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The loss of sex in clonal plants

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Abstract

Most plants combine sexual and clonal reproduction, and the balance between the two may vary widely between and within species. There are many anecdotal reports of plants that appear to have abandoned sex for clonal reproduction, yet few studies have quantified the degree of sexual variation in clonal plants and fewer still have determined the underlying ecological and/or genetic factors. Recent empirical work has shown that some clonal plants exhibit very wide variation in sexual reproduction that translates into striking variation in genotypic diversity and differentiation of natural populations. Reduced sexual reproduction may be particularly common at the geographical margins of species' ranges. Although seed production and sexual recruitment may often be limited by biotic and abiotic aspects of the environment in marginal populations, genetic factors, including changes in ploidy and sterility mutations, may also play a significant role in causing reduced sexual fertility. Moreover, environmental suppression of sexual recruitment may facilitate the evolution of genetic sterility because natural selection no longer strongly maintains the many traits involved in sex. In addition to the accumulation of ‘neutral’ sterility mutations in highly clonal populations, the evolution of genetic infertility may be facilitated if sterility is associated with enhanced vegetative growth, clonal propagation or survival through either resource reallocation or pleiotropy. However, there are almost no experimental data with which to distinguish among these possibilities. Ultimately, wide variation in genotypic diversity and gene flow associated with the loss of sex may constrain local adaptation and the evolution of the geographical range limit in clonal plants.

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References

  • Abrahamson, W.G. (1980) Demography and vegetative reproduction. In O.T. Solbrig (ed.) Demography and Evolution in Plant Populations. Blackwell, Oxford, UK, pp. 89-106.

    Google Scholar 

  • Ashton, P.J. and Mitchell, D.S. (1989) Aquatic plants: Patterns and modes of invasion, attributes of invading species and assessment of control programs. In J.A. Drake, H.A. Mooney, F. Di Castri, R.H. Groves, F.J. Kruger, M. Rejmánek and M.H. Williamson (eds) Biological Invasions: A Global Perspective. John Wiley & Sons Ltd., London, UK, pp. 111-154.

    Google Scholar 

  • Aspinwall, N. and Christian, T. (1992) Clonal structure, genotypic diversity, and seed production in populations of Filipendula rubra (Rosaceae) from the northcentral United States. Amer. J. Bot. 79, 294-299.

    Google Scholar 

  • Baker, H.G. (1965) Characteristics and modes of origins of weeds. In H.G. Baker and G.L. Stebbins (eds) The Genetics of Colonizing Species. Academic Press, New York, NY, USA, pp. 147-172.

    Google Scholar 

  • Barrett, S.C.H. (1980a) Sexual reproduction in Eichhornia crassipes (water hyacinth). II. Seed production in natural populations. J. Appl. Ecol. 17, 113-124.

    Google Scholar 

  • Barrett, S.C.H. (1980b) Sexual reproduction in Eichhornia crassipes (water hyacinth). I. Fertility of clones from diverse regions. J. Appl. Ecol. 17, 101-112.

    Google Scholar 

  • Barrett, S.C.H., Eckert, C.G. and Husband, B.C. (1993) Evolutionary processes in aquatic plants. Aquatic Bot. 44, 105-145.

    Google Scholar 

  • Bhardwaj, M. and Eckert, C.G. (2001) Functional analysis of synchronous dichogamy in flowering rush, Butomus umbellatus (Butomaceae). Amer. J. Bot. 88, 2204-2213.

    Google Scholar 

  • Bierzychudek, P. (1987) Patterns in plant parthenogenesis. In S.C. Stearns (ed.) The Evolution of Sex and its Consequences. Birkhäuser Verlag, Basel, Switzerland, pp. 197-217.

    Google Scholar 

  • Brace, C.L. (1963) Structural reduction in evolution. Amer. Nat. 97, 39-49.

    Google Scholar 

  • Byers, D.L. and Meagher, T.R. (1992) Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68, 353-359.

