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Sexual specialization and inbreeding avoidance in the evolution of dioecy

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Abstract

Dioecy has evolved independently, many times, among unrelated taxa. It also appears to have evolved along two contrasting pathways: (1) from hermaphroditism via monoecy to dioecy and (2) from hermaphroditism via gynodioecy to dioecy. Most dioecious plants have close cosexual relatives with some means of promoting outcrossing (e.g., herkogamy, dichogamy, self-incompatibility, or monoecy). To the extent that these devices prevent inbreeding, the evolution of dioecy in these species cannot logically be attributed to selection for outcrossing. In these cases, the evolution of dioecy is, we believe, due to selection for sexual specialization. However, in other species, that lack outbreeding close relatives, dioecy may have evolved from gynodioecy (males and hermaphrodites) as an outbreeding device. Subsequent disruptive selection and selection for sexual specialization may have also shaped the evolution of dioecy from gynodioecy in these species, resulting in two genetically determined, constant sex morphs.

Both pathways for the evolution of dioecy require the operation of disruptive selection, though the gynodioecy route involves more restrictive disruptive selection and a genetic designation of gender. In contrast, the monoecy route is not dependent on the genetic designation of two sex morphs, but, rather, allows the possibility of sexual intermediates and sexual lability. Both pathways produce one morph in which maleness is suppressed and another in which the female function is negligible or nonexistent—the reproductive mode recognized as dioecy.

Evidence is presented here to support the thesis that instances of sexual lability, the presence of an array of sexual intermediates, sex-switching, and sexual niche segregation can be explained in terms of the pathway that was taken in the evolution of a particular dioecious species. In addition, the degree of sexual dimorphism seen in dioecious species is correlated with mode of pollination (insector wind-pollinated) and other ecological factors.

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Literature Cited

  • Agren, J. 1988. Sexual differences in biomass and nutrient allocation in the dioecious shrubRubus chamaemorus. Ecology69:962–973.

    Google Scholar 

  • Allen, G. A. &J. A. Antos. 1988. Relative reproductive effort in males and females of the dioecious shrubOemleria cerasiformis. Oecologia76:111–118.

    Google Scholar 

  • Anderson, G. J. 1989. Functional dioecy and andromonoecy inSolarium. Evolution43:204–219.

    Google Scholar 

  • Antos, J. A. &G. A. Allen. 1990. A comparison of reproductive effort in the dioecious shrubOemleria cerasiformis using nitrogen, energy and biomass as currencies. Amer. Midl. Naturalist124:254–262.

    Google Scholar 

  • Arnold, S. J. 1994a. Is there a unifying concept of sexual selection that applies to both plants and animals? Amer. Naturalist144(Suppl.):S1-S12.

    Google Scholar 

  • — 1994b. Bateman’s principles and the measurement of sexual selection in plants and animals. Amer. Naturalist144(Suppl.):S126-S149.

    Google Scholar 

  • Ashman, T. L. 1994. Reproductive allocation in hermaphrodite and female plants ofSidalcea oregana ssp.spicata (Malvaceae) using four currencies. Amer. J. Bot.81:433–438.

    Google Scholar 

  • — &I. Baker. 1992. Variation in floral sex allocation with time of season and currency. Ecology73:1237–1243.

    Google Scholar 

  • — &M. Stanton. 1991. Seasonal variation in pollination dynamics of sexually dimorphicSidalcea oregana ssp.spicata (Malvaceae). Ecology72:993–1003.

    Google Scholar 

  • Baker, H. G. 1959. Reproductive methods as factors in speciation in flowering plants. Cold Spring Harbor Symp. Quant. Biol.24:177–191.

    PubMed  CAS  Google Scholar 

  • — &P. D. Hurd. 1968. Intrafloral ecology. Ann. Rev. Entomol.13:385–414.

    Google Scholar 

  • Barrow, J. R. 1986. Effects of chromosome number on sex expression inAtriplex canescens. Bot. Gaz.148:379–385.

    Google Scholar 

  • Bawa, K. S. 1980. Evolution of dioecy in flowering plants. Ann. Rev. Ecol. Syst.11:15–39.

    Google Scholar 

  • —. 1982. Outcrossing and the incidence of dioecism in island floras. Amer. Naturalist119:866–871.

