1932

Abstract

Mating in seed plants arises from interactions between plant traits and the environmental and demographic context in which individuals reside. These interactions commonly cause nonrandom mating, including selfing and promiscuous outcrossing within local neighborhoods. Shared features of seed plants, specifically immobility, hermaphroditism, and modularity, shape the essential character of mating mediated by animals, wind, and water. In addition, diverse floral strategies promote cross- and self-mating, depending on environmental circumstances. Extrinsic ecological factors influence all stages of the mating process—pollination, pollen-tube growth, ovule fertilization—as well as seed development, determining offspring quantity and quality. Traditionally, measures of plant mating systems have focused on a single axis of variation, the maternal outcrossing rate. Instead, we argue for an expanded perspective encompassing mating portfolios, which include all offspring to which individuals contribute genetically as maternal or paternal parents. This approach should expose key ecological determinants of mating-system variation and their evolutionary consequences.

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2017-11-02
2024-03-28
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Literature Cited

  1. Angeloni F, Ouborg NJ, Leimu R. 2011. Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol. Conserv. 144:35–43 [Google Scholar]
  2. Ashley MV. 2010. Plant parentage, pollination, and dispersal: how DNA microsatellites have altered the landscape. Crit. Rev. Plant Sci. 29:148–61 [Google Scholar]
  3. Baker HG. 1955. Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9:347–49 [Google Scholar]
  4. Barrett SCH. 2002. Sexual interference of the floral kind. Heredity 88:154–59 [Google Scholar]
  5. Barrett SCH. 2003. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philos. Trans. R. Soc. B 358:991–1004 [Google Scholar]
  6. Barrett SCH. 2015. Influences of clonality on plant sexual reproduction. PNAS 112:8859–66 [Google Scholar]
  7. Barrett SCH, Arunkumar R, Wright SI. 2014. The demography and population genomics of evolutionary transitions to self-fertilization in plants. Philos. Trans. R. Soc. B 369:20130344 [Google Scholar]
  8. Bell JM, Karron JD, Mitchell RJ. 2005. Interspecific competition for pollination lowers seed production and outcrossing in Mimulus ringens. Ecology 86:762–71 [Google Scholar]
  9. Bhattacharya S, Baldwin IT. 2012. The post-pollination ethylene burst and the continuation of floral advertisement are harbingers of non-random mate selection in Nicotiana attenuata. Plant J. 71:587–601 [Google Scholar]
  10. Bodbyl Roels SA, Kelly JK. 2011. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65:2541–52 [Google Scholar]
  11. Briscoe Runquist R, Grossenbacher D, Porter S, Kay K, Smith J. 2016. Pollinator‐mediated assemblage processes in California wildflowers. J. Evol. Biol. 29:1045–58 [Google Scholar]
  12. Brunet J, Charlesworth D. 1995. Floral sex allocation in sequentially blooming plants. Evolution 49:70–79 [Google Scholar]
  13. Charlesworth D, Willis JH. 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10:783–96 [Google Scholar]
  14. Cheptou P-O, Avendaño V LG. 2006. Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phytol 172:774–83 [Google Scholar]
  15. Cheptou P-O, Donohue K. 2011. Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol 189:395–407 [Google Scholar]
  16. Cheptou P-O, Lepart J, Escarre J. 2001. Inbreeding depression under intraspecific competition in a highly outcrossing population of Crepis sancta (Asteraceae): evidence for frequency-dependent variation. Am. J. Bot. 88:1424–29 [Google Scholar]