    Google Scholar 

  • Case, T.J. and Taper, M.L. (2000) Interspecific competition, environmental gradients, gene flow, and the coevolution of species' borders. Amer. Nat. 155, 583-605.

    Google Scholar 

  • Caughley, G., Grice, D., Barker, R. and Brown, B. (1988) The edge of the range. J. Anim. Ecol. 57, 771-785.

    Google Scholar 

  • Charpentier, A., Grillas, P. and Thompson, J.D. (2000) The effect of population size limitation on fecundity in mosaic populations of the clonal macrophyte Scirpus maritimus (Cyperaceae). Amer. J. Bot. 87, 502-507.

    Google Scholar 

  • Culver, D.C. (1982) Cave Life: Evolution and Ecology. Harvard University Press, Cambridge, MA, USA.

    Google Scholar 

  • Dorken, M.E. and Eckert, C.G. (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J. Ecol. 89, 339-350.

    Google Scholar 

  • Eckert, C.G. (1999) Clonal plant research: proliferation, integration, but not much evolution. Amer. J. Bot. 86, 1649-1654.

    Google Scholar 

  • Eckert, C.G. (2000) Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology 82, 532-542.

    Google Scholar 

  • Eckert, C.G. and Barrett, S.C.H. (1992) Stochastic loss of style morphs from populations of tristylous Lythrum salicaria and Decodon verticillatus (Lythraceae). Evolution 46, 1014-1029.

    Google Scholar 

  • Eckert, C.G. and Barrett, S.C.H. (1993) Patterns of genotypic diversity and clonal reproduction in Decodon verticillatus (Lythraceae). Amer. J. Bot. 80, 1175-1182.

    Google Scholar 

  • Eckert, C.G. and Barrett, S.C.H. (1995) Style morph ratios in tristylous Decodon verticillatus (Lythraceae): selection versus historical contingency. Ecology 76, 1051-1066.

    Google Scholar 

  • Eckert, C.G., Dorken, M.E. and Mitchell, S.A. (1999) Loss of sex in clonal populations of a flowering plant, Decodon verticillatus (Lythraceae). Evolution 53, 1079-1092.

    Google Scholar 

  • Eckert, C.G., Manicacci, D. and Barrett, S.C.H. (1996) Genetic drift and founder effect in native versus introduced populations of an invading plant, Lythrum salicaria (Lythraceae). Evolution 50, 1512-1519.

    Google Scholar 

  • Eckert, C.G., Massonnet, B. and Thomas, J.J. (2000) Variation in sexual and clonal reproduction among introduced populations of flowering rush, Butomus umbellatus (Butomaceae). Can. J. Bot. 78, 437-446.

    Google Scholar 

  • Ellstrand, N.C. and Roose, K.L. (1987) Patterns of genotypic diversity in clonal plant species. Amer. J. Bot. 74, 123-131.

    Google Scholar 

  • Emerson, A.E. (1961) Vestigial characters of termites and processes of regressive evolution. Evolution 15, 115-131.

    Google Scholar 

  • Eriksson, O. (1989) Seedling dynamics and life histories in clonal plants. Oikos 55, 231-238.

    Google Scholar 

  • Eriksson, O. (1992) Evolution of seed dispersal and recruitment in clonal plants. Oikos 63, 439-448.

    Google Scholar 

  • Eriksson, O. (1996) Regional dynamics of plants: a review of evidence for remnant, source-sink and metapopulations. Oikos 77, 248-258.

    Google Scholar 

  • Fong, D.W., Kane, T.C. and Culver, D.C. (1995) Vestigialization and loss of nonfunctional characters. Ann. Rev. Ecol. Syst. 26, 249-268.

    Google Scholar 

  • Gliddon, C., Belhassen, E. and Gouyon, P.-H. (1987) Genetic neighbourhoods in plants with diverse systems of mating and different patterns of growth. Heredity 59, 29-32.

    Google Scholar 

  • Haldane, J.B.S. (1933) The part played by recurrent mutation in evolution. Amer. Nat. 67, 5-19.

