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Part of the book series: Monographs on Theoretical and Applied Genetics ((GENETICS,volume 15))

Abstract

Charles Darwin was fascinated by the phenomenon of heterostyly. He described (1862, 1877) how he first thought that pin and thrum plants of Primula species represented female and male sexes respectively, but found that they were both functionally hermaphroditic. He demonstrated the infertility of self-pollinations and crosses between plants of the same form, and concluded that the two forms, although hermaphrodites, are “related to each other like males and females… [because plants of each form]… must unite with one of the other form” (Darwin 1862)3.

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References

  • Anderson WR (1973) A morphological hypothesis for the origin of heterostyly in the Rubiaceae. Taxon 22:537–542

    Article  Google Scholar 

  • Anderson JM, Barrett SCH (1986) Pollen tube growth in tristylous Pontederia cordata (Pon-tederiaceae). Can J Bot 64:2602–2607

    Article  Google Scholar 

  • Baker HG (1962) Heterostyly in the Connaraceae, with special reference by Byrsocarpus coccineus. Bot Gaz Chicago 123:206–211

    Article  Google Scholar 

  • Baker HG (1964) Variation in style length in relation to outbreeding in Mirabilis (Nyctaginaceae). Evolution 18:507–509

    Article  Google Scholar 

  • Baker HG (1966) The evolution, functioning and breakdown of heteromorphic incompatibility systems. I. The Plumbaginaceae. Evolution 20:349–368

    Article  Google Scholar 

  • Barrett SCH, Richards JH (1990) Heterostyly in tropical plants. In: Gottsberger G, Prance GT (eds) Reproductive biology and evolution of tropical woody angiosperms. Mem N Y Bot Gard 55:35–61

    Google Scholar 

  • Barrett SCH, Shore JS (1987) Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41:340–354

    Article  Google Scholar 

  • Bateman AJ (1952) Trimorphism and self-incompatibility in Narcissus. Nature (Lond) 170:496–497

    Article  Google Scholar 

  • Bateman AJ (1954a) The genetics of Narcissus. 1 — sterility. Daffodil Tulip Year Book 1954:23–29

    Google Scholar 

  • Bateman AJ (1954b) Self-incompatibility systems in angiosperms. II. Iberis amarà. Heredity 8:305–332

    Article  Google Scholar 

  • Bawa KS, Beach JH (1983) Self-incompatibility systems in the Rubiaceae of a tropical lowland wet forest. Am J Bot 70:1281–1288

    Article  Google Scholar 

  • Beach JH, Bawa KS (1980) Role of pollinators in the evolution of dioecy from distyly. Evolution 34:1138–1142

    Article  Google Scholar 

  • Bir Bahadur (1970) Heterostyly in Hedyotis nigricans (Lam.) Fosb. J Genet 60:175–177

    Article  Google Scholar 

  • Brewbaker JL (1959) Biology of the angiosperm pollen grain. Indian J Genet Plant Breed 19:121–133

    Google Scholar 

  • Brown N, Crowden RK (1984) Evidence of heterostyly in Epacris impressa Labill. (Epacridaceae). In: Williams EG, Knox RB (eds) Pollination 1984: Proceedings of a Symposium held at the Plant Cell Biology Research Centre, University of Melbourne. Melbourne Univ Press, Melbourne, pp 187–193

    Google Scholar 

  • Charlesworth D (1979) The evolution and breakdown of tristyly. Evolution 33:486–498

    Article  Google Scholar 

  • Charlesworth D (1982) On the nature of the self-incompatibility locus in homomorphic and heteromorphic systems. Am Nat 119:732–735

    Article  Google Scholar 

  • Charlesworth B, Charlesworth D (1979) The maintenance and breakdown of distyly. Am Nat 114:499–513

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Correns C (1924) Lang- und kurzgrifflige Sippen bei Veronica gentianoides. Biol Zentralbl 42:610–630

    Google Scholar 

  • Cronquist A (1981) An integrated system of classification of flowering plants. Columbia Univ Press, New York

    Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York

    Google Scholar 

  • Crowe LK (1964) The evolution of outbreeding in plants. I. The angiosperms. Heredity 19:435–457

    Article  Google Scholar 

  • Dahlgren R (1983) General aspects of angiosperm evolution and macrosystematics. Nord J Bot 3:119–149

    Article  Google Scholar 

  • Darwin C (1862) On the two forms, or dimorphic conditions in the species of Primula, and on their remarkable sexual relations. J Linn Soc Lond Bot 6:77–96

    Article  Google Scholar 

  • Darwin C (1864) On the two forms, or dimorphic conditions in the species of Primula, and on their remarkable sexual relations. J Linn Soc Lond Bot 6:77–96

    Google Scholar 

  • Darwin C (1865) On the sexual relations of the three forms of Lythrum salicaria. J Linn Soc Lond Bot 8:169–196

    Google Scholar 

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

    Google Scholar 

  • Dowrick VPJ (1956) Heterostyly and homostyly in Primula obconica. Heredity 10:219–236

    Article  Google Scholar 

  • Dulberger R (1964) Flower dimorphism and self-incompatibility in Narcissus tazetta L. Evolution 18:361–363

    Article  Google Scholar 

  • Dulberger R (1970) Floral dimorphism in Anchusa hybrida Ten. Isr J Bot 19:37–41

    Google Scholar 

  • Dulberger R (1975a) S-gene action and the significance of characters in the heterostylous syndrome. Heredity 35:407–415

    Article  Google Scholar 

  • Dulberger R (1975b) Intermorph structural differences between stigmatic papillae and pollen grains in relation to incompatibility in Plumbaginaceae. Proc R Soc Lond Ser B 188:257–274

    Article  Google Scholar 

  • Dulberger R (1987) Fine structure and cytochemistry of the stigma surface and incompatibility in some distylous Linum species. Ann Bot 59:203–217

    Google Scholar 

  • Eckenwalder JE, Barrett SCH (1986) Phylogenese systematics of Pontederiaceae. Syst Bot 11:373–391

    Article  Google Scholar 

  • Ernst A (1955) Self-fertility in monomorphic primulas. Genetica 27:391–448

    Article  Google Scholar 

  • Faegri K, van der Pijl L (1979) The principles of pollination ecology, 3rd edn. Pergamon, Oxford New York

    Google Scholar 

  • Fernandes A (1964) Contribution à la connaissance de la génétique de l’hétérostylie chez le genre Narcissus L. I. Resultats de quelques croisements. Bol Soc Broteriana 38:81–96

    Google Scholar 

  • Fernandes A (1966) Contribution à la connaissance de la génétique de l’hétérostylie chez le genre

    Google Scholar 

  • Narcissus L. II. L’hétérostylie chez quelques populations de N triandrus var. cernuus et N. triandrus var. concolor. Genet Iber 17:215–239

    Google Scholar 

  • Fisher RA (1922) On the dominance ratio. Proc R Soc Edinb 52:321–341

    Google Scholar 

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

    Article  Google Scholar 

  • Ghosh S, Shivanna KR (1980) Pollen-pistil interaction in Linum grandiflorum. Planta 149:257–261

    Article  CAS  Google Scholar 

  • Gibbs PE (1986) Do homomorphic and heteromorphic self-incompatibility systems have the same sporophytic mechanism? Plant Syst Evol 154:285–323

    Article  Google Scholar 

  • Golynskaya EL, Bashkirova NV, Tomchuk NN (1976) Phytohemagglutins of the pistil in Primula as possible proteins of generative incompatibility. Sov Plant Physiol 23:69–76

    Google Scholar 

  • Haidane JBS (1927) A mathematical theory of natural and artificial selection. Part V. Selection and mutation. Proc Camb Philos Soc 23:838–844