    Google Scholar 

  • — &P. A. Opler. 1975. Dioecism in tropical forest trees. Evolution29:167–179.

    Google Scholar 

  • Bell, C. R. 1976. Inflorescence shape and pollinator activity inDaucus carota L. (Apiaceae). ASB Bull23:42 (abstract).

    Google Scholar 

  • Bertin, R. I. 1993a. Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. Amer. J. Bot.80:557–560.

    Google Scholar 

  • —. 1993b. Dichogamy in angiosperms. Bot. Rev. (Lancaster)59:112–152.

    Google Scholar 

  • Bickel, A. M. &D. C. Freeman. 1993. Effects of pollen vector and plant geometry on floral sex ratio in monoecious plants. Amer. Midl. Naturalist130:239–247.

    Google Scholar 

  • Bierzchudek, P. 1984. Determinants of gender in jack-in-the-pulpit: The influence of plant size and reproductive history. Oecologia65:14–18.

    Google Scholar 

  • — &V. Eckhart. 1988. Spatial segregation of the sexes in dioecious plants. Amer. Naturalist132:34–43.

    Google Scholar 

  • Boecklen, W. J. &T. M. Hoffman. 1993. Sex biased herbivory inEphedra trifurca: The importance of sex-by-environment interactions. Oecologia96:49–55.

    Google Scholar 

  • Bond, W. &J. Midgley. 1988. Allometry and sexual differences in leaf size. Amer. Naturalist131:901–910.

    Google Scholar 

  • Breese, E. L. 1959. Selection for differing degrees of out-breeding inNicotiana rustica. Ann. Bot.23:331–344.

    Google Scholar 

  • Burd, M. &G. Head. 1992. Phenological aspects of male and female function in hermaphroditic plants. Amer. Naturalist140:305–324.

    Google Scholar 

  • Charlesworth, B. &D. Charlesworth. 1978. A model for the evolution of dioecy and gynodioecy. Amer. Naturalist112:975–997.

    Google Scholar 

  • Charlesworth, D. 1985. Distribution of dioecy and self-incompatibility in angiosperms. Pages 237–268in P. J. Greenwood, P. H. Harvey & M. Slatkin (eds.), Evolution: Essays in honour of John Maynard Smith. Cambridge University Press, Cambridge.

    Google Scholar 

  • — 1993. Why are unisexual flowers associated with wind-pollination and unspecialized pollinators? Amer. Naturalist141:481–490.

    Google Scholar 

  • — &B. Charlesworth. 1978. Population genetics of partial male-sterility and the evolution of monoecy and dioecy. Heredity41:137–153.

    Google Scholar 

  • ——. 1987. The effect of investment in attractive structures and allocation to male and female functions in plants. Evolution41:948–968.

    Google Scholar 

  • Charnov, E. L. 1982. The theory of sex allocation. Monographs in population biology. Princeton University Press, Princeton.

    Google Scholar 

  • Cipollini, M. L. &D. F. Whigham. 1994. Sexual dimorphism and cost of reproduction in the dioecious shrubLindera benzoin (Lauraceae) Amer. J. Bot.81:65–75.

    Google Scholar 

  • Clarke, A. E. &E. Newbigin. 1993. Molecular aspects of self-incompatibility in flowering plants. Annual Rev. Genet.27:257–279.

    CAS  Google Scholar 

  • Condon, M. A. &L. E. Gilbert. 1988. Sex expression ofGurania psiguria (Cucurbitaceae): Neotropical vines that change sex. Amer. J. Bot.75:875–884.

    Google Scholar 

  • Cox, P. A. 1982. Vertebrate pollination and the maintenance of dioecism inFreycinetia. Amer. Naturalism120:65–80.

    Google Scholar 

  • —. 1988. Monomorphic and dimorphic sexual strategies: A modular approach. Pages 80–97in J. Lovett Doust & L. Lovett Doust (eds.), Plant reproductive ecology: Patterns and strategies. Oxford University Press, Oxford.

    Google Scholar 

  • Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York.

    Google Scholar 

  • Cruden, R. W. 1988. Temporal dioecism: Systematic breadth, associated traits and temporal patterns. Bot. Gaz.149:1–15.

