The incidence and selection of multiple mating in plants

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1613, 2013, Pages

  Pannell, John R ^a   Labouche, Anne Marie ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Multiple paternity; Plant pollinator interaction; Pollen competition; Pollen dispersal; Pollination; Polyandry

Indexed keywords

COMPETITION (ECOLOGY); DISPERSION; FERTILIZATION (REPRODUCTION); FRUIT; GEITONOGAMY; LAND SURFACE; MATING BEHAVIOR; PLANT COMMUNITY; POLLEN LIMITATION; POLYANDRY;

EMBRYOPHYTA; MAGNOLIOPHYTA;

EVOLUTION; FLOWER; GENETIC SELECTION; HISTOLOGY; PHYSIOLOGY; PLANT PHYSIOLOGY; POLLINATION; REPRODUCTION; REVIEW; SEX DIFFERENCE; SPECIES DIFFERENCE;

BIOLOGICAL EVOLUTION; FLOWERS; PLANT PHYSIOLOGICAL PHENOMENA; POLLINATION; REPRODUCTION; SELECTION, GENETIC; SEX FACTORS; SPECIES SPECIFICITY;

MLCS; MLOWN;

EID: 84872729758     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0051     Document Type: Review

References (143)

1. Bernasconi G et al. 2004 Evolutionary ecology of the prezygotic stage. Science 303, 971-975. (doi:10. 1126/science.1092180)
2. Schmid-Hempel P, Speiser B. 1988 Effects of inflorescence size on pollination in Epilobium angustifolium. Oikos 53, 98-104. (doi:10.2307/ 3565669)
3. Karron JD, Mitchell RJ. 2012 Effects of floral display size on male and female reproductive success in Mimulus ringens. Ann. Bot. 109, 563-570. (doi:10. 1093/aob/mcr193)
4. Harder LD, Barrett SCH. 1995 Mating cost of large floral displays in hermaphrodite plants. Nature 373, 512-515. (doi:10.1038/373512a0)
5. de Jong TJ, Waser NM, Klinkhamer PGL. 1993 Geitonogamy: the neglected side of selfing. Trends Ecol. Evol. 8, 321-325. (doi:10.1016/0169-5347(93)90239-L)
6. Judd WS, Campbell CS, Kellogg EA, Stevens P. 2008 Plant systematics: a phylogenetic perspective. Sunderland, MA: Sinauer.
7. Nathan R, Muller-Landau HC. 2000 Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol. Evol. 15, 278-285. (doi:10.1016/S0169-5347(00)01874-7)
8. Ingvarsson PK, Giles BE. 1999 Kin-structured colonization and small-scale genetic differentiation in Silene dioica. Evolution 53, 605-611. (doi:10. 2307/2640796)
9. Goodwillie C, Kalisz S, Eckert CG. 2005 The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 36, 47-79. (doi:10.1146/annurev.ecolsys.36.091704. 175539)
10. Vogler DW, Kalisz S. 2001 Sex among the flowers: the distribution of plant mating systems. Evolution 55, 202-204.
11. Barrett SCH. 2002 The evolution of plant sexual diversity. Nat. Rev. Genet. 3, 274-284. (doi:10. 1038/nrg776)
12. Lloyd DG. 1984 Gender allocation in outcrossing cosexual plants. In Perspectives on plant population ecology (eds R Dirzo, J Sarukhan), pp. 277-300. Sunderland, MA: Sinauer.
13. Banks JA. 1997 Sex determination in the fern Ceratopteris. Trends Plant Sci. 2, 175-180. (doi:10.1016/S1360-1385(97)85223-5)
14. Haig D, Westoby M. 1988 Sex expression in homosporous ferns: an evolutionary perspective. Evol. Trends Plant 2, 111-120.
