Gynodioecy to dioecy: Are we there yet?

Annals of Botany

Volumn 109, Issue 3, 2012, Pages 531-543

  Spigler, Rachel B ^a   Ashman, Tia Lynn ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Breeding system; dioecy; gynodioecy; male fertility; plasticity; pollen limitation; sex ratio; sexual systems; subdioecy; trioecy

Indexed keywords

COEXISTENCE; DIOECY; EMPIRICAL ANALYSIS; EVOLUTIONARY BIOLOGY; FERTILITY; GYNODIOECY; HERMAPHRODITE; LIFE HISTORY TRAIT; POLLEN LIMITATION; REPRODUCTIVE STRATEGY; SEX RATIO;

ANGIOSPERM; ECOLOGY; EVOLUTION; FERTILITY; FLOWER; GENETIC SELECTION; GENETICS; HERMAPHRODITIC SPECIES; INBREEDING; PHYSIOLOGY; PLANT SEED; POLLINATION; REPRODUCTION; REVIEW; SPECIES DIFFERENCE;

ANGIOSPERMS; BIOLOGICAL EVOLUTION; ECOLOGY; FERTILITY; FLOWERS; HERMAPHRODITIC ORGANISMS; INBREEDING; POLLINATION; REPRODUCTION; SEEDS; SELECTION, GENETIC; SPECIES SPECIFICITY;

EID: 84857461203     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr170     Document Type: Review

References (133)

1. Agren J, Danell K, Elmqvist T, Ericson L, Hjältén J. 1999. Sexual dimorphism and biotic interactions. In: Geber MA, Dawson TE, Delph LF. eds. Gender and sexual dimorphism in flowering plants. Berlin, Springer, 217-246.
2. Aguirre A, Vallejo-Marin M, Piedra-Malagon EM, Cruz-Ortega R, Dirzo R. 2009. Morphological variation in the flowers of Jacaratia mexicana A. DC. (Caricaceae), a subdioecious tree. Plant Biology 11: 417-424.
3. Alonso C. 2003. Herbivores do not discriminate between leaves of female and hermaphrodite individuals of gynodioecious Daphne laureola (Thymelaeaceae). Oikos 101: 505-510. (Pubitemid 36599470)
4. Angers B, Castonguay E, Massicotte R. 2010. Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Molecular Ecology 19: 1283-1295.
5. Ashley MV. 2010. Plant parentage, pollination, and dispersal: how DNA microsatellites have altered the landscape. Critical Reviews in Plant Sciences 29: 148-161.
6. Ashman TL. 1998. Is relative pollen production or removal a good predictor of relative male fitness? An experimental exploration with a wild strawberry (Fragaria virginiana, Rosaceae). American Journal of Botany 85: 1166-1171.
7. Ashman TL. 2000. Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81: 2577-2591.
8. Ashman TL. 2002. The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology 83: 1175-1184.
9. Ashman TL. 2005. The limits on sexual dimorphism in vegetative traits in a gynodioecious plant. American Naturalist 166: S5-S16.
10. Ashman TL. 2006. The evolution of separate sexes: a focus on the ecological context. In: Harder LD, Barrett SCH. eds. The ecology and evolution of flowers. New York, Oxford University Press, 204-222.
11. Ashman T-L, Diefenderfer C. 2001. Sex ratio represents a unique context for selection on attractive traits: consequences for the evolution of sexual dimorphism. The American Naturalist 157: 334-347. (Pubitemid 32214666)
12. Ashman TL, Penet L. 2007. Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender-dimorphic plant. American Naturalist 169: 595-608. (Pubitemid 46651165)
13. Ashman T, Stanton M. 1991. Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72: 993-1003.
14. Ashman TL, Cole DH, Bradburn M. 2004. Sex-differential resistance and tolerance to herbivory in a gynodioecious wild strawberry. Ecology 85: 2550-2559. (Pubitemid 39348547)
15. Ashman T, Spigler RB, Goldberg M, Govindarajulu R. 2011. Fragaria: a polyploid lineage for understanding sex chromosome evolution. In: Navajas-Pérez R. ed. New insights on plant sex chromosomes, Chap. VI. Hauppauge, NY: Nova Science Publishers, in press.