  17. Cruzan MB, Barrett SCH. 2016. Postpollination discrimination between self and outcross pollen covaries with the mating system of a self-compatible flowering plant. Am. J. Bot. 103:568–76 [Google Scholar]
  18. Dart S, Eckert CG. 2013. Experimental and genetic analyses reveal that inbreeding depression declines with increased self-fertilization among populations of a coastal dune plant. J. Evol. Biol. 26:587–99 [Google Scholar]
  19. Delmas CEL, Cheptou P-O, Escaravage N, Pornon A. 2014. High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub. BMC Evol. Biol. 14:243 [Google Scholar]
  20. Devaux C, Lepers C, Porcher E. 2014. Constraints imposed by pollinator behaviour on the ecology and evolution of plant mating systems. J. Evol. Biol. 27:1413–30 [Google Scholar]
  21. Diggle PK. 2003. Architectural effects on floral form and function: a review. Deep Morphology: Toward a Renaissance of Morphology in Plant Systematics T Stuessy, E Hörandl, V Mayer 63–80 Königtein, Ger.: Koeltz [Google Scholar]
  22. Dorken ME, Pannell JR. 2009. Hermaphroditic sex allocation evolves when mating opportunities change. Curr. Biol. 19:514–17 [Google Scholar]
  23. Dorken ME, Perry LE. 2017. Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection. J. Evol. Biol. 30:377–87 [Google Scholar]
  24. Dorken ME, Van Drunen WE. 2010. Sex allocation in clonal plants: Might clonal expansion enhance fitness gains through male function?. Evol. Ecol. 24:1463–74 [Google Scholar]
  25. Dubois S, Cheptou P-O, Petit C, Meerts P, Poncelet M. et al. 2003. Genetic structure and mating systems of metallicolous and nonmetallicolous populations of Thlaspi caerulescens. New Phytol. 157:633–41 [Google Scholar]
  26. Duminil J, Hardy OJ, Petit RJ. 2009. Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evol. Biol. 9:177 [Google Scholar]
  27. Eckert CG, Kalisz S, Geber MA, Sargent RD, Elle E. et al. 2010. Plant mating systems in a changing world. Trends Ecol. Evol. 25:35–43 [Google Scholar]
  28. Ehrlén J, Lehtilä K. 2002. How perennial are perennial plants. Oikos 98:308–22 [Google Scholar]
  29. Franklin-Tong VE. 2008. Self-Incompatibility in Flowering Plants: Evolution, Diversity, and Mechanisms Berlin: Springer-Verlag
  30. Friedman J, Barrett SCH. 2009. The consequences of monoecy and protogyny for mating in wind-pollinated Carex. New Phytol. 181:489–97 [Google Scholar]
  31. Garcia-Gonzalez F, Yasui Y, Evans JP. 2015. Mating portfolios: bet-hedging, sexual selection and female multiple mating. Proc. R. Soc. B 282:20141525 [Google Scholar]
  32. Gervasi DDL, Schiestl FP. 2017. Real-time divergent evolution in plants driven by pollinators. Nat. Commun. 8:14691 [Google Scholar]
  33. Ghazoul J. 2005. Pollen and seed dispersal among dispersed plants. Biol. Rev. 80:413–43 [Google Scholar]
  34. González-Varo JP, Albaladejo RG, Aparicio A. 2009. Mating patterns and spatial distribution of conspecific neighbours in the Mediterranean shrub Myrtus communis (Myrtaceae). Plant Ecol 203:207–15 [Google Scholar]
  35. 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 [Google Scholar]
  36. Goodwillie C, Sargent RD, Eckert CG, Elle E, Geber MA. et al. 2010. Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation. New Phytol 185:311–21 [Google Scholar]
  37. Grossenbacher D, Briscoe Runquist R, Goldberg EE, Brandvain Y. 2015. Geographic range size is predicted by plant mating system. Ecol. Lett. 18:706–13 [Google Scholar]
  38. Grossenbacher DL, Brandvain Y, Auld JR, Burd M, Cheptou P-O. et al. 2017. Self-compatibility is over-represented on islands. New Phytol 215:469–78 [Google Scholar]
  39. Harder LD, Aizen MA. 2010. Floral adaptation and diversification under pollen limitation. Philos. Trans. R. Soc. B 365:529–43 [Google Scholar]