15. Fernando DD, Lazzaro MD, Owens JN. 2005 Growth and development of conifer pollen tubes. Sexual Plant Reprod. 18, 149-162. (doi:10.1007/s00497-005-0008-y)
16. Ollerton J, Winfree R, Tarrant S. 2011 How many flowering plants are pollinated by animals? Oikos 120, 321-326. (doi:10.1111/j.1600-0706.2010.18644.x)
17. Thomson JD, Plowright RC. 1980 Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46, 68-74. (doi:10.1007/BF00346968)
18. Campbell DR. 1998 Multiple paternity in fruits of Ipomopsis aggregata (Polemoniaceae). Am. J. Bot. 85, 1022-1027. (doi:10.2307/2446369)
19. Ellstrand NC. 1984 Multiple paternity within the fruits of the wild radish, Raphanus sativus. Am. Nat. 123, 819-828. (doi:10.1086/284241)
20. Labouche AM, Bernasconi G. 2010 Male moths provide pollination benefits in the Silene latifolia-Hadena bicruris nursery pollination system. Func. Ecol. 24, 534-544. (doi:10.1111/j.1365-2435. 2009.01658.x)
21. Addicott JF, Tyre AJ. 1995 Cheating in an obligate mutualism: how often do yucca moths benefit yuccas? Oikos 72, 382-394. (doi:10.2307/3546124)
22. Karron JD, Mitchell RJ, Bell JM. 2006 Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. Am. J. Bot. 93, 1306-1312. (doi:10.3732/ajb.93.9.1306)
23. Dudash MR, Ritland K. 1991 Multiple paternity and self-fertilization in relation to floral age in Mimulus guttatus (Scrophulariaceae). Am. J. Bot. 78, 1746-1753. (doi:10.2307/2444854)
24. Engel EC, Irwin RE. 2003 Linking pollinator visitation rate and pollen receipt. Am. J. Bot. 90, 1612-1618. (doi:10.3732/ajb.90.11.1612)
25. Ibarra-Perez FJ, Ellstrand NC, Waines JG. 1996 Multiple paternity in common bean (Phaseolus vulgaris L, Fabaceae). Am. J. Bot. 83, 749-758. (doi:10.2307/2445852)
26. Friedman J, Barrett SCH. 2011 The evolution of ovule number and flower size in wind-pollinated plants. Am. Nat. 177, 246-257. (doi:10. 1086/657954)
27. Friedman J, Barrett SCH. 2009 Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann. Bot. 103, 1515-1527. (doi:10.1093/aob/mcp035)
28. Bernasconi G. 2003 Seed paternity in flowering plants: an evolutionary perspective. Perspect. Plant Ecol. 6, 149-158. (doi:10.1078/1433-8319-00075)
29. Hardy OJ, Vekemans X. 2002 SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2, 618-620. (doi:10.1046/j.1471-8286. 2002.00305.x)
30. Ritland K. 2002 Extensions of models for the estimation of mating systems using n independent loci. Heredity 88, 221-228. (doi:10.1038/sj.hdy. 6800029)
31. Ritland K. 1989 Correlated matings in the partial selfer Mimulus guttatus. Evolution 43, 848-859. (doi:10.2307/2409312)
32. Broyles SB, Wyatt R. 1990 Paternity analysis in a natural population of Asclepias exalta: multiple paternity, functional gender, and the pollen donation hypothesis. Evolution 44, 1454-1468. (doi:10.2307/2409329)
33. Teixeira S, Bernasconi G. 2007 High prevalence of multiple paternity within fruits in natural populations of Silene latifolia, as revealed by microsatellite DNA analysis. Mol. Ecol. 16, 4370-4379. (doi:10.1111/j.1365-294X.2007.03493.x)
34. Mitchell RJ, Karron JD, Holmquist KG, Bell JM. 2005 Patterns of multiple paternity in fruits of Mimulus ringens (Phrymaceae). Am. J. Bot. 92, 885-890. (doi:10.3732/ajb.92.5.885)
35. Massey LK, Hamrick JL. 1999 Breeding structure of a Yucca filamentosa (Agavaceae) population. Evolution 53, 1293-1298. (doi:10.2307/2640832)
36. Brown AHD, Grant JE, Pullen R. 1986 Outcrossing and paternity in Glycine argyrea by paired fruit analysis. Biol. J. Linnean Soc. 29, 283-294. (doi:10. 1111/j.1095-8312.1986.tb00280.x)
37. Hoebee SE, Young AG. 2001 Low neighbourhood size and high interpopulation differentiation in the endangered shrub Grevillea iaspicula McGill (Proteaceae). Heredity 86, 489-496. (doi:10.1046/j. 1365-2540.2001.00857.x)