    Google Scholar 

  • Hamrick, J.L. and Godt, M.J. (1990) Allozyme diversity in plant species. In A.H.D. Brown, M.T. Clegg, A.L. Kahler and B.S. Weir (eds) Plant Population Genetics, Breeding, and Genetic Resources. Sinauer, Sunderland, MA, USA, pp. 43-63.

    Google Scholar 

  • Harada, Y., Kawano, S. and Iwasa, Y. (1997) Probability of clonal identity: inferring the relative success of sexual versus clonal reproduction from spatial genetic patterns. J. Ecol. 85, 591-600.

    Google Scholar 

  • Hebert, P.D.N., Ward, R.D. and Weider, L.J. (1988) Clonal-diversity patterns and breeding system variation in Daphnia pulex, an asexual-sexual complex. Evolution 42, 147-159.

    Google Scholar 

  • Holt, R.D. and Keitt, T.H. (2000) Alternative causes for range limits: a metapopulation perspective. Ecology Letters 3, 41-47.

    Google Scholar 

  • Hutchinson, G.E. (1975) A Treatise on Limnology. Volume III. Limnological Botany. John Wiley & Sons, New York, NY, USA.

    Google Scholar 

  • Kirkpatrick, M. and Barton, N.H. (1997) Evolution of a species' range. Amer. Nat. 150, 1-23.

    Google Scholar 

  • Klekowski, E.J. Jr. (1988a) Mutation, Developmental Selection and Plant Evolution. Columbia University Press, New York, NY, USA.

    Google Scholar 

  • Klekowski, E.J. Jr. (1988b) Progressive cross-and self-sterility associated with aging in fern clones and perhaps other plants. Heredity 61, 247-253.

    Google Scholar 

  • Klekowski, E.J. Jr. (1988c) Mechanisms that maintain the genetic integrity of plants. In W. Greuter and B. Zimmer (eds) Proceedings of the XIV International Botanical Congress. Königstein/Taunus, Koeltz, Germany, pp. 137-152.

  • Klekowski, E.J. Jr. (1997) Somatic mutation theory of clonality. In H. de Kroon and J. van Groenendael (eds) The Ecology and Evolution of Clonal Plants. Backhuys, Leiden, The Netherlands, pp. 227-241.

    Google Scholar 

  • Krahulcová, A. and Jarolímová, V. (1993) Ecology of two cytotypes of Butomus umbellatus I. Karyology and breeding. Folia Geobot. Phytotax. 28, 385-411.

    Google Scholar 

  • Kudoh, H., Shibaike, H., Takasu, H., Whigham, D.F. and Kawano, S. (1999) Genet structure and determinants of clonal structure in a temperate deciduous woodland herb, Uvularia perfoliata. J. Ecol. 87, 244-257.

    Google Scholar 

  • Les, D.H. (1991) Genetic diversity in the monoecious hydrophile Ceratophyllum (Ceratophyllaceae). Amer. J. Bot. 78, 1070-1082.

    Google Scholar 

  • Les, D.H. and Philbrick, C.T. (1993) Studies of hybridization and chromosome number variation in aquatic angiosperms: evolutionary implications. Aquat. Bot. 44, 181-228.

    Google Scholar 

  • Levin, D.A. (1983) Polyploidy and novelty in flowering plants. Amer. Nat. 122, 1-25.

    Google Scholar 

  • Lloyd, D.G. and Webb, C.J. (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. N. Zeal. J. Bot. 24, 135-162.

    Google Scholar 

  • Lynch, M. and Ritland, K. (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152, 1753-1766.

    Google Scholar 

  • Lynch, M. and Walsh, B. (1998) Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA, USA.

    Google Scholar 

  • Lynch, M., Bürger, R., Butcher, D. and Gabriel, W. (1993) The mutational meltdown in asexual populations. J. Hered. 84, 339-344.

    Google Scholar 

  • McKee, J. and Richards, A.J. (1996) Variability in seed production and germinability in common reed (Phragmites australis) in Britain and France with respect to climate. New Phytol. 133, 233-243.

