Skip to main content
Log in

The cleistogamous breeding system: A review of its frequency, evolution, and ecology in angiosperms

  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

Cleistogamy, a breeding system in which permanently closed, self-pollinated flowers are produced, has received increasing attention in recent years, but the last comprehensive review of this system was over 20 years ago. The goal of this paper is to clarify the different types of cleistogamy, quantify the number of families, genera, and species in which cleistogamy occurs, and estimate the number of times and potential reasons why cleistogamy has evolved within angiosperms. Cleistogamous species were identified through a literature survey using 13 online databases with references dating back to 1914; only those species well-supported by floral descriptions or empirical data were included in the data set. On the basis of this survey, we suggest the use of three different categories of cleistogamy in future studies: dimorphic, complete, and induced. Based on these categories, cleistogamy in general is present in 693 angiosperm species, distributed over 228 genera and 50 families. When analyzed on a family level across the angiosperms, the breeding system has evolved approximately 34 to 41 times. Theoretical investigations indicate that the evolution of cleistogamy in taxa may be influenced by the presence of heterogeneous environments, inbreeding depression and geitonogamy, and differential seed dispersal, as well as by various ecological factors and plant size. Cleistogamy will undoubtedly be discovered in additional species as the reproductive biology of more taxa is examined in the future. Such information will be invaluable for understanding the selective pressures and factors favoring the evolution of cleistogamy as well as the evolutionary loss of this breeding system, a subject that has received little attention to date.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature Cited

  • Angiosperm Phylogeny Group. 2003. An update of the Angiosperra Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141: 399–436.

    Article  Google Scholar 

  • Antlfinger, A. E. 1986. Field germination and seedling growth of CH and CL progeny ofImpatiens capensis (Balsaminaceae). Amer. J. Bot. 73:1267–1273.

    Article  Google Scholar 

  • Ballard, H. E. 1994. Violets of Michigan. Michigan Botanist 33:131–199.

    Google Scholar 

  • — &D. E. Wujek. 1994. Evidence for the recognition ofViola appalachiensis. Syst. Bot. 19(4): 523–538.

    Article  Google Scholar 

  • —,K. J. Sytsma &R. R. Kowal. 1999. Shrinking the violets: phylogenetic relationships of infrageneric groups inViola (Violaceae) based on internal transcribed spacer DNA sequences. Syst. Bot. 23: 439–458.

    Article  Google Scholar 

  • Bartlett, E., S. J. Novak &R. N. Mack. 2002. Genetic variation inBromus tectorum (Poaceae): differentiation in the eastern United States. Amer. J. Bot. 89(4): 602–612.

    Article  Google Scholar 

  • Beardsley, P. M. &R. G. Olmstead. 2002. Redefining Phrymaceae: the placement ofMimulus, tribe Mimuleae, andPhryma. Amer. J. Bot. 89(7): 1093–1102.

    Article  Google Scholar 

  • Beattie, A. J. 1969. Studies in the pollination ecology ofViola. I. The pollen-content of stigmatic cavities. Watsonia 7:142–156.

    Google Scholar 

  • Bell, T. J. &J. A. Quinn. 1985. Relative importance of chasmogamously and cleistogamously derived seeds ofDichanthelium clandestinum (L.) Gould. Bot. Gaz. 146(2): 252–258.

    Article  Google Scholar 

  • ——. 1987. Effects of soil moisture and light intensity on the chasmogamous and cleistogamous components of reproductive effort ofDichanthelium clandestinum populations. Canad. J. Bot. 65: 2243–2249.

    Article  Google Scholar 

  • Bennington, C. C. &J.B. McGraw. 1995. Natural selection and ecotypic differentiation inImpatiens pallida. Ecol. Monogr. 65: 303–323.

    Article  Google Scholar 

  • Berg, H. 2003. Factors influencing seed: ovule ratios and reproductive success in four cleistogamous species: a comparison between two flower types. Pl. Biol. 5: 194–202.

    Article  Google Scholar 

  • — &P. Redbo-Torstensson. 1998. Cleistogamy as a bet-hedging strategy inOxalis acetosella, a perennial herb. J. Ecol. 86: 491–500.

    Article  Google Scholar 

  • Calvino, A. &L. Galetto. 2003. Cleistogamy in the rare high Andean perennial herbCryptantha capituliflora (Boraginaceae). Pl. Syst. Evol. 237(1-2): 41–50.