    Article  Google Scholar 

  • Hemsley JH (1956) Connaraceae. In: Turrill WB, Milne-Redhead E (eds) Flora of Tropical East Africa. Crown Agents for Overseas Governments and Administrations, Lond

    Google Scholar 

  • Henriques JA (1887) Amaryllideas de Portugal. Bol Soc Broteriana 5:159–174

    Google Scholar 

  • Henriques JA (1888) Additamento ao catalogo das Amaryllideas de Portugal. Bol Soc Broteriana 6:45–47

    Google Scholar 

  • Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Ann Bot 41:1233–1258

    Google Scholar 

  • Heywood VH (ed) (1978) Flowering plants of the world. Oxford Univ Press, Oxford Lond

    Google Scholar 

  • Hildebrand F (1866) Ueber den Trimorphisms in der Gattung Oxalis. Monatsber König Preuss Akad Wiss Berl 1866:352–374

    Google Scholar 

  • Imrie BC, Kirkman CJ, Ross DR (1972) Computer simulation of a sporophytic self-incompatibility breeding system. Aust J Biol Sci 25:343–349

    Google Scholar 

  • Jernstedt JA (1982) Floral variation in Chlorogalum angustifolium. Madrono 29:87–94

    Google Scholar 

  • Lawrence MJ, Marshall DF, Curtis VE, Fearon CH (1985) Gametophytic self-incompatibility re-examined: a reply. Heredity 54:131–138

    Article  Google Scholar 

  • Lemmens RHMJ (1989) Heterostyly in Connaraceae. Acta Bot Neerl (Abstr) 38:224–225

    Google Scholar 

  • Leppik EE (1972) Origin and evolution of bilateral symmetry in flowers. Evol Biol 5:49–72

    Article  Google Scholar 

  • Lewis D (1943) The physiology of incompatibility in plants. II. Linum grandiflorum. Ann Bot 7:115–122

    Google Scholar 

  • Lewis D (1949) Incompatibility in flowering plants. Biol Rev Camb Philos Soc 24:472–496

    Article  Google Scholar 

  • Lewis D (1960) Genetic control of specificity and activity of the S antigen in plants. Proc R Soc Lond Ser B 151:468–477

    Article  CAS  Google Scholar 

  • Lewis D (1949) Incompatibility in flowering plants. Biol Rev Camb Philos Soc 24:472–496

    Article  Google Scholar 

  • Lewis D (1960) Genetic control of specificity and activity of the S antigen in plants. Proc R Soc Lond Ser B 151:468–477

    Article  CAS  Google Scholar 

  • Lewis D (1982) Incompatibility, stamen movement and pollen economy in a heterostyled tropical forest tree, Cratoxylum formosum (Guttiferae). Proc R Soc Lond Ser B 214:273–283

    Article  Google Scholar 

  • Lewis D, Rao AN (1971) Evolution of dimorphim and population polymorphism in Pemphis acidula Forst. Proc R Soc Lond Ser B 118:247–256

    Google Scholar 

  • Lloyd DG (1979) Some reproductive factors affecting the selection of self-fertilisation in plants. Am Nat 113:67–79

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lloyd DG, Yates JMA (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphroditic plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36:903–913

    Article  Google Scholar 

  • Lloyd DG, Webb CJ, Dulberger R (1990) Heterostyly in species of Narcissus (Amaryllidaceae), Hugonia (Linaceae) and other disputed cases. Plant Syst Evol 172:215–227

    Article  Google Scholar 

  • Lord EM, Eckard KJ (1984) Incompatibility between the dimorphic flowers of Collomia gran-diflora, a cleistogamous species. Science 223:695–696

    Article  PubMed  CAS  Google Scholar 

  • Lord EM, Eckard KJ (1986) Ultrastructure of the dimorphic pollen and stigmas of the cleistogamous species, Collomia grandiflora. Protoplasma 132:12–22

    Article  Google Scholar 

  • Martin FW (1965) Distyly and incompatibility in Turnera ulmifolia. Bull Torrey Bot Club 92:185–192

