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Evolution of sex

The evolution of plant sexual diversity

Nature Reviews Genetics volume 3, pages 274–284 (2002)Cite this article

Key Points

  • Flowers, the reproductive organs of angiosperms, are more varied than the equivalent structures of any other group of organisms, and flowering plants also have an unrivalled diversity of sexual systems. This variation provides outstanding opportunities for evolutionary and functional studies of the costs and benefits of alternative sexual strategies.

  • The two main evolutionary transitions in sexual systems of flowering plants involve the shift from predominant outcrossing to predominant selfing, and the evolution of separate sexes from combined sexes. Comparative studies indicate that these transitions have originated independently on numerous occasions in angiosperm families.

  • Many floral mechanisms that have been traditionally interpreted as 'anti-selfing mechanisms' might have an alternative role in promoting fitness through male reproductive function by limiting gamete losses through pollen discounting. This is particularly likely in self-incompatible plants because they are already protected from the harmful effects of inbreeding by physiological mechanisms.

  • Sexual polymorphisms, such as heterostyly and enantiostyly, that are characterized by reciprocal herkogamy, function to increase the precision of animal-mediated cross-pollination, while reducing the costs that are associated with sexual interference between female and male sexual organs. The principal cost is pollen wastage through self-pollination.

  • The two main evolutionary routes for the origin of dioecy — the gynodioecy and monoecy pathways — differ in the types of gender variation on which selection acts, and in the relative importance of major versus minor genes that govern changes to sexuality. The fitness consequences of selfing and outcrossing, and the optimal allocation of resources to female and male function, are key factors that promote transitions to dioecy and other forms of gender dimorphism.

  • Flowering plants have a wide range of mating patterns, from obligate outcrossing to predominant selfing. Selfing is commonly associated with the annual life form, and uncertain pollination conditions implicate reproductive assurance as the principal mechanism that drives the evolution of autonomous modes of selfing in plants.

  • Future work on plant sexual systems should abandon the myopic view of flowers as the sole reproductive unit and begin investigations into the functional interrelations between flowers, inflorescences and plant architecture, within the broader context of life-history evolution.

Abstract

Charles Darwin recognized that flowering plants have an unrivalled diversity of sexual systems. Determining the ecological and genetic factors that govern sexual diversification in plants is today a central problem in evolutionary biology. The integration of phylogenetic, ecological and population-genetic studies have provided new insights into the selective mechanisms that are responsible for major evolutionary transitions between reproductive modes.

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Figure 1: Floral design and pollen transfer in animal-pollinated plants.
Figure 2: The forms of enantiostyly in flowering plants.
Figure 3: Flexistyly in Alpinia (Zingiberaceae).
Figure 4: Intraspecific variation as a tool for studying the evolution and maintenance of monoecy and dioecy.
Figure 5: Multiple origins of predominant self-fertilization in flowering plants.
Figure 6: The difference in the distribution of outcrossing rates in animal-pollinated and wind-pollinated plant species.

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References

  1. Charlesworth, D. in Gender and Sexual Dimorphism in Flowering Plants (eds Geber, M. A., Dawson, T. E. & Delph, L. F.) 33–60 (Springer, Berlin, 1999).

    Book  Google Scholar 

  2. Uyenoyama, M. K. A prospectus for new developments in the evolutionary theory of self-incompatibility. Ann. Bot. 85, 247–252 (2000).

    Article  CAS  Google Scholar 

  3. Pannell, J. R. & Barrett, S. C. H. Effects of drift, selection and population turnover on a mating-system polymorphism. Theor. Popul. Biol. 59, 145–155 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Barrett, S. C. H., Harder, L. D. & Worley, A. C. The comparative biology of pollination and mating in flowering plants. Phil. Trans. R. Soc. Lond. B 351, 1271–1280 (1996).This paper uses comparative and phylogenetic analyses to show significant associations between mating systems and life history in plants.

    Article  Google Scholar 

  5. Weller, S. G. & Sakai, A. K. Using phylogenetic approaches for the analysis of plant breeding system evolution. Annu. Rev. Ecol. Syst. 30, 167–199 (1999).