    Google Scholar 

  • McLellan, A.J., Prati, D., Kaltz, O. and Schmid, B. (1997) Structure and analysis of phenotypic and genetic variation in clonal plants. In H. de Kroon and J. van Groencndael (eds) The Ecology and Evolution of Clonal Plants. Backhuys Publishers, Leiden, The Netherlands, pp. 185-210.

    Google Scholar 

  • Muirhead, C.A. and Lande, R. (1997) Inbreeding depression under joint selfing, outcrossing, and asexuality. Evolution 51, 1409-1015.

    Google Scholar 

  • Muller, H.J. (1949) The Darwinian and modern conceptions of natural selection. Proc. Am. Philos. Soc. 93, 459-470.

    Google Scholar 

  • Nakamura, T., Suzuki, T. and Kadono, Y. (1998) A comparative study of isoenzyme patterns of Hydrilla verticillata (L.f.) Royle in Japan. J. Plant Res. 111, 581-585.

    Google Scholar 

  • O'Connell, L.M. and Eckert, C.G. (1999) Differentiation in sexuality among populations of Antennaria parlinii (Asteraceae). Int. J. Pl. Sci. 160, 567-575.

    Google Scholar 

  • Olivieri, I. and Gouyon, P. (1997) Evolution of migration rate and other traits. In I.A. Hanski and M.A. Gilpin (eds) Metapopulation Biology. Ecology, Genetics and Evolution. Academic Press, San Diego, CA, USA, pp. 293-323.

    Google Scholar 

  • Orive, M.E. (1993) Effective population size in organisms with complex life-histories. Theor. Pop. Biol. 44, 316-340.

    Google Scholar 

  • Philbrick, C.T. and Les, D.H. (1996) Evolution of aquatic angiosperm reproductive systems. Bioscience 46, 813-826.

    Google Scholar 

  • Pigott, C.D. (1981) Nature of seed sterility and natural regeneration of Tilia cordata at the northern limit in Finland. Ann. Bot. Fennici. 18, 255-263.

    Google Scholar 

  • Pigott, C.D. and Huntley, J.P. (1981) Factors controlling the distribution of Tilia cordata at the northern limit of its geographical range. III. Nature and causes of seed sterility. New Phytol. 87, 817-839.

    Google Scholar 

  • Piquot, Y., Petit, D., Valero, M., Cuguen, J., de Laguerie, P. and Vernet, P. (1998) Variation in sexual and asexual reproduction among young and old populations of the perennial macrophyte Sparganium erectum. Oikos 82, 139-148.

    Google Scholar 

  • Piquot, Y., Samitou-Laprade, P., Petit, D., Vernet, P. and Epplen, J.T. (1996) Genotypic diversity revealed by allozymes and oligonucleotide DNA fingerprinting in French populations of the aquatic macrophyte Sparganium erectum. Mol. Ecol. 5, 251-258.

    Google Scholar 

  • Poulson, T.L. and White, W.B. (1969) The cave environment. Science 165, 971-981.

    Google Scholar 

  • Preston, C.D. and Croft, J.M. (1997) Aquatic Plants in Britain and Ireland. Harley Books, Colchester, UK.

    Google Scholar 

  • Preuss, D. (1995) Being fruitful: genetics of reproduction in Arabidopsis. Tr. Genet. 11, 147-153.

    Google Scholar 

  • Prout, T. (1964) Observations on structural reduction in evolution. Amer. Nat. 98, 239-249.

    Google Scholar 

  • Regal, P.J. (1977) Evolutionary loss of useless features: is it molecular noise suppression? Amer. Nat. 111, 123-133.

    Google Scholar 

  • Reinartz, J.A. and Les, D.H. (1994) Bottleneck-induced dissolution of self-incompatibility and breeding system consequences in Aster furcatus (Asteraceac). Amer. J. Bot. 81, 446-455.