  40. Harder LD, Aizen MA, Richards SA. 2016. The population ecology of male gametophytes: the link between pollination and seed production. Ecol. Lett. 19:497–509 [Google Scholar]
  41. Harder LD, Barrett SCH. 1995. Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–15 [Google Scholar]
  42. Harder LD, Barrett SCH, Cole WW. 2000. The mating consequences of sexual segregation within inflorescences of flowering plants. Proc. R. Soc. B 267:315–20 [Google Scholar]
  43. Harder LD, Johnson SD. 2005. Adaptive plasticity of floral display size in animal-pollinated plants. Proc. R. Soc. B 272:2651–57 [Google Scholar]
  44. Harder LD, Richards SA, Routley MB. 2008. Effects of reproductive compensation, gamete discounting and reproductive assurance on mating-system diversity in hermaphrodites. Evolution 62:157–72 [Google Scholar]
  45. Harder LD, Wilson WG. 1994. Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol. Ecol. 8:542–59 [Google Scholar]
  46. Harder LD, Wilson WG. 1998. A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. Am. Nat. 152:684–95 [Google Scholar]
  47. Hargreaves AL, Eckert CG. 2014. Evolution of dispersal and mating systems along geographic gradients: implications for shifting ranges. Funct. Ecol. 28:5–21 [Google Scholar]
  48. Hedhly A, Hormaza JI, Herrero M. 2005. Influence of genotype-temperature interaction on pollen performance. J. Evol. Biol. 18:1494–502 [Google Scholar]
  49. Herlihy CR, Eckert CG. 2002. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416:320–23 [Google Scholar]
  50. Herrera CM. 2009. Multiplicity in Unity: Plant Subindividual Variation and Interactions with Animals Chicago: Univ. Chicago Press437 pp.
  51. Hobbhahn N, Johnson SD, Harder LD. 2017. The mating consequences of rewarding versus deceptive pollination systems: Is there a quantity–quality trade-off. Ecol. Monogr. 87:91–104 [Google Scholar]
  52. Hove AA, Mazer SJ, Ivey CT. 2016. Seed set variation in wild Clarkia populations: teasing apart the effects of seasonal resource depletion, pollen quality, and pollen quantity. Ecol. Evol. 6:6524–36 [Google Scholar]
  53. Hu Y, Barrett SCH, Zhang D-Y, Liao W-J. 2015. Experimental analysis of mating patterns in a clonal plant reveals contrasting modes of self-pollination. Ecol. Evol. 5:5423–31 [Google Scholar]
  54. Husband BC. 2016. Effect of inbreeding on pollen tube growth in diploid and tetraploid Chamerion angustifolium: Do polyploids mask mutational load in pollen?. Am. J. Bot. 103:532–40 [Google Scholar]
  55. Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70 [Google Scholar]
  56. Ida TY, Harder LD, Kudo G. 2013. Demand-driven resource investment in annual seed production by a perennial angiosperm precludes resource limitation. Ecology 94:51–61 [Google Scholar]
  57. Igic B, Kohn JR. 2006. The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60:1098–103 [Google Scholar]
  58. Johnson MTJ, Campbell SA, Barrett SCH. 2015. Evolutionary interactions between plant reproduction and defense against herbivores. Annu. Rev. Ecol. Evol. Syst. 46:191–213 [Google Scholar]
  59. Johnston MO, Porcher E, Cheptou P-O, Eckert CG, Elle E. et al. 2009. Correlations among fertility components can maintain mixed mating in plants. Am. Nat. 173:1–11 [Google Scholar]
  60. Jordan CY, Otto SP. 2012. Functional pleiotropy and mating system evolution in plants: frequency-independent mating. Evolution 66:957–72 [Google Scholar]
  61. Kalisz S, Randle A, Chaiffetz D, Faigeles M, Butera A, Beight C. 2012. Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia. Ann. Bot. 109:571–82 [Google Scholar]
  62. Kalisz S, Vogler DW, Hanley KM. 2004. Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 403:884–87 [Google Scholar]