    Article  Google Scholar 

  6. Weiblen, G. D., Oyama, R. K. & Donoghue, M. J. Phylogenetic analysis of dioecy in monocotyledons. Am. Nat. 155, 46–58 (2000).

    Article  PubMed  Google Scholar 

  7. Cresswell, J. E. Manipulation of female architecture in flowers reveals a narrow optimum for pollen deposition. Ecology 81, 3244–3249 (2000).

    Article  Google Scholar 

  8. Walker-Larson, J. & Harder, L. D. Vestigial organs as opportunities for functional innovation: the example of the Penstemon staminode. Evolution 55, 477–487 (2001).

    Article  Google Scholar 

  9. Fetscher, A. E. Resolution of male–female conflict in a hermaphrodite flower. Proc. R. Soc. Lond. B 268, 525–529 (2001).The first experimental demonstration that a floral trait can function to reduce female interference with pollen dispersal in a hermaphrodite plant.

    Article  CAS  Google Scholar 

  10. Lloyd, D. G. & Barrett, S. C. H. (eds) Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (Chapman & Hall, New York, 1996).

    Book  Google Scholar 

  11. Charlesworth, D. & Charlesworth, B. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237–268 (1987).The classic review of the significance of inbreeding depression for the evolution of mating systems.

    Article  Google Scholar 

  12. Lloyd, D. G. Parental strategies of angiosperms. NZ J. Bot. 17, 595–606 (1979).

    Article  Google Scholar 

  13. Lloyd, D. G & Schoen, D. J. Self- and cross-fertilization in plants. I. Functional dimensions. Int. J. Plant Sci. 153, 358–369 (1992).

    Article  Google Scholar 

  14. Geber, M. A., Dawson, T. E. & Delph, L. F. (eds) Gender and Sexual Dimorphism in Flowering Plants (Springer, Berlin, 1999).

    Book  Google Scholar 

  15. Harder, L. D. & Barrett, S. C. H. in Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (eds Lloyd, D. G. & Barrett, S. C. H.) 140–190 (Chapman & Hall, New York, 1996).

    Book  Google Scholar 

  16. Barrett, S. C. H., Jesson, L. K. & Baker, A. M. The evolution and function of stylar polymorphisms in flowering plants. Ann. Bot. 85, 253–265 (2000).The first attempt to provide a unified explanation for the adaptive significance of the four main stylar polymorphisms in plants.

    Article  Google Scholar 

  17. Barrett, S. C. H., Cole, W. W., Arroyo, J., Cruzan, M. B. & Lloyd, D. G. Sexual polymorphisms in Narcissus triandrus (Amaryllidaceae): is this species tristylous? Heredity 78, 135–145 (1997).

    Article  Google Scholar 

  18. Barrett, S. C. H., Wilken, D. H. & Cole, W. W. Heterostyly in the Lamiaceae: the case of Salvia brandegeei. Plant Syst. Evol. 223, 211–219 (2000).

    Article  Google Scholar 

  19. Lewis, D. & Jones, D. A. in Evolution and Function of Heterostyly (ed. Barrett, S. C. H.) 129–150 (Springer, Berlin, 1992).

    Book  Google Scholar 

  20. McCubbin, A. G. & Kao, T. Molecular recognition and response in pollen and pistil interactions. Annu. Rev. Cell. Dev. Biol. 16, 333–364 (2000).

    Article  CAS  PubMed  Google Scholar 

  21. Jesson, L. K. The Evolution and Functional Significance of Enantiostyly in Flowering Plants. Ph.D. Thesis, University of Toronto (2002).

    Google Scholar 

  22. Luo, D., Carpenter, C., Vincent, L., Copsey, L. & Coen, E. Origin of floral asymmetry in Antirrhinum. Nature 383, 794–799 (1996).

