The contribution of a pollinating seed predator to selection on Silene latifolia females

Journal of Evolutionary Biology

Volumn 25, Issue 3, 2012, Pages 461-472

  Burkhardt, A ^a,b   Ridenhour, B J ^c   Delph, L F ^d   Bernasconi, G ^a,b  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF NOTRE DAME   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Hadena bicruris; Mutualism; Parasitism; Phenotypic selection; Pollination; Sexual dimorphism

Indexed keywords

DICOTYLEDON; DIOECY; FEMALE BEHAVIOR; FLORAL TRAIT; FRUITING; LIFE HISTORY TRAIT; MOTH; MUTUALISM; NATURAL SELECTION; PARASITISM; PHENOTYPE; PLANT-POLLINATOR INTERACTION; POLLINATOR; PREDATOR; SEED PREDATION; SEXUAL DIMORPHISM;

ANIMAL; ARTICLE; COMPARATIVE STUDY; FEEDING BEHAVIOR; FEMALE; FLOWER; FRUIT; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOTH; PHYSIOLOGY; PLANT SEED; POLLINATION; SILENE; STATISTICAL MODEL;

ANIMALS; FEEDING BEHAVIOR; FEMALE; FLOWERS; FRUIT; LINEAR MODELS; MOTHS; POLLINATION; SEEDS; SELECTION, GENETIC; SILENE;

HADENA BICRURIS; LEPIDOPTERA; SILENE; SILENE LATIFOLIA;

EID: 84857048048     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02436.x     Document Type: Article

References (81)