  63. Kameyama Y, Kudo G. 2015. Intrinsic and extrinsic factors acting on the reproductive process in alpine-snowbed plants: roles of phenology, biological interaction, and breeding system. Plant Spec. Biol. 30:3–15 [Google Scholar]
  64. Kamran-Disfani A, Agrawal AF. 2014. Selfing, adaptation and background selection in finite populations. J. Evol. Biol. 27:1360–71 [Google Scholar]
  65. Kirkpatrick M, Jarne P. 2000. The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155:154–67 [Google Scholar]
  66. Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M. et al. 2005. Pollen limitation of plant reproduction: pattern and process. Annu. Rev. Ecol. Evol. Syst. 36:467–97 [Google Scholar]
  67. Kohn JR, Barrett SCH. 1994. Pollen discounting and the spread of a selfing variant in tristylous Eichhornia paniculata: evidence from experimental populations. Evolution 48:1576–94 [Google Scholar]
  68. Korbecka G, Klinkhamer PGL, Vrieing K. 2002. Selective embryo abortion hypothesis revisited—a molecular approach. Plant Biol 4:298–310 [Google Scholar]
  69. Kuester A, Fall E, Chang S-M, Baucom RS. 2017. Shifts in outcrossing rates and changes to floral traits are associated with the evolution of herbicide resistance in the common morning glory. Ecol. Lett. 20:41–49 [Google Scholar]
  70. Kulbaba MW, Worley AC. 2012. Selection on floral design in Polemonium brandegeei (Polemoniaceae): female and male fitness under hawkmoth pollination. Evolution 66:1344–59 [Google Scholar]
  71. Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40 [Google Scholar]
  72. Lande R, Schemske DW, Schultz ST. 1994. High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutations. Evolution 48:965–78 [Google Scholar]
  73. Lankinen Å, Larsson MC. 2009. Conflicting selection pressures on reproductive functions and speciation in plants. Evol. Ecol. 23:147–57 [Google Scholar]
  74. Lankinen Å, Skogsmyr I. 2001. Evolution of pistil length as a choice mechanism for pollen quality. Oikos 92:81–90 [Google Scholar]
  75. Lankinen Å, Skogsmyr I. 2002. Pollen competitive ability: the effect of proportion in two-donor crosses. Evol. Ecol. Res. 4:687–700 [Google Scholar]
  76. Layman NC, Fernando MTR, Herlihy CR, Busch JW. 2017. Costs of selfing prevent the spread of a self‐compatibility mutation that causes reproductive assurance. Evolution 71:884–97 [Google Scholar]
  77. Leslie AB, Beaulieu JM, Crane PR, Donoghue MJ. 2013. Explaining the distribution of breeding and dispersal syndromes in conifers. Proc. R. Soc. B 280:20131812 [Google Scholar]
  78. Levin DA. 2011. Mating system shifts on the trailing edge. Ann. Bot. 109:613–20 [Google Scholar]
  79. Liao W-J, Harder LD. 2014. Consequences of multiple inflorescences and clonality for pollinator behavior and plant mating. Am. Nat. 184:580–92 [Google Scholar]
  80. Lloyd DG. 1980. Demographic factors and mating patterns in angiosperms. Demography and Evolution in Plant Populations OT Solbrig 67–88 Oxford, UK: Blackwell [Google Scholar]
  81. Lloyd DG. 1992. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153:370–80 [Google Scholar]
  82. Losdat S, Chang S-M, Reid JM. 2014. Inbreeding depression in male gametic performance. J. Evol. Biol. 27:992–1011 [Google Scholar]
  83. Maki M. 1993. Outcrossing and fecundity advantage of females in gynodioecious Chionographis japonica var. kurohimensis (Liliaceae). Am. J. Bot 80:629–34 [Google Scholar]
  84. Matsuo A, Tomimatsu H, Suzuki J-I, Saitoh T, Shibata S. et al. 2014. Female and male fitness consequences of clonal growth in a dwarf bamboo population with a high degree of clonal intermingling. Ann. Bot. 114:1035–41 [Google Scholar]
  85. Medrano M, Requerey R, Karron JD, Herrera CM. 2012. Herkogamy and mate diversity in the wild daffodil Narcissus longispathus: beyond the selfing–outcrossing paradigm in the evolution of mixed mating. Plant Biol 14:801–10 [Google Scholar]
