Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-20T17:47:13.227Z Has data issue: false hasContentIssue false
  • English
  • Français

Seed germination in cleistogamous species: theoretical considerations and a literature survey of experimental results

Published online by Cambridge University Press:  07 April 2017

Jerry M. Baskin  and
Carol C. Baskin
Jerry M. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA
Carol C. Baskin*
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546-0312, USA
*
*Correspondence Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

A cleistogamous species consists of individuals that produce both chasmogamous (open, CH) and cleistogamous (permanently closed, CL) flowers, which facilitates a mixed-mating system. In contrast to what one might expect, CL (obligately selfed) seeds and the plants derived from them can be more fit than CH (potentially outcrossed) seeds and the plants they give rise to. Our aim was to review some theoretical aspects of mixed mating in relation to retention of both CH and CL in cleistogamous species and to determine if data on germination support the notion that CL is advantageous over that of CH. Based on germination (or seedling emergence) of CH vs CL seeds in 29 species in 21 genera and 11 families of monocots and eudicots, CL seeds germinated better in 107 and equally well as in 64 of 252 case studies as CH seeds (67.9%), and the (CH < CL):(CH > CL) ratio was 107/81 (1.32). We conclude that our study lends support to the notion that production of CL seeds by cleistogamous species is advantageous over that of CH seeds. Retention of CH by CL species may be due to the need to prevent complete selfing (s= 1.0) and thus total inbreeding depression (δ), which theory predicts would decrease reproductive success. Some caveats concerning the results of comparative studies on the germination biology of CH vs CL seeds of amphicarpic sensu stricto Fabaceae species and Commelina benghalensis and the aerial cleistogamous grass Danthonia spicata are discussed.

Keywords

amphicarpychasmogamycleistogamyinbreeding depressionmixed-mating systempollen discountingpollen limitationseed germination
Type
Review Papers
Information
Seed Science Research , Volume 27 , Special Issue 2: Seed Ecology , June 2017 , pp. 84 - 98
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ågren, J. and Schemske, D.W. (1993) Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B . semiovata. Evolution 47, 125–135.Google Scholar
Aide, T.M. (1986) The influence of wind and animal pollination on variation in outcrossing rates. Evolution 40, 434–435.Google Scholar
Aitken, Y. (1939) The problem of hard seeds in subterranean clover. Proceedings of the Royal Society of Victoria 51 (N.S.), part II, 187–213.Google Scholar
Alinoglu, N. and Durlu, N. (1970) Subterranean vetch seed enhances persistence under grazing and severe climates. Journal of Range Management 23, 61–63.Google Scholar
Antlfinger, A.E. (1986) Field germination and seedling growth of CH and CL progeny of Impatiens capensis (Balsaminaceae). American Journal of Botany 73, 1267–1273.CrossRefGoogle Scholar
Argel, P.J. and Paton, C.J. (1999) Overcoming legume hardseededness. In Loch, D. S. and Ferguson, J.E. (eds), Forage Seed Production. Volume 2: Tropical and Subtropical Species, pp. 247–265. Oxon, UK: CABI Publishing.Google Scholar
Barrett, S.C.H. (2013) The evolution of plant reproductive systems: how often are transitions irreversible? Proceedings of the Royal Society B 280, 20130913.Google Scholar