    Google Scholar 

  • — &S. Hermann-Parker. 1977. Temporal dioecism: An alternative to dioecism? Evolution31:863–866.

    Google Scholar 

  • — &D. L. Lyon. 1985. Patterns of biomass allocation to male and female functions in plants with different mating systems. Oecologia66:299–306.

    Google Scholar 

  • Darwin, C. 1877. The different forms of flowers on plants of the same species. Murray, London.

    Google Scholar 

  • Dawson, T. E. &L. C. Bliss. 1989. Patterns of water use and the tissue-water relations in the dioecious shrub,Salix artica: The physiological basis for habitat partitioning between the sexes. Oecologia79:332–343.

    Google Scholar 

  • —. 1993. Gender-specific physiology, carbon isotope discrimination, and habitat distribution in box elder,Acer negundo. Ecology74:798–815.

    Google Scholar 

  • De Jong, T. J. &P. G. L. Klinkhamer. 1994. Plant size and reproductive success through female and male function. J. Ecol.82:399–402.

    Google Scholar 

  • Delph, L. F. 1990. Sex-differential resource allocation patterns in the subdioecious shrubHebe subalpina. Ecology71:1342–1351.

    Google Scholar 

  • De Nettancourt, D. 1977. Incompatibility in angiosperms. Springer-Verlag, New York.

    Google Scholar 

  • Dommee, B., L. Bompar &N. Denelle. 1990. Sexual tetramorphism inThymelaea hirsuta (Thymelaeaceae): Evidence of the pathway from heterodichogamy to dioecy at the interspecific level. Amer. J. Bot.77:1449–1462.

    Google Scholar 

  • Dulberger, R. &A. Horowitz. 1984. Gender polymorphism in flowers ofSilene vulgaris (Moench) Garcke (Caryophyllaceae). J. Linn. Soc., Bot.89:101–117.

    Google Scholar 

  • Eckart, V. M. 1992. Resource compensation and the evolution of gynodioecy inPhacelia linearis (Hydrophyllaceae). Evolution46:1313–1328.

    Google Scholar 

  • El-Keblawy, A., J. Lovett Doust, L. Lovett Doust &K. H. Shaltout. 1995. Labile sex expression and dynamics of gender inThymelaea hirsuta. Ecoscience2:55–66.

    Google Scholar 

  • ———. 1996. Gender variation and the evolution of dioecy inThymelaea hirsuta (Thymelaeaceae). Canad. J. Bot.74:1596–1601.

    Google Scholar 

  • Faegri, K. &L. van der Pijl. 1971. The principles of pollination ecology. Pergamon Press, New York.

    Google Scholar 

  • Fisher, R. A. 1930. The genetical theory of natural selection. Oxford University Press, Oxford.

    Google Scholar 

  • Flemming, T. H., S. Maurice, S. L. Buchmann &M. D. Tuttle. 1994. Reproductive biology and relative male and female fitness in a trioecious cactus,Pachycereus pringlei (Cactaceae). Amer. J. Bot.81:858–867.

    Google Scholar 

  • Flores, S. &D. Schemske. 1984. Dioecy and monoecy in the flora of Puerto Rico and the Virgin Islands: Ecological correlates. Biotropica16:132–139.

    Google Scholar 

  • Fox, J. F. 1985. Incidence of dioecy in relation to growth form, pollination and dispersal. Oecologia67:244–249.

    Google Scholar 

  • —. 1991. Costs of reproduction in a willow: Experimental responses vs. natural variation. Ecology72:1013–1023.

    Google Scholar 

  • —. 1993. Size and sex allocation in monoecious woody plants. Oecologia94:110–113.

    Google Scholar 

  • — &G. C. Stevens. 1993. Costs of reproduction in a willow: Experimental responses vs. natural variation. Ecology72:1013–1023.

    Google Scholar 

  • Frankel, R. &E. Galun. 1977. Pollination mechanisms, reproduction and plant breeding. Springer-Verlag, New York.

    Google Scholar 

  • Freeman, D. C. &E. D. McArthur. 1982. A comparison of water stress between males & females of four species of desert shrubs. Forest Sci.28:304–308.

    Google Scholar 

  • ——. 1984. The relative influence of mortality, nonflowering and sex change. Bot. Gaz.145:385–394.