    Article  CAS  PubMed  Google Scholar 

  23. Jesson, L. K. & Barrett, S. C. H. Enantiostyly in Wachendorfia (Haemodoraceae): the influence of reproductive systems on the maintenance of the polymorphism. Am. J. Bot. 89, 253–262 (2002).

    Article  PubMed  Google Scholar 

  24. Li, Q.-J. et al. Flexible style that encourages outcrossing. Nature 410, 432 (2001).

    Article  CAS  PubMed  Google Scholar 

  25. Li, Q.-J. et al. Study on the flexistyly pollination mechanism in Alpinia plants (Zingiberaceae). Acta Bot. Sin. 43, 364–369 (2001).

    Google Scholar 

  26. Renner, S. S. How common is heterodichogamy? Trends Ecol. Evol. 16, 595–597 (2001).

    Article  Google Scholar 

  27. Gleeson, S. K. Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36, 892–902 (1982).

    Article  PubMed  Google Scholar 

  28. Thompson, T. E. & Romberg, L. D. Inheritance of heterodichogamy in pecan. J. Hered. 76, 456–458 (1985).

    Article  Google Scholar 

  29. Lloyd, D. G. Sexual strategies in plants. III. A quantitative method for describing the gender of plants. NZ J. Bot. 18, 103–108 (1980).

    Article  Google Scholar 

  30. Delph, L. F. Sex-ratio variation in the gynodioecious shrub Hebe strictissima (Scrophulariaceae). Evolution 44, 134–142 (1990).

    Article  PubMed  Google Scholar 

  31. Liston, A., Rieseberg, L. H. & Elias, T. S. Functional androdioecy in the flowering plant Datisca glomerata. Nature 343, 641–642 (1992).

    Article  Google Scholar 

  32. El-Keblawy, A., Lovett Doust, J. & Lovett Doust, L. Gender variation and the evolution of dioecy in Thymelaea hirsuta (Thymelaeaceae). Can. J. Bot. 74, 1596–1601 (1996).

    Article  Google Scholar 

  33. Pailler, T., Humeau, L., Figier, J. & Thompson, J. D. Reproductive trait variation in the functionally dioecious and morphologically heterostylous island endemic Chassalia corallioides (Rubiaceae). Biol. J. Linn. Soc. 64, 297–313 (1998).

    Google Scholar 

  34. Lebel-Hardenack, S. & Grant, S. R. Genetics of sex determination in flowering plants. Trends Plant Sci. 2, 130–139 (1997).

    Article  Google Scholar 

  35. Wolfe, D. E., Satkoski, J. A., White, K. & Rieseberg, L. H. Sex determination in the androdioecious plant Datisca glomerata, and its dioecious sister species, D. cannabina. Genetics 159, 1243–1257 (2001).

    Article  Google Scholar 

  36. Parker, J. S. Sex chromosomes and sexual differentiation in flowering plants. Chromosomes Today 10, 187–198 (1990).

    CAS  Google Scholar 

  37. Louis, J. P., Augur, C. & Teller, G. Cytokinins and differentiation process in Mercurialis annua. Plant Physiol. 94, 1535–1541 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Yin, T. & Quinn, J. A. Tests of a mechanistic model of one hormone regulating both sexes in Cucumis sativus (Cucurbitaceae). Am. J. Bot. 82, 1537–1546 (1995).

    Article  CAS  Google Scholar 

  39. Maurice, S., Belhassen, E., Couvet, D. & Gouyon, P.-H. Evolution of dioecy: can nuclear cytoplasmic interactions select for maleness? Heredity 73, 346–354 (1994).

    Article  PubMed  Google Scholar 

  40. Schultz, S. Nucleo-cytoplasmic male sterility and alternative routes to dioecy. Evolution 48, 1933–1945 (1994).

    Article  PubMed  Google Scholar 

  41. Pannell, J. R. The maintenance of gynodioecy and androdioecy in a metapopulation. Evolution 51, 10–20 (1997).The first use of metapopulation theory to inform understanding of the evolution and maintenance of plant sexual systems.