16. Bailey MF, Delph LF. 2007. A field guide to models of sex-ratio evolution in gynodioecious species. Oikos 116: 1609-1617. (Pubitemid 47397204)
17. Barr CM. 2004. Soil moisture and sex ratio in a plant with nuclear-cytoplasmic sex inheritance. Proceedings of the Royal Society of London Biological Sciences 271: 1935-1939.
18. Barr CM, Fishman L. 2011. The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 184: 455-465.
19. Barrett SCH. 1992. Gender variation and the evolution of dioecy in Wurmbea dioica (Liliaceae). Journal of Evolutionary Biology 5: 423-444. (Pubitemid 23402478)
20. Barrett SCH, Case AL, Peters GB. 1999. Gender modification and resource allocation in subdioecious (Colchicaceae). Journal of Ecology 87: 123-137. (Pubitemid 29077686)
21. Bawa KS. 1980. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11: 15-39.
22. Bell G. 1985. On the function of flowers. Proceedings of the Royal Society of London. Series B, Biological Sciences 224: 223-265.
23. Bishop E, Spigler R, Ashman T. 2010. Sex-allocation plasticity in hermaphrodites of sexually dimorphic Fragaria virginiana (Rosaceae). Botany 88: 231-240.
24. Boyko A, Kovalchuk I. 2008. Epigenetic control of plant stress response. Environmental and Molecular Mutagenesis 49: 61-72. (Pubitemid 351293012)
25. Broyles SB, Wyatt R. 1990. Paternity analysis in a natural population of asclepias exaltata: multiple paternity, functional gender,, the 'pollen-donation hypothesis'. Evolution 44: 1454-1468.
26. Campbell D. 2000. Experimental tests of sex-allocation theory in plants. Trends in Ecology and Evolution 15: 227-231.
27. Carr DE, Dudash MR. 1997. The effects of five generations of enforced selfing on potential male and female function in Mimulus guttatus. Evolution 51: 1797-1807.
28. Case AL, Ashman TL. 2009. Resources and pollinators contribute to population sex-ratio bias and pollen limitation in Fragaria virginiana (Rosaceae). Oikos 118: 1250-1260.
29. Cepeda-Cornejo V, Dirzo R. 2010. Sex-related differences in reproductive allocation, growth, defense and herbivory in three dioecious neotropical palms. PLoS ONE 5: e9824. doi:10.1371/journal.pone.0009824.
30. Chang SM. 2007. Gender-specific inbreeding depression in a gynodioecious plant, Geranium maculatum (Geraniaceae). American Journal of Botany 94: 1193.
31. Charlesworth B, Charlesworth D. 1978. A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975-997.
32. Charlesworth D. 1989. Allocation to male and female function in hermaphrodites, in sexually polymorphic populations. Journal of Theoretical Biology 139: 327-342.
33. 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.
34. Charnov EL. 1982. The theory of sex allocation. Princeton, NJ: Princeton University Press.
35. Charnov EL, Maynard Smith J, Bull JJ. 1976. Why be a hermaphrodite? Nature 263: 125-126.
36. Chinnusamy V, Zhu J-K. 2009. Epigenetic regulation of stress responses in plants. Current Biology 12: 1-9.
37. Cole DH, Ashman TL. 2005. Sexes show differential tolerance to Spittlebug damage and consequences of damage for multi-species interactions. American Journal of Botany 92: 1708-1713. (Pubitemid 41426907)
38. Collin CL, Shykoff JA. 2010. Flowering phenology and female fitness: impact of a pre-dispersal seed predator on a sexually polymorphic species. Plant Ecology 206: 1-13.
39. Conner JK, Rush S, Kercher S, Jennetten P. 1996. Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum). 2. Selection through lifetime male and total fitness. Evolution 50: 1137-1146.
40. Cornelissen T, Stiling P. 2005. Sex-biased herbivory: a meta-analysis of the effects of gender on plant-herbivore interactions. Oikos 111: 488-500. (Pubitemid 41802894)
41. Couvet D, Atlan A, Belhassen E, Gliddon C, Gouyon PH, Kjellberg F. 1990. Coevolution between two symbionts: the case of cytoplasmic malesterility in higher plants. In: Futuyma D, Antonovics J. eds. Oxford surveys in evolutionary biology, Vol. 7. Oxford: Oxford University Press, 225-249.