    Google Scholar 

  • ——. 1989.Atriplex canescens. Pages 75–86in A. Halvey (ed.), The handbook of flowering. Vol. 6. CRC Press, London.

    Google Scholar 

  • — &J. J. Vitale. 1985. The influence of environment on the sex ratio of spinach. Bot. Gaz.146:137–142.

    Google Scholar 

  • —,K. T. Harper &E. L. Charnov. 1980a. Sex change in plants: Old and new observations and new hypotheses. Oecologia47:222–232.

    Google Scholar 

  • —— &W. K. Ostler. 1980b. Ecology of plant dioecy in the intermountain region of western North America. Oecologia44:410–417.

    Google Scholar 

  • —,L. G. Klikoff &K. T. Harper. 1976. Differential resource utilization by the sexes of dioecious plants. Science193:597–599.

    PubMed  Google Scholar 

  • —,E. D. McArthur, S. C. Sanderson &A. R. Tiedemann. 1993. The influence of topography on male and female fitness components ofAtriplex canescens. Oecologia93:538–547.

    Google Scholar 

  • Gehring, J. L. &R. K. Monson. 1994. Sexual difference in gas exchange and response to environmental stress in dioeciousSilene latifolia (Caryophyllaceae). Amer. J. Bot.81:166–174.

    Google Scholar 

  • Ghiselin, M. T. 1969. The evolution of hermaphroditism among animals. Quart. Rev. Biol.44:189–208.

    PubMed  CAS  Google Scholar 

  • Givnish, T. J. 1980. Ecological constraints on the evolution of breeding systems in seed plants: Dioecy and dispersal in gymnosperms. Evolution34:959–972.

    Google Scholar 

  • Grant, V. 1951. The fertilization of flowers. Sci. Amer.184:52–56.

    Google Scholar 

  • —. 1995. Sexual selection in plants: Pros and cons. Proc. Natl. Acad. U.S.A.92:1247–1250.

    CAS  Google Scholar 

  • Gregg, K.B. 1973. Studies on the control of sex expression in the generaCychnoches andCatesetum, subtribe Catasetinae, Orchidaceae. Ph.D. dissertation, University of Miami, Coral Gables.

    Google Scholar 

  • —. 1975. The effect of light intensity on sex expression in species ofCychnoches andCatesetum (Orchidaceae). Selbyana1:101–113.

    Google Scholar 

  • —. 1978. Ethylene physiology, sunlight intensity and sex in the orchid generaCychnoches (Orchidaceae). Selbyana2:212–223.

    Google Scholar 

  • —. 1982. Sunlight-enhanced ethylene evolution by developing inflorescences ofCatasetum andCychnoches and its relation to female flower production. Bot. Gaz.143:466–475.

    CAS  Google Scholar 

  • Heinrich, B. 1975. Energetics of pollination. Annual Rev. Ecol. Syst.6:139–170.

    Google Scholar 

  • Hoffmann, M. T. 1992. Functional dioecy inEchinocereus coccineus (Cactaceae): Breeding system, sex ratios and geographical range of floral dimorphism. Amer. J. Bot.79:1382–1388.

    Google Scholar 

  • Holtsford, T. P. &N. C. Ellstrand. 1992. Genetic and environmental variation in floral traits affecting outcrossing rate inClarkia tembloriensis. Evolution46:216–255.

    Google Scholar 

  • Horowitz, A. 1978. Is the hermaphroditic flowering plant equisexual? Amer. J. Bot.65:485–486.

    Google Scholar 

  • — &R. Dulberger. 1983. The genetic basis of gender inSilene vulgaris. Heredity51:371–376.

    Google Scholar 

  • Irish, E. &T. Nelson. 1989. Sex determination in monoecious and dioecious plants. Pl. Cell1:737–744.

    Google Scholar 

  • Kessili, R. &S. K. Jain. 1984. An ecological genetic study of gynodioecy inLimnanthes douglassi (Limnanthaceae). Amer. J. Bot.71:775–786.

    Google Scholar 

  • Kohn, J. R. 1989. Sex ratio, seed production, biomass allocation and the cost of male function inCucurbita foetidissma HBK (Cucurbitaceae). Evolution43:1424–1434.

