The joint evolution of mating system and pollen performance: Predictions regarding male gametophytic evolution in selfers vs. outcrossers

Perspectives in Plant Ecology, Evolution and Systematics

Volumn 12, Issue 1, 2010, Pages 31-41

  Mazer, Susan J ^a   Hove, Alisa A ^a   Miller, Brent S ^a   Barbet Massin, Morgane ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gametophytic competition; Mating system; Pollen competition; Pollen tube growth; Self fertilization; Sexual selection

Indexed keywords

AUTOGAMY; EVOLUTIONARY BIOLOGY; GAMETOPHYTE; GENETIC VARIATION; GENOTYPE; GROWTH RATE; POLLEN; REPRODUCTIVE STRATEGY; SEXUAL SELECTION;

EID: 75849121947     PISSN: 14338319     EISSN: 16180437     Source Type: Journal    
DOI: 10.1016/j.ppees.2009.06.005     Document Type: Article

References (118)

1. Awadalla P., and Ritland K. Microsatellite variation and evolution in the Mimulus guttatus species complex with contrasting mating systems. Mol. Biol. Evol. 14 (1997) 1023-1034
2. Barnes D.K., and Cleveland R.W. Genetic evidence for nonrandom fertilization in alfalfa as influenced by differential pollen tube growth. Crop Sci. 3 (1963) 295-297
3. Barrett S.C.H. The evolution of mating strategies in flowering plants. Trends Plant Sci. 3 (1998) 335-341
4. Bernasconi G. Seed paternity in flowering plants: an evolutionary perspective. Perspect. Plant Ecol. Evol. Syst. 6 (2004) 149-158
5. Bernasconi G., Ashman T.L., Birkhead T.R., Bishop J.D.D., Grossniklaus U., Kubli E., Marshall D.L., Schmid B., Skogsmyr I., Snook R.R., Taylor D., Till-Bottraud I., Ward P.I., Zeh D.W., and Hellriegel B. Evolutionary ecology of the prezygotic stage. Science 303 (2004) 971-975
6. Birkhead T.R., and Pizzari T. Postcopulatory sexual selection. Nat. Rev. Genet. 3 (2002) 262-273
7. Campbell D.R. Multiple paternity in fruits of Ipomopsis aggregata (Polemoniaceae). Am. J. Bot. 85 (1998) 1022-1027
8. Chapman T., Arnqvist G., Bangham J., and Rowe L. Sexual conflict. Trends Ecol. Evol. 18 (2003) 41-47
9. Charlesworth D., and Charlesworth B. The effects of selection in the gametophyte stage on mutational load. Evolution 46 (1992) 703-720
10. Charlesworth D., and Charlesworth B. Quantitative genetics in plants: the effect of the breeding system on genetic variability. Evolution 49 (1995) 911-920
11. Cruden R.W. Pollen-ovule ratios - conservative indicator of breeding systems in flowering plants. Evolution 31 (1977) 32-46
12. Cruzan M.B. Pollen-tube distributions in Nicotiana glauca - evidence for density dependent growth. Am. J. Bot. 73 (1986) 902-907
13. Davis L.E., Stephenson A.G., and Winsor J.A. Pollen competition improves performance and reproductive output of the common zucchini squash under field conditions. J. Am. Soc. Hortic. Sci. 112 (1987) 712-716
14. Delesalle V.A., Mazer S.J., and Paz H. Temporal variation in the pollen: ovule ratios of Clarkia (Onagraceae) taxa with contrasting mating systems: field populations. J. Evol. Biol. 21 (2008) 310-323
15. Delph L.F., and Ashman T.L. Trait selection in flowering plants: how does sexual selection contribute?. Integr. Comp. Biol. 46 (2006) 465-472
16. Delph L.F., Jóhannsson M.H., and Stephenson A.G. How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78 (1997) 1632-1639
17. Delph L.F., Weinig C., and Sullivan K. Why fast-growing pollen tubes give rise to vigorous progeny: the test of a new mechanism. Proc. R. Soc. London B 265 (1998) 935-939
18. Dudley L.S., Mazer S.J., and Galusky P. The joint evolution of mating system, floral traits and life history in Clarkia (Onagraceae): genetic constraints vs. independent evolution. J. Evol. Biol. 20 (2007) 2200-2218
19. Dudash M.R., and Ritland K. Multiple paternity and self-fertilization in relation to floral age in Mimulus guttatus (Scrophulariaceae). Am. J. Bot. 78 (1991) 1746-1753
20. Fenster C.B., and Sork V.L. Effect of crossing distance and male parent on in vivo pollen tube growth in Chamaecrista fasciculata. Am. J. Bot. 75 (1988) 1893-1903
