Parental effects in a partially self-incompatible herb Campanula rapunculoides L. (Campanulaceae): Influence of variation in the strength of self-incompatibility on seed set and progeny performance

American Naturalist

Volumn 161, Issue 4, 2003, Pages 615-630

  Good Avila, Sara V ^a,b   Stephenson, Andrew G ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b ACADIA UNIVERSITY   (Canada)

Author keywords

Breeding system; Campanula rapunculoides; Parental effects; Partial self incompatibility; Quantitative genetic variance

Indexed keywords

GENETIC VARIATION; HERB; INCOMPATIBILITY;

ARTICLE; BIOLOGICAL MODEL; BREEDING; CAMPANULACEAE; EVOLUTION; GENETIC VARIABILITY; GENETICS; PHENOTYPE; PHYSIOLOGY; PLANT SEED; REPRODUCTION;

BREEDING; CAMPANULACEAE; EVOLUTION; MODELS, BIOLOGICAL; PHENOTYPE; REPRODUCTION; SEEDS; VARIATION (GENETICS);

CAMPANULA RAPUNCULOIDES; CAMPANULACEAE; EMBRYOPHYTA;

EID: 0037392599     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/368290     Document Type: Article

References (107)

1. Antonovics, J., and J. Schmitt. 1986. Paternal and maternal effects on propagule size in Anthoxanthum odoratum. Oecologia (Berlin) 69:277-282.
2. Arnold, S. J. 1994. Is there a unifying concept of sexual selection that applies to both plants and animals? American Naturalist 144(suppl.):S1-S12.
3. Ascher, P. D. 1976. Self-incompatibility systems in floricultural crops. Acta Horticulturae 63:205-215.
4. Ashman, T.-L. 1999. Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. Journal of Evolutionary Biology 12:648-661.
5. Atwood, S. S. 1942. Genetics of pseudo-self-compatibility and its relation to cross-incompatibility in Trifolium repens. Journal of Agricultural Research 64:699-709.
6. Barrett, S. C. H. 1988. The evolution, maintenance, and loss of self-incompatibility systems. Pages 98-124 in J. L. Doust and L. L. Doust, eds. Plant reproductive ecology: patterns and strategies. Oxford University Press, New York.
7. Becerra, J. X., and D. G. Lloyd. 1992. Competition-dependent abscission of self-pollinated flowers of Phormium tenax (Agavaceae): a second action of self-incompatibility at the whole flower level? Evolution 46:458-469.
8. Bertin, R. I. 1986. Consequences of mixed pollinations in Campsis radicans. Oecologia (Berlin) 70:1-5.
9. Bertin, R. I., and P. J. Peters. 1992. Paternal effects on offspring quality in Campsis radicans. American Naturalist 140:166-178.
10. Biere, A. 1991. Paternal effects in Lychnis flos-cuculi. 2. Selection on time of emergence and seedling performance in the field. Journal of Evolutionary Biology 3:447-465.
11. Borba, E. L., J. Semir, and G. J. Shepherd. 2001. Self-incompatibility, inbreeding depression and crossing potential in five Brazilian Pleurothallis (Orchidaceae) species. Annals of Botany (London) 88:89-99.
12. Brunet, J. 1992. Sex allocation in hermaphrodite plants. Trends in Ecology & Evolution 7:79-84.
13. Byers, D. L., and D. M. Waller. 1999. Do plant populations purge their genetic load: effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30:479-513.
14. Byers, D. L., G. A. J. Platenkamp, and R. G. Shaw. 1997. Variation in seed characters in Nemophila menziesii: evidence of a genetic basis for maternal effect. Evolution 51:1445-1456.
15. Charlesworth, D., D. W. Schemske, and V. Sork. 1987. The evolution of plant reproductive characters: sexual versus natural selection. Pages 317-335 in S. C. Stearns, ed. Evolution of sex. Birkhauser, Basel.
16. Chen, L., H. J. Sidney, and M. S. Helen. 1997. Self-incompatibility, seed abortion and clonality in the breeding systems of several Western Australian Drosera species (Droseraceae). Australian Journal of Botany 45:191-201.
17. Cockerham, C. C., and B. S. Weir. 1977. Quadratic analyses of reciprocal crosses. Biometrics 33:187-203.