    Article  Google Scholar 

  • Camp, W. H. &C. L. Gilly. 1943. The structure and origin of species with a discussion of intraspecific variability and related nomenclatural problems. Brittonia 4: 323–385.

    Article  Google Scholar 

  • Campbell, C. S. 1982. Cleistogamy inAndropogon L. (Gramineae). Amer. J. Bot. 69(10): 1625–1635.

    Article  Google Scholar 

  • —,J. A. Quinn, G. P. Cheplick &T. J. Bell. 1983. Cleistogamy in grasses. Annual. Rev. Ecol. Syst. 14:411–441.

    Article  Google Scholar 

  • Catling, P. M. 1990. Auto-pollination in the Orchidaceae. Pp. 121–158in J. Arditti (ed.), Orchid biology, reviews and perspectives. Timber Press, Portland, Oregon.

    Google Scholar 

  • Charlesworth, B. &D. Charlesworth. 1978. A model for the evolution of dioecy and gynodioecy. Amer. Naturalist 112: 975–997.

    Article  Google Scholar 

  • Cheplick, G. P. 1996. Cleistogamy and seed heteromorphism inTriplasis purpurea (Poaceae). Bull. Torrey Bot. Club 123: 25–33.

    Article  Google Scholar 

  • — 2005a. Biomass partitioning and reproductive allocation in the invasive, cleistogamous grassMicrostegium vimineum: influence of the light environment. J. Torrey Bot. Soc. 132: 214–224.

    Article  Google Scholar 

  • — 2005b. Plasticity of chasmogamous and cleistogamous reproductive allocation in grasses. Pp. 145–155in J. T. Columbus, E. A. Friar, C. W. Hamilton, J M. Porter, L. M. Price & M. G. Simpson (eds.), Monocots: comparative biology and evolution. Rancho Santa Ana Botanical Garden, Claremont, California.

    Google Scholar 

  • — &K. Clay. 1989. Convergent evolution of cleistogamy and seed heteromorphism in two perennial grasses. Evol. Trends Pl. 3: 127–136.

    Google Scholar 

  • Clay, K. 1982. Environmental and genetic determinants of cleistogamy in a natural population of the grassDanthonia spicata. Evolution 36: 734–741.

    Article  Google Scholar 

  • — 1983a. Variation in the degree of cleistogamy within and among species of the grassDanthonia. Amer. J. Bot. 70(6): 835–843.

    Article  Google Scholar 

  • — 1983b. The differential establishment of seedlings from chasmogamous and cleistogamous flowers in natural populations of the grassDanthonia spicata (L.) Beauv. Oecologia 57: 183–188.

    Article  Google Scholar 

  • — &J. Antonovics. 1985. Demographic genetics of the grassDanthonia spicata: success of progeny from chasmogamous and cleistogamous flowers. Evolution 39: 205–210.

    Article  Google Scholar 

  • Cole, C. T. &D. D. Biesboer. 1992. Monomorphism, reduced gene flow, and cleistogamy in rare and common species ofLespedeza (Fabaceae). Amer. J. Bot. 79: 567–575.

    Article  Google Scholar 

  • Columbus, T. J. 1998. Morphology and leaf blade anatomy suggest a close relationship betweenBouteloua aristidoides andB. (Chondrosium) eriopoda (Gramineae: Chloroideae). Syst. Bot. 23(4): 467–478.

    Article  Google Scholar 

  • Connor H. E. 1979. Breeding systems in the grasses: a survey. New Zealand J. Bot. 17: 547–574.

    Google Scholar 

  • — 1998. Breeding systems in New Zealand grasses. XII. Cleistogamy inFestuca. New Zealand J. Bot. 36: 471–476.

    Google Scholar 

  • Cortes-Palomec, A. C. 2005. Ecological factors, mixed breeding system and population genetic structure in a subtropical and a temperate violet species. Ph.D. diss., Ohio Univ., Athens, Ohio.

    Google Scholar 

  • Crozier, T. S. &J. F. Thomas. 1993. Normal floral ontogeny and cool temperature-induced aberrant floral development inGlycine max (Fabaceae). Amer. J. Bot. 80(4): 429–448.

    Article  Google Scholar 

  • Cruden, R. W. 1977. Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31(1): 32–46.

    Article  Google Scholar 

  • Culley, T. M. 2000. Inbreeding depression and floral type differences inViola canadensis (Violaceae), a perennial herb with chasmogamous and cleistogamous flowers. Canad. J. Bot. 78(11): 1420–1429.