Barrett, S.C.H., Arunkumar, R. and Wright, S.I. (2014) The demography and population genomics of evolutionary transitions to self-fertilization in plants. Philosophical Transactions of the Royal Society B 369, 20130344.CrossRefGoogle ScholarPubMed
Barringer, B.C. and Geber, M.A. (2008) Mating system and ploidy influence levels of inbreeding depression in Clarkia (Onagraceae). Evolution 62, 1040–1051.Google Scholar
Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination, 2nd edition. San Diego, California: Elsevier/Academic Press.Google Scholar
Baskin, J.M. and Baskin, C.C. (1975) Observations on the ecology of the cedar glade endemic Viola egglestonii . The American Midland Naturalist 93, 320–329.Google Scholar
Baskin, J.M. and Baskin, C.C. (2015) Inbreeding depression and the cost of inbreeding on seed germination. Seed Science Research 25, 355–385.Google Scholar
Bell, T.J. and Quinn, J.A. (1985) Relative importance of chasmogamously and cleistogamously derived seeds of Dichanthelium clandestinum (L.) Gould. Botanical Gazette 146, 252–258.CrossRefGoogle Scholar
Berg, H. and Redbo-Torstensson, P. (1999) Offspring performance in three cleistogamous Viola species. Plant Ecology 145, 49–58.Google Scholar
Berg, H. and Redbo-Torstensson, P. (2000) Offspring performance in Oxalis acetosella, a cleistogamous perennial herb. Plant Biology 2, 638–645.CrossRefGoogle Scholar
Berjano, R, Arista, M., Talavera, M., Ariza, M.J. and Ortiz, P.l. (2014) Plasticity and within plant sex ratio variation in monoecious Emex spinosa . Turkish Journal of Botany 38, 258–267.Google Scholar
Budd, G.D., Thomas, P.E.L. and Allison, J.C.S. (1979) Vegetative regeneration, depth of germination and seed dormancy in Commelina benghalensis L. Rhodesian Journal of Agricultural Research 17, 151–153.Google Scholar
Burns, J.H. (2008) Demograhic performance predicts invasiveness for species in the Commelinaceae under high-nutrient conditions. Ecological Applications 18, 335–346.Google Scholar
Busch, J.W. and Delph, L.F. (2012) The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Annals of Botany 109, 553–562.Google Scholar
Busch, J.W., Joly, W and Schoen, D.J. (2011) Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica . Molecular Biology and Evolution 28, 1717–1729.Google Scholar
Busch, J.W. and Schoen, D.J. (2008) The evolution of self-incompatibility when mates are limiting. Trends in Plant Science 12, 128–136.Google Scholar
Busch, J.W. and Urban, L. (2011) Insights gained from 50 years of studying the evolution of self-compatibility in Leavenworthia (Brassicaceae). Evolutionary Biology 38, 15–27.CrossRefGoogle Scholar
Call, C.A. and Spoonts, B.O. (1989) Characterization and germination of chasmogamous and basal axillary cleistogamous florets of Texas wintergrass. Journal of Range Management 42, 51–55.CrossRefGoogle Scholar
Campbell, C.S., Quinn, J.A., Cheplick, G.P. and Bell, T.J. (1983) Cleistogamy in grasses. Annual Review of Ecology and Systematics 14, 411–441.Google Scholar
Charlesworth, D. and Charlesworth, B. (1987) Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237–268.CrossRefGoogle Scholar
Carta, A., Bedini, G., Giannotti, A., Savio, L. and Peruzzi, L. (2015) Mating system modulates degree of seed dormancy in Hypericum elodes L. (Hypericaceae). Seed Science Research 25, 299–305.CrossRefGoogle Scholar
Chase, A. (1908) Notes on cleistogamy of grasses. Botanical Gazette 45, 135–136.Google Scholar
Chase, A. (1918) Axillary cleistogenes in some American grasses. American Journal of Botany 5, 254–258.Google Scholar
Cheplick, G.P. (1987) The ecology of amphicarpic plants. Trends in Ecology and Evolution 2, 97–101.Google Scholar