42. Del Castillo RF, Argueta ST. 2009. Reproductive implications of combined and separate sexes in a trioecious population of Opuntia robusta (Cactaceae). American Journal of Botany 96: 1148-1158.
43. Delph LF. 1990. Sex-differential resource allocation patterns in the subdioecious shrub Hebe subalpina. Ecology 71: 1342-1351.
44. Delph LF. 2003. Sexual dimorphism in gender plasticity and its consequences for breeding system evolution. Evolution & Development 5: 34-39. (Pubitemid 36174975)
45. Delph LF, Wolf DE. 2005. Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems. New Phytologist 166: 119-128. (Pubitemid 40428138)
46. Delph LF, Touzet P, Bailey MF. 2007. Merging theory and mechanism in studies of gynodioecy. Trends in Ecology & Evolution 22: 17-24. (Pubitemid 44959172)
47. Dorken ME, Barrett SCH. 2003. Gender plasticity in Sagittaria sagittifolia (Alismataceae), a monoecious aquatic species. Plant Systematics and Evolution 237: 99-106.
48. Dorken ME, Barrett SCH. 2004. Phenotypic plasticity of vegetative and reproductive traits in monoecious and dioecious populations of Sagittaria latifolia (Alismataceae): a clonal aquatic plant. Journal of Ecology 92: 32-44. (Pubitemid 38143411)
49. Dorken ME, Mitchard ETA. 2008. Phenotypic plasticity of hermaphrodite sex allocation promotes the evolution of separate sexes: an experimental test of the sex-differential plasticity hypothesis using Sagittaria latifolia (Alismataceae). Evolution 62: 971-978. (Pubitemid 351489929)
50. Dorken ME, Pannell JR. 2009. Hermaphroditic sex allocation evolves when mating opportunities change. Current Biology 19: 514-517.
51. Dufay M, Billard E. 2011. How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Annals of Botany 109: 505-519.
52. Dufay M, Pannell JR. 2010. The effect of pollen versus seed flow on the maintenance of nuclear-cytoplasmic gynodioecy. Evolution 64: 772-784.
53. Dufay M, Lahiani E, Brachi B. 2010. Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). International Journal of Plant Sciences 171: 53-62.
54. Eckhart VM. 1992. Spatio-temporal variation in abundance and variation in foraging behavior of the pollinators of gynodioecious Phacelia linearis (Hydrophyllaceae). Oikos 64: 573-586.
55. Ehlers BK, Bataillon T. 2007. 'Inconstant males' and the maintenance of labile sex expression in subdioecious plants. New Phytologist 174: 194-211. (Pubitemid 46333300)
56. Ehlers BK, Thompson JD. 2004. Temporal variation in sex allocation in hermaphrodites of gynodioecious Thymus vulgaris L. Journal of Ecology 92: 15-23. (Pubitemid 38143409)
57. Elle E, Hare JD. 2002. Environmentally induced variation in floral traits affects the mating system in Datura wrightii. Functional Ecology 16: 79-88. (Pubitemid 34220030)
58. Fishman L, Willis JH. 2006. A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60: 1372-1381. (Pubitemid 44795581)
59. Fleming TH, Maurice S, Buchmann SL, Tuttle MD. 1994. Reproductive biology and relative male and female fitness in a trioecious cactus, Pachycereus pringlei (Cactaceae). American Journal of Botany 81: 858-867. (Pubitemid 2113672)
60. Glaettli M, Goudet J. 2006. Inbreeding effects on progeny sex ratio and gender variation in the gynodioecious Silene vulgaris (Caryophyllaceae). New Phytologist 172: 763-773. (Pubitemid 44691633)
61. Goldberg MT, Spigler RB, Ashman T-L. 2010. Comparative genetic mapping points to different sex chromosomes in sibling species of wild strawberry (Fragaria). Genetics 186: 1425-1433.
62. Gorelick R. 2003. Evolution of dioecy and sex chromosomes via methylation driving Muller's ratchet. Biological Journal of the Linnean Society 80: 353-368. (Pubitemid 37274332)
63. Gregorius H, Ross M, Gillet E. 1983. Selection in plant populations of effectively infinite size. V. Biallelic models of trioecy. Genetics 103: 529.