    Article  Google Scholar 

  • — 2002. Reproductive biology and delayed selfing inViola pubescens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. Int. J. Pl. Sci. 163: 113–122.

    Article  Google Scholar 

  • Culver, D. C. &A. J. Beattie. 1978. Myrmecochory inViola: dynamics of seed-ant interactions in some West Virginia species. J. Ecol. 66: 53–72.

    Article  Google Scholar 

  • Darwin, C. 1877. The different forms of flowers on plants of the same species. John Murray, London. Reprint, 1986. University of Chicago Press, Chicago, Illinois.

    Google Scholar 

  • Delgado-Salinas, A. 2000. New species of MexicanPhaseolus (Fabaceae). Syst. Bot. 25(3): 414–436.

    Article  Google Scholar 

  • De-yuan, H. 1990. A biosystematic study onRanunculus subgenusBatrachium in S. Sweden. Nordic J. Bot. 11:41–59.

    Article  Google Scholar 

  • Diaz, A., &M. R. Macnair. 1999. Pollen tube competition as a mechanism of prezygotic reproductive isolation betweenMimulus nasutus and its presumed progenitorM. buttatus. New Phytol. 144: 471–478.

    Article  Google Scholar 

  • Dinc, M. &S. Yildirimli. 2002. A new species ofViola (Violaceae) from Turkey. Bot. J. Linn. Soc. 138: 483–487.

    Article  Google Scholar 

  • —,Y. Bağci &S. Yildirimli. 2003. A new species ofViola L. (Violaceae) from South Anatolia. Bot. J. Linn. Soc. 141: 477–482.

    Article  Google Scholar 

  • Drewes, S. I. &P. S. Hoc. 2000. Morphology and development of cleistogamous flowers inMacroptilium fraternum (Fabaceae). Kurtziana 28(2): 229–238.

    Google Scholar 

  • Eckstein, R. L. &A. Otte. 2005. Effects of cleistogamy and pollen source on seed production and offspring performance in three endangered violets. Basic Appl. Ecol. 6: 339–350.

    Article  Google Scholar 

  • Edgar, E. &H. E. Connor. 1982.Dichelachne (Gramineae) in New Zealand. New Zealand J. Bot. 20: 303–309.

    Google Scholar 

  • Ehrenfeld, J. G. 1999. A rhizomatous, perennial form ofMicrostegium vimineum (Trin.) A. Camus in New Jersey. J. Torrey Bot. Soc. 126(4): 352–358.

    Article  Google Scholar 

  • Elisafenko, T. V. 1998. The two types of flowering in the rare Siberian species ofViola (Violaceae). Bot. Zhurn. (St. Petersburg) 83(6): 66–72.

    Google Scholar 

  • Endress, P. K. 1999. Symmetry in flowers: diversity and evolution. Int. J. Pl. Sci. 160 (6 Suppl.): S3-S23.

    Article  Google Scholar 

  • Evans, L. T. 1956. Chasmogamous flowering inViola palustris L. Nature 178: 1301.

    Article  Google Scholar 

  • Freitas, B. M., J. E. Alves, G. F. Brandão &Z. B. Araujo. 1995. Pollination requirements of West Indian cherry (Malpighia emarginata) and its putative pollinators,Centris bees, in NE Brazil. J. Agric. Sci. 133: 303–311.

    Article  Google Scholar 

  • Freudenstein, J. V. 1994. Character transformation and relationships inCorallorhiza (Orchidaceae: Epidendroideae). II. Morphological variation and phylogenetic analysis. Amer. J. Bot. 81: 1458–1467.

    Article  Google Scholar 

  • — 1999. A new species of Corallorhiza (Orchidaceae) from West Virginia, U.S.A. Novon 9: 511–513.

    Article  Google Scholar 

  • Gallardo, R., E. Dominguez &J. M. Muñoz. 1993. The heterochronic origin of the cleistogamous flower inAstragalus cymbicarpos (Fabaceae). Amer. J. Bot. 80(7): 814–823.

    Article  Google Scholar 

  • Gardner, C. S. 1982. Systematic study ofTillandsia subgenusTillandsia. Ph.D. diss., Texas A&M Univ., College Station, Texas.

    Google Scholar 

  • Gil-Ad, N. L. 1997. Systematics ofViola subsection Boreali-Americanae. Boissiera 53: 1–130.

    Google Scholar 

  • Gilmartin, A. J. &G. K. Brown. 1985. Cleistogamy inTillandsia capillaries (Bromeliaceae). Biotropica 17(3): 256–259.