18. Crow, J. F., and M. Kimura. 1970. An introduction to population genetics theory. Harper & Row, New York.
19. Crowe, L. 1971. The polygenic control of outbreeding in Borago officinalis. Heredity 27:111-118.
20. Daehler, C. C. 1999. Inbreeding depression in smooth cordgrass Spartina alterniflora (Poaceae) invading San Francisco Bay. American Journal of Botany 86:131-139.
21. Damgaard, C. 2000. Fixation of advantageous alleles in partially self-fertilizing populations: the effect of different selection modes. Genetics 154:813-821.
22. de Nettancourt, D. 1977. Incompatibility in angiosperms. Springer, New York.
23. Eckert, C. G., and S. C. H. Barrett. 1994. Inbreeding depression in partially self-fertilizing Decodon verticillatus (Lythraceae): population-genetic and experimental analyses. Evolution 48:952-964.
24. Elgersma, A., A. G. Stephenson, and A. P. M. den Nijs. 1986. Effects of genotype and temperature on pollen tube growth in perennial ryegrass Lolium perenne L. Sexual Plant Reproduction 2:225-230.
25. Elle, E. 1998. The quantitative genetics of sex allocation in the andromonoecious perennial, Solanum carolinense. Heredity 80:481-488.
26. Falconer, D. S. 1989. Introduction to quantitative genetics. Wiley, New York.
27. Flaschenriem, D. R., and P. D. Ascher. 1979. S-allele discrimination in styles of Petunia hybrida bearing stylar-conditioned pseudo-self-compatibility. Theoretical and Applied Genetics 55:23-28.
28. Gaude, T., A. Friry, P. Heizmann, C. Mariac, M. Rougier, I. Fobis, and C. Dumas. 1993. Expression of a self-incompatibility gene in a self-compatible line of Brassica oleracea. Plant Cell 5:75-86.
29. Gawel, N. J., and C. D. Robacker. 1986. Effect of pollen-style interaction on the pollen tube growth of Gossypium hirsutum. Theoretical and Applied Genetics 72:84-87.
30. Good, S. V. 2000. Partial self-incompatibility in Campanula rapunculoides L. (Campanulaceae): genetic and molecular bases, parental effects and the influence of pollinator availability on the selfing rate. Ph.D. diss. Pennsylvania State University, University Park.
31. Good-Avila, S. V., and A. Stephenson. 2002. The inheritance of modifiers conferring self-fertility in Campanula rapunculoides L. (Campanulaceae). Evolution 56:263-272.
32. Good-Avila, S. V., F. Frey, and A. G. Stephenson. 2001. The effect of partial self-incompatibility on the breeding system of Campanula rapunculoides L. (Campanulaceae) under conditions of natural pollination. International Journal of Plant Sciences 162:1081-1087.
33. Hanson, M. R. 1991. Plant mitochondrial mutations and male sterility. Annual Review of Genetics 25:461-486.
34. Henny, R., and P. D. Ascher. 1976. The inheritance of pseudo-self-compatibility (PSC) in Nemesia strumosa Benth. Theoretical and Applied Genetics 48:185-195.
35. Hiscock, S. J. 2000. Self-incompatibility in Senecio squalidus L. (Asteraceae). Annals of Botany (London) 85:181-190.
36. Hiscock, S. J., and U. Kües. 1999. Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. International Review of Cytology 193:165-295.
37. Holland, R. L., and T. McNeilly. 1990. Influence of timing of cross- versus self-pollination on self-incompatibility in Brussels sprout inbreds. Euphytica 45:49-57.
38. Inoue, K. 1988. Pattern of breeding-system change in the Izu Island in Campanula punctata: bumblebee-absence hypothesis. Plant Species Biology 3:125-128.
39. Kempthorne, O. 1969. An introduction to genetic statistics. Iowa State University Press, Ames.
40. Kim, S.-C., and L. H. Rieseberg. 1999. Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153:965-977.
41. Kowyama, Y., C. Kunz, I. Lewis, E. Newbigin, A. E. Clarke, and M. A. Anderson. 1994. Self-compatibility in a Lycopersicon peruvianum variant (LA2157) is associated with a lack of style S-RNase activity. Theoretical and Applied Genetics 88:859-864.