64. Ho TY, Ross M. 1974. Maintenance of males and females in hermaphrodite populations. Heredity 32: 113-118.
65. Jacobs MS, Wade MJ. 2003. A synthetic review of the theory of gynodioecy. American Naturalist 161: 837-851. (Pubitemid 36821258)
66. de Jong TJ, Geritz SAH. 2001. Gradual evolution towards dioecy in cosexual plants. Selection 2: 133-146.
67. de Jong TJ, Klinkhamer PGL. 1989. Size-dependency of sex-allocation in hermaphroditic, monocarpic plants. Functional Ecology 3: 201-206. (Pubitemid 20417473)
68. de Jong TJ, Klinkhamer PGL, Rademaker MCJ. 1999. How geitonogamous selfing affects sex allocation in hermaphrodite plants. Journal of Evolutionary Biology 12: 166-176. (Pubitemid 29033119)
69. Jones A, Burd M. 2001. Vegetative and reproductive variation among unisexual and hermaphroditic individuals of Wurmbea dioica (Colchicaceae). Australian Journal of Botany 49: 603-609. (Pubitemid 33066310)
70. Kay Q. 1985. Hermaphrodites and subhermaphrodites in a reputedly dioecious plant, Cirsium arvense (L.) Scop. New Phytologist 100: 457-472.
71. Klinkhamer PGL, de Jong TJ, Metz H. 1997. Sex and size in cosexual plants. TREE 12: 260-265.
72. Knight TM, Steets JA, Vamosi JC, et al. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution & Systematics 36: 467-497. (Pubitemid 43068867)
73. Lande R, Arnold SJ. 1983. The measurement of selection on correlated characters. American Naturalist 37: 1210-1226.
74. Lewis D. 1941. Male sterility in natural populations of hermaphrodite plants the equilibrium between females and hermaphrodites to be expected with different types of inheritance. New Phytologist 40: 56-63.
75. Lewis D. 1942. The evolution of sex in flowering plants. Biological Reviews 17: 46-67.
76. Lloyd DG. 1974. Theoretical sex ratios of dioecious and gynodioecious angiosperms. Heredity 32: 11-34.
77. Lloyd DG. 1975. Maintenance of gynodioecy and andriodioecy in angiosperms. Genetica 45: 325-339.
78. Lloyd DG. 1976. Transmission of genes via pollen and ovules in gynodioecious angiosperms. Theoretical Population Biology 9: 299-316.
79. Lopes AV, Machado IC. 1998. Floral biology and reproductive ecology of Clusia nemorosa (Clusiaceae) in northeastern Brazil. Plant Systematics and Evolution 213: 71-90. (Pubitemid 28562829)
80. Manicacci D, Atlan A, Rossello JAE, Couvet D. 1998. Gynodioecy and reproductive trait variation in three Thymus species (Lamiaceae). International Journal of Plant Sciences 159: 948-957. (Pubitemid 29009900)
81. Marguerit E, Boury C, Minicki A, et al. 2009. Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theoretical and Applied Genetics 118: 1261-1278.
82. Maurice S, Fleming TH. 1995. The effect of pollen limitation on plant reproductive systems and the maintenance of sexual polymorphisms. Oikos 74: 55-60. (Pubitemid 3005223)
83. Maurice S, Belhassen E, Couvet D, Gouyon PH. 1994. Evolution of dioecy: can nuclear-cytoplasmic interactions select for maleness? Heredity 73: 346-354. (Pubitemid 2141348)
84. Maurice S, Desfeux C, Mignot A, Henry J. 1998. Is Silene acaulis (Caryophyllaceae) a trioecious species? Reproductive biology of two subspecies. Botany 76: 478-485. (Pubitemid 28407740)
85. McCall AC, Irwin RE. 2006. Florivory: the intersection of pollination and herbivory. Ecology Letters 9: 1351-1365. (Pubitemid 44789727)
86. McCauley DE, Bailey MF. 2009. Recent advances in the study of gynodioecy: the interface of theory and empiricism. Annals of Botany 104: 611-620.