    Article  Google Scholar 

  • Gleason, H. A. &A. Cronquist. 1991. Manual of vascular plants of northeastern United States and adjacent Canada. Ed. 2. New York Botanical Garden, New York.

    Google Scholar 

  • Gomez, S. M. &A. Kalamani. 2003. Butterfly pea (Clitoria teratea): a nutritive multipurpose forage legume for the tropics—an overview. Pakistan J. Nutr. 2(6): 374–379.

    Article  Google Scholar 

  • Gopinathan, M. C. &C. R. Babu. 1987. Breeding systems and pollination inVigna minima (Leguminosae, Papilionoideae). Pl. Syst. Evol. 156: 117–126.

    Article  Google Scholar 

  • Grau, J. 1981. Two new species of the genusCryptantha (Boraginaceae) and their taxonomic position. Mitt. Bot. Staatssamml. München 17: 511–526.

    Google Scholar 

  • Hackel, E. 1906. Über Cleristogamie bei den Grasern. Oesterr. Bot. Z. 56: 81–88.

    Article  Google Scholar 

  • Hardy, C. R. &R. B. Faden. 2004.Plowmanianthus, a new genus of Commelinaceae with five new species from tropical America. Syst. Bot. 29: 316–333.

    Article  Google Scholar 

  • Herrera, J. 1992. Flowering variation and breeding systems in the Cistaceae. Pl. Syst. Evol. 179(3-4): 245–255.

    Article  Google Scholar 

  • Hilu, K. W., T. Borsch, K. Müller, D. E. Soltis, P. S. Soltis, V. Savolainen, M. W. Chase, M. P. Powell, L. A. Alice, R. Evans, H. Sauquet, C. Neinhuis, T. A. B. Slotta, J. G. Rohwer, C. S. Campbell &L. W. Chatrou. 2003. Angiosperm phylogeny based onmatK sequence information. Amer. J. Bot. 90: 1758–1776.

    Article  CAS  Google Scholar 

  • Holderegger, R., I. Stehlik, R. I. Lewis Smith &R. J. Abbott. 2003. Populations of Antarctic hairgrass (Deschampsia antarctica) show low genetic diversity. Arctic Antarc. Alpine Res. 35(2): 214–217.

    Article  Google Scholar 

  • Holsinger, K. E. 1986. Dispersal and plant mating systems: the evolution of self-fertilization in subdivided populations. Evolution 40: 405–413.

    Article  Google Scholar 

  • Howes, M. 1999. Beechdrops. Newslett. Ohio Div. Nat. Areas Preserves 21(1): 5.

    Google Scholar 

  • Jacobs, S. W. L., J. Everett, H. E. Connor &E. Edgar. 1989. Stipoid grasses in New Zealand. New Zealand J. Bot. 27: 569–582.

    Google Scholar 

  • Jacquemart, A. L. &J. R. Desloover. 1992. The part taken by cleistogamy inNarthecium ossifragum reproductive strategy. Flora 187 (1-2): 67–72.

    Google Scholar 

  • Jamison, D. S. &J. I. Yoder. 2001. Heritable variation in quinine-induced haustorium development in the parasitic plantTriphysaria. Pl. Physiol. 125: 1870–1880.

    Article  CAS  Google Scholar 

  • Jasieniuk, M. &M. J. Lechowicz. 1987. Spatial and temporal variation in chasmogamy and cleistogamy inOxalis montana (Oxalidaceae). Amer. J. Bot. 74:1672–1680.

    Article  Google Scholar 

  • Jiang, M. &Y. Kadono. 2001. Growth and reproduction characteristics of an aquatic macrophyteOttelia alismoides (L.) Pers. (Hydrocharitaceae). Ecol. Res. 16(4): 687–695.

    Article  Google Scholar 

  • Jones, D. L. 1997. A taxonomic revision ofCheirostylis (Orchidaceae) in Australia. Muelleria 10: 75–83.

    Google Scholar 

  • Judziewicz, E. J. &P. M. Peterson. 1990. A new cleistogamous South American species ofEragrostis (Poaceae Chloridoideae). Brittonia 42: 47–49.

    Article  Google Scholar 

  • Kadono, Y. &E. L. Schneider. 1987. The life history of theEuryale ferox Salisb. in southwestern Japan with special reference to reproductive ecology. Pl. Spec. Biol. 2: 109–115.

    Article  Google Scholar 

  • Kaul, V., A. K. Koul &M. C. Sharma. 2000. The underground flower. Curr. Sci. 78: 39–44.