  86. Mitchell RJ, Wilson WG, Holmquist KG, Karron JD. 2013. Influence of pollen transport dynamics on sire profiles and multiple paternity in flowering plants. PLOS ONE 8:e76312 [Google Scholar]
  87. Moeller DA, Briscoe Runquist RD, Moe AM, Geber MA, Goodwillie C. et al. 2017. Global biogeography of mating system variation in seed plants. Ecol. Lett. 20:375–84 [Google Scholar]
  88. Moeller DA, Geber MA, Eckhart VM, Tiffin P. 2012. Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93:1036–48 [Google Scholar]
  89. Morgan MT. 2001. Consequences of life history for inbreeding depression and mating system evolution in plants. Proc. R. Soc. B 268:1817–24 [Google Scholar]
  90. Morgan MT, Schoen DJ, Bataillon TM. 1997. The evolution of self-fertilization in perennials. Am. Nat. 150:618–38 [Google Scholar]
  91. Morgan MT, Wilson WG. 2005. Self-fertilization and the escape from pollen limitation in variable pollination environments. Evolution 59:1143–48 [Google Scholar]
  92. Munoz F, Violle C, Cheptou P-O. 2016. CSR ecological strategies and plant mating systems: Outcrossing increases with competitiveness but stress-tolerance is related to mixed mating. Oikos 125:1296–303 [Google Scholar]
  93. Nora S, Aparicio A, Albaladejo RG. 2016. High correlated paternity leads to negative effects on progeny performance in two Mediterranean shrub species. PLOS ONE 11:e0166023 [Google Scholar]
  94. Oakley CG, Moriuchi KS, Winn AA. 2007. The maintenance of outcrossing in predominantly selfing species: ideas and evidence from cleistogamous species. Annu. Rev. Ecol. Evol. Syst. 38:437–57 [Google Scholar]
  95. Otto SP, Orive ME. 1995. Evolutionary consequences of mutation and selection within an individual. Genetics 141:1173–87 [Google Scholar]
  96. Pannell JR. 2015. Evolution of the mating system in colonizing plants. Mol. Ecol. 24:2018–37 [Google Scholar]
  97. Pannell JR, Barrett SCH. 1998. Baker's Law revisited: reproductive assurance in a metapopulation. Evolution 52:657–68 [Google Scholar]
  98. Pannell JR, Labouche A-M. 2013. The incidence and selection of multiple mating in plants. Philos. Trans. R. Soc. B 368:20120051 [Google Scholar]
  99. Peterson ML, Kay KM. 2015. Mating system plasticity promotes persistence and adaptation of colonizing populations of hermaphroditic angiosperms. Am. Nat. 185:28–43 [Google Scholar]
  100. Pujol B, Zhou S-R, Sanchez Vilas J, Pannell JR. 2009. Reduced inbreeding depression after species range expansion. PNAS 106:15379–83 [Google Scholar]
  101. Rhodes MK, Fant JB, Skogen KA. 2017. Pollinator identity and spatial isolation influence multiple paternity in an annual plant. Mol. Ecol. 26:4296–308 [Google Scholar]
  102. Richards SA, Williams NM, Harder LD. 2009. Variation in pollination: causes and consequences for plant reproduction. Am. Nat. 174:382–98 [Google Scholar]
  103. Rigney LP. 1995. Postfertilization causes of differential success of pollen donors in Erythronium grandiflorum (Liliaceae): nonrandom ovule abortion. Am. J. Bot. 82:578–84 [Google Scholar]
  104. Ritland K. 1989. Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848–59 [Google Scholar]
  105. Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M. et al. 2014. A quantitative review of pollination syndromes: Do floral traits predict effective pollinators?. Ecol. Lett. 17:388–400 [Google Scholar]
  106. Ruane LG. 2009. Post-pollination processes and non-random mating among compatible mates. Evol. Ecol. Res. 11:1031–51 [Google Scholar]
  107. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K. 2009. Is there a latitudinal gradient in the importance of biotic interactions?. Annu. Rev. Ecol. Evol. Syst. 40:245–69 [Google Scholar]