1. Arista, M. & Ortiz, P.L. 2007. Differential gender selection on floral size: an experimental approach using Cistus salvifolius. J. Ecol. 95: 973-982.
2. Arnold, S.J. & Wade, M.J. 1984. On the measurement of natural and sexual selection: theory. Evolution 38: 709-719.
3. Arvanitis, L., Wiklund, C. & Ehrlen, J. 2008. Plant ploidy level influences selection by butterfly seed predators. Oikos 117: 1020-1025.
4. Arvanitis, L., Wiklund, C., Muenzbergova, Z., Dahlgren, J.P. & Ehrlen, J. 2010. Novel antagonistic interactions associated with plant polyploidization influence trait selection and habitat preference. Ecol. Lett. 13: 330-337.
5. Biere, A. & Honders, S.J. 1996. Impact of flowering phenology of Silene alba and S. dioica on susceptibility to fungal infection and seed predation. Oikos 77: 467-480.
6. Biere, A., Elzinga, J.A., Honders, S.C. & Harvey, J.A. 2002. A plant pathogen reduces the enemy-free space of an insect herbivore on a shared host plant. Proc. Biol. Sci. 269: 2197-2204.
7. Blackman, R.L. & Eastop, V.F. 2006. Aphids on the World's Herbaceous Plants and Shrubs. 2. The Aphids, 1st edn. John Wiley & Sons Ltd, Chichester.
8. Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. et al. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24: 127-135.
9. Brantjes, N.B.M. 1976. Riddles around pollination of Melandrium album (Mill) Garcke (Caryophyllaceae) during oviposition by Hadena bicruris Hufn. (Noctuidae, Lepidoptera). Proceedings of the Koninklijke Nederlandse Akademie Van Wetenschappen Series C - Biological and Medical Sciences 79: 1-12.
10. Brody, A.K. 1992. Oviposition choices by a predispersal seed predator (Hylemya sp). I. Correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology. Oecologia 91: 56-62.
11. Brody, A.K. 1997. Effects of pollinators, herbivores, and seed predators on flowering phenology. Ecology 78: 1624-1631.
12. Brody, A.K. & Mitchell, R.J. 1997. Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant Ipomopsis aggregata. Oecologia 110: 86-93.
13. Brown, E. & Kephart, S. 1999. Variability in pollen load: implications for reproduction and seedling vigor in a rare plant, Silene douglasii var. oraria. Int. J. Plant Sci. 160: 1145-1152.
14. Buide, M.L. 2006. Pollination ecology of Silene acutifolia (Caryophyllaceae): floral traits variation and pollinator attraction. Ann. Bot. 97: 289-297.
15. Burkhardt, A., Delph, L.F. & Bernasconi, G. 2009. Benefits and costs to pollinating, seed-eating insects: the effect of flower size and fruit abortion on larval performance. Oecologia 161: 87-98.
16. Cariveau, D., Irwin, R.E., Brody, A.K., Garcia-Mayeya, L.S. & von der Ohe, A. 2004. Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos 104: 15-26.
17. Carroll, S.B. & Delph, L.F. 1996. The effects of gender and plant architecture on allocation to flowers in dioecious Silene latifolia (Caryophyllaceae). Int. J. Plant Sci. 157: 493-500.
18. Conner, J.K. 2003. Artificial selection: a powerful tool for ecologists. Ecology 84: 1650-1660.
19. Conner, J.K. & Rush, S. 1996. Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia 105: 509-516.
20. Crawley, M.J. 2007. The R Book, 1st edn. John Wiley & Sons, Ltd, Chichester.
21. Davis, M.A. 1981. The effect of pollinators, predators, and energy constraints on the floral ecology and evolution of Trillium erectum. Oecologia 48: 400-406.
22. Delph, L.F. 2007. The genetic integration of sexually dimorphic traits in the dioecious Silene latifolia. In: Sex, Size and Gender Roles: Evolutionary Studies of Sexual Dimorphism (D.F. Fairbairn, W.U. Blanckenhorn & T. Szekely, eds), pp. 115-123. Oxford University Press, Oxford.
23. Delph, L.F., Galloway, L.F. & Stanton, M.L. 1996. Sexual dimorphism in flower size. Am. Nat. 148: 299-320.
24. Delph, L.F., Knapczyk, F.N. & Taylor, D.R. 2002. Among population variation and correlations in sexually dimorphic traits of Silene latifolia. J. Evol. Biol. 15: 1011-1020.
25. Delph, L.F., Frey, F.M., Steven, J.C. & Gehring, J.L. 2004a. Investigating the independent evolution of the size of floral organs via G-matrix estimation and artificial selection. Evol. Dev. 6: 438-448.
26. Delph, L.F., Gehring, J.L., Frey, F.M., Arntz, A.M. & Levri, M. 2004b. Genetic constraints on floral evolution in a sexually dimorphic plant revealed by artificial selection. Evolution 58: 1936-1946.
