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Biased Sex Ratios in Plants: Theory and Trends

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Abstract

This paper examines the history of sex ratio theory and the effects of multiple variables on individual and population sex ratios. It also provides examples where plants have been used to test major predictions of sex ratio theory. Then, using over 200 studies from the literature, dioecious plant species are categorized based on their life form, pollination agent, fruit dispersal agent, and sex ratio. A loglinear analysis is used to look at possible correlations between the sex ratio of a population and other life history characteristics. These data are used to examine the predictions made by De Jong et al. (Journal of Evolutionary Biology 15:7, 2002), that relative pollen and seed dispersal distances can be used to predict sex ratio bias. Despite the limited sample size, strong relationships are still observed. 93% of insect pollinated dioecious vines that have biotically dispersed fruit have male-biased sex ratios. Conversely, 61% of shrubs that are wind pollinated and have abiotic fruit dispersal have female-biased sex ratios.

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Literature Cited

  • Ainsworth, C. 2000. Boys and girls come out to play: The molecular biology of dioecious plants. Annals of Botany 86: 211–221.

    Article  Google Scholar 

  • Allen, Ga. J. A. A. 1993. Sex ratio variation in the dioecious shrub Oemleria Cerasiformis. The American Naturalist 141: 17.

    Article  Google Scholar 

  • Antos, J. A. & G. A. Allen. 1990. A comparison of reproductive effort in the dioecious shrub Oemleria cerasiformis using nitrogen, energy and biomass as currencies. American Midland Naturalist 124: 9.

    Article  Google Scholar 

  • Armstrong, J. E. & A. K. Irvine. 1989. Flowering, sex ratios, pollen-ovule ratios, fruit set, and reproductive effort of a dioecious tree, Myristica insipida (Myristicaceae), in two different rain forest communities. American Journal of Botany 76: 12.

    Google Scholar 

  • Arnbom, T., M. A. Fedak & P. Rothery. 1994. Offspring sex ratio in relation to female size in southern elephant seals, Mirounga leonina. Behavioral Ecology and Sociobiology 35: 6.

    Article  Google Scholar 

  • Ashman, T. L. 1994. A dynamic perspective on the physiological cost of reproduction in plants. The American Naturalist 144: 17.

    Article  Google Scholar 

  • Augspurger, C. K. & K. P. Hogan. 1983. Wind dispersal of fruits with variable seed number in a tropical tree (Lonchocarpus pentaphyllus: Leguminosae). Botanical Journal of Botany 70: 7.

    Google Scholar 

  • Bailey, M. F. & D. E. McCauley. 2005. Offspring sex ratio under inbreeding and outbreeding in a gynodioecious plant. Evolution 59: 9.

    Google Scholar 

  • Barlow, B. A. & D. Wiens. 1976. Translocation heterozygosity and sex ratio in Viscum fischeri. Heredity 37: 27–40.

    Article  Google Scholar 

  • Bawa, K. S. 1980. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11: 15–39.

    Article  Google Scholar 

  • Berger, A. 1985. Seed dimorphism and germination behaviour in Salicornia patula. Plant Ecology 61: 7.

    Google Scholar 

  • Bertin RaCN. 1993. Dicogamy in angiosperms. The Botanical Review 59: 41

  • Bickel AaDCF. 1993. Effects of pollen vector and plant geometry on floral sex ratio in monoecious plants. American Midland Naturalist 130: 9.

  • Bierzychudek, P. & V. Eckhart. 1988. Spatial segregation of the sexes of dioecious plants. The American Naturalist 132: 34.

    Article  Google Scholar 

  • Bittencourt, J. V. M. & A. M. Sebbenn. 2007. Patterns of pollen and seed dispersal in a small, fragmented population of the wind-pollinated tree Araucaria angustifolia in southern Brazil. Heredity 99: 580–591.

    Article  PubMed  CAS  Google Scholar 

  • Cain, M. L., H. Damman & A. Muir. 1998. Seed dispersal and the holocene migration of woodland herbs. Ecological Monographs 63: 27.

