Skip to main content
Log in

Stylar polymorphism, reciprocity and incompatibility systems in Nymphoides montana (Menyanthaceae) endemic to southeastern Australia

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Heterostyly is a stylar polymorphism that has been shaped by the evolution of floral characters adapted for efficient pollen transfer. Different types of stylar polymorphism are described in which the discrete characterization of the exact polymorphic type (e.g., distyly vs. stigma-height dimorphism) requires detailed floral measurements (e.g., sex-organ reciprocity). In clonal and aquatic Nymphoides montana, although the presence of two floral morphs that contain styles of two lengths has been previously reported, no studies have quantitatively estimated the level of reciprocity and/or described the stylar condition. Morphological variations and incompatibility relationships were explored between the two morphs in three southeastern Australian populations. In this study, one population is characterized as stigma-height dimorphism (i.e., two morphs with discrete variation in stigma height but little variation in anther height), whereas the other two populations are typical distylous (i.e., two morphs for reciprocal stigma and anther height). Nymphoides montana is dimorphic in a wide range of ancillary characters, including corolla size, stigma size, shape and papillae morphology, and pollen size, number and exine sculpture. Following glasshouse pollinations, full incompatibility systems were observed in the distylous populations, whereas the stigma-height dimorphic population showed between-morph variation in the extent of incompatibility. Despite the variation in sex-organ reciprocity and incompatibility, other lines of evidence appear to assure the maintenance of the stylar polymorphism in the N. montana study populations. All populations are nearly isoplethic (i.e., both morphs in equal frequencies), which is indicative of balanced polymorphisms that appear to be maintained by legitimate pollen transfer between the morphs.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arceo-Gómez G, Martínez ML, Parra-Tabla V, García-Franco JG (2011) Anther and stigma morphology in mirror-image flowers of Chamaecrista chamaecristoides (Fabaceae): implications for buzz pollination. Plant Biol 13:19–24

    Article  PubMed  Google Scholar 

  • Arroyo J, Barrett SCH (2000) Discovery of distyly in Narcissus (Amaryllidaceae). Am J Bot 87:748–751

    Article  PubMed  CAS  Google Scholar 

  • Arroyo J, Barrett SCH, Hidalgo R, Cole WW (2002) Evolutionary maintenance of stigma-height dimorphism in Narcissus papyraceus (Amaryllidaceae). Am J Bot 89:1242–1249

    Article  PubMed  Google Scholar 

  • Aston HI (1982) New Australian species of Nymphoides Séguier (Menyanthaceae). Muelleria 5:35–51

    Google Scholar 

  • Australia’s Virtual Herbarium (2007) via Centre for Plant Biodiversity Research, Council of Heads of Australian Herbaria, viewed at 10 September 2007. <http://www.cpbr.gov.au/cgi-bin/avh.cgi>

  • Baker HG (1955) Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9:347–349

    Article  Google Scholar 

  • Barrett SCH (1990) The evolution and adaptive significance of heterostyly. Trends Ecol Evol 5:144–148

    Article  PubMed  CAS  Google Scholar 

  • Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284

    Article  PubMed  CAS  Google Scholar 

  • Barrett SCH, Husband BC (1990) Variation in outcrossing rate in Eichhornia paniculata: the role of demographic and reproductive factors. Plant Species Biol 5:41–56

    Article  Google Scholar 

  • Barrett SCH, Morgan MT, Husband BC (1989) The dissolution of a complex polymorphism: The evolution of self-fertilization in tristylous Eichhornia paniculata (Pontederiaceae). Evolution 43:1398–1416

    Article  Google Scholar 

  • Barrett SCH, Lloyd DG, Arroyo J (1996) Stylar polymorphisms and the evolution of heterostyly in Narcissus (Amaryllidaceae). In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, pp 339–376

    Google Scholar 

  • Barrett SCH, Jesson LK, Baker AM (2000) The evolution and function of stylar polymorphisms in flowering plants. Ann Bot 85:253–265

    Article  Google Scholar 

  • Brys R, Jacquemyn H, Hermy M (2007) Impact of mate availability, population size, and spatial aggregation of morphs on sexual reproduction in a distylous, aquatic plant. Am J Bot 94:119–127

    Article  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B (1979) A model for the evolution of distyly. Am Nat 114:467–498

    Article  Google Scholar 

  • Cheptou P-O, Schoen DJ (2007) Combining population genetics and demographical approaches in evolutionary studies of plant mating systems. Oikos 116:271–279