    Article  PubMed  Google Scholar 

  42. Barrett, S. C. H. Gender variation in Wurmbea (Liliaceae) and the evolution of dioecy. J. Evol. Biol. 5, 423–444 (1992).

    Article  Google Scholar 

  43. Wolfe, L. M. & Shmida, A. The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology 78, 101–110 (1997).

    Article  Google Scholar 

  44. Delph, L. F. & Carroll, S. B. Factors affecting the relative seed fitness and female frequency in a gynodioecious species, Silene acaulis. Evol. Ecol. Res. 3, 487–505 (2001).

    Google Scholar 

  45. de Jong, T. J. From pollen dynamics to adaptive dynamics. Plant Species Biol. 15, 31–41 (2000).

    Article  Google Scholar 

  46. Sarkissian, T. S., Barrett, S. C. H. & Harder, L. D. Gender variation in Sagittaria latifolia (Alismataceae): is size all that matters? Ecology 82, 360–373 (2001).

    Article  Google Scholar 

  47. Renner, S. S. & Ricklefs, R. E. Dioecy and its correlates. Am. J. Bot. 82, 596–606 (1995).

    Article  Google Scholar 

  48. Renner, S. S. & Won, H. Repeated evolution of monoecy in Siparunaceae (Laurales). Syst. Biol. 50, 700–712 (2001).

    Article  CAS  PubMed  Google Scholar 

  49. Kohn, J. R. & Biardi, J. E. Outcrossing rates and inferred levels of inbreeding depression in gynodioecious Cucurbita foetidissima (Cucurbitaceae). Heredity 75, 77–83 (1995).

    Article  Google Scholar 

  50. Schultz, S. T. & Ganders, F. R. Evolution of unisexuality in the Hawaiian flora: a test of microevolutionary theory. Evolution 50, 842–855 (1996).

    Article  PubMed  Google Scholar 

  51. Sakai, A. K., Weller, S. G., Chen, M.-L., Chou, S.-Y. & Tasanont, C. Evolution of gynodioecy and maintenance of females: the role of inbreeding depression, outcrossing rates and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution 51, 724–736 (1997).

    Article  PubMed  Google Scholar 

  52. Seger, J. & Eckhart, V. M. Evolution of sexual systems and sex allocation in plant species when growth and reproduction overlap. Proc. R. Soc. Lond. B 263, 833–841 (1996).

    Article  Google Scholar 

  53. Schultz, S. T. Can females benefit from selfing avoidance? Genetic associations and the evolution of plant gender. Proc. R. Soc. Lond. B 266 1967–1973 (1999).

    Article  Google Scholar 

  54. Takebayashi, N. & Delph, L. F. An association between a floral trait and inbreeding depression. Evolution 54, 840–846 (2000).The first empirical evidence for a genetic association between a sexual trait that influences mating and loci that determine fitness.

    Article  CAS  PubMed  Google Scholar 

  55. Chawla, B., Bernatzky, R., Liang, W. & Marcotrigiano, M. Breakdown of self-incompatibility in tetraploid Lycopersicon peruvianum: inheritance and expression of S-related proteins. Theor. Appl. Genet. 95, 992–996 (1997).

    Article  CAS  Google Scholar 

  56. Miller, J. S. & Venable, D. L. Polyploidy and the evolution of gender dimorphism. Science 289, 2335–2338 (2000).

    Article  CAS  PubMed  Google Scholar 

  57. Willis, J. H. Effects of different levels of inbreeding on fitness components in Mimulus guttatus. Evolution 47, 864–876 (1993).

    Article  PubMed  Google Scholar 

  58. Carr, D. E. & Dudash, M. R. The effects of five generations of enforced selfing on potential male and female function. Evolution 51, 1797–1807 (1997).

    Article  PubMed  Google Scholar 

  59. Eckert, C. G. Contributions of autogamy and geitonogamy to self-fertilization in a mass flowering, clonal plant. Ecology 81, 532–542 (2000).