    Google Scholar 

  • Charlesworth, B. & D. Charlesworth. 1987a. The effect of investment in attractive structures on allocation to male and female functions in plants. Evolution 41: 21.

    Article  Google Scholar 

  • ———, ———. 1987b. Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst. 18:32

    Article  Google Scholar 

  • ———, ———, Marais G. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118–128.

    Article  PubMed  CAS  Google Scholar 

  • Charnov BBCaEL. 1982a. Sex allocation in heterostylous plants.

  • Charnov E. 1982b. The theory of sex allocation. Princeton University Press.

  • Charnov, E. L. & J. Bull. 1977. When is sex environmentally determined? Nature 266: 828–830.

    Article  PubMed  CAS  Google Scholar 

  • Clark, C. J., J. R. Poulsen, B. M. Bolker, E. F. Connor & V. T. Parker. 2005. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 86: 11.

    Google Scholar 

  • Cole, S. 1979. Aberrant sex ratios in Joyoba associated with environmental factors. Desert Plants 1: 4.

    Google Scholar 

  • Correns, C. 1928. Bestimmung, Vererbung und Verteilung des Geschlechtes bei den hoheren Pflanzen. Handbuch der Vererbungswissen-schaft, Borntraeger, Berlin.

    Google Scholar 

  • Davey AaCG. 1917. Note on the distribution of sexes in Myrica gale. New Phytologist 16: 6.

  • Dawson TE. 1993. Gender-specific physiology, carbon isotope discrimination, and habitat distribution in Boxelder, Acer Negundo. Ecology.

  • ———, Bliss L. 1989. Patterns of water use and the tissue water relations in the dioecious shrub, Salix arctica: The physiological basis for habitat partitioning between the sexes. Oecologia 79: 12.

    Google Scholar 

  • De Jong, T., F. V. Batenburg & J. V. Dijk. 2002. Seed sex ratio in dioecious plants depends on relative dispersal of pollen and seeds: an example using a chessboard simulation model. Journal of Evolutionary Biology 15: 7.

    Google Scholar 

  • Delph, L. F. 1990. Sex-differential resource allocation patterns in the subdioecious shrub hebe subalpina. Ecology 71: 1342–1351.

    Article  Google Scholar 

  • Dick, C., G. Etchelecu & F. Austerlitz. 2003. Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology 12: 11.

    Article  Google Scholar 

  • Dodson, C. 1962. Pollination and variation in the subtribe Catasetinae (Orchidaceae). Annals of the Missouri Botanical Garden 49: 23.

    Article  Google Scholar 

  • Eppley, S. M. 2001. Gender-specific selection during early life history stages in the dioecious grass Distichlis spicata. Ecology 82: 2022–2031.

    Google Scholar 

  • Fisher RA. 1930. The genetical theory of natural selection. Oxford University Press.

  • Freeman DC, McArthur ED. 1982. Notes: A comparison of twig water stress between males and females of six species of desert shrubs. Forest Science 28: 5.

    Google Scholar 

  • ———, ———. 1984. The relative influences of mortality, nonflowering, and sex change on the sex ratios of six atriplex species. Botanical Gazette 145: 10.

    Google Scholar 

  • ———, Vitale J. 1985. The influence of environment on the sex ratio and fitness of spinach. Botanical Gazette 146: 6.

    Article  Google Scholar 

  • ———, Klikoff LG, Harper KT. 1976. Differential Resource Utilization by the Sexes of Dioecious Plants. Science 193: 597–599.

    Article  PubMed  CAS  Google Scholar 

  • ———, Harper KT, Charnov EL. 1980. Sex change in plants: Old and new observations and new hypotheses. Oecologia 47: 11.

    Article  Google Scholar 

  • ———, McArthur ED, Harper KT. 1984. The adaptive significance of sexual lability in plants using atriplex canescens as a principal example. Annals of the Missouri Botanical Garden 71: 13.

    Article  Google Scholar 

  • ———, Wachocki BA, Stendler MJ, Goldschlag DE, Michaels HJ. 1994. Seed size and sex ratio in spinach: Application of the Trivers-Williard hypothesis to plants. EcoScience.