38. Coates DJ, Hamley VL. 1999 Genetic divergence and the mating system in the endangered and geographically restricted species, Lambertia orbifolia Gardner (Proteaceae). Heredity 83, 418-427. (doi:10.1038/sj.hdy.6885760)
39. Irwin AJ, Hamrick JL, Godt MJW, Smouse PE. 2003 A multiyear estimate of the effective pollen donor pool for Albizia julibrissin. Heredity 90, 187-194. (doi:10.1038/sj.hdy.6800215)
40. Quesada M, Fuchs EJ, Lobo JA. 2001 Pollen load size, reproductive success, and progeny kinship of naturally pollinated flowers of the tropical dry forest tree Pachira quinata (Bombacaceae). Am. J. Bot. 88, 2113-2118. (doi:10.2307/3558436)
41. Morgan MT, Barrett SCH. 1990 Outcrossing rates and correlated mating within a population of Eichhornia paniculata (Pontederiaceae). Heredity 64, 271-280. (doi:10.1038/hdy.1990.33)
42. Hardy OJ, González-Martínez SC, Colas B, Fréville H, Mignot A, Olivieri I. 2004 Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships. Genetics 168, 1601-1614. (doi:10.1534/genetics.104.027714)
43. Young AG, Brown AHD. 1998 Comparative analysis of the mating system of the rare woodland shrub Daviesia suaveolens and its common congener D. mimosoides. Heredity 80, 374-381. (doi:10. 1046/j.1365-2540.1998.00304.x)
44. Oddou-Muratorio S, Klein EK, Demesure-Musch B, Austerlitz F. 2006 Real-time patterns of pollen flow in the wild-service tree, Sorbus torminalis (Rosaceae). III. Mating patterns and the ecological maternal neighborhood. Am. J. Bot. 93, 1650-1659. (doi:10.3732/ajb.93.11.1650)
45. Collevatti RG, Grattapaglia D, Hay JD. 2001 High resolution microsatellite based analysis of the mating system allows the detection of significant biparental inbreeding in Caryocar brasiliense, an endangered tropical tree species. Heredity 86, 60-67. (doi:10.1046/j.1365-2540. 2001.00801.x)
46. Sun M, Ritland K. 1998 Mating system of yellow starthistle (Centaurea solstitialis), a successful colonizer in North America. Heredity 80, 225-232. (doi:10.1046/j.1365-2540.1998.00290.x)
47. Sampson JF. 1998 Multiple paternity in Eucalyptus 9rameliana (Myrtaceae). Heredity 81, 349-355. (doi:10.1046/j.1365-2540.1998.00404.x)
48. Llaurens V, Castric V, Austerlitz F, Vekemans X. 2008 High paternal diversity in the self-incompatible herb Arabidopsis halleri despite clonal reproduction and spatially restricted pollen dispersal. Mol. Ecol. 17, 1577-1588. (doi:10.1111/j.1365-294X.2007.03683.x)
49. Ellstrand NC, Marshall DL. 1985 Interpopulation gene flow by pollen in wild radish, Raphanus sativus. Am. Nat. 126, 606-616. (doi:10. 1086/284442)
50. Muona O, Moran GF, Bell JC. 1991 Hierarchical patterns of correlated mating in Acacia melanoxylon. Genetics 127, 619-626.
51. Zeh JA, Zeh DW. 2001 Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61, 1051-1063. (doi:10.1006/anbe.2000.1705)
52. Birkhead TR, Pizzari T. 2002 Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262-273. (doi:10. 1038/nrg774)
53. Cornell SJ, Tregenza T. 2007 A new theory for the evolution of polyandry as a means of inbreeding avoidance. Proc. R. Soc. B 274, 2873-2879. (doi:10. 1098/rspb.2007.0926)
54. Antonovics J. 2005 Plant venereal diseases: insights from a messy metaphor. New Phytol. 165, 71-80. (doi:10.1111/j.1469-8137.2004.01215.x)
55. Stephenson AG. 2012 Safe sex in plants. New Phytol. 193, 827-829. (doi:10.1111/j.1469-8137. 2011.04035.x)
56. Shykoff JA, Bucheli E, Kaltz O. 1996 Flower lifespan and disease risk. Nature 379, 779. (doi:10.1038/379779a0)
57. Kaltz O, Shykoff JA. 2001 Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease. J. Ecol. 89, 99-109. (doi:10.1046/j.1365-2745.2001.00527.x)
58. Arnqvist G, Nilsson T. 2000 The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60, 145-164. (doi:10.1006/ anbe.2000.1446)