Cheplick, G.P. (1996) Cleistogamy and seed heteromorphism in Triplasis purpurea (Poaceae). Bulletin of the Torrey Botanical Club 123, 25–33.Google Scholar
Cheplick, G.P and Clay, K. (1989) Convergent evolution of cleistogamy and seed heteromorphism in two perennial grasses. Evolutionary Trends in Plants 3, 127–136.Google Scholar
Cheplick, G.P and Grandstall, K. (1997) Effects of sand burial on purple sandgrass (Triplasis purpurea): the significance of seed heteromorphism. Plant Ecology 133, 79–89.CrossRefGoogle Scholar
Cheplick, G.P, Quinn, J.A. (1986) Self-fertilization in Amphicarpum purshii: its influence on fitness and variation of progeny from aerial panicles. The American Midland Naturalist 116, 394–402.Google Scholar
Cheplick, G.P and Sung, L.Y. (1998) Effects of maternal nutrient environment and maturation position on seed heteromorphism, germination, and seedling growth in Triplasis purpurea (Poaceae). International Journal of Plant Sciences 159, 338–350.Google Scholar
Christiansen, S., Abd El Monein, A.M., Cocks, P.S and Singh, M. (1996) Seed yield and hardseededness of two amphicarpic pasture legumes (Vicia sativa ssp. amphicarpa and Lathyrus ciliolatus) and two annual medics (Medicago rigidula and M. noeana). The Journal of Agricultural Science 126, 421–427.Google Scholar
Choo, Y.-H., Kim, H.-T., Nam, J.M. and Kim, J.G. (2014) Flooding effects on seed production of the amphicarpic plant Persicaria thunbergii . Aquatic Botany 119, 15–19.CrossRefGoogle Scholar
Clay, K. (1982) Environmental and genetic determinants of cleistogamy in a natural population of the grass Danthonia spicata . Evolution 36, 734–741.Google Scholar
Clay, K. (1983a) The differential establishment of seedlings from chasmogamous and cleistogamous flowers in natural populations of the grass Danthonia spicata (L.) Beauv. Oecologia 57, 183–188.CrossRefGoogle ScholarPubMed
Clay, K. (1983b) Variation in the degree of cleistogamy within and among species of the grass Danthonia . American Journal of Botany 70, 835–843.Google Scholar
Culley, T.M. (2000) Inbreeding depression and floral type fitness differences in Viola canadensis (Violaceae), a species with chasmogamous and cleistogamous flowers. Canadian Journal of Botany 78, 1420–1429.Google Scholar
Culley, T.M. (2002) Reproductive biology and delayed selfing in Viola pubescens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. International Journal of Plant Sciences 63, 113–122.CrossRefGoogle Scholar
Culley, T.M. and Klooster, M.R. (2007) The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms. The Botanical Review 73, 1–30.Google Scholar
Culley, T.M., Weller, S.G., Sakai, A.K. and Rankin, A.E. (1999) Inbreeding depression and selfing rates in a self-compatible, hermaphroditic species, Schiedea membranacea (Caryophyllaceae). American Journal of Botany 86, 980–987.Google Scholar
Darwin, C. (1889 [1876]) The effects of cross and self fertilization in the vegetable kingdom. New York: D. Appleton and Company,.Google Scholar
Dias, A.C.R., Carvalho, S.J.P., Brancalion, P.H.S., Novembre, A.D.L.C. and Christoffolet, P.J. (2009) Germinação de sementes aéreas pequenas de Trapoeraba (Commelina benghalensis). Planta Daninha, Viçosa-MG 27, 931–939.Google Scholar
Dobrenz, A.K. and Beetle, A.A. (1966) Cleistogenes in Danthonia . Journal of Range Management 19, 292–296.Google Scholar
Durlu, N. and Cornelius, D.R. (1970) A vetch producing both subterranean and aerial seeds. Agronomy Journal 62, 55–56.Google Scholar