87. McCauley D, Brock M. 1998. Frequency-dependent fitness in Silene vulgaris, a gynodioecious plant. Evolution 52: 30-36. (Pubitemid 28195147)
88. McCauley DE, Olson MS. 2008. Do recent findings in plant mitochondrial molecular and population genetics have implications for the study of gynodioecy and cytonuclear conflict? Evolution 62: 1013-1025. (Pubitemid 351623948)
89. Miyake K, Olson MS. 2009. Experimental evidence for frequency dependent self-fertilization in the gynodioecious plant, Silene vulgaris. Evolution 63: 1644-1652.
90. Morand-Prieur ME, Raquin C, Shykoff JA, Frascaria-Lacoste N. 2003. Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae). American Journal of Botany 90: 949-953. (Pubitemid 36738456)
91. Narbona E, Dirzo R. 2010. Experimental defoliation affects male but not female reproductive performance of the tropical monoecious plant Croton suberosus (Euphorbiaceae). Annals of Botany 106: 359-369.
92. Olson MS. 2001. Patterns of fruit production in the subdioecious plant Astilbe biternata (Saxifragaceae). Ecology 89: 600-607. (Pubitemid 32778800)
93. Paquin V, Aarssen LW. 2004. Allometric gender allocation in Ambrosia artemisiifolia (Asteraceae) has adaptive plasticity. American Journal of Botany 91: 430-438. (Pubitemid 38370888)
94. Penet L, Collin CL, Ashman TL. 2009. Florivory increases selfing: an experimental study in the wild strawberry, Fragaria virginiana. Plant Biology 11: 38-45.
95. Philipp M, Jakobsen RB, Nachman G. 2009. A comparison of pollen-siring ability and life history between males and hermaphrodites of subdioecious Silene acaulis. Evolutionary Ecology Research 11: 787-801.
96. Pickering C, Ash J. 1993. Gender variation in hermaphrodite plants: evidence from five species of alpine Ranunculus. Oikos 68: 539-548.
97. Queller D. 1997. Pollen removal, paternity, and the male function of flowers. American Naturalist 149: 585-594. (Pubitemid 127738103)
98. Ramsey M, Vaughton G. 2001. Sex expression and sexual dimorphism in subdioecious Wurmbea dioica (Colchicaceae). International Journal of Plant Sciences 162: 589-597. (Pubitemid 32437295)
99. Renner S, Ricklefs R. 1995. Dioecy and its correlates in the flowering plants. American Journal of Botany 82: 596-606.
100. Richards AJ. 1986. Plant breeding systems. London: George Allen & Unwin.
101. Ross MD. 1977. Behavior of a sex-differential fertility gene in hermaphrodite populations. Heredity 38: 279-290. (Pubitemid 8102975)
102. Ross MD. 1978. The evolution of gynodioecy and subdioecy. Evolution 32: 147-188.
103. Ross MD. 1982. Five evolutionary pathways to subdioecy. American Naturalist 119: 297-318.
104. Ross M, Weir B. 1976. Maintenance of males and females in hermaphrodite populations and the evolution of dioecy. Evolution 30: 425-441.
105. Sakai AK, Weller SG. 1991. Ecological aspects of sex expression in subdioecious Schiedea globosa (Caryophyllaceae). American Journal of Botany 78: 1280-1288.
106. Sakai AK, Weller SG. 1999. Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In: Geber MA, Dawson TE, Delph LF. eds. Gender and sexual dimorphism in flowering plants. Berlin: Springer.
107. Sakai AK, Weller SG, Chen ML, Chou SY, Tasanont C. 1997. 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. (Pubitemid 27331543)
108. Saumitou-Laprade P, Vernet P, Vassiliadis C, et al. 2010. A selfincompatibility system explains high male frequencies in an androdioecious plant. Science 327: 1648-1650.
109. Schoen DJ, Stewart SC. 1986. Variation in male reproductive investment and male reproductive success in white spruce. Evolution 40: 1109-1120.
110. Schultz ST. 1994. Nucleo-cytoplasmic male sterility and alternative routes to dioecy. Evolution 48: 1933-1945.
111. Seger J, Eckhart VM. 1996. Evolution of sexual systems and sex allocation in plants when growth and reproduction overlap. Proceedings of the Royal Society B, Biological Sciences 263: 833-841.