    Article  Google Scholar 

  60. Reusch, T. B. H. Fitness-consequences of geitonogamous selfing in a clonal marine angiosperm (Zostera marina). J. Evol. Biol. 14, 129–138 (2001).A pioneering study that uses microsatellites to estimate mating patterns and provides evidence that clonal reproduction promotes geitonogamous selfing.

    Article  CAS  PubMed  Google Scholar 

  61. Harder, L. D. & Wilson, W. G. A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. Am. Nat. 152, 684–695 (1998).

    Article  CAS  PubMed  Google Scholar 

  62. Harder, L. D. & Barrett, S. C. H. Mating cost of large floral displays in hermaphrodite plants. Nature 373, 512–515 (1995).The first experimental evidence that large floral displays can exert a male mating cost as a result of geitonogamous pollen discounting, with important implications for floral evolution.

    Article  CAS  Google Scholar 

  63. Harder, L. D., Barrett, S. C. H. & Cole, W. W. The mating consequences of sexual segregation within inflorescences of flowering plants. Proc. R. Soc. Lond. B 267, 315–320 (2000).

    Article  CAS  Google Scholar 

  64. Dorken, M. E., Friedman, J. E. & Barrett, S. C. H. The evolution and maintenance of monoecy and dioecy in Sagittaria latifolia. Evolution 56, 31–41 (2002).

    Article  PubMed  Google Scholar 

  65. Heilbuth, J. Lower species richness in dioecious clades. Am. Nat. 156, 221–241 (2000).By using sister-group comparisons, this study provides the first evidence in plants of differences in species richness between clades with contrasting sexual systems.

    Article  PubMed  Google Scholar 

  66. Heilbuth, J., Ilves, K. L. & Otto, S. P. The consequences of dioecy for seed dispersal: modeling the seed-shadow handicap. Evolution 55, 880–888 (2001).

    Article  CAS  PubMed  Google Scholar 

  67. Johnson, S. D., Linder, H. P. & Steiner, K. E. Phylogeny and radiation of pollination systems in Disa (Orchidaceae). Am. J. Bot. 85, 402–411 (1998).

    Article  CAS  PubMed  Google Scholar 

  68. Hodges, S. A. & Arnold, M. L. Spurring plant diversification: are floral nectar spurs a key innovation? Proc. R. Soc. Lond. B 262, 343–348 (1995).

    Article  Google Scholar 

  69. Kohn, J. R., Graham, S. W., Morton, B., Doyle, J. J. & Barrett, S. C. H. Reconstruction of the evolution of reproductive characters in Pontederiaceae using phylogenetic evidence from chloroplast DNA restriction-site variation. Evolution 50, 1454–1469 (1996).

    PubMed  Google Scholar 

  70. Schoen, D. J., Johnston, M. O., L'Heureux, A. & Marsolais, J. V. Evolutionary history of the mating system in Amsinckia (Boraginaceae). Evolution 51, 1090–1099 (1997).

    Article  PubMed  Google Scholar 

  71. Goodwillie, C. Multiple origins of self-compatibility in Linanthus section Leptosiphon (Polemoniaceae): phylogenetic evidence from internal-transcribed-spacer sequence data. Evolution 53, 1387–1395 (1999).References 69–71 use molecular data to reconstruct the phylogenetic histories of outcrossing and selfing in different taxa of flowering plants — all three studies show multiple origins of selfing from outcrossing.

    PubMed  Google Scholar 

  72. Charlesworth, D. & Charlesworth, B. Quantitative genetics in plants: the effects of breeding systems on genetic variability. Evolution 49, 911–920 (1995).

    Article  CAS  PubMed  Google Scholar 

  73. Hamrick, J. L. & Godt, M. J. W. Effects of life history traits on genetic diversity in plant species. Phil. Trans. R. Soc. Lond. B 351, 1291–1298 (1996).

    Article  Google Scholar 

  74. Liu, F., Charlesworth, D. & Kreitman, M. The effect of mating system differences on nucleotide diversity at the phosphoglucose isomerase locus in the plant genus Leavenworthia. Genetics 151, 343–357 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Savolainen, O., Langley, C. H., Lazzaro, B. P. & Freville, H. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol. Biol. Evol. 17, 645–655 (2000).