    Article  Google Scholar 

  • Mather K, de Winton D (1941) Adaptation and counter-adaptation of the breeding system in Primula. Ann Bot 5:297–311

    Google Scholar 

  • Muenchow G (1982) A loss-of-alleles model for the evolution of distyly. Heredity 49:81–93

    Article  Google Scholar 

  • Mulcahy DL, Mulcahy GB (1983) Gametophytic self-incompatibility reexamined. Science 220:1247–1251

    Article  PubMed  CAS  Google Scholar 

  • Nagylaki T (1976) A model for the evolution of self-fertilisation and vegetation reproduction. J Theor Biol 58:55–58

    Article  PubMed  CAS  Google Scholar 

  • Nettancourt D de (1977) Incompatibility in angiosperms. Springer, Berlin Heidelberg New York

    Google Scholar 

  • O’Brien SP, Calder DM (1989) The breeding biology of Epacris impressa. Is this species, hetero-stylous? Aust J Bot 37:43–54

    Article  Google Scholar 

  • Olesen JM (1987) Heterostyly, homostyly, and long-distance dispersal of Menyanthes trifoliata to Greenland. Can J Bot 65:1509–1513

    Article  Google Scholar 

  • Ornduff R (1972) The breakdown of trimorphic incompatibility in Oxalis section Corniculatae. Evolution 26:52–65

    Article  Google Scholar 

  • Ornduff R (1974) Heterostyly in South African flowering plants: a conspectus. J S Afr Bot 40:169–187

    Google Scholar 

  • Ornduff R (1975) Heterostyly and pollen flow in Hypericum aegypticum (Guttiferae). J Lin Soc Lond Bot 71:51–57

    Article  Google Scholar 

  • Ornduff R (1978) Features of pollen flow in dimorphic species of Lythrum section Euhyssopifolia. Am J Bot 65:1077–1083

    Article  Google Scholar 

  • Ornduff R (1979) The genetics of heterostyly in Hypericum aegypticum. Heredity 42:271–272

    Article  Google Scholar 

  • Ornduff R (1986) Comparative fecundity and population composition of heterostylous and non-heterostylous species of Villarsia (Menyanthaceae) 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 

  • Pandey KK (1960) Evolution of gametophytic and sporophytic systems of self-incompatibility in angiosperms. Evolution 14:98–115

    Article  Google Scholar 

  • Philipp M, Schou O (1981) An unusual heteromorphic incompatibility system. Distyly, self-incompatibility, pollen load and fecundity in Anchusa officinalis (Boraginaceae). New Phytol 89:693–703

    Article  Google Scholar 

  • Philipson MN, Philipson WR (1975) A revision of Rhododendron section Lapponicum. Notes R Bot Gard Edinb 34:1–72

    Google Scholar 

  • Richards AJ (1986) Plant breeding systems. Allen and Unwin, Lond

    Google Scholar 

  • Richards JH, Barrett SCH (1987) Development of tristyly in Pontederia cordata (Pontederiaceae). I. Mature floral structure and patterns of relative growth of reproductive organs. Am J Bot 74:1831–1841

    Article  Google Scholar 

  • Robson NKB (1972) Evolutionary recall in Hypericum (Guttiferae)? Trans Proc Bot Soc Edinb 41:365–383

    Article  Google Scholar 

  • Sampson DR (1967) Frequency and distribution of self-incompatibility alleles in Raphanus raphanistrum. Genetics 56:241–251

    PubMed  CAS  Google Scholar 

  • Schill R, Baumm A, Wolter M (1985) Vergleichende Mikromorphologie der Narbenoberflachen bei den Angiospermen; Zusammenhange mit Pollenoberflachen bei heterostylen Sippen. Plant Syst Evol 148:185–214

    Article  Google Scholar 

  • Schou O, Philipp M (1984) An unusual heteromorphic incompatibility system. III. On the genetic control of distyly and self-incompatibility in Anchusa officinalis L. (Boraginaceae). Theor Appl Genet 68:139–144