    Google Scholar 

  • Lloyd, D. G. 1975. The maintenance of gynodioecy and androdioecy in angiosperms. Genetica45:325–339.

    Google Scholar 

  • —. 1979. Evolution towards dioecy in heterostylous populations. Pl. Syst. Evol.131:71–80.

    Google Scholar 

  • — &K. S. Bawa. 1984. Modification of gender of seed plants in varying conditions. Evol. Biol.17:255–338.

    Google Scholar 

  • — &C. J. Webb. 1977. Secondary sex characters in plants. Bot. Rev. (Lancaster)43:177–215.

    Google Scholar 

  • Lovett Doust, J. &P. B. Cavers. 1982. Sex and gender dynamics in jack-in-the-pulpit,Arisaema triphyllum (Araceae). Ecology63:797–808.

    Google Scholar 

  • — &L. Lovett Doust. 1985. Sex ratios, clonal growth and herbivory inRumex acetosella. Pages 327–341in J. White (ed.), Studies on plant demography: A festschrift for John L. Harper. Academic Press, London.

    Google Scholar 

  • ——. 1988. Sociobiology of plants: An emerging synthesis. Pages 5–29in J. Lovett Doust & L. Lovett Doust (eds.), Plant reproductive ecology: Patterns and strategies. Oxford University Press, New York.

    Google Scholar 

  • Lovett Doust, L. 1981. Population dynamics and local specialization in a clonal perennial (Ranunculus repens). 1. The dynamics of ramets in contrasting habitats. J. Ecol.69:743–755.

    Google Scholar 

  • Mayer, S. S. &D. Charlesworth. 1991. Cryptic dioecy in flowering plants. Tree6:320–325.

    Google Scholar 

  • McArthur, E. D. 1977. Environmental induced changes of sex expression inAtriplex canescens. Heredity38:97–103.

    Google Scholar 

  • —. 1989. Breeding systems in shrubs. Pages 341–361in C. M. McKell (ed.), The biology and utilization of shrubs. Academic Press, San Diego.

    Google Scholar 

  • — &D. C. Freeman. 1982. Sex expression inAtriplex canescens, genetics and environment. Bot. Gaz.143:476–482.

    Google Scholar 

  • — &S. C. Sanderson. 1984. Distribution, systematics, and evolution of Chenopodiaceae: An overview. Pages 14–24in A. R. Tiedemann, E. D. McArthur, H. C. Stutz, R. Stevens & K. L. Johnson (compilers), Proceedings—Symposium on the biology ofAtriplex and related chenopods, 2–6 May 1983, Provo, Utah. Gen. Tech. Rep. INT-172. U.S.D.A. Forest Service, Intermountain Forest and Range Experiment Station, Ogden, Utah.

    Google Scholar 

  • —,D. C. Freeman, L. Luckinbill, S. C. Sanderson &G. L. Noller. 1992. Are trioecy and sexual lability inAtriplex canescens genetically based: Evidence from clonal studies. Evolution46:1708–1721.

    Google Scholar 

  • -,McArthur, E. D., A. P. Plummer, G. A. Van Epps, D. C. Freeman & K. R. Jorgensen. 1978. Producing fourwing saltbush seed in seed orchards. Pages 406–410in Proceedings of the First International Rangeland Congress.

  • Miglia, K. J. &D. C. Freeman. 1996. The effect of delayed pollination on stigma length, sex expression, and progeny sex ratio in spinach,Spinacia oleracea (Chenopodiaceae). Amer. J. Bot. 83:326–332.

    Google Scholar 

  • Miller, J. &J. Lovett Doust. 1987. The effects of plant density and snail grazing on female and male spinach plants. New Phytol.107:613–621.

    Google Scholar 

  • Moore, D. M. &H. Lewis. 1965. The evolution of self-pollination inClarkia xantiana. Evolution19:104–114.

    Google Scholar 

  • Nakamura, R. R., M. L. Stanton &S. J. Mazer. 1989. Effects of mate size and mate number on male reproductive success in plants. Ecology70:71–76.

    Google Scholar 

  • Niklas, K. J. 1985. The aerodynamics of wind pollination. Bot. Rev. (Lancaster)51: 328–386.

    Google Scholar 

  • Peitgen, H., H. Jurgens &D. Saupe. 1992. Chaos and fractals, new frontiers of science. Springer-Verlag, New York.