    Article  CAS  PubMed  Google Scholar 

  76. Takebayashi, N. & Morrell, P. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am. J. Bot. 88, 1143–1150 (2001).

    Article  CAS  PubMed  Google Scholar 

  77. Pannell, J. R. & Barrett, S. C. H. Baker's law revisited: reproductive assurance in a metapopulation. Evolution 53, 664–676 (1998).

    Article  Google Scholar 

  78. Lande, R. & Schemske, D. W. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39, 24–40 (1985).This paper, and reference 11 , stimulated a large amount of theoretical and empirical work on the joint evolution of inbreeding depression and mating systems in plants.

    PubMed  Google Scholar 

  79. Uyenoyama, M. K., Holsinger, K. E. & Waller, D. M. Ecological and genetic factors directing the evolution of self-fertilization. Oxf. Surv. Evol. Biol. 9, 327–381 (1993).

    Google Scholar 

  80. Vogler, D. W. & Kalisz, S. Sex among the flowers: the distribution of plant mating systems. Evolution 55, 202–204 (2001).

    Article  CAS  PubMed  Google Scholar 

  81. Barrett, S. C. H. & Husband, B. C. Variation in outcrossing rates in Eichhornia paniculata: the role of demographic and reproductive factors. Plant Species Biol. 5, 41–56 (1990).

    Article  Google Scholar 

  82. Dole, J. & Ritland, K. Inbreeding depression in two Mimulus taxa measured by multigenerational changes in the inbreeding coefficient. Evolution 47, 361–373 (1993).The first application of genetic markers to infer levels of inbreeding depression in the field.

    Article  PubMed  Google Scholar 

  83. Eckert, C. G. & Barrett, S. C. H. Inbreeding depression in partially self-fertilizing Decodon verticillatus (Lythraceae): population genetic and experimental analyses. Evolution 48, 952–964 (1994).

    Article  PubMed  Google Scholar 

  84. Husband, B. C. & Schemske, D. W. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50, 54–70 (1996).

    Article  PubMed  Google Scholar 

  85. Sage, T. L., Strumas, F., Cole, W. W. & Barrett, S. C. H. Differential ovule development following self- and cross-fertilization: the basis of self-sterility in Narcissus triandrus (Amaryllidaceae). Am. J. Bot. 86, 855–870 (1999).The discovery of a unique form of self-incompatibility in plants that operates through differential ovule development after cross-pollination as opposed to self-pollination.

    Article  CAS  PubMed  Google Scholar 

  86. Barrett, S. C. H. Sexual interference of the floral kind. Heredity 88, 154–159 (2002).

    Article  CAS  PubMed  Google Scholar 

  87. Fishman, L. & Wyatt, R. Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53, 1723–1733 (1999).

    PubMed  Google Scholar 

  88. Schoen, D. J., Morgan, M. T. & Batallion, T. How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Phil. Trans. R. Soc. Lond. B 351, 1281–1290 (1996).

    Article  Google Scholar 

  89. Herlihy, C. R. & Eckert, C. G. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 415 (in the press).The first experimental evidence for seed discounting in plants.

  90. Lloyd, D. G. Self and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153, 370–382 (1992).

    Article  Google Scholar 

  91. Reusch, T. B. H. Pollination in the marine realm: microsatellites reveal high outcrossing rates and multiple paternity in eelgrass Zostera marina. Heredity 85, 459–464 (2000).

    Article  PubMed  Google Scholar 

  92. Pagel, M. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48, 612–622 (1999).

    Article  Google Scholar 

  93. Templeton, A. R. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol. Ecol. 7, 381–398 (1998).

    Article  CAS  PubMed  Google Scholar 

  94. Charlesworth, D. & Pannell, J. R. in Integrating Ecology and Evolution in a Spatial Context (eds Silvertown, J. & Antonovics, J.) 73–95 (Blackwell Science, Oxford, 2001).

