The evolution of gender specialization from dimorphic hermaphroditism: Paths from heterodichogamy to gynodioecy and androdioecy

Evolution

Volumn 60, Issue 4, 2006, Pages 660-673

  Pannell, John R ^a   Verdú, Miguel ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CDIS UV Generalitat Valenciana)   (Spain)

Author keywords

Dioecy; Distyly; Functional gender; Protandry; Protogyny; Sex allocation

Indexed keywords

ANDRODIOECY; EVOLUTIONARY BIOLOGY; GENDER; GYNODIOECY; MUTATION; PROTANDRY; PROTOGYNY; SEX ALLOCATION; SEXUAL DIMORPHISM; SPECIALIZATION; STERILITY;

ARTICLE; BIOLOGICAL MODEL; FLOWER; GENDER AND SEX; GENE; MOLECULAR EVOLUTION; MUTATION; PLANT PHYSIOLOGY; PLANT SEED; SEX DIFFERENCE;

EVOLUTION, MOLECULAR; FLOWERS; GENES, PLANT; MODELS, GENETIC; MUTATION; PLANT PHYSIOLOGY; SEEDS; SEX DETERMINATION (GENETICS); SEX FACTORS;

EID: 33745275858     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1554/05-481.1     Document Type: Article

References (71)

1. Ashman, T.-L., and I. Baker. 1992. Variation in floral sex allocation with time of season and currency. Ecology 73:1237-1243.
2. Ashman, T. L., T. M. Knight, J. A. Steets, P. Amarasekare, M. Burd, D. R. Campbell, M. R. Dudash, M. O. Johnston, S. J. Mazer, R. J. Mitchell, M. T. Morgan, and W. G. Wilson. 2004. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408-2421.
3. Baker, H. G. 1958. Studies of the reproductive biology of West African Rubiaceae. J. West Afr. Sci. Assoc. 4:9-24.
4. Barrett, S. C. H. 1992. Heterostylous genetic polymorphisms: model systems for evolutionary analysis. Pp. 1-39 in S. C. H. Barrett, ed. Evolution and function of heterostyly. Springer Verlag, New York.
5. _. 2002. The evolution of plant sexual diversity. Nat. Rev. Genet. 3:274-284.
6. Bawa, K. S. 1980. Evolution of dioecy in flowering plants. Annu. Rev. Ecol. Syst.: 11:15-39.
7. _. 1982. Seed dispersal and the evolution of dioecism in flowering plants: a response. Evolution 36:1322-1325.
8. Bawa, K. S., and J. H. Beach. 1981. Evolution of sexual systems in flowering plants. Ann. Mo. Bot. Gard. 68:254-274.
9. Beach, J. H., and K. S. Bawa. 1980. Role of pollinators in the evolution of dioecy from distyly. Evolution 34:1138-1142.
10. Bond, W. J., and K. E. Maze. 1999. Survival costs and reproductive benefits of floral display in a sexually dimorphic dioecious shrub, Leucadendron xanthoconus. Evol. Ecol. 13:1-18.
11. Charlesworth, D. 1984. Androdioecy and the evolution of dioecy. Biol. J. Linn. Soc. 23:333-348.
12. _. 1993. Why are unisexual flowers associated with wind-pollination and unspecialised pollinators? Am. Nat. 141:481-490.
13. _. 1999. Theories of the evolution of dioecy. Pp. 33-60 in M. A. Geber, T. E. Dawson, and L. F. Delph, eds. Gender and sexual dimorphism in flowering plants. Springer, Berlin.
14. Charlesworth, D., and B. Charlesworth. 1978. A model for the evolution of dioecy and gynodioecy. Am. Nat. 112:975-997.
15. _. 1981. Allocation of resources to male and female functions in hermaphrodites. Biol. J. Linn. Soc. 15:57-74.
16. Charnov, E. L., J. Maynard Smith, and J. J. Bull. 1976. Why be an hermaphrodite? Nature 263:125-126.
17. Darwin, C. 1877. The different forms of flowers on plants of the same species. Appleton, New York.
18. Davis, H. G., C. M. Taylor, J. G. Lambrinos, and D. R. Strong. 2004. Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). Proc. Natl. Acad. Sci. USA 101:13804-13807.
19. de Jong, P. C. 1976. Flowering and sex expression in Acer L.: a biosystematic study. Mededelingen Landbouwhogeschool, Wageningen, The Netherlands.
20. Dommée, B., J. L. Bompar, and N. Denelle. 1990. Sexual tetramorphism in Thymelaea hirsuta (Thymelaeaceae): evidence of the pathway from heterodichogamy to dioecy at the infraspecific level. Am. J. Bot. 77:1449-1462.