    Article  Google Scholar 

  • Cohen JI, Litt A, Davis JI (2012) Comparative floral development in Lithospermum (Boraginaceae) and implications for the evolution and development of heterostyly. Am J Bot 99:797–805

    Article  PubMed  Google Scholar 

  • Cruzan MB, Barrett SCH (1993) Contribution of cryptic incompatibility to the mating system of Eichhornia paniculata (Pontederiaceae). Evolution 47:925–934

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Darwin C (1878) The effects of cross and self-fertilisation in the vegetable kingdom (2nd edition). John Murray, London

    Google Scholar 

  • de Castro CC, Araujo AC (2004) Distyly and sequential pollinators of Psychotria nuda (Rubiaceae) in the Atlantic rain forest, Brazil. Plant Syst Evol 244:131–139

    Article  Google Scholar 

  • Dulberger R (1992) Floral polymorphisms and their functional significance in the heterostylous syndrome. In: Barrett SCH (ed) Evolution and function of heterostyly, vol 15. Springer, Berlin, pp 41–84

    Google Scholar 

  • Dulberger R, Ornduff R (2000) Stigma morphology in distylous and non-heterostylous species of Villarsia (Menyanthaceae). Plant Syst Evol 225:171–184

    Article  Google Scholar 

  • Eckert CG, Barrett SCH (1995) Style morph ratios in tristylous Decodon verticillatus (Lythraceae): Selection vs. historical contingency. Ecology 76:1051–1066

    Article  Google Scholar 

  • Faivre AE, McDade LA (2001) Population-level variation in the expression of heterostyly in three species of Rubiaceae: does reciprocal placement of anthers and stigmas characterize heterostyly? Am J Bot 88:841–853

    Article  PubMed  CAS  Google Scholar 

  • Ferrero V, Arroyo J, Vargas P, Thompson JD, Navarro L (2009) Evolutionary transitions of style polymorphisms in Lithodora (Boraginaceae). Perspect Plant Ecol 11:111–125

    Article  Google Scholar 

  • Ferrero V, Castro S, Sánchez J, Navarro L (2011a) Stigma–anther reciprocity, pollinators, and pollen transfer efficiency in populations of heterostylous species of Lithodora and Glandora (Boraginaceae). Plant Syst Evol 291:267–276

    Article  Google Scholar 

  • Ferrero V, Chapela I, Arroyo J, Navarro L (2011b) Reciprocal style polymorphisms are not easily categorised: the case of heterostyly in Lithodora and Glandora (Boraginaceae). Plant Biol 13:7–18

    Article  PubMed  Google Scholar 

  • Ferrero V, Arroyo J, Castro S, Navarro L (2012) Unusual heterostyly: style dimorphism and self-incompatibility are not tightly associated in Lithodora and Glandora (Boraginaceae). Ann Bot 109:655–665

    Article  PubMed  CAS  Google Scholar 

  • Fisher RA (1941) The theoretical consequences of polyploid inheritance for the mid style form of Lythrum salicaria. Ann Hum Genet 11:31–38

    Article  Google Scholar 

  • Ganders FR (1979) The biology of heterostyly. N Z J Bot 17:607–635

    Article  Google Scholar 

  • Haddadchi A (2008) Floral variation and breeding system in distylous and homostylous species of clonal aquatic Nymphoides (Menyanthaceae). PhD dissertation, University of New England, Armidale NSW Australia

  • Jacobs SWL (1992) Menyanthaceae. In: Harden GJ (ed) Flora of New South Wales, vol 3. Royal Botanic Gardens, Sydney, pp 506–508

    Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot

    Google Scholar 

  • Lloyd DG (1982) Selection of combined versus separate sexes in seed plants. Am Nat 120:571–585

    Article  Google Scholar 

  • Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. N Z J Bot 24:135–162

    Article  Google Scholar 

  • Lloyd DG, Webb CJ (1992a) The evolution of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly, vol 15. Springer, Berlin, pp 151–178

    Google Scholar 

  • Lloyd DG, Webb CJ (1992b) The selection of heterostyly. In: Barret SCH (ed) Evolution and function of heterostyly, vol 15. Springer, Berlin, pp 179–208

    Google Scholar 

  • Naiki A (2012) Heterostyly and the possibility of its breakdown by polyploidization. Plant Species Biol 27:3–29

    Article  Google Scholar 

  • Ornduff R (1966) The origin of dioecism from heterostyly in Nymphoides (Menyanthaceae). Evolution 20:309–314