    Google Scholar 

  95. Bradshaw, H. D. Jr, Otto, K. G., Frewen, B. E., McKay, J. K. & Schemske, D. W. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflowers (Mimulus). Genetics 149, 367–382 (1998).A more detailed sequel to the authors' 1995 Nature paper, this publication confirms that a small number of genes of large effect contribute towards reproductive isolation between two species of monkeyflower serviced by different pollinators.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Fishbein, M. & Venable, D. L. Evolution of inflorescence design: theory and data. Evolution 50, 2165–2177 (1996).

    Article  PubMed  Google Scholar 

  97. Worley, A. C. & Barrett, S. C. H. Evolution of floral display in Eichhornia paniculata (Pontederiaceae): direct and correlated response to selection on flower size and number. Evolution 54, 1533–1545 (2000).

    Article  CAS  PubMed  Google Scholar 

  98. Venable, D. L. Packaging and provisioning in plant reproduction. Phil. Trans. R. Soc. Lond. B 351, 1319–1329 (1996).

    Article  Google Scholar 

  99. Pannell, J. P. Mixed genetic and environmental sex determination in an androdioecious population of Mercurialis annua. Heredity 78, 50–56 (1997).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I thank W. Cole for assistance with figures; M. Dorken, C. Eckert, J. Heilbuth, L. Jesson and J. Willis for valuable discussion; and the Natural Sciences and Engineering Research Council of Canada for financial support.

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  1. Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, M5S 3B2, Ontario, Canada

    Spencer C. H. Barrett

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Glossary

SEXUAL POLYMORPHISM

The co-occurrence within a single interbreeding population of morphologically distinct mating groups that are distinguished by differences in their sexual organs.

DICHOGAMY

Differences in the timing of pollen dispersal from anthers and stigma receptivity of flowers. In protandry, pollen is dispersed before stigmas are receptive, and in protogyny, stigmas are receptive before pollen is dispersed from anthers.

INBREEDING DEPRESSION

The reduction in viability and fertility of inbred offspring compared with outbred offspring.

SUPERGENE CONTROL

A cluster of tightly linked co-adapted genes that are inherited as a single unit and carry out related functions.

ENANTIOSTYLY

Mirror-image flowers in which the style bends either to the left side or the right side of the floral axis. The phenomenon can exist as a sexual polymorphism with left-styled and right-styled plants.

MONOCOTYLEDON

(Monocot). One of the two classes of flowering plants, monocots are characterized by one embryonic leaf (cotyledon). Maize, rice and other grasses are common monocots.

RECIPROCAL HERKOGAMY

Sexual polymorphisms in which floral morphs differ reciprocally in the locations of female and male sex organs within flowers (for example, heterostyly and enantiostyly).

FLEXISTYLY

A sexual polymorphism in which populations contain two floral morphs that differ in the temporal patterns of style growth and orientation.

DIOECY

A sexual polymorphism in which populations contain female and male plants.

DISRUPTIVE SELECTION

Natural selection against the mean value of a quantitative trait, therefore favouring individuals at the two tails of the phenotypic distribution.

LIFE-HISTORY TRADE-OFF

When allocation of resources to one life-history trait reduces investment in another trait.

POLLEN DISCOUNTING

The loss of outcrossed siring success as a result of self-pollination.

ALLOZYME LOCI

Loci that code for different electrophoretic forms of the same enzyme as a result of allelic differences.

SEED DISCOUNTING

The formation of self-fertilized seeds from ovules that, if they had not been self-fertilized, would have been cross-fertilized.

COALESCENT ANALYSIS

A means of investigating the shared genealogical history of genes. A genealogy is constructed backwards in time starting with the present-day sample. Lineages coalesce when they have a common ancestor.

QUANTITATIVE TRAIT LOCI

(QTL). Loci that control quantitative traits identified by showing a statistical association between genetic markers and phenotypes that can be measured.

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Barrett, S. The evolution of plant sexual diversity. Nat Rev Genet 3, 274–284 (2002). https://doi.org/10.1038/nrg776

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