59. Thompson JD. 1994 The coevolutionary process. Chicago, IL: University of Chicago Press.
60. Pellmyr O, Huth CJ. 1994 Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372, 257-260. (doi:10.1038/372257a0)
61. Gwynne DT. 2008 Sexual conflict over nuptial gifts in insects. In Annual review of entomology, pp. 83-101. Palo Alto, CA: Annual Reviews.
62. Tregenza T, Wedell N. 2002 Polyandrous females avoid costs of inbreeding. Nature 415, 71-73. (doi:10.1038/415071a)
63. Hosken DJ, Stockley P. 2003 Benefits of polyandry: a life history perspective. Evol. Biol. 33, 173-194.
64. Bateman AJ. 1948 Intra-sexual selection in Drosophila. Heredity 2, 349-368. (doi:10.1038/hdy. 1948.21)
65. Wilson P, Thomson JD, Stanton ML, Rigney LP. 1994 Beyond floral Batemania: gender biases in selection for pollination success. Am. Nat. 143, 283-296. (doi:10.1086/285604)
66. Ashman TL et al. 2004 Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408-2421. (doi:10.1890/03-8024)
67. Aizen MA, Harder LD. 2007 Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88, 271-281. (doi:10. 1890/06-1017)
68. Haig D, Westoby M. 1988 On limits to seed production. Am. Nat. 131, 757-759. (doi:10.1086/284817)
69. 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. (doi:10.1086/314198)
70. Niesenbaum RA. 1999 The effects of pollen load size and donor diversity on pollen performance, selective abortion, and progeny vigor in Mirabilis jalapa (Nyctaginaceae). Am. J. Bot. 86, 261-268. (doi:10.2307/2656941)
71. Kron P, Husband BC. 2006 The effects of pollen diversity on plant reproduction: insights from apple. Sexual Plant Reprod. 19, 125-131. (doi:10.1007/ s00497-006-0028-2)
72. Delph LF, Havens K. 1998 Pollen competition in flowering plants. In Sperm competition and sexual selection (eds T Birkhead, A Møller), pp. 149-173. San Diego, CA: Academic Press.
73. Darwin C. 1876 The effects of cross-and self-fertilization in the vegetable kingdom. London, UK: John Murray.
74. Jain SK. 1976 The evolution of inbreeding in plants. Annu. Rev. Ecol. Syst. 7, 469-495. (doi:10.1146/annurev.es.07.110176.002345)
75. Jarne P, Charlesworth D. 1993 The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annu. Rev. Ecol. Syst. 24, 441-466. (doi:10.1146/annurev.es.24.110193.002301)
76. Aguirre JD, Marshall DJ. 2012 Does genetic diversity reduce sibling competition? Evolution 66, 94-102. (doi:10.1111/j.1558-5646.2011.01413.x)
77. Karron JD, Marshall DL. 1990 Fitness consequences of multiple paternity in wild radish, Raphanus sativus. Evolution 44, 260-268. (doi:10.2307/ 2409405)
78. Janzen DH. 1970 Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501-528. (doi:10.1086/282687)
79. Schmitt J, Antonovics J. 1986 Experimental studies of the evolutionary significance of sexual reproduction. IV. Effect of neighbor relatedness and aphid infestation on seedling performance. Evolution 40, 830-836. (doi:10.2307/2408467)
80. Griffin CAM, Eckert CG. 2003 Experimental analysis of biparental inbreeding in a self-fertilizing plant. Evolution 57, 1513-1519.
81. Knowlton N, Greenwell SR. 1984 Male sperm competition avoidance mechanisms: the influence of female interests. In Sperm competition and the evolution of animal mating systems (ed. RL Smith), pp. 61-84. Orlando, FL: Academic Press.