42. Lau, T.-C., X. Lu, R. T. Koide, and A. G. Stephenson. 1995. Effects of soil fertility and mycorrhizal infection on pollen production and pollen grain size of Curcubita pepo (Curcurbitaceae). Plant Cell and Environment 18:169-177.
43. Le Roux, L. G., and P. J. Robbertse. 1997. Aspects relating to seed production in Gloriosa superba L. South African Journal of Botany 63:191-197.
44. Levin, D. A. 1993. S-gene polymorphism in Phlox drummondii. Heredity 71:193-198.
45. _. 1996. The evolutionary significance of pseudo self-fertility. American Naturalist 148:321-332.
46. Lipow, S. R., and R. Wyatt. 1999. Diallel crosses reveal patterns of variation in fruit-set, seed mass, and seed number in Asclepias incarnata. Heredity 83:310-318.
47. _. 2000. Single gene control of postzygotic self-incompatibility in poke milkweed, Asclepias exaltata L. Genetics 154:893-907.
48. Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS system for mixed models. SAS Institute, Cary, N.C.
49. Lloyd, D. G. 1968. Pollen tube growth and seed set in self-incompatible and self-compatible Leavenworthia (Cruciferae) populations. New Phytologist 67:179-195.
50. _. 1979. Parental strategies of angiosperms. New Zealand Journal of Botany 17:595-606.
51. Lloyd, D. G., and D. J. Schoen. 1992. Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Science 153:358-369.
52. Luijten, S. H., J. G. B. Oostermeijer, C. Van Leeuwen Nico, and C. M. Den Nijs Hans. 1996. Reproductive success and clonal genetic structure of the rare Arnica montana (Compositae) in the Netherlands. Plant Systematics and Evolution 201:15-30.
53. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, Mass.
54. Lyons, E. E. 1996. Breeding system evolution in Leavenworthia. II. Genetic and nongenetic parental effects on reproductive success in selfing and more outcrossing populations of Leavenworthia crassa. American Naturalist 147:65-85.
55. Marshall, D. L. 1998. Pollen donor performance can be consistent across maternal plants in wild radish: a necessary condition for the action of sexual selection. American Journal of Botany 85:1389-1397.
56. Marshall, D. L., and N. C. Ellstrand. 1986. Sexual selection in Raphanus sativus: experimental data on nonrandom fertilization, maternal choice, and consequences of multiple paternity. American Naturalist 127:446-461.
57. Marshall, D. L., W. Folsom, C. Hatfield, and T. Bennett. 1996. Does interference competition among pollen grains occur in wild radish? Evolution 50:1842-1848.
58. Mazer, S. J., and V. A. Delesalle. 1998. Contrasting variation within and covariation between gender-related traits in autogamous versus outcrossing species: alternative evolutionary predictions. Evolutionary Ecology 12:403-425.
59. Mazer, S. J., and L. M. Wolfe. 1998. Density-mediated maternal effects on seed size in wild radish: genetic variation and its evolutionary implications. Pages 323-343 in T. A. Mousseau and C. W. Fox, eds. Maternal effects as adaptations. Oxford University Press, New York.
60. Mazer, S. J., V. A. Delesalle, and P. Neal. 1999. Responses of floral traits to selection on primary sexual investment in Spergularia marina (Caryophyllaceae): the battle between the sexes. Evolution 53:717-731.
61. Melser, C., M. C. J. Rademake, and P. G. L. Klinkhamer. 2001. Selection on pollen donors by Ecium vulgare. Sexual Plant Reproduction 10:305-312.
62. Miller, J., and D. Venable. 2000. Polyploidy and the evolution of gender dimorphism in plants. Science (Washinton, D.C.) 289:2335-2338.
63. Mitchell-Olds, T., and J. Bergelson. 1990. Statistical genetics of an annual plant, Impatiens capensis. 1. Genetic basis of quantitative variation. Genetics 124:407-415.
