Abstract
Populations of trioecious plants consists of individuals with staminate, pistillate, and hermaphrodite flowers. Trioecy is extremely rare in angiosperms, and relevant data are scarce. A list of trioecious plants found in the global flora was compiled on the basis of literature data and original research. The list includes 80 species of 46 genera, which represent 33 families and 21 orders of flowering plants. Trioecy is found in 7.9% of families, 0.3% of genera, and 0.03% of species in angiosperms. Trioecious species are now unknown in basal angiosperms, uncommon in magnoliids, and rather rare in monocots. The overwhelming majority (87.5%) of trioecious plants belong to Superrosids (30 species) and Superasterids (40 species). The greatest numbers of trioecious species are found in the families Rosaceae (nine species of two genera), Caprifoliaceae (seven species of one genus), Scrophulariaceae (seven species of one genus), Caryophyllaceae (six species of two genera), and Celastraceae (six species of two genera). Almost half of the identified trioecious species represent five genera: Fragaria L. (eight species), Valeriana L. (seven species), Buddleja L. (seven species), Maytenus Molina (five species), and Silene L. (five species). An association with trioecy was analyzed for several biological and ecological factors, such as the life form, the method of pollination, the perianth color, the pericarp consistency, the presence of related dioecious species in the same genus, the latitudinal position, and the distribution through floristic phytochoria. A lability of sex differentiation in certain trioecious plants, the proportion of sex forms in a population, a possible association with polyploidy, and mechanisms of trioecy maintenance and evolution in flowering plants are discussed.
REFERENCES
Akemine, T., On the sex expression of Coptis japonica Makino, J. Fac. Sci. Hokkaido Imp. Univ., 1935, vol. 5, no. 1, pp. 1–7.
Albert, B., Morand-Prieur, M.-É., Brachet, S., Gouyon, P.-H., Frascaria-Lacoste, N., and Raquin, C., Sex expression and reproductive biology in a tree species, Fraxinus excelsior L., Compt. R. Biol., 2013, vol. 336, no. 10, pp. 479–485.
Anmol Singh, S.K., Species diversity and genetic evolution in Fragaria, in Advances in Horticultural Crop Management and Value Addition, 2019, pp. 75–89.
Armoza-Zvuloni, R., Kramarsky-Winter, E., Loya, Y., Schlesinger, A., and Rosenfeld, H., Trioecy, a unique breeding strategy in the sea anemone Aiptasia diaphana and its association with sex steroids, Biol. Reprod., 2014, vol. 90, no. 6, pp. 1–8.
Ashman, T.-L., Kwok, A., and Husband, B.C., Revisiting the dioecy–polyploidy association: Alternate pathways and research opportunities, Cytogenet. Genome Res., 2013, vol. 140, nos. 2–4, pp. 241–255.
Atalano, J.M. and Molau, U., Pollen viability and limitation of seed production in a population of the circumpolar cushion plant, Silene acaulis (Caryophyllaceae), Nord. J. Bot., 2001, vol. 21, no. 4, pp. 365–372.
Baker, H.G., Some functions of dioecy in seed plants, Am. Nat., 1984, vol. 124, no. 2, pp. 149–158.
Banziger, H. and Bertel, H., A new taxonomic revision of a deceptive flower, Rhizanthes Dumortier (Rafflesiaceae), Nat. Hist. Bull. Siam Soc., 2000, vol. 48, no. 1, pp. 117–143.
Barroso, G.M., Baccharidiopsis—um gênero novo da subtribo Baccharidinae Hoffmann (tribo Astereae), Sellowia, 1975, vol. 27, no. 26, pp. 95–101.
Bobrov, A.V., Melikian, A.P., and Romanov, M.S., Morphogenesis of Fruits of Magnoliophyta, Moscow, 2009.
Brizicky, G.K., The genera of Vitaceae in the southeastern United States, J. Arnold Arbor., 1965, vol. 46, no. 1, pp. 48–67.
Castillo, R.F. and Argueta, S.T., Reproductive implications of combined and separate sexes in a trioecious population of Opuntia robusta (Cactaceae), Am. J. Bot., 2009, vol. 96, no. 6, pp. 1148–1158.
Cook, C.D.K., Symoens, J.-J., and Urmi-König, K., A revision of the genus Ottelia (Hydrocharitaceae) I. Generic considerations, Aquat. Bot., 1984, vol. 18, no. 3, pp. 263–274.
Cruden, R.W. and Lloyd, R.M., Embryophytes have equivalent sexual phenotypes and breeding systems: why not a common terminology to describe them?, Am. J. Bot., 1995, vol. 82, no. 6, pp. 816–825.
Cutter, A.D., Mutation and the experimental evolution of outcrossing in Caenorhabditis elegans, J. Evol. Biol., 2005, vol. 18, no. 1, pp. 27–34.
Darwin, C., The Different Forms of Flowers on Plants of the Same Species, London, 1877.
Demissew, S., The genus Maytenus (Celastraceae) in NE tropical Africa and tropical Arabia, Acta Univ. Ups., Symb. Bot. Ups., 1985, vol. 25, no. 2, pp. 1–101.
Demyanova, E.I., The Spectrum of sexual types and forms in the local floras of the Urals (Cis- And Trans-Urals), Bot. Zh., 2011, vol. 96, no. 10, pp. 1297–1315. https://doi.org/10.1134/S1234567811100016
Ehlers, B.K. and Bataillon, T., “Inconstant males” and the maintenance of labile sex expression in subdioecious plants, New Phytol., 2007, vol. 174, no. 1, pp. 194–211.
Elumeev, E.A., Opening and blooming of flowers Eleutherococcus senticosus (Araliaceae), Bot. Zh., 1978, vol. 63, no. 1, pp. 52–59.