27. Dufaÿ, M. & Anstett, M.C. 2003. Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100: 3-14.
28. Eckhart, V.M. 1991. The effects of floral display on pollinator visitation vary among populations of Phacelia linearis (Hydrophyllaceae). Evol. Ecol. 5: 370-384.
29. Efron, B. & Tibshirani, R.J. 1993. An Introduction to the Bootstrap, 1st edn. Chapman and Hall, Boca Raton, Florida.
30. Elston, D.A., Moss, R., Boulinier, T., Arrowsmith, C. & Lambin, X. 2001. Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122: 563-569.
31. Elzinga, J.A. 2005. The Effects of Habitat Fragmentation on a Tritrophic System: Silene latifolia, Hadena bicruris and its Parasitoids. Thesis Utrecht University, Wageningen.
32. Elzinga, J.A. & Bernasconi, G. 2009. Enhanced frugivory on invasive Silene latifolia in its native range due to increased oviposition. J. Ecol. 97: 1010-1019.
33. Elzinga, J.A., Turin, H., van Damme, J.M.M. & Biere, A. 2005. Plant population size and isolation affect herbivory of Silene latifolia by the specialist herbivore Hadena bicruris and parasitism of the herbivore by parasitoids. Oecologia 144: 416-426.
34. Elzinga, J.A., Atlan, A., Biere, A., Gigord, L., Weis, A.E. & Bernasconi, G. 2007a. Time after time: flowering phenology and biotic interactions. Trends Ecol. Evol. 22: 432-439.
35. Elzinga, J.A., van Nouhuys, S., van Leeuwen, D.J. & Biere, A. 2007b. Distribution and colonisation ability of three parasitoids and their herbivorous host in a fragmented landscape. Basic Appl. Ecol. 8: 75-88.
36. Forde, S.E., Thompson, J.N. & Bohannan, B.J.M. 2004. Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431: 841-844.
37. Frey, F.M. 2004. Opposing natural selection from herbivores and pathogens may maintain floral-color variation in Claytonia virginica (Portulacaceae). Evolution 58: 2426-2437.
38. Galen, C. 1996. Rates of floral evolution: adaptation to bumblebee pollination in an alpine wildflower, Polemonium viscosum. Evolution 50: 120-125.
39. Galen, C. 1999. Flowers and enemies: predation by nectar-thieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85: 426-434.
40. 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.
41. Gomez, J.M., Bosch, J., Perfectti, F., Fernandez, J.D., Abdelaziz, M. & Camacho, J.P.M. 2008. Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc. Biol. Sci. 275: 2241-2249.
42. Gomulkiewicz, R., Drown, D.M., Dybdahl, M.F., Godsoe, W., Nuismer, S.L., Pepin, K.M. et al. 2007. Dos and don'ts of testing the geographic mosaic theory of coevolution. Heredity 98: 249-258.
43. Goto, R., Okamoto, T., Kiers, E.T., Kawakita, A. & Kato, M. 2010. Selective flower abortion maintains moth cooperation in a newly discovered pollination mutualism. Ecol. Lett. 13: 321-329.
44. Grindeland, J.M., Sletvold, N. & Ims, R.A. 2005. Effects of floral display size and plant density on pollinator visitation rate in a natural population of Digitalis purpurea. Funct. Ecol. 19: 383-390.
45. Harder, L.D. & Johnson, S.D. 2009. Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol. 183: 530-545.
46. Heie, O.E. 1992. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. IV: Family Aphididae. Part 1 of Tribe Macrosiphini of Subfamily Aphidinae, 1st edn. Scandinavian Science Press Ltd., Leiden, New York, Kobenhavn, Köln.
47. Herrera, C.M., Medrano, M., Rey, P.J., Sanchez-Lafuente, A.M., Garcia, M.B., Guitian, J. et al. 2002. Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc. Natl Acad. Sci. USA 99: 16823-16828.
48. Holland, J.N. & DeAngelis, D.L. 2006. Interspecific population regulation and the stability of mutualism: fruit abortion and density-dependent mortality of pollinating seed-eating insects. Oikos 113: 563-571.
49. Irwin, R.E. 2009. Realized tolerance to nectar robbing: compensation to floral enemies in Ipomopsis aggregata. Ann. Bot. 103: 1425-1433.
50. Irwin, R.E., Strauss, S.Y., Storz, S., Emerson, A. & Guibert, G. 2003. The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84: 1733-1743.
51. Jolivet, C. & Bernasconi, G. 2006. Experimental analysis of constitutive and induced defence in a plant-seed-predator system. Funct. Ecol. 20: 966-972.
52. Jurgens, A., Witt, T. & Gottsberger, G. 1996. Reproduction and pollination in central European populations of Silene and Saponaria species. Bot. Acta 109: 316-324.