21. Dorken, M. E., and S. C. H. Barrett. 2003. Life-history differentiation and the maintenance of monoecy and dioecy in Sagittaria latifolia (Alismataceae). Evolution 57:1973-1988.
22. _. 2004. Sex determination and the evolution of dioecy from monoecy in Sagittaria latifolia (Alismataceae). Proc. R. Soc. Lond. B. 271:213-219.
23. Ehlers, B. K., and J. D. Thompson. 2004. Temporal variation in sex allocation in hermaphrodites of gynodioecious Thymus vulgaris. L. J. Ecol. 92:15-23.
24. El-Keblawy, A., J. Lovett Doust, and L. Lovett Doust. 1996. Gender variation and the evolution of dioecy in Thymelaea hirsuta (Thymeleaceae). Can. J. Bot. 74:1597-1601.
25. Fenster, C. B. 1991. Effect of seed parent and pollen donor on the allocation of resources to developing seeds and fruit in Chamaecrista fasciculata. Am. J. Bot. 78:13-23.
26. Freeman, D. C., J. Lovett Doust, A. El-Keblawy, K. J. Miglia, and E. D. McArthur. 1997. Sexual specialization and inbreeding avoidance in the evolution of dioecy. Bot. Rev. 63:65-92.
27. Givnish, T. J. 1980. Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. Evolution 34:959-972.
28. Gleeson, S. K. 1982. Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36:892-902.
29. Gleiser, G., and M. Verdú. 2005. Repeated evolution of dioecy from androdioecy in Acer. New Phytol. 165:633-640.
30. Gomez-Aparicio, L., R. Zamora, and J. M. Gomez. 2005. The regeneration status of the endangered Acer opalus subsp. granatense throughout its geographical distribution in the Iberian Peninsula. Biol. Conserv. 121:195-206.
31. Karron, J. D., N. N. Thumser, R. Tucker, and A. J. Hessenauer. 1995. The influence of population density on outcrossing rates in Mimulus ringens. Heredity 75:175-180.
32. Klinkhamer, P. G. L., T. J. de Jong, and J. A. J. Metz. 1994. Why plants can be too attractive: a discussion of measures to estimate male fitness. J. Ecol. 82:191-194.
33. Knight, T. M. 2003. Floral density, pollen limitation, and reproductive success in Trillium grandiflorum. Oecologia 137:557-563.
34. Kubitzki, K., and H. Kurz. 1984. Synchronized dichogamy and dioecy in neotropical Lauraceae. Plant Syst. Evol. 147:253-266.
35. Kunin, W. E. 1993. Sex and the single mustard: population density and pollination behaviour effects on seed set. Ecology 74:2145-2160.
36. Lack, A. J., and P. G. Kevan. 1987. The reproductive biology of a distylous tree, Sarcotheca celebica (Oxalidaceae), in Sulawesi, Indonesia. Bot. J. Linn. Soc. 95:1-8.
37. Lewis, D. 1941. Male sterility in natural populations of hermaphrodite plants. New Phytol. 40:56-63.
38. _. 1942. The evolution of sex in flowering plants. Cambr. Philos. Soc. Biol. Rev. 17:46-67.
39. Li, Q. J., Z. F. Xu, W. J. Kress, Y. M. Xia, L. Zhang, X. B. Deng, J. Y. Gao, and Z. L. Bai. 2001. Flexible style that encourages outcrossing. Nature 410:432.
40. Lloyd, D. G. 1974. Theoretical sex ratios of dioecious and gynodioecious angiosperms. Heredity 32:11-34.
41. _. 1975. The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45:325-339.
42. _. 1977. Genetic and phenotypic models of natural selection. J. Theor. Biol. 69:543-560.
43. _. 1979. Evolution towards dioecy in heterostylous populations. Plant Syst. Evol. 131:71-80.
44. _. 1980. The distribution of gender in four angiosperm species illustrating two evolutionary pathways to dioecy. Evolution 34:123-134.
45. _. 1982. Selection of combined versus separate sexes in seed plants. Am. Nat. 120:571-585.
46. Miglia, K. J., and D. C. Freeman. 1996. Delayed pollination, stigma length, sex expression, and progeny sex ratio in spinach, Spinacea oleracea (Chenopodiaceae). Am. J. Bot. 83:326-332.