64. Montalvo, A. M., and R. G. Shaw. 1994. Quantitative genetics of sequential life-history and juvenile traits in the partially selfing perennial, Aquilegia caerulea. Evolution 48:828-841.
65. Morse, D. H., and J. Schmitt. 1991. Maternal and paternal effects on follicle production in the milkweed Asclepias syriaca (Asclepiadaceae). American Journal of Botany 78:1304-1309.
66. Nyman, Y. 1992. Pollination mechanisms in six Campanula species (Campanulaceae). Plant Systematics and Evolution 181:97-108.
67. _. 1993. The pollen-collecting hairs of Campanula (Campanulaceae). 2. Functional and adaptive significance in relation to pollination. American Journal of Botany 80:1437-1443.
68. Orr, H. A. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805-1813.
69. Ottaviano, E. M., M. Sari-Gorla, and D. L. Mulcahy. 1975. Genetic and intergametophytic influences on pollen tube growth. Pages 125-134 in D. L. Mulcahy, ed. Gamete competition in plants and animals. North-Holland, Amsterdam.
70. Ottaviano, E. M., M. Sari-Gorla, and I. Arenari. 1983. Male gametophyte competition in maize: selection and implications with regard to breeding systems. Pages 367-374 in D. L. Mulcahy and E. M. Ottaviano, eds. Pollen: biology and implications for plant breeding. Elsevier Biomedical, New York.
71. Pfahler, P. L. 1967. Fertilization ability of maize pollen grains. 2. Pollen genotype, female sporophyte and pollen storage interactions. Genetics 57:513-521.
72. Pittman, K. E., and D. A. Levin. 1986. Cross-compatibilityYork in an annual hermaphroditic plant, Phlox drummondii Hook. Pages 477-482 in D. L. Mulcahy, G. B. Mulcahy, and E. M. Ottaviano, eds. Biotechnology and ecology of pollen. Springer, New York.
73. Platenkamp, G. A. J., and R. G. Shaw. 1993. Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution 47:540-555.
74. Ramsey, M., and G. Vaughton. 1996. Inbreeding depression and pollinator availability in a partially self-fertile perennial herb Blandfordia grandiflora (Liliaceae). Oikos 76:465-474.
75. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
76. Richards, A. J. 1986. Plant breeding systems. Chapman &Hall, London. Hall, London.
77. Richardson, T. E., and A. G. Stephenson. 1991. Effects of parentage, prior fruit set and pollen load on fruit and seed production in Campanula americana L. Oecologia (Berlin) 87:80-95.
78. Richardson, T. E., A. Hrincevich, T. H. Kao, and A. G. Stephenson. 1990. Preliminary studies into age-dependent breakdown of self-incompatibility in Campanula rapunculoides: seed set, pollen tube growth, and molecular data. Plant Cell Incompatibility Newsletter 22:41-47.
79. Rieseberg, L. H., J. Whitton, and K. Gardner. 1999. Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152:713-727.
80. Rodriguez, R. T., O. A. Ortega, and J. A. Devesa. 1999. Reproductive biology in two Genisteae (Papilionoideae) endemic of the western Mediterranean region: Cytisus striatus and Retama sphaerocarpa. Canadian Journal of Botany 77:809-820.
81. Rosatti, T. J. 1986. The genera of Sphenocleaceae and Campanulaceae in the southeastern United States. Journal of the Arnold Arboretum Harvard University 67:1-64.
82. Sage, T. L., F. Strumas, W. W. Cole, and S. C. H. Barrett. 1999. Differential ovule development following self- and cross-pollination: the basis of self-sterility in Narcissus triandrus (Amaryllidaceae). American Journal of Botany 86:855-870.
83. Sari-Gorla, M., E. Ottaviano, and D. Faini. 1975. Genetic variability of gametophyte growth rate in maize. Theoretical and Applied Genetics 46:289-294.
84. SAS Institute. 1990. SAS user's guide. SAS Institute, Cary, N.C.
85. Schlichting, C. D., and B. Devlin. 1989. Male and female reproductive success in the hermaphroditic plant Phlox drummondii. American Naturalist 133:212-227.