    Google Scholar 

  • Keighery, G. J. 1984. Cleistogamy inElatine gratioloides A. Cunn. (Elatinaceae). W. Austral. Naturalist 16(1): 22.

    Google Scholar 

  • — 1988. Breeding systems of the Western Australian flora. W. Austral. Naturalist 17(5): 121–125.

    Google Scholar 

  • Kerner von Marilaun, A. 1902. The natural history of plants. Vol. II. Translated by F.W. Oliver, Blackie and Son, London.

    Google Scholar 

  • Khosla, C., K. R. Shivanna &H. Y. Mohan Ram. 1998. Pollination in the aquatic insectivoreUtricularia inflexa var. stellaris. Phytomorphology 48(4): 417–425.

    Google Scholar 

  • ———. 2001. Cleistogamy inGriffithella hookeriana (Podostemaceae). S. African J. Bot. 67(2): 320–324.

    Google Scholar 

  • Kim, I. &G. D. Carr. 1990. Reproductive biology and uniform culture ofPortulaca in Hawaii. Pacific Sci. 44: 123–129.

    Google Scholar 

  • Kim, K. S., B. Y. Sun, S. S. Whang &G. H. Chung. 1991. Biosystematic study on the genusViola in Korea: comparative morphology of theViola albida complex. Korean J. Bot. 34(3): 229–238.

    Google Scholar 

  • Knight, S. E. &D. M. Waller. 1987. Genetic consequences of outcrossing in the cleistogamous annualImpatiens capensis. I Population genetic structure. Evolution 41: 969–978.

    Article  Google Scholar 

  • Koller, D. &N. Roth. 1964. Studies on the ecological and physiological significance of amphicarpy inGymnarrhena micrantha (Compositae). Amer. J. Bot. 51: 26–35.

    Article  Google Scholar 

  • Kuhn, M. 1867. Einige Bemerkungen überVandellia und den Blüten Dimorphismus. Bot. Zeitung 25: 65–67.

    Google Scholar 

  • Lazarides, M., J. B. Hacker &M. H. Andrew. 1991. Taxonomy, cytology and ecology of indigenous Australian sorgums (Sorghum Moench: Andropogoneae: Poaceae). Austral. Syst. Bot. 4(4): 591–635.

    Article  Google Scholar 

  • Le Corff, J. 1993. Effects of light and nutrient availability on chasmogamy and cleistogamy in an understory tropical herb,Calathea micans (Marantaceae). Amer. J. Bot. 80:1392–1399.

    Article  Google Scholar 

  • Lesica, P., R. F. Leary, F. W. Allendorf &D. E. Bilderback. 1988. Lack of genie diversity within and among populations of an endangered plant,Howellia aquatilis. Conservation Biol. 2: 275–282.

    Article  Google Scholar 

  • Levin, R. A. 2000. Phylogenetic relationships within Nyctaginaceae tribe Nyctagineae: evidence from nuclear and chloroplast genomes. Syst. Bot. 25: 738–750.

    Article  Google Scholar 

  • — 2002. Taxonomic status ofAcleisanthes, Selinocarpus, andAmmocodon (Nyctaginaceae). Novon 12: 58–63.

    Article  Google Scholar 

  • Lloyd, D. G. 1984. Variation strategies of plants in heterogeneous environments. Biol. J. Linn. Soc. 21: 357–385.

    Article  Google Scholar 

  • — andD. J. Schoen. 1992. Self- and cross-fertilization in plants. I. Functional dimensions. Int. J. Pl. Sci. 153: 358–369.

    Article  Google Scholar 

  • Lord, E. M. 1981. Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. Bot. Rev. 47:421–449.

    Article  Google Scholar 

  • — &L. U. Kohorn. 1986. Gynoecial development, pollination, and the path of pollen tube growth in the Tepary bean,Phaseolus acutifolius. Amer. J. Bot. 73(1): 70–78.

    Article  Google Scholar 

  • Lu, Y. 2002. Why is cleistogamy a selected reproductive strategy inImpatiens capensis (Balsaminaceae)? Biol. J. Linn. Soc. 75: 543–553.

    Article  Google Scholar 

  • Mayers, A. M. &E. M. Lord. 1983a. Comparative flower development in the cleistogamous speciesViola odorata. I. A growth rate study. Amer. J. Bot. 70: 1548–1555.