21. Fishman L., Kelly A.J., and Willis J.H. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56 (2002) 2138-2155
22. Fishman L., and Stratton D.A. The genetics of floral divergence and postzygotic barriers between outcrossing and selfing populations of Arenaria uniflora (Caryophyllaceae). Evolution 5 (2004) 296-307
23. French G.C., Ennos R.A., Silverside A.J., and Hollingsworth P.M. The relationship between flower size, inbreeding coefficient and inferred selfing rate in British Euphrasia species. Heredity 94 (2005) 44-51
24. Galen C.J., Shykoff A., and Plowright R.C. Consequences of stigma receptivity schedules for sexual selection in flowering plants. Am. Nat. 127 (1986) 462-476
25. Goodwillie C., Kalisz S., and Eckert C.G. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Ann. Rev. Ecol. Syst. 36 (2005) 47-79
26. Goodwillie C., and Ness J.M. Correlated evolution in floral morphology and the timing of self-compatibility in Leptosiphon jepsonii (Polemoniaceae). Int. J. Plant Sci. 166 (2005) 741-751
27. Goodwillie C., Ritland C., and Ritland K. The genetic basis of floral traits associated with mating system evolution in Leptosiphon (Polemoniaceae): an analysis of quantitative trait loci. Evolution 60 (2006) 491-504
28. Gottlieb L.D. Electrophoretic analysis of the phylogeny of the self-pollinating populations of Clarkia xantiana. Plant Syst. Evol. 147 (1984) 91-102
29. Hamrick J.L., Linhart Y.B., and Mitton J.B. Relationships between life-history characteristics and detectable genetic variation in plants. Ann. Rev. Ecol. Syst. 10 (1979) 173-200
30. Havens K. Clonal repeatability of in vitro pollen tube growth rates in Oenothera organensis (Onagraceae). Am. J. Bot. 81 (1994) 161-165
31. Hedhly A., Hormaza J.I., and Herrero M. Influence of genotype-temperature interaction on pollen performance. J. Evol. Biol. 18 (2005) 1494-1502
32. Herrera C.M. Distribution ecology of pollen tubes: fine-grained, labile spatial mosaics in the southern Spanish Lamiaceae. New Phytol. 161 (2004) 473-484
33. Herrero M., and Hormaza J.I. Pistil strategies controlling pollen tube growth. Sex. Plant Reprod. 9 (1996) 343-347
34. Holdaway-Clarke T.L., and Hepler P.K. Control of pollen tube growth: role of ion gradients and fluxes. New Phytol. 159 (2003) 539-563
35. Holtsford T.P., and Ellstrand N.C. Variation in outcrossing rate and population genetic structure of Clarkia tembloriensis (Onagraceae). Theor. Appl. Genet. 78 (1989) 480-488
36. Honnay O., and Jacquemyn H. A meta-analysis of the relation between mating system, growth form and genotypic diversity in clonal plant species. Evol. Ecol. 22 (2008) 299-312
37. Hormaza J.I., and Herrero M. Pollen selection. Theor. Appl. Genet. 83 (1992) 663-672
38. Hormaza J.I., and Herrero M. Dynamics of pollen tube growth under different competition regimes. Sex. Plant Reprod. 9 (1996) 153-160
39. Igic B., and Kohn J.R. The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60 (2006) 1098-1103
40. Jóhannsson M.H., and Stephenson A.G. Effects of pollination intensity on the vigor of the sporophytic and gametophytic generation of Cucurbita texana. Sex. Plant Reprod. 10 (1997) 236-240
41. Jóhannsson M.H., and Stephenson A.G. Variation in sporophytic and gametophytic vigor in wild and cultivated varieties of Cucurbita pepo and their F1 and F2 generations. Sex. Plant Reprod. 11 (1998) 265-271
42. Jóhannsson M.H., Gates M.J., and Stephenson A.G. Inbreeding depression affects pollen performance in Cucurbita texana. J. Evol. Biol. 11 (1998) 579-588
43. Johnson C.M., and Mulcahy D.L. Male gametophyte in maize. II. Pollen vigor in inbred plants. Theor. Appl. Genet. 51 (1978) 211-215
44. Kalla S.E., and Ashman T.L. The effects of pollen competition on progeny vigor in Fragaria virginiana (Rosaceae) depend on progeny growth environment. Int. J. Plant Sci. 163 (2002) 335-340