Eckert, C.G., Kalisz, S., Geber, M.A., Sargent, R., Elle, E., Cheptou, P.-O., Goodwillie, C., Johnston, M.O., Kelly, J.K., Moeller, D.A., Porcher, E., Ree, R.H., Vallejo-Marín, and Winn, A.A. (2010) Plant mating systems in a changing world. Trends in Ecology and Evolution 25, 35–43.Google Scholar
Escobar, J.S., Cenci, A., Bolognini, J., Haudry, A., Laurent, S., David, J. and Glémin, S. (2010) An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64, 2855–2872.Google Scholar
Evenari, M., Kadouri, A. and Gutterman, Y. (1977) Eco-physiological investigations on the amphicarpy of Emex spinosa (L.) Campd. Flora 166, 223–238.Google Scholar
Ferreira, M.I. and Reinhardt, C.F. (1999) The role of temperature in the germination of subterranean and aerial seeds of Commelina benghalensis L. South African Journal of Plant and Soil 16, 165–168.CrossRefGoogle Scholar
Forrest, J. and Thomson, J.D. (2008) Pollen limitation and cleistogamy in subalpine Viola praemorsa . Botany 86, 511–519.Google Scholar
Gamisch, A., Fischer, G.A. and Comes, H.P. (2015) Multiple independent origins of auto-pollination in tropical orchids (Bulbophyllum) in light of the hypothesis of selfing as an evolutionary dead end. Evolutionary Biology 15, 192.Google Scholar
Gamm, R. (1983) Notes on amphicarpy – shown by the annual species Cardamine chenopodiifolia Pers. (Brassicaceae). Acta Botanica Neerlandica 32, 346.Google Scholar
Gara, B. and Muenchow, G. (1990) Chasmogamy/cleistogamy in Triodanis perfoliata (Campanulaceae): some CH/CL comparisons in fitness parameters. American Journal of Botany 77, 1–6.Google Scholar
Goddard, R.H., Webster, T.M., Carter, R. and Grey, T.L. (2009) Resistance of benghal dayflower (Commelina benghalensis) seeds to harsh environments and the implications for dispersal by mourning doves (Zenaida macroura) in Georgia, USA. Weed Science 57, 603–612.Google Scholar
Goldberg, E. E. and Igić, B. (2012) Tempo and mode in plant breeding system evolution. Evolution 66, 3701–3709.Google Scholar
Goldberg, E.E., Kohn, J.R., Lande, R., Robertson, K.A., Smith, S.A. and Igić, B. (2010) Species selection maintains self-incompatibility. Science 330, 493–495.Google Scholar
Goodwillie, C. (1999) Multiple origins of self-compatibility in Linanthus section Leptosiphon (Polemoniaceae): phylogenetic evidence from internal-transcribed-spacer sequence data. Evolution 53, 1387–1395.Google Scholar
Goodwillie, C., Kalisz, S. and Eckert, C.G. (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics 36, 47–79.Google Scholar
Hayden, W.J. and Fagan, C. (2016) Anatomy and pollination of cleistogamous flowers of benghal dayflower (Commelina benghalensis). Weed Science 64, 455–462.Google Scholar
Herman, A.C., Busch, J.W. and Schoen, D.J. (2012) Phylogeny of Leavenworthia S-alleles suggests unidirectional mating system evolution and enhanced positive selection following an ancient population bottleneck. Evolution 66, 1849–1861.Google Scholar
Huebner, C.D. (2011) Seed mass, viability, and germination of Japanese stiltgrass (Microstegium vimineum) under variable light and moisture conditions. Invasive Plant Science and Management 4, 274–283.Google Scholar
Husband, B.C. and Schemske, D.W. (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50, 54–70.Google Scholar
Igić, B., Bohs, L. and Kohn, J.R. (2003) Historical inferences from the self-incompatibility locus. New Phytologist 161, 97–105.Google Scholar
Igić, B., Bohs, L. and Kohn, J.R. (2006) Ancient polymorphism reveals unidirectional breeding system shifts. Proceedings of the National Academy of Sciences of the United States of America 103, 1359–1363.Google Scholar
Igić, B. and Busch, J.W. (2013) Is self-fertilization an evolutionary dead end? New Phytologist 198, 386–397.Google Scholar