53. Labouche, A.-M. & Bernasconi, G. 2010. Male moths provide pollination benefits in the Silene latifolia-Hadena bicruris nursery pollination system. Funct. Ecol. 24: 534-544.
54. Laine, A.L. 2009. Role of coevolution in generating biological diversity: spatially divergent selection trajectories. J. Exp. Bot. 60: 2957-2970.
55. Lande, R. & Arnold, S.J. 1983. The measurement of selection on correlated characters. Evolution 37: 1210-1226.
56. Lord, J.M. & Westoby, M. 2006. Accessory costs of seed production. Oecologia 150: 310-317.
57. Magalhaes, I.S., Gleiser, G., Labouche, A.-M. & Bernasconi, G. 2011. Comparative population genetic structure in a plant-pollinator/seed predator system. Mol. Ecol. 20: 4618-4630.
58. Meagher, T.R. 1992. The quantitative genetics of sexual dimorphism in Silene latifolia (Caryophyllaceae). 1. Genetic variation. Evolution 46: 445-457.
59. Meagher, T.R. & Delph, L.F. 2001. Individual flower demography, floral phenology and floral display size in Silene latifolia. Evol. Ecol. Res. 3: 845-860.
60. Nuismer, S.L. & Ridenhour, B.J. 2008. The contribution of parasitism to selection on floral traits in Heuchera grossulariifolia. J. Evol. Biol. 21: 958-965.
61. Ohara, M. & Higashi, S. 1994. Effects of inflorescence size on visits from pollinators and seed set of Corydalis ambigua (Papaveraceae). Oecologia 98: 25-30.
62. Parachnowitsch, A.L. & Caruso, C.M. 2008. Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89: 1802-1810.
63. Paterson, S. & Lello, J. 2003. Mixed models: getting the best use of parasitological data. Trends Parasitol. 19: 370-375.
64. Pellmyr, O. & Huth, C.J. 1994. Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372: 257-260.
65. R Development Core Team. 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
66. Rey, P.J., Herrera, C.M., Guitian, J., Cerda, X., Sanchez-Lafuente, A.M., Medrano, M. et al. 2006. The geographic mosaic in predispersal interactions and selection on Helleborus foetidus (Ranunculaceae). J. Evol. Biol. 19: 21-34.
67. Richter, K.S. & Weis, A.E. 1995. Differential abortion in the yucca. Nature 376: 557-558.
68. Ridenhour, B.J. 2005. Identification of selective sources: partitioning selection based on interactions. Am. Nat. 166: 12-25.
69. Sandring, S. & Ågren, J. 2009. Pollinator-mediated selection on floral display and flowering time in the perennial herb Arabidopsis lyrata. Evolution 63: 1292-1300.
70. Shykoff, J.A., Bucheli, E. & Kaltz, O. 1997. Anther smut disease in Dianthus silvester (Caryophyllaceae): natural selection on floral traits. Evolution 51: 383-392.
71. Steven, J.C., Delph, L.F. & Brodie, E.D. III 2007. Sexual dimorphism in the quantitative-genetic architecture of floral, leaf, and allocation traits in Silene latifolia. Evolution 61: 42-57.
72. Strauss, S.Y. & Whittall, B. 2006. Non-pollinator agents of selection on floral traits. In: Ecology and Evolution of Flowers (L.D. Harder & C.H. Barett, eds), pp. 120-138. Oxford University Press, Oxford.
73. Thompson, J.N. 2005. Coevolution: the geographic mosaic of coevolutionary arms races. Curr. Biol. 15: R992-R994.
74. Thompson, J.N. & Cunningham, B.M. 2002. Geographic structure and dynamics of coevolutionary selection. Nature 417: 735-738.
75. Vaughton, G. & Ramsey, M. 1998. Floral display, pollinator visitation and reproductive success in the dioecious perennial herb Wurmbea dioica (Liliaceae). Oecologia 115: 93-101.
76. Westerbergh, A. & Westerbergh, J. 2001. Interactions between seed predators/pollinators and their host plants: a first step towards mutualism? Oikos 95: 324-334.
77. Wolfe, L.M. 2002. Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am. Nat. 160: 705-711.
78. Wolfe, L.M., Elzinga, J.A. & Biere, A. 2004. Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol. Lett. 7: 813-820.
79. Wright, J.W. & Meagher, T.R. 2003. Pollination and seed predation drive flowering phenology in Silene latifolia (Caryophyllaceae). Ecology 84: 2062-2073.
80. Young, H. & Gravitz, L. 2002. The effects of stigma age on receptivity in Silene alba (Caryophyllaceae). Am. J. Bot. 89: 1237-1241.
81. Zimmerman, M. & Brody, A.K. 1998. Choices and consequences of oviposition by Hylemya (Delia) sp. (Diptera: Anthomyiidae). J. Insect Behav. 11: 371-381.