82. Schlichting CD, Stephenson AG, Small LE. 1990 Pollen loads and progeny vigor in Cucurbita pepo: the next generation. Evolution 44, 1358-1372. (doi:10.2307/2409295)
83. Lankinen A, Maad J, Armbruster WS. 2009 Pollen-tube growth rates in Collinsia heterophylla (Plantaginaceae): one-donor crosses reveal heritability but no effect on sporophytic-offspring fitness. Ann. Bot. 103, 941-950. (doi:10.1093/aob/ mcp014)
84. Kress WJ. 1981 Sibling competition and evolution of pollen unit, ovule number, and pollen vector in angiosperms. Syst. Bot. 6, 101-112. (doi:10.2307/ 2418541)
85. Delph LF, Weinig C, Sullivan K. 1998 Why fast-growing pollen tubes give rise to vigorous progeny: the test of a new mechanism. Proc. R. Soc. Lond. B 265, 935-939. (doi:10.1098/rspb. 1998.0381)
86. Honys D, Twell D. 2004 Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85. (doi:10.1186/gb-2004-5-11-r85)
87. Chibalina MV, Filatov DA. 2011 Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr. Biol. 17, 1475-1479. (doi:10.1016/ j.cub.2011.07.045)
88. Skogsmyr I, Lankinen A. 2002 Sexual selection: an evolutionary force in plants. Biol. Rev. 77, 537-562. (doi:10.1017/S1464793102005973)
89. Mitchell RJ. 1997 Effects of pollen quantity on progeny vigor: evidence from the desert mustard Lesquerella fendleri. Evolution 51, 1679-1684. (doi:10.2307/2411219)
90. Kalla SE, Ashman TL. 2002 The effects of pollen competition on progeny vigor in Fragaria virginiana (Rosaceae) depend on progeny growth environment. Int. J. Plant Sci. 163, 335-340. (doi:10.1086/338395)
91. Charlesworth D. 1988 Evidence for pollen competition in plants and its relationship to progeny fitness: a comment. Am. Nat. 132, 298-302. (doi:10.1086/284852)
92. Paschke M, Abs C, Schmid B. 2002 Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). Am. J. Bot. 89, 1250-1259. (doi:10.3732/ajb.89.8.1250)
93. Schemske DW, Pautler LP. 1984 The effects of pollen composition on fitness components in a neotropical herb. Oecologia 62, 31-36. (doi:10. 1007/BF00377369)
94. Haig D, Bergstrom CT. 1995 Multiple mating, sperm competition and meiotic drive. J. Evol. Biol. 8, 265-282. (doi:10.1046/j.1420-9101.1995. 8030265.x)
95. Taylor DR, Saur MJ, Adams E. 1999 Pollen performance and sex-ratio evolution in a dioecious plant. Evolution 53, 1028-1036. (doi:10.2307/ 2640808)
96. Heslop-Harrison J. 1968 Pollen wall development. Science 161, 230. (doi:10.1126/science.161.3838.230)
97. Charlesworth D, Charlesworth B, Marais G. 2005 Steps in the evolution of heteromorphic sex chromosomes. Heredity 95, 118-128. (doi:10.1038/sj.hdy.6800697)
98. Field DL, Pickup M, Barrett SCH. 2012 The influence of pollination intensity on fertilization success, progeny sex ratio, and fitness in a wind-pollinated, dioecious plant. Int. J. Plant Sci. 173, 184-191. (doi:10.1086/663164)
99. Stehlik I, Friedman J, Barrett SCH. 2008 Environmental influence on primary sex ratio in a dioecious plant. Proc. Natl Acad. Sci. USA 105, 10847-10 852. (doi:10.1073/pnas.0801964105)
100. Charlesworth D, Mank JE. 2010 The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 186, 9-31. (doi:10.1534/genetics.110.117697)
101. Zahavi A. 1975 Mate selection: selection for a handicap. J. Theor. Biol. 53, 205-214. (doi:10.1016/0022-5193(75)90111-3)
102. Andersson M. 1982 Sexual selection, natural selection and quality advertisement. Biol. J. Linnean Soc. 17, 375-393. (doi:10.1111/j.1095-8312.1982. tb02028.x)
103. Barrett SCH. 1992 Heterostylous genetic polymorphisms: model systems for evolutionary analysis. In Evolution and function of heterostyly (ed. SCH Barrett), pp. 1-39. New York, NY: Springer.