    Article  Google Scholar 

  • Ornduff R (1986) Comparative fecundity and population composition of heterostylous and non-heterostylous species of Villarsia (Menyanthaceace) in Western Australia. Am J Bot 73:282–286

    Article  Google Scholar 

  • Ornduff R (1988) Distyly and monomorphism in Villarsia (Menyanthaceae): some evolutionary considerations. Ann Mo Bot Gard 75:761–767

    Article  Google Scholar 

  • Pailler T, Thompson J (1997) Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Reunion Island. Am J Bot 84:315–327

    Article  PubMed  CAS  Google Scholar 

  • Pauw A (2005) Inversostyly: a new stylar polymorphism in an oil-secreting plant, Hemimeris racemosa (Scrophulariaceae). Am J Bot 92:1878–1886

    Article  PubMed  Google Scholar 

  • Pérez-Barrales R, Vargas P, Arroyo J (2006) New evidence for the Darwinian hypothesis of heterostyly: breeding systems and pollinators in Narcissus sect. Apodanthi. New Phytol 171:553–567

    Article  PubMed  Google Scholar 

  • Price MV, Waser NM (1982) Population structure, frequency-dependent selection, and the maintenance of sexual reproduction. Evolution 36:35–43

    Article  Google Scholar 

  • Richards AJ (1997) Plant breeding systems, vol 2, 2nd edn. Chapman and Hall, London

    Google Scholar 

  • Richards JH, Barrett SCH (1992) The development of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly, vol 15. Springer, New York, pp 85–128

    Google Scholar 

  • Richards JH, Koptur S (1993) Floral variation and distyly in Guettarda scabra (Rubiaceae). Am J Bot 80:31–40

    Article  Google Scholar 

  • Rodrigues Faria R, Ferrero V, Navarro L, Araujo A (2012) Flexible mating system in distylous populations of Psychotria carthagenensis Jacq. (Rubiaceae) in Brazilian Cerrado. Plant Syst Evol 298:619–627

    Article  Google Scholar 

  • Sánchez JM, Ferrero V, Navarro L (2008) A new approach to the quantification of degree of reciprocity in distylous (sensu lato) plant populations. Ann Bot 102:463–472

    Article  PubMed  Google Scholar 

  • Satterthwaite FE (1946) An approximate distribution of estimates of variance components. Biometrics Bull 2:110–114

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, vol 3. W. H Freeman and Company, New York

    Google Scholar 

  • Thompson JD, Dommee B (2000) Morph-specific patterns of variation in stigma height in natural populations of distylous Jasminum fruticans. New Phytol 148:303–314

    Article  Google Scholar 

  • Thompson FL, Hermanutz LA, Innes DJ (1998) The reproductive ecology of island populations of distylous Menyanthes trifoliata (Menyanthaceae). Can J Bot 76:818–828

    Google Scholar 

  • Tippery NP, Les DH (2011) Evidence for the hybrid origin of Nymphoides montana Aston (Menyanthaceae). Telopea 13:285–294

    Google Scholar 

  • Tippery NP, Les DH, Padgett DJ, Jacobs SWL (2008) Generic circumscription in Menyanthaceae: a phylogenetic evaluation. Syst Bot 33:598–612

    Article  Google Scholar 

  • Vaughton G, Ramsey M (2010) Pollinator-mediated selfing erodes the flexibility of the best-of-both-worlds mating strategy in Bulbine vagans. Funct Ecol 24:374–382

    Article  Google Scholar 

Download references

Acknowledgments

I wish to thank G. Vaughton and M. Ramsey for comments on the earlier draft and assistance with designing the experiments, V. Ferrero and J. M. Sánchez for valuable suggestions and discussions, M. Fatemi and L. Vary for comments on the final draft, I. Simpson and M. Fatemi for field assistance, R. Willis for glasshouse assistance, P. Littlefield in the scanning electron microscopy unit and I. Telford in the NCW Beadle Herbarium. This study was supported by the financial assistance of the International Postgraduate Research Scholarship (IPRS) and UNE Research Assistantship (UNERA) scholarships and the School of Environmental and Rural Science, UNE.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Azadeh Haddadchi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haddadchi, A. Stylar polymorphism, reciprocity and incompatibility systems in Nymphoides montana (Menyanthaceae) endemic to southeastern Australia. Plant Syst Evol 299, 389–401 (2013). https://doi.org/10.1007/s00606-012-0729-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-012-0729-y

Keywords

Navigation