Igić, B. and Kohn, J.R. (2006) The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60, 1098–1103.Google Scholar
Igić, B., Lande, R. and Kohn, J.R. (2008) Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169, 93–104.Google Scholar
Jain, S. K. (1976) The evolution of inbreeding in plants. Annual Review of Ecology and Systematics 7, 469–495.Google Scholar
Jasieniuk, M. and Lechowicz, M.J. (1987) Spatial and temporal variations in chasmogamy and cleistogamy in Oxalis montana (Oxalidaceae). American Journal of Botany 74, 1672–1680.Google Scholar
Kaul, V. and Koul, A.K. (2009) Sex expression and breeding strategy in Commelina benghalensis L. Journal of Biosciences 24, 977–990.Google Scholar
Kaul, V., Koul, A.K. and Sharma, M.C. (2000) The underground flower. Current Science 78, 39–44.Google Scholar
Kepart, S.R., Brown, E. and Hall, J. (1999) Inbreeding depression and partial selfing: evolutionary implications of mixed-mating in a coastal endemic, Silene douglasii var. oraria (Caryophyllaceae). Heredity 82, 543–660.CrossRefGoogle Scholar
Kim, J.H., Nam, J.M. and Kim, J. (2016) Effects of nutrient availability on the amphicarpic traits of Persicaria thunbergii . Aquatic Botany 131, 45–50.Google Scholar
Kim, S.Y. (1998) Growth and development of Commelina benghalensis L. from four seed types. Korean Journal of Weed Science 18, 42–47.Google Scholar
Kim, S.Y. and De Datta, S.K. (1993) Ultrastructure of seed coat and its relation to the germination of Commelina benghalensis 1. Seeds. Phillipine Journal of Weed Science 20, 1–7.Google Scholar
Kim, S.Y., De Datta, S.K. and Mercado, B.L. (1990) The effect of chemical and heat treatments on germination of Commelina benghalensis L. aerial seeds. Weed Research 30, 109–116.Google Scholar
Koller, D. and Roth, N. (1964) Studies on the ecological and physiological significance of amphicarpy in Gymnarrhena micrantha (Compositae). American Journal of Botany 51, 26–35.Google Scholar
Lande, R. and Porcher, E. (2015) Maintenance of quantitative genetic variance under partial self-fertilization, with implications for evolution of selfing. Genetics 200, 891–906.Google Scholar
Lande, R. and Schemske, D.W. (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39, 24–40.Google Scholar
Lande, R., Schemske, D.W. and Schultz, S.T. (1994) High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutations. Evolution 48, 965–978.Google Scholar
Le Corff, J. (1993) Effects of light and nutrient availability on chasmogamy and cleistogamy in an understory tropical herb, Calathea micans (Marantaceae). American Journal of Botany 80, 1392–1399.Google Scholar
Le Corff, J. (1996) Establishment of chasmogamous and cleistogamous seedlings of an ant-dispersed understory herb, Calathea micans (Marantaceae). American Journal of Botany 83, 155–161.Google Scholar
Le Corff, J. and Horvitz, C.C. (1995) Dispersal of seeds from chasmogamous and cleistogamous flowers in an ant-dispersed neotropical herb. Oikos 73, 59–64.Google Scholar
Lev-Yadun, S. (2000) Why are underground flowering and fruiting more common in Israel than anywhere else in the world? Current Science 79, 289.Google Scholar
Lloyd, A.G. (1992) Self- and cross-fertilization in plants. II. The selection of self-fertilization. International Journal of Plant Sciences 153, 370–380.Google Scholar
Lord, E.M. (1981) Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. The Botanical Review 47, 421–449.Google Scholar
Maheshwari, P. and Maheshwari, J.K. (1955) Floral dimorphism in Commelina forskalaei Vahl and C . benghalensis L. Phytomorphology 5, 413–422.Google Scholar