    Google Scholar 

  • Pendleton, R., E. D. McArthur, A. C. Blauer &D. C. Freeman. 1989. Heterodichogamy inGrayia brandegii. Amer. J. Bot.75:267–274.

    Google Scholar 

  • Ramadan, A. A., A. El-Keblawy, K. H. Shaltout &J. Lovett Doust 1994. Sexual polymorphism, growth and reproductive effort in EgyptianThymelaea hirsuta (Thymelaeaceae). Amer. J. Bot.81:847–857.

    Google Scholar 

  • Reinartz, J. A. &D. H. Les. 1994. Bottleneck-induced dissolution of self-incompatibility and breeding system consequences inAster furcatus. Amer. J. Bot.81:446–455.

    Google Scholar 

  • Renner, S. S. &R. E. Ricklefs. 1995. Dioecy and its correlates in the flowering plants. Amer. J. Bot.82:596–606.

    Google Scholar 

  • Rick, C. M., M. Holle &R. W. Thorp. 1978. Rates of cross pollination inLycopersicon pimpinellifolium. Impact of genetic variation in floral characters. Pl. Syst. Evol.129:31–44.

    Google Scholar 

  • Ritland, C. &K. Ritland. 1989. Variation of sex allocation among eight taxa of theMimulus guttatus species complex (Scrophulariaceae). Amer. J. Bot.76:1731–1739.

    Google Scholar 

  • Ross, M. D. 1970. Evolution of dioecy from gynodioecy. Evolution30:425–441.

    Google Scholar 

  • —. 1982. Five evolutionary pathways to subdioecy. Amer. Naturalist119:297–318.

    Google Scholar 

  • — &R. F. Shaw. 1971. Maintenance of male sterility in plant populations. Heredity26:1–8.

    Google Scholar 

  • Schaffner, J. H. 1925. Experiments with various plants to produce change of sex in the individual. Bull. Torrey Bot. Club52:35–47.

    Google Scholar 

  • Shaw, R. F. &J. D. Mohler. 1953. The selective advantage of the sex ratio. Amer. Naturalist87:337–342.

    Google Scholar 

  • Shea, M. M., P. M. Dixon &R. R. Sharitz. 1993. Size differences, sex ratio, and spatial distribution of male and female water tupelo,Nyssa aquatica (Nyssaceae). Amer. J. Bot.80:26–30.

    Google Scholar 

  • Shmida, A. & H. Leschner. In review. About humble females and dandy males: Why do old red crown anemones have a white ring?

  • Shoen, D. J. 1982. The breeding system ofGilia achilleifolia: Variation in floral characteristics and outcrossing rate. Evolution36:352–360.

    Google Scholar 

  • Smith, B. N. 1982. General characteristics of terrestrial plants (agronomic and forests)—C3, C4 and Crassulacean acid metabolism plants. Pages 99–118in O. R. Zaborsky (ed.), CRC handbook of biosolar resources. Vol. 1. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Solomon, B. P. 1985. Environmentally influenced changes in sex expression in an andromonoecious plant. Ecology66:1321–1223.

    Google Scholar 

  • Snow, A. 1994. Postpollination selection and male fitness in plants. Amer. Naturalist144(Suppl.):S69-S83.

    Google Scholar 

  • Stebbins, G. L. 1974. Flowering plants: Evolution above the species level. Harvard University Press, Cambridge.

    Google Scholar 

  • Sutherland, S. &L. F. Delph. 1984. On the importance of male fitness in plants: Patterns of fruit-set. Ecology65:1093–1104.

    Google Scholar 

  • Takhtajan, A. L. 1980. Outline of the classification of flowering plants (Magnoliophyta). Bot. Rev. (Lancaster)46:225–359.

    Google Scholar 

  • Thomas, S. M. &B. G. Murray. 1981. Breeding systems and hybridization inPetrorhagia sect.Kohlrauschia (Caryophyllaceae). Pl. Syst. Evol.139:77–94.

    Google Scholar 

  • Tiedemann, A. R., E. D. McArthur &D. C. Freeman. 1987. Variation in physiological metabolites and chlorophyll in sexual phenotypes of “Rincon” fourwing saltbush. J. Range Managern.40:151–155.