86. Schmidt, A. G., K. S. Gould, and B. G. Murray. 1999. Floral biology and breeding system of pohutukawa Metrosideros excelsa (Myrtaceae). New Zealand Journal of Botany 37:687-702.
87. Schwaegerle, K. E., and D. A. Levin. 1990. Quantitative genetics of seed size variation in Phlox. Evolutionary Ecology 4:143-148.
88. Shaw, R. G., D. L. Byers, and F. H. Shaw. 1998. Genetic components of variation in Nemophila menziesii undergoing inbreeding: morphology and flowering time. Genetics 150:1649-1661.
89. Snow, A. A., and T. P. Spira. 1991. Pollen vigor and the potential for sexual selection in plants. Nature 352:796-797.
90. Sokal, R. R., and F. J. Rolph. 1981. Biometry. W. H. Freeman, New York.
91. Stephenson, A. G., and R. I. Bertin. 1983. Male competition, female choice and sexual selection in plants. Pages 110-151 in L. Real, ed. Pollination biology. Academic Press, Orlando, Fla.
92. Stephenson, A. G., S. V. Good, and D. W. Vogler. 2000. Interrelationships among inbreeding depression, plasticity in the self-incompatibility system, and the breeding system of Campanula rapunculoides L. (Campanulaceae). Annals of Botany (London) 85:211-220.
93. Thompson, F. L., L. A. Hermanutz, and D. J. Innes. 1998. The reproductive ecology of island populations of distylous Menyanthes trifoliata (Menyanthaceae). Canadian Journal of Botany 76:818-828.
94. Thorogood, D., and M. D. Hayward. 1992. Self-compatibility in Lolium temulentum L.: its genetic control and transfer into L. perenne L. and L. mutliflorum Lam. Heredity 68:71-78.
95. Townsend, C. E. 1966. Self-compatibility studies with diploid alsike clover, Trifolium hybridum L. 2. Inheritance of a self-compatibility factor with gametophytic and sporophytic characteristics. Crop Science 6:415-419.
96. Van Damme, J. M. M. 1991. A restorer gene in gynodioecious Plantago coronopus subject to selection in the gametophytic and seedling stage. Heredity 66:19-27.
97. Vogler, D. W., C. Das, and A. G. Stephenson. 1998. Phenotypic plasticity in the expression of self-incompatibility in Campanula rapunculoides. Heredity 81:546-555.
98. Vogler, D. W., S. Peretz, and A. G. Stephenson. 1999a. Floral plasticity in an iteroparous plant: the interactive effects of genotype, environment, and ontogeny in Campanula rapunculoides (Campanulaceae). American Journal of Botany 86:484-494.
99. Vogler, D. W., K. Filmore, and A. G. Stephenson. 1999b. Inbreeding depression in Campanula rapunculoides L. 1. A comparison of inbreeding depression in plants derived from strong and weak self-incompatibility phenotypes. Journal of Evolutionary Biology 12:483-94.
100. Waser, N. M., and M. V. Price. 1989. Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43:1097-1109.
101. _. 1991. Outcrossing distance effects on Delphinium nelsonii: pollen loads, pollen tubes, and seed set. Ecology 72:171-179.
102. Waser, N. M., R. G. Shaw, and M. V. Price. 1995. Seed set and seed mass in Ipomopsis aggregata: variance partitioning and inferences about postpollination selection. Evolution 49:80-88.
103. Willson, M. F. 1994. Sexual selection in plants: perspective and overview. American Naturalist 144(suppl.):S13-S39.
104. Wilsie, C. P. 1958. Effect of inbreeding on fertility and vigor in alfalfa. Agronomy Journal 50:182-185.
105. Wolff, K., B. Friso, and J. M. van Damme. 1988. Outcrossing rates and male sterility in natural populations of Plantago coronopus. Theoretical and Applied Genetics 76:190-196.
106. Wu, C.-I., N. A. Johnson, and M. F. Palopoli. 1996. Haldane's rule and its legacy: why are there so many sterile males? Trends in Ecology & Evolution 11:281-285.
107. Young, A. G., A. H. D. Brown, and F. A. Zich. 1999. Genetic structure of fragmented populations of the endangered daisy Rutidosis leptorrhynchoides. Conservation Biology 13:256-265.