Maki, M. (1993) Outcrossing and fecundity advantage of female in gynodioecious Chionographis japonica var. kurohimensis (Liliaceae). American Journal of Botany 80, 629–634.Google Scholar
Mattila, T. and Salonen, V. (1995) Reproduction of Viola mirabilis in relation to light and nutrient availability. Canadian Journal of Botany 73, 1917–1924.Google Scholar
Masuda, M. and Yahara, T. (1992) Dispersal of chasmogamous and cleistogamous seeds in Viola hondoensis W. Backer et H. Boiss. Botanical Magazine Tokyo 105, 323–326.Google Scholar
Matsuo, M., Michinaga, H., Terao, H. and Tsuzuki, E. (2004) Aerial seed germination and morphological characteristics of juvenile seedlings in Commelina benghalensis L. Weed Biology and Management 4, 148–153.Google Scholar
McCall, C., Mitchell-Olds, T. and Waller, D.M. (1989) Fitness consequences of outcrossing in Impatiens capensis: tests of the frequency-dependent and sib-competition models. Evolution 43, 1075–1084.Google Scholar
McNamara, J. and Quinn, J.A. (1977) Resource allocation and reproduction in populations of Amphicarpum purshii (Gramineae). American Journal of Botany 54, 17–23.Google Scholar
Oakley, C.G., Moriuchi, K.S and Winn, A.A. (2007) The maintenance of outcrossing in predominantly selfing species: ideas and evidence from cleistogamous species. Annual Review of Ecology, Evolution and Systematics 38, 437–457.Google Scholar
Oakley, C.G. and Winn, A.A. (2008) Population-level and family-level inbreeding depression in a cleistogamous perennial. International Journal of Plant Sciences 169, 523–530.Google Scholar
Olivieri, I. Swan, M. and Pierre-Henri, G. (1983) Reproductive system and colonizing strategy of two species of Carduus (Compositae). Oecologia 60, 114–117.Google Scholar
Opedal, Ø.H., Armbruster, W.S. and Pélabon, C. (2015) Inbreeding effects in a mixed-mating vine: effects of mating history, pollen competition and stress on the cost of inbreeding. AoB Plants 7, plv133. doi: 10.1093/aobpla/plv133 Google Scholar
Ortiz, P.L., Berjano, R., Talavera, M. and Arista, M. (2009) The role of resources and architecture in modeling floral variability for the monoecious amphicarpic Emex spinosa (Polygonaceae). American Journal of Botany 96, 2062–2073.Google Scholar
Philipson, M.A. (1986) A re-assessment of the form of reproduction in Danthonia spicata (L.) Beauv. New Phytologist 103, 231–243.Google Scholar
Plitmann, U. (1973) Biological flora of Israel. 4. Vicia sativa subsp. amphicarpa (Dorth.) Aschers. & Graebn. Israel Journal of Botany 22, 178–194.Google Scholar
Porcher, E. and Lande, R. (2005) The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. Journal of Evolutionary Biology 18, 497–508.Google Scholar
Porras, R. and Muñoz, J.M. (2000) Achene heteromorphism in the cleistogamous species Centaurea melitensis . Acta Oecologica 21, 231–243.Google Scholar
Riar, M.K., Webster, T.M., Brecke, B.J., Jordan, D.L., Burton, M.G., Telenko, D.P. and Rufty, T.W. (2012) Benghal dayflower (Commelina benghalensis) seed viability in soil. Weed Science 60, 589–592.Google Scholar
Ruiz de Clavijo, E. (1995) The ecological significance of fruit heteromorphism in the amphicarpic species Catananche lutea (Asteraceae). International Journal of Plant Sciences 156, 824–833.Google Scholar
Ruiz de Clavijo, E. and Jiménez, M.J. (1998) The influence of achene type and plant density on growth and biomass allocation in the heterocarpic annual Catananche lutea (Asteraceae). International Journal of Plant Sciences 159, 637–647.Google Scholar