    Google Scholar 

  • Vasek, F. C. 1977. Phenotypic variation and adaptation inClarkia sectionPhaeostoma. Syst. Bot.2:251–279.

    Google Scholar 

  • Vitale, J. J. &D. C. Freeman. 1985. Secondary sex characteristics inSpinacia oleracea L.: Quantitative evidence for the existence of at least three sexual morphs. Amer. J. Bot.72:1061–1066.

    Google Scholar 

  • ——. 1986. Partial niche separation inSpinacia oleracea L.: An examination of reproductive allocation. Evolution40:426–430.

    Google Scholar 

  • ——,L. Merlotti &M. Delassandro. 1987. Resource allocation inSpinacia oleracea. Amer. J. Bot.74:1049–1054.

    Google Scholar 

  • Wachocki, B. A. 1992. Maternal effects on sex ratio and sex expression in spinach. Ph.D. dissertation, Wayne State University, Detroit.

    Google Scholar 

  • Warner, R. R., D. R. Robertson &E. G. Leigh. 1975. Sex change and sexual selection. Science190:633–638.

    PubMed  CAS  Google Scholar 

  • Watson, M. 1995. Sexual differences in plant developmental phenology affect plant-herbivore interactions. Tree10:180–182.

    Google Scholar 

  • Welkie, G.W. &M. Caldwell. 1970. Leaf anatomy of species in some dicotyledon families as related to the C3 and C4 pathways of carbon fixation. Canad. J. Bot.48:2135–2146.

    Google Scholar 

  • Weller, S. G. &R. Ornduff. 1977. Cryptic self-incompatibility inAmsinckia grandiflora. Evolution31:47–51.

    Google Scholar 

  • Westergaard, M. 1958. The mechanisms of sex determination in dioecious flowering plants. Adv. Genet.9:217–281.

    PubMed  CAS  Google Scholar 

  • Willson, M. F. 1979. Sexual selection in plants. Amer. Naturalist113: 777–790.

    Google Scholar 

  • —. 1983. Plant reproductive ecology. John Wiley, New York.

    Google Scholar 

  • —. 1994. Sexual selection in plants: Perspective and overview. Amer. Naturalist144(Suppl.):S13-S39.

    Google Scholar 

  • — &P. W. Price. 1977. The evolution of inflorescence size inAsclepias (Asclepiadaceae). Evolution31:495–511.

    Google Scholar 

  • Wolfe, L. M. &A. Shmida. 1996. Regulation of gender and flowering behavior in a sexually dimorphic desert shrub (Ochradenus baccatus ssp.delete (Resedaceae)). Israel J. Pl. Sci.43: 325–337.

    Google Scholar 

  • Wyatt, R. 1982. Inflorescence architecture: How flower number, arrangement and phenology affect pollination and fruit set. Amer. J. Bot.69:585–594.

    Google Scholar 

  • Yeo, P. F. 1975. Some aspects of heterostyly. New Phytol.75:147–153.

    Google Scholar 

  • Yin, T. &J. A. Quinn. 1992. A mechanistic model of a single hormone regulating both sexes in flowering plants. Bull. Torrey Bot. Club119:431–441.

    Google Scholar 

  • ——. 1994. Effects of exogenous growth regulators and a gibberellin inhibitor on the sex expression and growth form of buffalograss (Buchloe dactyloides) and their ecological significance. Bull. Torrey Bot. Club1221:170–179.

    Google Scholar 

  • ——. 1995. Tests of a mechanistic model of one hormone regulating both sexes inBuchloe dactyloides (Poaceae). Amer. J. Bot.82:745–751.

    Google Scholar 

  • Zaharan, M. A. &A. J. Willis. 1992. The vegetation of Egypt. Chapman & Hall, London.

    Google Scholar 

  • Zimmerman, J. K. &M. J. Lechowicz. 1982. Responses to moisture stress in male and female plants ofRumex acetosella L. (Polygonaceae). Oecologia53:305–309.

    Google Scholar 

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Freeman, D.C., Doust, J.L., El-Keblawy, A. et al. Sexual specialization and inbreeding avoidance in the evolution of dioecy. Bot. Rev 63, 65–92 (1997). https://doi.org/10.1007/BF02857918

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