104. Marshall DL, Folsom MW. 1991 Mate choice in plants: an anatomical to population perspective. Annu. Rev. Ecol. Syst. 22, 37-63. (doi:10.1146/ annurev.es.22.110191.000345)
105. Marshall DL, Shaner MGM, Oliva JP. 2007 Effects of pollen load size on seed paternity in wild radish: the roles of pollen competition and mate choice. Evolution 61, 1925-1937. (doi:10.1111/j.1558-5646.2007.00167.x)
106. Korbecka G, Klinkhamer PGL, Vrieling K. 2002 Selective embryo abortion hypothesis revisited: a molecular approach. Plant Biol. 4, 298-310. (doi:10.1055/s-2002-32331)
107. Jennions MD, Petrie M. 2000 Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21-64. (doi:10.1017/S0006323199005423)
108. Marshall DL, Avritt JJ, Shaner M, Saunders RL. 2000 Effects of pollen load size and composition on pollen donor performance in wild radish, Raphanus sativus (Brassicaceae). Am. J. Bot. 87, 1619-1627. (doi:10.2307/2656738)
109. Charlesworth D, Willis JH. 2009 Fundamental concepts in genetics: the genetics of inbreeding depression. Nat. Rev. Genet. 10, 783-796. (doi:10. 1038/nrg2664)
110. Charlesworth D, Charlesworth B. 1987 Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 273-288. (doi:10.1146/ annurev.es.18.110187.001321)
111. Hiscock SJ, McInnis SM. 2003 The diversity of self-incompatibility systems in flowering plants. Plant Biol. 5, 23-32. (doi:10.1055/s-2003-37981)
112. Wright S. 1939 The distribution of self-sterility alleles in populations. Genetics 24, 538-552.
113. Castric V, Vekemans X. 2004 Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances. Mol. Ecol. 13, 2873-2889. (doi:10.1111/ j.1365-294X.2004.02267.x)
114. Young AG, Brown AHD, Murray BG, Thrall PH, Miller CH. 2000 Genetic erosion, restricted mating and reduced viability in fragmented populations of the endangered grassland herb Rutidosis leptorrhynchoides. In Genetics, demography and viability of fragmented populations (eds AG Young, GM Clarke), pp. 335-359. Cambridge, UK: Cambridge University Press.
115. Young AG, Pickup M. 2010 Low S-allele numbers limit mate availability, reduce seed set and skew fitness in small populations of a self-incompatible plant. J. Appl. Ecol. 47, 541-548. (doi:10.1111/j. 1365-2664.2010.01798.x)
116. Primack RB. 1985 Longevity of individual flowers. Annu. Rev. Ecol. Syst. 16, 15-37. (doi:10.1146/annurev.es.16.110185.000311)
117. Spira TP, Snow AA, Puterbaugh MN. 1996 The timing and effectiveness of sequential pollinations in Hibiscus moscheutos. Oecologia 105, 230-235.
118. Burkhardt A, Internicola A, Bernasconi G. 2009 Effects of pollination timing on seed paternity and seed mass in Silene latifolia (Caryophyllaceae). Ann. Bot. 104, 767-773. (doi:10.1093/aob/mcp154)
119. Klinkhamer PGL, Dejong TJ, Metz JAJ. 1994 Why plants can be too attractive: a discussion of measures to estimate male fitness. J. Ecol. 82, 191-194. (doi:10.2307/2261399)
120. Eckert CG. 2000 Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology 81, 532-542. (doi:10.1890/0012-9658(2000)081[0532:COAAGT]2.0.CO;2)
121. Armbruster WS. 1996 Evolution of floral morphology and function: an integrative approach to adaptation, constraint and compromise in Dalechampia (Euphorbiaceae). In Floral biology (eds LD Harder, SCH Barrett), pp. 241-272. New York, NY: Chapman and Hall.
