L.A. 2001. Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58 : 429 440.
56. Loughrin, J.H., Hamiltonkemp, T.R., Andersen, R.A. Hildebrand, D.F. 1990. Volatiles from flowers of Nicotiana sylvestris, Nicotiana otophora and malus x domestica- headspace components and day night changes in their relative concentrations. Phytochemistry 29 : 2473 2477.
57. McNeill, J. 1977. Biology of Canadian weeds.25. Silene alba (Miller) Krause, EHL. Can. J. Plant Sci. 57 : 1103 1114.
58. McNeill, J. 1978. Silene alba and Silene dioica in North America and generic delimitation of Lychnis, Melandrium, and Silene (Caryophyllaceae). Can. J. Bot. Rev. Can. Bot. 56 : 297 308.
59. Meagher, R.L. 2001. Collection of soybean looper and other noctuids in phenylacetaldehyde-baited field traps. Fla. Entomol. 84 : 154 155.
60. Meagher, R.L. 2002. Trapping noctuid moths with synthetic floral volatile lures. Entomol. Exp. Appl. 103 : 219 226.
61. Meusel, H. Mühlberg, H. 1979. Unterfamilie Silenoideae. In : Illustrierte Flora von Mitteleuropa, Vol. 3 (G. Hegi, ed Paul Parey, Berlin.
62. Minder, A.M., Rothenbühler, C. Widmer, A. 2007. Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Mol. Ecol. 16 : 2504 2516.
63. Miyake, T. Yahara, T. 1998. Why does the flower of Lonicera japonica open at dusk? Can. J. Bot. Rev. Can. Bot. 76 : 1806 1811.
64. Muhlemann, J.K., Waelti, M.O., Widmer, A. Schiestl, F.P. 2006. Postpollination floral odour in Silene latifolia: adaptive mechanisms for seed-predator avoidance? J. Chem. Ecol. 32 : 1855 1860.
65. Muller, H.J. 1942. Isolating mechanism, evolution and temperature. Biol. Symp. 6 : 71 125.
66. Nilsson, L.A., Rabakonandrianina, E., Pettersson, B. Ranaivo, J. 1990. Ixoroid secondary pollen presentation and pollination by small moths in the malagasy treelet Ixora platythyrsa (Rubiaceae). Plant Syst. Evol. 170 : 161 175.
67. Nogueira, P.C.D., Bittrich, V., Shepherd, G.J., Lopes, A.V. Marsaioli, A.J. 2001. The ecological and taxonomic importance of flower volatiles of Clusia species (Guttiferae). Phytochemistry 56 : 443 452.
68. Omura, H., Honda, K. Hayashi, N. 1999a. Chemical and chromatic bases for preferential visiting by the cabbage butterfly, Pieris rapae, to rape flowers. J. Chem. Ecol. 25 : 1895 1906.
69. Omura, H., Honda, K., Nakagawa, A. Hayashi, N. 1999b. The role of floral scent of the cherry tree, Prunus yedoensis, in the foraging behavior of Leuhdorfia japonica (Lepidoptera: Papilionidae). Appl. Entomol. Zool. 34 : 309 313.
70. Pierce, A.M., Pierce, H.D., Oehlschlager, A.C. Borden, J.H. 1990. Attraction of Oryzaephilus surinamensis (L) and Oryzaephilus mercator (Fauvel) (Coleoptera, Cucujidae) to some common volatiles of food. J. Chem. Ecol. 16 : 465 475.
71. Plepys, D., Ibarra, F., Francke, W. Lofstedt, C. 2002a. Odour-mediated nectar foraging in the silver Y moth, Autographa gamma (Lepidoptera: Noctuidae): behavioural and electrophysiological responses to floral volatiles. Oikos 99 : 75 82.
72. Plepys, D., Ibarra, F. Lofstedt, C. 2002b. Volatiles from flowers of Platanthera bifolia (Orchidaceae) attractive to the silver Y moth, Autographa gamma (Lepidoptera: Noctuidae). Oikos 99 : 69 74.
73. Raguso, R.A. Light, D.M. 1998. Electroantennogram responses of male Sphinx perelegans hawkmoths to floral and 'green-leaf volatiles'. Entomol. Exp. Appl. 86 : 287 293.
74. Raguso, R.A., Light, D.M. Pickersky, E. 1996. Electroantennogram responses of Hyles lineata (Sphingidae: Lepidoptera) to volatile compounds from Clarkia breweri (Onagraceae) and other moth-pollinated flowers. J. Chem. Ecol. 22 : 1735 1766.
75. Raguso, R.A., Levin, R.A., Foose, S.E., Holmberg, M.W. McDade, L.A. 2003. Fragrance chemistry, nocturnal rhythms and pollination "syndromes" in Nicotiana. Phytochemistry 63 : 265 284.
76. Raguso, R.A., Schlumpberger, B.O., Kaczorowski, R.L. Holtsford, T.P. 2006. Phylogenetic fragrance patterns in Nicotiana sections Alatae and Suaveolentes. Phytochemistry 67 : 1931 1942.
77. Richards, O.W. Baker, H.G. 1947. Insects and fungi associated with Melandrium in the British Isles - insects. J. Ecol. 35 : 271 274.
78. Salzmann, C.C., Brown, A. Schiestl, F.P. 2006. Floral scent emission and pollination syndromes: evolutionary changes from food to sexual deception. Int. J. Plant Sci. 167 : 1197 1204.
79. Schemske, D.W. Bradshaw, H.D. 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. USA 96 : 11910 11915.
80. Schemske, D.W. Bradshaw, H.D. 2003. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426 : 176 178.
81. Schiestl, F.P., Ayasse, M., Paulus, H.F., Erdmann, D. Francke, W. 1997. Variation of floral scent emission and postpollination changes in individual flowers of Ophrys sphegodes subsp. sphegodes. J. Chem. Ecol. 23 : 2881 2895.
82. Schomburg, G. 1990. Gas Chromatography: A Practical Course. VCH Verlagsgesellschaft mbH, Weinheim, Germany.
83. Shykoff, J.A. Bucheli, E. 1995. Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a venereal-disease of plants. J. Ecol. 83 : 189 198.
84. Stebbins, G.L. 1950. Variation and Evolution in Plants. Columbia University Press, New York.
85. Tollstein, L., Knudsen, J.T. Bergstrom, L.G. 1994. Floral scent in generalistic Angelica (Apiaceae) - an adaptive character. Biochem. Syst. Ecol. 22 : 161 169.
86. Van Putten, W.F. 2002. On the host race differentiation in smut fungi. Biology Thesis, University of Utrecht : 152.
87. Waser, N.M. Price, M.V. 1982. A comparison of pollen and fluorescent dye carry-over by natural pollinators of Ipomopsis aggregata (Polemoniaceae). Ecology 63 : 1168 1172.
88. Wells, P.H. Wells, H. 1985. Ethological isolation of plants. 2. Odor selection by honeybees. J. Apic. Res. 24 : 86 92.
89. Westerbergh, A. Saura, A. 1994. Gene flow and pollinator behavior in Silene dioica populations. Oikos 71 : 215 224.