    Article  Google Scholar 

  • ——. 1983b. Comparative flower development in the cleistogamous speciesViola odorata. II. An organographic study. Amer. J. Bot. 70: 1556–1563.

    Article  Google Scholar 

  • Maheshwari, J. K. 1962. Cleistogamy in angiosperms. Pp. 145–155in P. Maheshwari, B. M. John & I. K. Vasil, (eds.), Proceedings of the Summer School of Botany June 2–15, 1960. Ministry of Scientific Research and Cultural Affairs, New Delhi, India.

    Google Scholar 

  • Marcussen, T. 2003. A new violet species (Violaceae) from the south-west Alps. Bot. J. Linn. Soc. 142: 119–123.

    Article  Google Scholar 

  • Márquez-Guzmán, J., S. Vázquez-Santana, E. M. Engleman, A. Martímez-Mena & E. Martínez. Pollen development and fertilization inLacandonia schismatica (Lacandoniaceae). Ann. Missouri Bot. Gard. 80: 891–897.

  • Masuda, M. &T. Yahara. 1994. Reproductive ecology of a cleistogamous annual,Impatiens nolitangere L. occurring under different environmental conditions. Ecol. Res. 9: 67–75.

    Article  Google Scholar 

  • —— &M. Maki. 2001. An ESS model for the mixed production of cleistogamous and chasmogamous flowers in a facultative cleistogamous plant. Evol. Ecol. Res. 3: 429–439.

    Google Scholar 

  • McCall, C., T. Mitchell-Olds &D. M. Waller. 1989. Fitness consequences of outcrossing inImpatiens capensis: tests of the frequency-dependent and sib-competition models. Evolution 43: 1075–1084.

    Article  Google Scholar 

  • Mitchell-Olds, T. &D. M. Waller. 1985. Relative performance of selfed and outcrossed progeny inImpatiens capensis. Evolution 39: 533–544.

    Article  Google Scholar 

  • Morin, N. 1983. Systematics ofGithopsis (Campanulaceae). Syst. Bot. 8(4): 436–468.

    Article  Google Scholar 

  • Moyle, L. C., M. S. Olson &P. Tiffin. 2004. Patterns of reproductive isolation in three angiosperm genera. Evolution 58: 1195–1208.

    PubMed  Google Scholar 

  • Munz, P. A. 1974. A flora of Southern California. Univ. of California Press, Berkeley, California.

    Google Scholar 

  • Nandi, O. I. 1998. Floral development and systematics of Cistaceae. Pl. Syst. Evol. 212(1-2): 107–134.

    Article  Google Scholar 

  • Nieuwland, J. A. 1914. Notes on cleistogamous flowers of violets. II. Amer. Midl. Naturalist 3(7): 198–200.

    Article  Google Scholar 

  • — 1916. Cleistogamous flowers in the Pansies. Amer. Midl. Naturalist 4(1): 464–466.

    Article  Google Scholar 

  • Novosyelova, L. V. 1998. The bud cleistogamy of some annual species of the genusMedicago (Fabaceae). Bot. Zhurn. (St. Petersburg) 83: 82–87.

    Google Scholar 

  • Oakley, C. G. 2004. Inbreeding depression and mating system evolution in the perennial herbViola septemloba; and the evolutionary maintenance of cleistogamy. M.S. thesis, Florida State Univ., Tallahassee.

    Google Scholar 

  • Oakley, C. G., K. S. Moriuchi & A. A. Winn. In prep. Stable mixed mating in cleistogamous species: a review of the ideas and evidence. Annual Rev. Ecol. Syst.

  • Ortega-Olivencia, A., J. A. López-Paredes, T. Rodríguez-Riaño &J. A. Devesa. 1998. Modes of selfpollination and absence of cryptic self-incompatibility inDrosophyllum lusitanicum (Droseraceae). Bot. Acta 111:474–480.

    Google Scholar 

  • Oyama, R. K. &D. A. Baum. 2004. Phylogenetic relationships of North AmericanAntirrhinum (Veronicaceae). Amer. J. Bot. 91(6): 918–925.

    Article  CAS  Google Scholar 

  • Pfeifer, H. W. 1966. Revision of the North and Central American hexandrous species ofAristolochia (Aristolochiaceae). Ann. Missouri Bot. Gard. 53: 116–196.

    Article  Google Scholar 

  • Plitmann, U. 1995. Distribution of dimorphic flowers as related to other elements of the reproductive strategy. Pl. Spec. Biol. 10: 53–60.