Sabila, M.F., Grey, T.L., Webster, T.M., Vencill, W.K. and Shilling, D.G. (2012) Evaluation of factors that influence benghal dayflower (Commelina benghalensis) seed germination and emergence. Weed Science 60, 75–80.Google Scholar
Sadeh, A., Guterman, H., Gersani, M. and Ovadia, O. (2009) Plastic bet-hedging in an amphicarphic annual: an integrated strategy under variable conditions. Evolutionary Ecology 23, 373–388.Google Scholar
Sander, T.M. and Matthies, D. (2016) The effects of stress intensity and stress type on inbreeding depression in Silene vulgaris . Evolution 70, 1225–1238.Google Scholar
Santos, I.C., Ferreira, F.A., Miranda, G.V. and Santos, L.D.T. (2001) Germinação de sementes aéreas e subterrâneas de Commelina benghalensis . Planta Daninha, Viçosa-MG 19, 163–170.Google Scholar
Schemski, D.W. (1978) Evolution of reproductive characteristics in Impatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Ecology 59, 596–613.Google Scholar
Schemske, D. and Lande, R. (1985) The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39, 41–52.Google Scholar
Schively, A.F. (1897) Contributions to the life history of Amphicarpaea monoica [ = A. bracteata]. Publications of the University of Pennsylvania. Contributions from the Botanical Laboratory 1, 270–363 + plates xxix-xxxvi.Google Scholar
Schmitt, J. and Ehrhardt, D.W. (1990) Enhancement of inbreeding depression by dominance and suppression in Impatiens capensis . Evolution 44, 269–278.Google Scholar
Schmitt, J. and Gamble, S.E. (1990) The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis. Evolution 44, 2022–2030.Google Scholar
Schnee, B.K. and Waller, D.M. (1986) Reproductive behavior of Amphicarpaea bracteata (Leguminosae), an amphicarpic annual. American Journal of Botany 73, 376–386.Google Scholar
Schoen, D.J. (1984) Cleistogamy in Microlaena polynoda (Gramineae): an examination of some model predictions. American Journal of Botany 71, 711–719.Google Scholar
Schoen, D.J., Johnston, M.O., L'Heureux, A.-M. and Marsolais, J.V. (1997) Evolutionary history of the mating system in Amsinckia (Boraginaceae). Evolution 51, 1090–1099.Google Scholar
Schoen, D. J. and Lloyd, D.G. (1984) The selection of cleistogamy and heteromorphic diaspores. Biological Journal of the Linnean Society 23, 303–322.Google Scholar
Schoen, D. J., Morgan, M.T. and Bataillon, T. (1996) How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Philosophical Transactions of the Royal Society of London B 351, 1281–1290.Google Scholar
Schutzenhofer, M.R. (2007) the effect of herbivory on the mating system of congeneric native and exotic Lespedeza species. International Journal of Plant Sciences 168, 1021–1026.Google Scholar
Sermons, S.M., Burton, M.G. and Rufty, T.W. (2008) Temperature response of benghal dayflower (Commelina benghalensis): implications for geographic range. Weed Science 56, 707–713.Google Scholar
Shaltout, K.H., Al-Sodany, Y.M., El-Keblawy, and Ahmed, A.M. (2009) Effect of seed type, water regime and partial cutting on the growth performance of Emex spinosa (L.) Campd. in Egypt. Journal of Applied Science Research 5, 648–661.Google Scholar
Stebbins, G.L. (1950) Variation and Evolution in Plants. New York: Columbia University Press.Google Scholar
Stebbins, G.L. (1957) Self fertilization and population variability in the higher plants. The American Naturalist 91, 337–354.Google Scholar
Stebbins, G.L. (1974) Flowering Plants: Evolution Above the Species Level. Cambridge, MA: Belknap Press of Harvard University Press.Google Scholar
Steinbachs, J.E. and Holsinger, K.E. (2002) S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Molecular Biology and Evolution 19, 825–829.Google Scholar