  • Gardocki ME. 2000. Heterocarpy in Calendula micrantha (Asteraceae): The effects of competition and availability of water on the performance of offspring from different fruit morphs. Evolutionary Ecology Research.

  • Ghiselin, M. T. 1969. The evolution of hermaphroditism among animals. The Quarterly Review of Biology 44: 189.

    Article  PubMed  CAS  Google Scholar 

  • Grant MaJM. 1979. Elevational gradients in adult sex ratios and sexual differentiation in vegetative growth rates of Populus tremuloides Michx. Evolution 33: 5.

  • Grant, S., et al. 1994. Genetics of sex determination in flowering plants. Developmental Genetics 15: 214–230.

    Article  Google Scholar 

  • Gregg, K. 1975. The effect of light intensity on sex expression in species of Cycnoches and Catasetum. Selbyana 1: 13.

    Google Scholar 

  • Gross, K. L. & J. D. Soule. 1981. Differences in biomass allocation to reproductive and vegetative structures of male and female plants of a dioecious, perennial herb, Silene alba (Miller) Krause. American Journal of Botany 68: 7.

    Article  Google Scholar 

  • Hamilton WD. 1967. Extradorinary sex ratios. Science.

  • Horvitz, C. C. & D. W. Schemske. 1988. Demographic cost of reproduction in a neotropical herb: An experimental field study. Ecology 69: 1741–1745.

    Article  Google Scholar 

  • Husband BaD & D. W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 17.

  • Janzen, D. H. 1971. Euglossine bees as long-distance pollinators of tropical plants. Science 171: 203–205.

    Article  PubMed  CAS  Google Scholar 

  • Jordano, P., C. García, J. A. Godoy & J. L. García-Castaño. 2007. Differential contribution of frugivores to complex seed dispersal patterns. Proceedings of the National Academy of Sciences 104: 3278–3282.

    Article  CAS  Google Scholar 

  • Kennedy, J. J. 1992. Analyzing qualitative data: Log-linear analysis for behavioral research, ed. 2nd. Praeger Publishers, New York.

    Google Scholar 

  • Korpelainen H. 1992. Patterns of resource allocation in male and female plants of Rumex acetosa and R. actosella. Oecologia.

  • ———. 1993. Phenological differentiation between the populations and sexes in the perennial species Rumex acetosa. Oecologica 14: 11.

    Google Scholar 

  • ———. 1998. Labile sex expression in plants. Biological Reviews 73: 157–180.

    Article  Google Scholar 

  • Lavigne, C., E. K. Klein, P. Vallée, J. Pierre, B. Godelle & M. Godelle. 1998. A pollen-dispersal experiment with transgenic oilseed rape. Estimation of the average pollen dispersal of an individual plant within a field. TAG Theoretical and Applied Genetics 96: 886–896.

    Article  Google Scholar 

  • Leigh, E. G. J., E. L. Charnov & R. R. Warner. 1976. Sex ratio, sex change, and natural selection. PNAS 73: 5.

    Article  Google Scholar 

  • Levins R. 1968. Evolution in changing environments. Princeton University Press.

  • Liu, Z., et al. 2004. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427: 348–352.

    Article  PubMed  CAS  Google Scholar 

  • Lloyd DGaCJW. 1977. Secondary sex characteristics in plants. Botanical Review 43: 40.

  • Lovett Doust, J. & P. B. Cavers. 1982. Sex and gender dynamics in Jack-in-the-Pulpit, Arisaema Triphyllum (Araceae). Ecology 63: 797–808.

    Article  Google Scholar 

  • Lysova, N. & N. I. Khizhnyak. 1975. Sex differences in trees in the dry steppe. Soviet Journal of Ecology 6: 6.

    Google Scholar 

  • McArthur, E. D. 1977. Environmentally induced changes of sex expression in Atriplex canescens. Heredity 38: 6.

    Article  Google Scholar 

  • ———, Freeman DC. 1982. Sex expression in atriplex canescens: genetics and environment. Botanical Gazette 143: 7.