    Article  Google Scholar 

  • Shivanna KR, Heslop-Harrison J, Heslop-Harrison Y (1981) Heterostyly in Primula. 2. Sites of pollen inhibition, and effects of pistil constituents on compatible and incompatible pollen-tube growth. Protoplasma 107:319–337

    Article  Google Scholar 

  • Shivanna KR, Heslop-Harrison Y, Heslop-Harrison J (1983) Heterostyly in Primula. 3. Pollen water economy as a factor in the intramorph-incompatibility response. Protoplasma 117:175–184

    Article  Google Scholar 

  • Shore JS, Barrett SCH (1985) The genetics of distyly and homostyly in Turnera ulmifolia L. (Turneraceae). Heredity 55:167–174

    Article  Google Scholar 

  • Sobrevila C, Ramirez N, Xena de Enrech N (1983) Reproductive biology of Palicourea fendleri and P. petiolaris (Rubiaceae), heterostylous shrubs of a tropical cloud forest in Venezuela. Biotropica 15:161–169

    Article  Google Scholar 

  • Stearn WT (1971) A survey of the tropical genera Oplonia and Psilanthele (Acanthaceae). Bull Br Mus Nat Hist Bot 4:259–323

    Google Scholar 

  • Stevens JP, Kay QON (1989) The number, dominance relationships and frequencies of self-incompatibility alleles in a natural population of Sinapis arvensis L. in south Wales. Heredity 62:199–206

    Article  Google Scholar 

  • Stevens VAM, Murray BG (1982) Studies on heteromorphic self-incompatibility systems: physiological aspects of the incompatibility system of Primula obconica. Theor Appl Genet 61:245–256

    Google Scholar 

  • Vogel S (1955) Über den Blütendimorphismus einiger südafrikanischer Pflanzen. Oesterr Bot Z 102:486–500

    Article  Google Scholar 

  • Vuilleumier BS (1967) The origin and evolutionary development of heterostyly in the angiosperms. Evolution 21:210–226

    Article  Google Scholar 

  • Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy. NZ J Bot 24:163–178

    Article  Google Scholar 

  • Wedderburn F, Richards AJ (1990) Variation in within-morph incompatibility inhibition sites in heteromorphic Primula L. New Phytol 116:149–162

    Article  Google Scholar 

  • Weller SG (1976) Breeding system polymorphism in a heterostylous species. Evolution 30:442–454

    Article  Google Scholar 

  • Weiler SG (1979) Variation in heterostylous reproductive systems among populations of Oxalis alpina in southeastern Arizona. Syst Bot 4:57–71

    Article  Google Scholar 

  • Williams EG, Rouse JL (1988) Disparate style lengths contribute to isolation of species in Rhododendron. Aust J Bot 36:183–191

    Article  Google Scholar 

  • Willis JC (1973) A dictionary of the flowering plants and ferns, 8th edn (revised by Airy Shaw HK). Cambridge Univ Press, Cambridge

    Google Scholar 

  • Wright S (1939) The distribution of self-sterility alleles in populations. Genetics 24:538–552

    PubMed  CAS  Google Scholar 

  • Wunderlin RP, Larsen K, Larsen SS (1981) Tribe 3. Cercideae Bronn (1822). In: Polhill RM, Raven PH (eds) Advances in legume systematics, vol 1. R Bot Gard Kew, pp 107–116

    Google Scholar 

  • Wyatt R (1983) Pollinator-plant interactions and the evolution of breeding systems. In: Real L (ed) Pollination biology. Academic Press, Orlando, pp 51–95

    Google Scholar 

  • Yeo PF (1975) Some aspects of heterostyly. New Phytol 75:147–153

    Article  Google Scholar 

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Lloyd, D.G., Webb, C.J. (1992). The Evolution of Heterostyly. In: Barrett, S.C.H. (eds) Evolution and Function of Heterostyly. Monographs on Theoretical and Applied Genetics, vol 15. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-86656-2_6

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