  108. Schreiber SJ, Rosenheim JA, Williams NW, Harder LD. 2015. Evolutionary and ecological consequences of multiscale variation in pollen receipt for seed production. Am. Nat. 185:E14–29 [Google Scholar]
  109. Scofield DG, Schultz ST. 2006. Mitosis, stature and evolution of plant mating systems: low-Φ and high-Φ plants. Proc. R. Soc. B 273:275–82 [Google Scholar]
  110. Simons AM. 2011. Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proc. R. Soc. B 278:1601–9 [Google Scholar]
  111. Simpson EH. 1949. Measurement of diversity. Nature 163:688 [Google Scholar]
  112. Stehlik I, Friedman J, Barrett SCH. 2008. Environmental influence on primary sex ratio in a dioecious plant. PNAS 105:10847–52 [Google Scholar]
  113. Swanson RJ, Hammond AT, Carlson AL, Gong H, Donovan TK. 2016. Pollen performance traits reveal prezygotic nonrandom mating and interference competition in Arabidopsis thaliana. Am. J. Bot. 103:498–513 [Google Scholar]
  114. Takebayashi N, Delph LF. 2000. An association between a floral trait and inbreeding depression. Evolution 54:840–46 [Google Scholar]
  115. Takebayashi N, Wolf DE, Delph LF. 2006. Effect of variation in herkogamy on outcrossing within a population of Gilia achilleifolia. Heredity 96:159–65 [Google Scholar]
  116. Uyenoyama MK, Waller DM. 1991. Coevolution of self-fertilization and inbreeding depression I. Mutation-selection balance at one and two loci. Theor. Popul. Biol. 40:14–46 [Google Scholar]
  117. Vallejo-Marín M, Dorken ME, Barrett SCH. 2010. The ecological and evolutionary consequences of clonality for plant mating. Annu. Rev. Ecol. Evol. Syst. 41:193–213 [Google Scholar]
  118. Vamosi JC, Knight TM, Steets JA, Mazer SJ, Burd M, Ashman T. 2006. Pollination decays in biodiversity hotspots. PNAS 103:956–61 [Google Scholar]
  119. Van Drunen WE, Dorken ME. 2014. Wind pollination, clonality, and the evolutionary maintenance of spatial segregation of the sexes. Evol. Ecol. 28:1121–38 [Google Scholar]
  120. Vaughton G, Ramsey M. 2010. Pollinator-mediated selfing erodes the flexibility of the best-of-both-worlds mating strategy in Bulbine vagans. Funct. Ecol. 24:374–82 [Google Scholar]
  121. Vekemans X, Hardy OJ. 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 13:921–35 [Google Scholar]
  122. Vranken S, Brys R, Hoffmann M, Jacquemyn H. 2014. Secondary pollen presentation and the temporal dynamics of stylar hair retraction and style elongation in Campanula trachelium (Campanulaceae). Plant Biol 16:669–76 [Google Scholar]
  123. Wang J, El-Kassaby YA, Ritland K. 2012. Estimating selfing rates from reconstructed pedigrees using multilocus genotype data. Mol. Ecol. 21:100–16 [Google Scholar]
  124. Williams JH. 2012. Pollen tube growth rates and the diversification of flowering plant reproductive cycles. Int. J. Plant Sci. 173:649–61 [Google Scholar]
  125. Wilson WG, Harder LD. 2003. Reproductive uncertainty and the relative competitiveness of simultaneous hermaphroditism versus dioecy. Am. Nat. 162:220–41 [Google Scholar]
  126. Wright SI, Kalisz S, Slotte T. 2013. Evolutionary consequences of self-fertilization in plants. Proc. R. Soc. B 280:20130133 [Google Scholar]
  127. Yin G, Barrett SCH, Luo Y-B, Bai W-N. 2016. Seasonal variation in the mating system of a selfing annual with large floral displays. Ann. Bot. 117:391–400 [Google Scholar]
  128. Young AG, Brown AHD. 1999. Paternal bottlenecks in fragmented populations of the grassland daisy Rutidosis leptorrhynchoides. Genet. Res. 73:111–17 [Google Scholar]
  129. Zhang D-Y. 2006. Evolutionarily stable reproductive investment and sex allocation in plants. Ecology and Evolution of Flowers LD Harder, SCH Barrett 41–60 Oxford, UK: Oxford Univ. Press [Google Scholar]
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