112. Shykoff JA, Kolokotronis S-O, Collin CL, López-Villavicencio M. 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1-9. (Pubitemid 36400231)
113. Silva CA, Oliva MA, Vieira MF, Fernandes GW. 2008. Trioecy in Coccoloba cereifera Schwacke (Polygonaceae), a narrow endemic and threatened tropical species. Brazilian Archives of Biology and Technology 51: 1003-1010.
114. Snow AA, Lewis PO. 1993. Reproductive traits and male fertility in plants: empirical approaches. Annual Review of Ecology and Systematics 24: 331-351.
115. Spigler RB, Ashman TL. 2011. Sex ratio and subdioecy in Fragaria virginiana: the roles of plasticity and gene flow examined. New Phytologist 190: 1058-1068.
116. Spigler RB, Lewers KS, Main DS, Ashman TL. 2008. Genetic mapping of sex determination in a wild strawberry, Fragaria virginiana, reveals earliest form of sex chromosome. Heredity 101: 507-517.
117. Spigler RB, Lewers K, Ashman T-L. 2011. Genetic architecture of sexual dimorphism in a subdioecious plant with a proto-sex chromosome. Evolution 65: 1114-1126.
118. Steets JA, Ashman T-L. 2004. Herbivory alters the expression of a mixedmating system. American Journal of Botany 91: 1046-1051. (Pubitemid 43175053)
119. Steets JA, Knight TM, Ashman TL. 2007. The interactive effects of herbivory and mixed mating for the population dynamics of Impatiens capensis. American Naturalist 170: 113-127. (Pubitemid 46984581)
120. Sutherland S. 1987. Why hermaphroditic plants produce many more flowers than fruits: experimental tests with Agave mckelveyana. Evolution 41: 750-759.
121. Thompson JD, Tarayre M. 2000. Exploring the genetic basis and proximate causes of female fertility advantage in gynodioecious Thymus vulgaris. Evolution 54: 1510-1520.
122. Torices R, Méndez M, Gómez JM. 2001. Where do monomorphic sexual systems fit in the evolution of dioecy? Insights from the largest family of angiosperms. New Phytologist 190: 234-248.
123. Tsuji K, Sota T. 2010. Sexual differences in flower defense and correlated male-biased florivory in a plant-florivore system. Oikos 119: 1848-1853.
124. Van Etten ML. 2009. The evolution and maintenance of gynodioecy in Geranium maculatum. PhD thesis, University of Georgia, Athens, GA.
125. Verdú M, García-Fayos P, Gleiser G. 2004. Mites attack males of the sexually polymorphic tree Acer opalus more harmfully and more often. Functional Ecology 18: 592-597. (Pubitemid 39059418)
126. Wang LH, Zhang BX, Lefebvre V, Huang SW, Daubèze AM, Palloix A. 2004. QTL analysis of fertility restoration in cytoplasmic male sterile pepper. Theoretical and Applied Genetics 109: 1058-1063. (Pubitemid 39348246)
127. Webb C. 1976. Flowering periods in the gynodioecious species Gingidia decipiens (Umbelliferae). New Zealand Journal of Botany 14: 207-210.
128. Webb CJ. 1999. Empirical studies: evolution and maintenance of dimorphic breeding systems. In: Geber MA, Dawson TE, Delph LF. eds. Gender and sexual dimorphism in flowering plants. Berlin, Springer, 61-95.
129. Weiblen GD, Oyama RK, Donoghue MJ. 2000. Phylogenetic analysis of dioecy in monocotyledons. American Naturalist 155: 46-58. (Pubitemid 30132334)
130. Wilcock C, Neiland R. 2002. Pollination failure in plants: why it happens and when it matters. Trends in Plant Science 7: 270-277. (Pubitemid 36726530)
131. Wise MJ, Hébert JB. 2010. Herbivores affect natural selection for floral-sex ratio in a field population of horsenettle, Solanum carolinense. Ecology 91: 937-943.
132. Wolfe LM, Shmida A. 1997. The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology 78: 101-110.
133. Zhang YW, Yang CF, Zhao JM, Guo YH. 2009. Selective nectar robbing in a gynodioecious plant (Glechoma longituba) enhances female advantage. Journal of Evolutionary Biology 22: 527-535.