122. Rodrigo J, Herrero M, Hormaza JI. 2009 Pistil traits and flower fate in apricot (Prunus armeniaca). Ann. Appl. Biol. 154, 365-375. (doi:10.1111/j.1744-7348.2008.00305.x)
123. Mulcahy D. 1983 Models of pollen tube competition Geranium maculatum. In Pollination biology (ed. L Real), pp. 151-161. Orlando, FL: Academic Press.
124. Ruane LG. 2009 Post-pollination processes and non-random mating among compatible mates. Evol. Ecol. Res. 11, 1031-1051.
125. Herrero M, Hormaza JI. 1996 Pistil strategies controlling pollen tube growth. Sexual Plant Reprod. 9, 343-347. (doi:10.1007/BF02441953)
126. Herrero M. 2003 Male and female synchrony and the regulation of mating in flowering plants. Phil. Trans. R. Soc. Lond. B 358, 1019-1024. (doi:10. 1098/rstb.2003.1285)
127. Castro S, Silveira P, Navarro L. 2008 Effect of pollination on floral longevity and costs of delaying fertilization in the out-crossing Polygala vayredae Costa (Polygalaceae). Ann. Bot. 102, 1043-1048. (doi:10.1093/aob/mcn184)
128. Marshall DL, Ellstrand NC. 1985 Proximal causes of multiple paternity in wild radish, Raphanus sativus. Am. Nat. 126, 596-605. (doi:10.1086/284441)
129. Epperson BK, Clegg MT. 1987 First pollination primacy and pollen selection in the morning glory, Ipomoea purpurea. Heredity 58, 5-14. (doi:10. 1038/hdy.1987.2)
130. Galen C. 1986 Floral morphology and pollen receipt in Polemonium viscosum: the shape of things to come. Am. J. Bot. 73, 667.
131. Lankinen A, Madjidian JA. 2011 Enhancing pollen competition by delaying stigma receptivity: pollen deposition schedules affect siring ability, paternal diversity, and seed production in Collinsia heterophylla (Plantaginaceae). Am. J. Bot. 98, 1191-1200. (doi:10.3732/ajb.1000510)
132. Dahl AE, Fredrikson M. 1996 The timetable for development of maternal tissues sets the stage for male genomic selection in Betula pendula (Betulaceae). Am. J. Bot. 83, 895-902. (doi:10. 2307/2446267)
133. Ashman TL, Schoen DJ. 1996 Floral longevity: fitness consequences and resource costs. In Studies on floral evolution in animal-pollinated plants (eds, DG Lloyd, SCH Barrett), pp. 112-138. New York, NY: Chapman and Hall.
134. Bell G. 1982 The materpiece of nature: the evolution and genetics of sexuality. Berkely, CA: University of California Press.
135. Charnov EL, Maynard Smith J, Bull JJ. 1976 Why be an hermaphrodite? Nature. 263, 125-126. (doi:10.1038/263125a0)
136. Charnov EL. 1982 The theory of sex allocation. Princeton, NJ: Princeton University Press.
137. Charlesworth D. 1999 Theories of the evolution of dioecy. In Gender and sexual dimorphism in flowering plants (eds MA Geber, TE Dawson, LF Delph), pp. 33-60. Heidelberg, Germany: Springer.
138. Perry LE, Dorken ME. 2011 The evolution of males: support for predictions from sex allocation theory using mating arrays of Satittaria latifolia (Alismataceae). Evolution 65, 2782-2791. (doi:10.1111/j.1558-5646.2011.01344.x)
139. Harder LD, Wilson WG. 1994 Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol. Ecol. 8, 542-559. (doi:10.1007/BF01238257)
140. Harder LD, Barclay RMR. 1994 The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon. Func. Ecol. 8, 509-517. (doi:10.2307/ 2390076)
141. Kawai Y, Kudo G. 2009 Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees. Ecol. Res. 24, 215-223. (doi:10.1007/s11284-008-0500-6)
142. Barrett SCH, Jesson LK, Baker AM. 2000 The evolution and function of stylar polymorphisms in flowering plants. Ann. Bot. 85, 253-265. (doi:10. 1006/anbo.1999.1067)
143. Lloyd DG, Webb CJ. 1992 The evolution of heterostyly. In Evolution and function of heterostyly (ed. SCH Barrett), pp. 151-178. Berlin, Germany: Springer.