    Article  Google Scholar 

  • Porras, R. &J. M. Muñoz Álvarez. 1999. Breeding system in the cleistogamous speciesCentaurea melitensis (Asteraceae). Canad. J. Bot. 77:1632–1640.

    Article  Google Scholar 

  • Primack, R. B. 1978. Evolutionary aspects of wind pollination in the genusPlantago (Plantaginaceae). New Phytol. 81(2): 449–458.

    Article  Google Scholar 

  • Pupulin, F. 1998. Orchid florula of Parque Nacional Manuel Antonio. Revista Biol. Trop. 46(4): 961–10317.

    Google Scholar 

  • Redbo-Torstensson, P. &H. Berg. 1995. Seasonal cleistogamy: a conditional strategy to provide reproductive assurance. Acta Bot. Neerl. 44: 247–256.

    Google Scholar 

  • Rickett, H. W. 1932. Distribution of cleistogamy among flowering plants. Typewritten notes available at the New York Botanical Garden Library.

  • Ritzerow, H. 1908. Über Bau und Befruchtung kleistogamer Blüten. Bot. Zeitung (Flora) 98: 163–212.

    Google Scholar 

  • Ruiz de Clavijo, E. 1997. A comparative study of the reproductive biology of twoAjuga species (Lamiaceae) in the southwest of the Iberian Peninsula. Int. J. Pl. Sci. 158:282–291.

    Article  Google Scholar 

  • — &M. J. Jimenez. 1993. Cleistogamy and chasmogamy inCeratocapnos heterocarpa (Fumariaceae). Int. J. Pl. Sci. 154: 325–333.

    Article  Google Scholar 

  • Sakai, S. &A. Sakai. 1996. Why is there variation in mean seed size among plants within single populations? Test of the fertilization efficiency hypothesis. Amer. J. Bot. 83(11): 1454–1457.

    Article  Google Scholar 

  • Schemske, D. W. 1978. Evolution of reproductive characteristics inImpatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Ecology 59: 596–613.

    Article  Google Scholar 

  • — 1984. Population structure and local selection inImpatiens pallida (Balsaminaceae), a selfing annual. Evolution 38: 817–832.

    Article  Google Scholar 

  • Schmitt, J. &D. W. Ehrhardt. 1987. A test of the sib-competition hypothesis for outcrossing advantage inImpatiens capensis. Evolution 41: 579–590.

    Article  Google Scholar 

  • ——. 1990. Enhancement of inbreeding depression by dominance and suppression inImpatiens capensis. Evolution 44: 269–278.

    Article  Google Scholar 

  • — &S. E. Gamble. 1990. The effect of distance from the parental site on offspring performance and inbreeding depression inImpatiens capensis: a test of the local adaptation hypothesis. Evolution 44: 202–230.

    Google Scholar 

  • —,D. Ehrhardt &D. Swartz. 1985. Differential dispersal of self-fertilized and outcrossed progeny in Jewelweed (Impatiens capensis). Amer. Naturalist 126: 570–575.

    Article  Google Scholar 

  • Schoen, D. J. &A. H. D. Brown. 1991. Whole- and part-flower self-pollination inGlycine clandestina andG. argyrea and the evolution of autogamy. Evolution 45:1651–1664.

    Article  Google Scholar 

  • — &D. G. Lloyd. 1984. The selection of cleistogamy and heteromorphic diaspores. Biol. J. Linn. Soc. 23: 303–322.

    Article  Google Scholar 

  • Sigrist, M. R. &M. Sazima. 2002.Ruellia brevifolia (Pohl) Ezcurra (Acanthaceae): flowering phenology, pollination biology and reproduction. Revista Brasil. Bot. 25: 35–42.

    Google Scholar 

  • Simpson, R. L., M. A. Leek &V. T. Parker. 1985. The comparative ecology ofImpatiens capensis Meerb. (Balsaminaceae) in central New Jersey. Bull. Torrey Bot. Club 112: 295–311.

    Article  Google Scholar 

  • Solbrig, O. T. 1981. Studies on the population biology of the genusViola. II. Effects of plant size on fitness inViola sororia. Evolution 35: 1080–1093.

    Article  Google Scholar 

  • Soltis, D. E., P. S. Soltis, M. W. Chase, M. E. Mort, D. C. Albach, M. Zanis, V. Savolainen, W. H. Hahn, S. B. Hoot, M. F. Fay, M. Axtell, S. M. Swensen, L. M. Prince, W. J. Kress, K. C. Nixon &J. S. Farris. 2000. Angiosperm phylogeny inferred from 18S rDNA,rbcL, andatpB sequences. Bot. J. Linn. Soc. 133: 381–461.