    Google Scholar 

  • ———, ———, Luckinbill LS, Sanderson SC, Noller GL. 1992. Are trioecy and sexual lability in atriplex canescens genetically based?: Evidence from clonal studies. Evolution 46: 14.

    Article  Google Scholar 

  • McLetchie, D. N. 1992. Sex ratio from germination through maturity and its reproductive consequences in the liverwort Sphaerocarpos texanus. Oecologia 92: 6.

    Article  Google Scholar 

  • Meagher, T. R. 1980. The population biology of Chamaelirium luteum, a dioecious lily I, spatial distributions of males and females. Evolution 34: 11.

    Article  Google Scholar 

  • ———. 1981. Population biology of Chamaelirium luteum, a dioecious lily. II. Mechanisms governing sex ratios. Evolution 35: 11.

    Article  Google Scholar 

  • ———. 1988. Sex determination in plants. In: Plant reproductive ecology patterns and strategies--Doust JL, Doust LL, eds. (New York, New York: Oxford University Press.

    Google Scholar 

  • ———. 2007. Linking the evolution of gender variation to floral development. Annals of Botany 100: 12.

    Article  Google Scholar 

  • Nicklas, K. 1985. The aerodynamics of wind pollination. The Botanical Review 51: 59.

    Google Scholar 

  • Nicotra, A. B. 1998. Sex ratio variation and spatial distribution of Siparuna grandiflora, a tropical dioecious shrub. Oecologia 115: 11.

    Article  Google Scholar 

  • Obeso, J. R. 2002. The costs of reproduction in plants. New Phytologist 155: 321–348.

    Article  Google Scholar 

  • Pannell, J. 1997. Mixed genetic and environmental sex determination in an androdioecious population of Mercurialis annua. Heredity 78: 50–56.

    Article  PubMed  CAS  Google Scholar 

  • Policansky, D. 1981. Sex choice and the size advantage model in jack-in-the-pulpit (Arisaema triphyllum). Proceedings of the National Academy of Sciences of the United States of America 78: 1306–1308.

    Article  PubMed  CAS  Google Scholar 

  • Purrington, C. B. 1993. Parental effects on progeny sex ratio, emergence, and flowering in Silene Latifolia (Caryophyllaceae). Journal of Ecology 81: 807–811.

    Article  Google Scholar 

  • Queenborough, S. A., D. F. R. P. Burslem, N. C. Garwood & R. Valencia. 2007. Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 88: 2248–2258.

    Article  PubMed  Google Scholar 

  • Redondo-Gomez, S., E. Mateos-Naranjo, J. Cambrolle, T. Luque, M. E. Figueroa & A. J. Davy. 2008. Carry-over of differential salt tolerance in plants grown from dimorphic seeds of suaeda splendens. Ann Bot 102: 103–112.

    Article  PubMed  Google Scholar 

  • Renner, S. & R. Ricklefs. 1995. Dioecy and its correlates in the flowering plants. American Journal of Botany 82: 10.

    Article  Google Scholar 

  • Reznick, D. 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44: 11.

    Article  Google Scholar 

  • Richards, A. 1975. Notes on the sex and age of Potentilla fruticosa L. in upper Teasdale. Trans. Nat. Hist. Soc. Northhumbria 42: 7.

    Google Scholar 

  • Robledo-Arnuncio, J. J. & L. Gil. 2004. Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total-exclusion paternity analysis. Heredity 94: 13–22.

    Article  Google Scholar 

  • Sather DN, Jovanovic M, Golenberg E. 2010. Functional analysis of B and C class floral organ genes in spinach demonstrates their role in sexual dimorphism http://www.biomedcentral.com/1471-2229/10/46 (accessed 46, 10) (Type of Medium).

  • Shaw, R. F. & J. D. Mohler. 1953. The selective significance of the sex ratio. The American Naturalist 87: 337.

    Article  Google Scholar 

  • Smith, C. A. & W. E. Evenson. 1978. Energy distribution in reproductive structures of amaryllis. American Journal of Botany 65: 3.