47. Miller, J. S., and D. L. Venable. 2000. Polyploidy and the evolution of gender dimorphism in plants. Science 289:2335-2338.
48. Muenchow, G. E., and M. Grebus. 1989. The evolution of dioecy from distyly: reevaluation of the hypothesis of the loss of long-tongued pollinators. Am. Nat. 133:149-156.
49. Niklas, K. J. 1985. The aerodynamics of wind-pollination. Bot. Rev. 51:328-386.
50. Ornduff, R. 1966. The origin of dioecism from heterostyly in Nymphoides (Menyanthaceae). Evolution 20:309-314.
51. _. 1975. Heterostyly and pollen flow in Hypericum aegypticum (Guttiferae). Bot. J. Linn. Soc. 71:51-57.
52. Pailler, T., L. Humeau, J. Figier, and J. D. Thompson. 1998. Reproductive trait variation in the functionally dioecious and morphologically heterostylous island endemic Chassalia corallioides (Rubiaceae). Biol. J. Linn. Soc. 64:297-313.
53. Pannell, J. R. 2001. A hypothesis for the evolution of androdioecy: the joint influence of reproductive assurance and local mate competition in a metapopulation. Evol. Ecol. 14:195-211.
54. _. 2002. The evolution and maintenance of androdioecy. Annu. Rev. Ecol. Syst. 33:397-425.
55. Pannell, J. R., D. J. Obbard, and R. J. A. Buggs. 2004. Polyploidy and the sexual system: What can we learn from Mercurialis annua? Biol. J. Linn. Soc. 82:547-560.
56. Pendleton, R. L., D. C. Freeman, E. D. McArthur, and S. C. Sanderson. 2000. Gender specialization in heterodichogamous Grayia brandegei (Chenopodiaceae): evidence for an alternative pathway to dioecy. Am. J. Bot. 87:508-516.
57. Renner, S. S. 2001. How common is heterodichogamy? Trends Ecol. Evol. 16:595-597.
58. Renner, S. S., and R. E. Ricklefs. 1995. Dioecy and its correlates in the flowering plants. Am. J. Bot. 82:596-606.
59. Ross, M. D. 1982. Five evolutionary pathways to subdioecy. Am. Nat. 119:297-318.
60. Sakai, A. K., and S. G. Weller. 1999. Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. Pp. 1-31 in M. A. Geber, T. E. Dawson, and L. F. Delph, eds. Gender and sexual dimorphism in flowering plants. Springer, Berlin.
61. Sato, T. 2002. Phenology of sex expression and gender variation in a heterodichogamous maple, Acer japonicum. Ecology 85:1226-1238.
62. Seger, J., and V. M. Eckhart. 1996. Evolution of sexual systems and sex allocation in plants when growth and reproduction overlap. Proc. R. Soc. Lond. B 263:833-841.
63. Thomson, J. D., and S. C. H. Barrett. 1981a. Selection for outcrossing, sexual selection, and the evolution of dioecy in plants. Am. Nat. 118:443-449.
64. _. 1981b. Temporal variation of gender in Aralia hispida Vent. (Arailiaceae). Evolution 35:1094-1107.
65. Wang, Y. Q., D. X. Zhang, and Z. Y. Chen. 2004. Pollen histochemistry and pollen: ovule ratios in Zingiberaceae. Ann. Bot. 94:583-591.
66. Webb, C. J. 1999. Empirical studies: evolution and maintenance of dimorphic breeding systems. Pp. 61-95 in M. A. Geber, T. E. Dawson, and L. F. Delph, eds. Gender and sexual dimorphism in flowering plants. Springer, Berlin.
67. Wilson, W. G., and L. D. Harder. 2003. Reproductive uncertainty and the relative competitiveness of simultaneous hermaphroditism versus dioecy. Am. Nat. 162:220-241.
68. Wolf, D. E., and N. Takebayashi. 2004. Pollen limitation and the evolution of androdioecy from dioecy. Am. Nat. 163:122-137.
69. Wyatt, R. 1983. Pollinator-plant interactions and the evolution of breeding systems. Pp. 51-95 in L. Real, ed. Pollination biology. Academic Press, Orlando, FL.
70. Yampolsky, C., and H. Yampolsky. 1922. Distribution of sex forms in the phanerogamic flora. Bibl. Gen. 3:4-62.
71. Zhang, L., Q. J. Li, X. B. Deng, P. Y. Ren, and J. Y. Gao. 2003. Reproductive biology of Alpinia blepharocalyx (Zingiberaceae): another example of flexistyly. Plant Syst. Evol. 241:67-76.