45. Kerwin M.A., and Smith-Huerta N.L. Pollen and pistil effects on pollen germination and tube growth in selfing and outcrossing populations of Clarkia tembloriensis (Onagraceae) and their hybrids. Int. J. Plant Sci. 161 (2000) 895-902
46. Krauss S.L. The realized effect of post-pollination sexual selection in a natural plant population. Proc. R. Soc. London B 267 (2000) 1925-1929
47. Kreitner G.L., and Sorensen E.L. Stigma development and the stigmatic cuticle of alfalfa, Medicago sativa L. Bot. Gaz. 145 (1984) 436-443
48. Landi P., Frascaroli E., Tuberosa R., and Conti S. Comparison between responses to gametophytic and sporophytic recurrent selection in maize (Zea mays L.). Theor. Appl. Genet. 77 (1989) 761-767
49. Lankinen Å. Effects of soil pH and phosphorus on in vitro pollen competitive ability and sporophytic traits in clones of Viola tricolor. Int. J. Plant Sci. 161 (2000) 885-893
50. Lankinen Å. In vitro pollen competitive ability in Viola tricolor: temperature and pollen donor effects. Oecologia 128 (2001) 492-498
51. Lankinen Å., and Kiboi S. Pollen donor identity affects timing of stigma receptivity in Collinsia heterophylla (Plantaginaceae): a sexual conflict during pollen competition?. Am. Nat. 170 (2007) 854-863
52. Lankinen Å., and Skogsmyr I. The effect of pollen competition on maintenance of variation in fertilisation ability. Oikos 93 (2001) 459-469
53. Lankinen Å., and Skogsmyr I. Pollen competitive ability: the effect of proportion in two-donor crosses. Evol. Ecol. Res. 4 (2002) 687-700
54. Lankinen Å., Maad J., and Armbruster W.S. Pollen-tube growth rates in Collinsia heterophylla (Plantaginaceae): one-donor crosses reveal heritability but no effect on sporophytic-offspring fitness. Ann. Bot. 103 (2009) 941-950
55. Lloyd D.G., and Yates J.M.A. Intrasexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36 (1982) 903-913
56. Loveless M.D., and Hamrick J.L. Ecological determinants of genetic structure in plant populations. Ann. Rev. Ecol. Syst. 15 (1984) 65-95
57. Marshall D.L., and Diggle P.K. Mechanisms of differential pollen donor performance in wild radish, Raphanus sativus (Brassicaceae). Am. J. Bot. 88 (2001) 242-257
58. Marshall D.L., and Ellstrand N.C. Sexual selection in Raphanus sativus: experimental data on nonrandom fertilization, maternal choice, and consequences of multiple paternity. Am. Nat. 127 (1986) 446-461
59. Marshall D.L., and Ellstrand N.C. Effective mate choice in wild radish: evidence for selective seed abortion and its mechanism. Am. Nat. 131 (1988) 736-759
60. Marshall D.L., Avritt J.J., Shaner M.G.M., and Saunders R.L. Effects of pollen load size and composition on pollen donor performance in wild radish, Raphanus sativus (Brassicaceae). Am. J. Bot. 87 (2000) 1619-1627
61. Marshall D.L., Shaner M.G.M., and Oliva J.P. Effects of pollen load size on seed paternity in wild radish: the roles of pollen competition and mate choice. Evolution 61 (2007) 1925-1937
62. Martin O.Y., and Hosken D.J. The evolution of reproductive isolation through sexual conflict. Nature 423 (2003) 979-982
63. Mazer S.J. Parental effects of seed development and seed yield in Raphanus raphanistrum: implications for natural and sexual selection. Evolution 41 (1987) 355-371
64. Mazer S.J., and Delesalle V.A. Contrasting variation within and covariation between gender-related traits in autogamous versus outcrossing species: alternative evolutionary predictions. Evol. Ecol. 12 (1998) 403-425
65. Mazer S.J., and Gorchov D.L. Parental effects on progeny phenotype in plants: distinguishing genetic and environmental causes. Evolution 50 (1996) 44-53
66. Mitchell R.J., Karron J.D., Holmquist K.G., and Bell J.M. Patterns of multiple paternity in fruits of Mimulus ringens (Phrymaceae). Am. J. Bot. 92 (2005) 885-890
67. Moeller D.A., and Geber M.A. Ecological context of the evolution of self-pollination in Clarkia xantiana: population size, plant communities, and reproductive assurance. Evolution 59 (2005) 786-799