    Google Scholar 

  • Sork, V. L., et al. 2002. Pollen movement in declining populations of California Valley oak, Quercus lobata: Where have all the fathers gone? Molecular Ecology 11: 1657–1668.

    Article  PubMed  CAS  Google Scholar 

  • Sprengel, C. 1793. Das entdeckte Geheimniss der Natur im Bau und un der Befruchtung der Blumen. Vieweg, Berlin.

    Book  Google Scholar 

  • Stacy, E. A., J. L. Hamrick, J. D. Nason, S. P. Hubbell, R. B. Foster & R. Condit. 1996. Pollen dispersal in low-density populaitons of three neotropical tree species. The American Naturalist 148: 24.

    Article  Google Scholar 

  • Stout, A. 1928. Dichogamy in flowering plants. Bulletin of the Torrey Botanical Club 55: 13.

    Article  Google Scholar 

  • Taylor, D. R., M. J. Saur & E. Adams. 1999. Pollen performance and sex-ratio evolution in a dioecious plant. Evolution 53: 9.

    Google Scholar 

  • Telenius, A. & P. Torstensson. 1988. The seed dimorphism of Spergularia marina in relation to dispersal by wind and water. Oecologia 80: 5.

    Google Scholar 

  • Tiedemann, A. R., E. D. McArthur & D. C. Freeman. 1987. Variations in physiological metabolites and chlorophyll in sexual phenotypes of ‘Rincon’ fourwing saltbrush. Journal of Range Management 40: 5.

    Google Scholar 

  • Tonsor, S. 1985. Leptokurtic pollen-flow, non-leptokurtic gene-flow in a wind-pollinated herb. Oecologia 67: 5.

    Article  Google Scholar 

  • Trivers, R. L. & D. E. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90–92.

    Article  PubMed  CAS  Google Scholar 

  • Vernet, P. 1971. La proportion des sexes chez Asparagus acutifolius. L. Bull. Soc. Bot. Fr. 118: 14.

    Google Scholar 

  • Vitale, J. J., D. C. Freeman, L. A. Merlotti & M. D'Alessandro. 1987. Patterns of biomass allocation in Spinacia oleraceae (Chenopodiaceae) across a salinity gradient: Evidence for a niche separation. American Journal of Botany 74: 6.

    Article  Google Scholar 

  • Wallace CS, Rundel PW. 1979. Sexual dimorphism and resource allocation in male and female shrubs of simmondsia chinensis. Oecologia.

  • Wang, L., Z. Huang, C. C. Baskin, J. M. Baskin & M. Dong. 2008. Germination of dimorphic seeds of the desert annual halophyte Suaeda aralocaspica (Chenopodiaceae), a C4 plant without Kranz Anatomy. Ann Bot 102: 757–769.

    Article  PubMed  Google Scholar 

  • Waser, N. 1984. Sex ratio variation in populations of a dioecious desert perennial, Simmondsia chinensis. Oikos 42: 6.

    Article  Google Scholar 

  • Webb, C. J. & K. S. Bawa. 1983. Pollen dispersal by hummingbirds and butterflies: A comparative study of two lowland troopical plants. Evolution 37: 13.

    Article  Google Scholar 

  • Westcott, D. A. & D. L. Graham. 2000. Patterns of movement and seed dispersal of a tropical frugivore. Oecologia 122: 249–257.

    Article  Google Scholar 

  • Widén, B. & M. Widén. 1990. Pollen limitation and distance-dependent fecundity in females of the clonal gynodioecious herb Glechoma hederacea (Lamiaceae). Oecologia 83: 191–196.

    Article  PubMed  Google Scholar 

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  1. Biological Sciences, Wayne State University, Detroit, MI, 48208, USA

    Jordan P. Sinclair & D. C. Freeman

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  1. Jordan P. Sinclair
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  2. J. Emlen
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Correspondence to Jordan P. Sinclair.

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Sinclair, J.P., Emlen, J. & Freeman, D.C. Biased Sex Ratios in Plants: Theory and Trends. Bot. Rev. 78, 63–86 (2012). https://doi.org/10.1007/s12229-011-9065-0

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