    Google Scholar 

  • Reusch, T.B.H., Hukriede, W., Stam, W.T. and Olsen, J.L. (1999) Differentiating between clonal growth and limited gene flow using spatial autocorrelation of microsatellites. Heredity 2, 120-126.

    Google Scholar 

  • Richards, A.J. (1986) Plant Breeding Systems. George Allen & Unwin, London, UK.

    Google Scholar 

  • Salisbury, E.J. (1942) The Reproductive Capacity of Plants. Bell, London, UK.

    Google Scholar 

  • Schmid, B. (1990) Some ecological and evolutionary consequences of modular organization and clonal growth in plants. Evol. Trends Plants 4, 25-34.

    Google Scholar 

  • Sculthorpe, C.D. (1967) The Biology of Aquatic Vascular Plants. Edward Arnold, London, UK.

    Google Scholar 

  • Silander, J.A. Jr. (1985) Microevolution in clonal plants. In J.B.C. Jackson, L.W. Buss and R.E. Cook (eds) Population Biology and Evolution of Clonal Organisms. Yale University Press, London, UK, pp. 107-152.

    Google Scholar 

  • Smouse, P.E. and Peakall, R. (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 5, 561-573.

    Google Scholar 

  • Soltis, D.E., Soltis, P.S. and Noyes, R.D. (1988) An electrophoretic investigation of intragametophytic selfing in Equisetum arvense. Amer. J. Bot. 75, 231-237.

    Google Scholar 

  • Starfinger, U. and Stöcklin, J. (1996) Seed, pollen, and clonal dispersal and their role in structuring plants populations. Prog. Bot. 57, 336-355.

    Google Scholar 

  • Stebbins, G.L. (1971) Chromosomal Evolution in Higher Plants. Edward Arnold, London, UK.

    Google Scholar 

  • Suda, Y. (1995) Differentiation of Adonis L. in Japan IV. Floral characters. Acta Phytotax. Geobot. 46, 29-46.

    Google Scholar 

  • Verkleij, J.A.C., Pieterse, A.H., Horneman, G.J.T. and Torenbeek, M. (1983) A comparative study of morphology and isoenzyme patterns of Hydrilla verticillata (L. f.) Royle. Aquatic Bot. 17, 43-59.

    Google Scholar 

  • Vuorisalo, T., Tuomi, J., Pederson, B. and Käär, P. (1997) Hierarchical selection in clonal plants. In H. de Kroon and J. van Groenendael (eds) The Ecology and Evolution of Clonal Plants. Backhuys, Leiden, The Netherlands, pp. 243-261.

    Google Scholar 

  • Watkinson, A.R. and Powell, J.C. (1993) Seedling recruitment and the maintenance of clonal diversity in plant populations: A computer simulation of Ranunculus repens. J. Ecol. 81, 707-717.

    Google Scholar 

  • Widén, B., Cronberg, N. and Widén, M. (1994) Genotypic diversity, molecular markers and spatial distribution of genets in clonal plants. In L. Soukupová, C. Marshall, T. Hara and T. Herben (eds) Plant Clonality, Biology and Diversity. Opulus Press, Uppsala, Sweden, pp. 139-157.

    Google Scholar 

  • Wilkens, H. (1988) Evolution and genetics of epigean and cave Astynax fasciatus (Characidae, Pisces), Support for the neutral mutation theory. Evol. Biol. 23, 271-367.

    Google Scholar 

  • Woodward, F.I. (1990) The impact of low temperatures in controlling the geographic distributions of plants. Phil. Trans. Roy. Soc. London B 326, 585-593.

    Google Scholar 

  • Wright, S. (1964) Pleiotropy in the evolution of structural reduction and of dominance. Amer. Nat. 98, 65-69.

    Google Scholar 

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  1. Department of Biology, Queen's University, Kingston, Ontario, Canada, K7L 3N6

    Christopher G. Eckert

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Eckert, C.G. The loss of sex in clonal plants. Evolutionary Ecology 15, 501–520 (2001). https://doi.org/10.1023/A:1016005519651

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