Takebayashi, N. and Morrell, P.L. (2001) Is self-fertilization an evolutionary dead end? Revisting an old hypothesis with genetic theories and a macroevolutionary approach. American Journal of Botany 88, 1143–1150.Google Scholar
Trapp, E.J. (1988). Dispersal of heteromorphic seeds in Amphicarpaea bracteata (Fabaceae). American Journal of Botany 75, 1535–1539.Google Scholar
Trapp, E.J. and Hendrix, S.D. (1988) Consequences of a mixed reproductive system in the hog peanut, Amphicarpaea bracteata (Fabaceae). Oecologia 75, 285–290.Google Scholar
Uphof, J.C.T. (1938) Cleistogamic flowers. The Botanical Review 4, 21–49.Google Scholar
Venable, D.L. (1985a) Ecology of achene dimorphism in Heterotheca latifolia. III. Consequences of varied water availability. Journal of Ecology 73, 757–763.Google Scholar
Venable, D.L. (1985b) The evolutionary ecology of seed heteromorphism. The American Naturalist 126, 577–595.Google Scholar
Vogler, D.W. and Kalisz, S. (2001) Sex among the flowers: the distribution of plant mating systems. Evolution 55, 202–204.Google Scholar
Voll, E., Brighenti, A.M., Gazziero, D.L.P. and Adegas, E.F.S. (2002) Aspectos fisiológicos da germinação de sementes de trapoeraba (Commelina benghalensis L.). Revista Brasileira de Sementes 24, 162–168.Google Scholar
Walker, S.R. and Evenson, J.P. (1985a) Biology of Commelina benghalensis L. in south-eastern Queensland. 1. Growth, development and seed production. Weed Research 25, 239–244.Google Scholar
Walker, S.R. and Evenson, J.P. (1985b) Biology of Commelina benghalensis L. in south-eastern Queensland. 2. Seed dormancy, germination and emergence. Weed Research 25, 245–250.Google Scholar
Waller, D.M. (1982) Factors influencing seed weight in Impatiens capensis (Balsaminaceae). American Journal of Botany 69, 1470–1475.Google Scholar
Waller, D.M. (1984) Differences in fitness between seedlings derived from cleistogamous and chasmogamous flowers in Impatiens capensis . Evolution 38, 427–440.Google Scholar
Weatherwax, P. (1928) Cleistogamy in two species of Danthonia . Botanical Gazette 85, 104–109.Google Scholar
Weiss, P.W. (1980) Germination, reproduction and interference in the amphicarpic annual Emex spinosa (L.) Campd. Oecologia 45, 244–251.Google Scholar
Winn, A.A., Elle, E., Kalisz, S., Cheptou, P.-O., Eckert, C.G., Goodwillie, C., Johnston, M.O., Moeller, D.A., Ree, R.H., Sargent, R.D and Vallejo-Marin, M. (2011) Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65, 3339–3359.Google Scholar
Winn, A.A. and Moriuchi, K.S. (2009) The maintenance of mixed mating by cleistogamy in the perennial violet Viola septemloba (Violaceae). American Journal of Botany 96, 2074–2079.Google Scholar
Wright, S.I., Kalisz, S. and Slotte, T. (2013) Evolutionary consequences of self-fertilization in plants. Proceedings of the Royal Society B 280, 20130133.Google Scholar
Zhang, K., Baskin, J.M., Baskin, C.C., Yang, X. and Huang, Z. (2015) Lack of divergence in seed ecology of two Amphicarpaea (Fabaceae) species disjunct between eastern Asia and eastern North America. American Journal of Botany 102, 860–869.Google Scholar
Zhang, Y., Yang, J. and Rao, G.-Y. (2005) Genetic diversity of an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae) based on RAPD markers. Biochemical Systematics and Ecology 33, 1246–1257.Google Scholar
Zhang, Y., Yang, J. and Rao, G.-Y. (2006) Comparative study on the aerial and subterranean flower development in Amphicarpaea edgeworthii Benth. (Leguminosae: Papilionoideae), an amphicarpic species. International Journal of Plant Sciences 167, 943–949.Google Scholar