    Google Scholar 

  • ——,P. K. Endress &M.W. Chase. 2005. Phylogeny and evolution of angiosperms. Sinauer Associates, Sunderland, Massachusetts.

    Google Scholar 

  • Stewart, S. C. 1994. Genetic constraints on mating system evolution in the cleistogamous annualImpatiens pallida: inbreeding in chasmogamous flowers. Heredity 73:265–274.

    Article  Google Scholar 

  • Sun, M. 1999. Cleistogamy inScutellaria indica (Labiatae): effective mating system and population genetic structure. Molec. Ecol. 8: 1285–1295.

    Article  CAS  Google Scholar 

  • Takahashi, R., H. Kurosaki., S. Yumoto, O. K. Han &J. Abe. 2001. Genetic and linkage analysis of cleistogamy in Soybean. J. Heredity 92(1): 89–92.

    Article  CAS  Google Scholar 

  • Trapp, E. J. 1988. Dispersal of heteromorphic seeds inAmphicarpaea bracteata (Fabaceae). Amer. J. Bot. 75: 1535–1539.

    Article  Google Scholar 

  • — &S. D. Hendrix. 1988. Consequences of a mixed reproductive system in the hog peanut,Amphicarpaea bracteata (Fabaceae). Oecologia 75: 285–290.

    Article  Google Scholar 

  • Trent, J. A. 1939. Studies pertaining to the life history ofSpecularia perfoliata (L.) A. DC., with special reference to cleistogamy. Ph.D. diss., Ohio State University, Columbus.

    Google Scholar 

  • Uphof, J. C. Th. 1938. Cleistogamic flowers. Bot. Rev. 4: 21–49.

    Article  Google Scholar 

  • Vander Kloet, S. P. 1993. Biosystematic studies ofVaccinium sectionMacropelma (Ericaceae) in Hawaii. Pacific Sci. 47(1): 76–85.

    Google Scholar 

  • Van Wyk, B.-E. 1990. Studies in the genusLotononis (Crotalaria, Fabaceae). 13. Two new species and notes on the occurrence of cleistogamy in the section Leptis. Bothalia 20(1): 17–22.

    Google Scholar 

  • Wagner, W. L., D. R. Herbst &S. H. Sohmer. 1990. Manual of the flowering plants of Hawai’i. University of Hawaii Press, Honolulu.

    Google Scholar 

  • —,S. G. Weiler &A. Sakai. 2005. Monograph ofSchiedea (Caryophyllaceae-Alsinoideae). Syst. Bot. Monogr. 72: 1–169.

    Google Scholar 

  • Waller, D. M. 1979. The relative costs of self- and cross-fertilized seeds inImpatiens capensis (Balsaminaceae). Amer. J. Bot. 66: 313–320.

    Article  Google Scholar 

  • — 1984. Differences in fitness between seedlings derived from cleistogamous and chasmogamous flowers inImpatiens capensis. Evolution 38: 427–440.

    Article  Google Scholar 

  • Watanabe, K., T. Yahara &H. Kadota. 1992. Natural hybrid populations between chasmogamous and cleistogamous species,Ainsliaea fauieana andAinsliaea apiculata (Asteraceae; Mutisiae): morphology, cytology, reproductive mode and allozyme variation. Pl. Spec. Biol. 7(1): 49–59.

    Article  Google Scholar 

  • Wilken, D. H. 1982. The balance between chasmogamy and cleistogamy inCollomia grandiflora (Polemoniaceae). Amer. J. Bot. 69: 1326–1333.

    Article  Google Scholar 

  • Wylie, R. B. 1917. Cleistogamy inHeteranthera dubia. Stud. Nat. Hist. Iowa Univ. 7: 48–58.

    Google Scholar 

  • Yamamoto, I. &Y. Kadono. 1990. A study of the reproductive biology of aquaticUtricularia species in Southwestern Japan. Acta Phytotax. Geobot. 41(4-6): 189–200.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Culley, T.M., Klooster, M.R. The cleistogamous breeding system: A review of its frequency, evolution, and ecology in angiosperms. Bot. Rev 73, 1–30 (2007). https://doi.org/10.1663/0006-8101(2007)73[1:TCBSAR]2.0.CO;2

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1663/0006-8101(2007)73[1:TCBSAR]2.0.CO;2

Keywords

Navigation