68. Moore D.M., and Lewis H. The evolution of self-pollination in Clarkia xantiana. Evolution 19 (1965) 104-114
69. Mulcahy D.L. The rise of angiosperms: a genecological factor. Science 206 (1979) 20-23
70. Mulcahy D.L., and Mulcahy G.L. The influence of gametophytic competition on sporophytic quality in Dianthus chinensis. Theor. Appl. Genet. 46 (1975) 277-284
71. Nemeth M.B., and Smith-Huerta N.L. Effects of pollen load size and maternal plant on pollen performance and seedling vigor in Clarkia unguiculata (Onagraceae). Int. J. Bot. 2 (2006) 83-92
72. Oakley C.G., Moriuchi K.S., and Winn A.A. The maintenance of outcrossing in predominantly selfing species: ideas and evidence from cleistogamous species. Ann. Rev. Ecol. Syst. 38 (2007) 437-457
73. Ornduff R. Ecology, morphology, and systematics of Jepsonia (Saxifragaceae). Brittonia 21 (1969) 286-298
74. Ottaviano E., Sari-Gorla M., and Mulcahy D.L. Pollen tube growth rates in Zea mays: implications for genetic improvement of crops. Science 210 (1980) 437-438
75. Pasonen H.L., Käpylä M., and Pulkkinen P. Effects of temperature and pollination site on pollen performance in Betula pendula Roth: evidence for genotype-environment interactions. Theor. Appl. Genet. 100 (2000) 1108-1112
76. Pasonen H.L., Pulkkinen P., Käpylä M., and Blom A. Pollen-tube growth rate and seed-siring success among Betula pendula clones. New Phytol. 143 (1999) 243-251
77. Pfahler P.L. Fertilization ability of maize pollen grains. II. Pollen genotype, female sporophyte, and pollen storage interactions. Genetics 57 (1967) 513-521
78. Pfahler P.L., Pereira M.J., and Barnett R.D. Genetic variation for in vitro sesame pollen germination and tube growth. Theor. Appl. Genet. 95 (1997) 1218-1222
79. Plitmann U. Pollen tube attrition as related to breeding systems in Brassicaceae. Plant Syst. Evol. 188 (1993) 65-72
80. Plitmann U. Assessing functional reproductive traits from herbarial material: the test case of pollen tubes in pistils of Polemoniaceae. Taxon 43 (1994) 63-69
81. Rosellini D., Veronesi F., and Falcinelli M. Recurrent selection for microgametophytic vigor in alfalfa and correlated responses at the sporophytic level. Crop Sci. 34 (1994) 933-936
82. Runions C.J., and Geber M.A. Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae). I. Size and development of floral organs. Am. J. Bot. 87 (2000) 1439-1451
83. Sampson J.F. Multiple paternity in Eucalyptus rameliana (Myrtaceae). Heredity 81 (1998) 349-355
84. Sari-Gorla, Ottaviano M.E., and Fiani D. Genetic variability of gametophytic growth rate in maize. Theor. Appl. Genet. 46 (1975) 289-294
85. Sato H., and Yahara T. Trade-offs between flower number and investment to a flower in selfing and outcrossing varieties of Impatiens hypophylla (Balsaminaceae). Am. J. Bot. 86 (1999) 1699-1707
86. Schlichting C.D., Stephenson A.G., Small L.E., and Winsor J.A. Pollen loads and progeny vigor in Cucurbita pepo: the next generation. Evolution 44 (1990) 1358-1372
87. Schoen D.J., and Busch J.W. On the evolution of self-fertilization in a metapopulation. Int. J. Plant Sci. 69 (2008) 119-127
88. Shaner M.G.M., and Marshall D.L. How robust is non-random mating in wild radish: do small pollen loads coupled with more competing pollen donors lead to random mating?. Am. J. Bot. 94 (2007) 266-273
89. Skogsmyr I., and Lankinen Å. Selection on pollen competitive ability in relation to stochastic factors influencing pollen deposition. Evol. Ecol. Res. 1 (1999) 971-985
90. Skogsmyr I., and Lankinen Å. Sexual selection: an evolutionary force in plants?. Biol. Rev 77 (2002) 537-562
91. Smith-Huerta N. Pollen germination and tube growth in selfing and outcrossing populations of Clarkia tembloriensis (Onagraceae). Int. J. Plant Sci. 157 (1996) 228-233
92. Smith-Huerta N. Pollen tube attrition in Clarkia tembloriensis (Onagraceae). Int. J. Plant Sci. 158 (1997) 519-524
93. Snow A.A., and Mazer S.J. Gametophytic selection in Raphanus raphanistrum: a test for heritable variation in pollen competitive ability. Evolution 42 (1988) 1065-1075
94. Snow A.A., and Spira T.P. Differential pollen-tube growth rates and nonrandom fertilization in Hibiscus moscheutos (Malvaceae). Am. J. Bot. 78 (1991) 1419-1426
95. Snow A.A., and Spira T.P. Pollen vigour and the potential for natural selection in plants. Nature 352 (1991) 796-797
96. Snow A.A., and Spira T.P. Individual variation in the vigor of self pollen and selfed progeny in Hibiscus moscheutos (Malvaceae). Am. J. Bot. 80 (1993) 160-164
97. Snow A.A., and Spira T.P. Pollen-tube competition and male fitness in Hibiscus moscheutos. Evolution 50 (1996) 1866-1870
98. Stebbins G.L. Adaptive radiation of reproductive characteristics in Angiosperms I: pollination mechanisms. Ann. Rev. Ecol. Syst. 1 (1970) 307-326
99. Stephenson A.G., Hayes C.N., Jóhannsson M.H., and Winsor J.A. The performance of microgametophytes is affected by inbreeding depression and hybrid vigor in the sporophytic generation. Sex. Plant Reprod. 14 (2001) 77-83
100. Stephenson A.G., Travers S.E., Mena-Ali J.I., and Winsor J.A. Pollen performance before and during the autotrophic-heterotrophic transition of pollen tube growth. Philos. Trans. R. Soc. London [Biol.] 358 (2003) 1009-1017
101. Swanson W.J., and Vacquier V.D. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3 (2002) 137-144
102. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105 (1983) 437-460
103. Tang W., Ezcurra I., Muschietti J., and McCormick S. A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14 (2002) 2277-2287
104. Tiffin P., and Hahn M.W. Coding sequence divergence between two closely related plant species: Arabidopsis thaliana and Brassica rapa ssp. pekinensis. J. Mol. Evol. 54 (2002) 746-753
105. Travers S.E., and Mazer S.J. Trade-offs between male and female reproduction associated with allozyme variation in phosphoglucoisomerase in an annual plant (Clarkia unguiculata: Onagraceae). Evolution 55 (2001) 2421-2428
106. Travers S.E., and Shea K. Individual variation, gametophytic competition and style length: does size affect paternity?. Evol. Ecol. Res. 3 (2001) 729-745
107. van Kleunen M., and Ritland K. Predicting evolution of floral traits associated with mating system in a natural plant population. J. Evol. Biol. 17 (2004) 1389-1399
108. Walsh N.E., and Charlesworth D. Evolutionary interpretation of differences in pollen tube growth rates. Q. Rev. Biol. 67 (1992) 19-37
109. Watterson G.A. On the number of segregation sites. Theor. Popul. Biol. 7 (1975) 256-276
110. Willson M.F., and Burley N. Mate Choice in Plants: Tactics, Mechanisms, and Consequences (1983), Princeton University Press, Princeton, New Jersey
111. Wilsen K.L., and Hepler P.K. Sperm delivery in flowering plants: the control of pollen tube growth. Bioscience 57 (2007) 835-844
112. Winsor J.A., S. Peretz S., and Stephenson A.G. Pollen competition in a natural population of Cucurbita foetidissima. Am. J. Bot. 87 (2000) 527-532
113. Wyatt R. The evolution of self-pollination in granite outcrop species of Arenaria (Caryophyllaceae). 1. Morphological correlates. Evolution 38 (1984) 804-816
114. Wyatt R. The evolution of self-pollination in granite outcrop species of Arenaria (Caryophyllaceae). 3. Reproductive effort and pollen-ovule ratios. Syst. Bot. 9 (1984) 432-440
115. Wyatt R. The evolution of sef-pollination in granite outcrop species of Arenaria (Caryophyllaceae). 4. Correlated changes in the gynoecium. Am. J. Bot. 71 (1984) 1006-1014
116. Yang Z., and Bielawski J.P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15 (2000) 496-503
117. Young H.J., and Stanton M.L. Influence of environmental quality on pollen competitive ability in wild radish. Science 248 (1990) 1631-1633
118. Zamir D., Tanksley S.D., and Jones R.A. Haploid selection for low-temperature tolerance of tomato pollen. Genetics 101 (1982) 129-137