Engler, A. and Krause, K., Loranthaceae, in Die Natürlichen Planzenfamilien, Leipzig, 1935, vol. 16b, pp. 98–203.
FitzJohn, R.G., Pennell, M.W., Zanne, A.E., Stevens, P.F., Tank, D.C., and Cornwell, W.K., How much of the world is woody?, J. Ecol., 2014, vol. 102, no. 5, pp. 1266–1272.
Fleming, T.H., Fruiting plant-frugivore mutualism: the evolutionary theater and the ecological play, in Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, New York, 1991, pp. 119–144.
Fleming, T.H., Maurice, S., Buchmann, S.L., and Tuttle, M.D., Reproductive biology and relative male and female fitness in a trioecious cactus, Pachycereus pringlei (Cactaceae), Am. J. Bot., 1994, vol. 81, no. 7, pp. 858–867.
Fleming, T.H., Maurice, S., and Hamrick, J.L., Geographic variation in the breeding system and the evolutionary stability of trioecy in Pachycereus pringlei (Cactaceae), Evol. Ecol., 1998, vol. 12, no. 3, pp. 279–289.
Fox, J., Incidence of dioecy in relation to growth form, pollination and dispersal, Oecologia, 1985, vol. 67, no. 2, pp. 244–249.
French, K., Characteristics and abundance of vertebrate-dispersed fruits in temperate wet sclerophyll forest in southeastern Australia, Aust. J. Ecol., 1991, vol. 16, no. 1, pp. 1–13.
Frodin, D.G., Guide to Standard Floras of the World. An annotated, Geographically Arranged Systematic Bibliography of the Principal Floras, Enumerations, Checklists, and Chorological Atlases of Different Areas, Cambridge: Cambridge Univ. Press, 2001.
Giussani, L.M., Gillespie, L.J., Scataglini, M.A., Negritto, M.A., Anton, A.M., and Soreng, R.J., Breeding system diversification and evolution in American Poa supersect. Homalopoa (Poaceae: Poeae: Poinae), Ann. Bot., 2016, vol. 118, no. 2, pp. 281–303.
Gleiser, G. and Verdú, M., Repeated evolution of dioecy from androdioecy in Acer, New Phytol., 2005, vol. 165, no. 2, pp. 633–640.
Glick, L., Sabath, N., Ashman, T.-L., Goldberg, E., and Mayrose, I., Polyploidy and sexual system in angiosperms: Is there an association?, Am. J. Bot., 2016, vol. 103, no. 7, pp. 1223–1235.
Godin, V.N., Sexual structure of coenopopulations of Pentaphylloides fruticosa (L.) O. Schwarz in natural conditions of Mountain Altai, Bot. Zh., 2002, vol. 87, no. 9, pp. 92–98.
Godin, V.N., Biological characters of Pentaphylloides fruticosa (Rosaceae) pollen in the context of sex differentiation, Bot. Zh., 2004, vol. 89, no. 4, pp. 631–638. https://doi.org/10.1134/S000681360404009X
Godin, V.N., Sex differentiation in plants, terms and notions, Zh. Obshch. Biol., 2007, vol. 68, no. 2, pp. 98–108.
Godin, V.N., Sexual structure of Potentilla fruticosa (Rosaceae) coenopopulations in the Altay-Sayan Mountain region, Bot. Zh., 2008, vol. 93, no. 9, pp. 1423–1444. https://doi.org/10.1134/S1234567808090073
Godin, V.N., Sexual forms and their ecological correlates of flowering plants in Siberia, Russ. J. Ecol., 2017, vol. 48, no. 5, pp. 433–439.
Godin, V.N., Distribution of gynodioecy in APG IV system, Bot. Zh., 2019, vol. 104, no. 5, pp. 669–683. https://doi.org/10.1134/S0006813619050053
Godin, V.N., Distribution of gynodioecy in flowering plants, Bot. Zh., 2020, vol. 105, no. 3, pp. 236–252. https://doi.org/10.31857/S0006813620030023
Godley, E.J., Breeding systems in New Zealand Plants, I, Fuchsia, Ann. Bot., 1955, vol. 19, no. 4, pp. 549–559.
Gschwend, A.R., Wai, C.M., Zee, F., Arumugana-than, A.K., and Ming, R., Genome size variation among sex types in dioecious and trioecious Caricaceae species, Euphytica, 2012, vol. 189, no. 3, pp. 461–469.
Hummer, K.E., A new species of Fragaria (Rosaceae) from Oregon, J. Bot. Res. Inst. Texas, 2012, vol. 6, no. 1, pp. 9–15.
Ishmuratova, M.M., Rhodiola iremelica (Crassulaceae) in the Southern Urals, Bot. Zh., 2002, vol. 87, no. 5, pp. 38–50.
Joseph, K.S. and Murthy, H.N., Sexual system of Garcinia indica Choisy: geographic variation in trioecy and sexual dimorphism in floral traits, Plant Syst. Evol., 2015, vol. 301, no. 3, pp. 1065–1071.
Kaliszewicz, A., Interference of asexual and sexual reproduction in the green hydra, Ecol. Res., 2011, vol. 26, no. 1, pp. 147–152.
Kier, G., Mutke, J., Dinerstein, E., Ricketts, T.H., Küper, W., Kreft, H., and Barthlott, W., Global patterns of plant diversity and floristic knowledge, J. Biogeogr., 2005, vol. 32, no. 7, pp. 1107–1116.
Klackenberg, J., The holarctic complex Potentilla fruticosa (Rosaceae), Nord. J. Bot., 1983, vol. 3, no. 2, pp. 181–191.
Knuth, P., Handbuch der Blütenbiologie, Leipzig, Bd. II, Teil I, 1898.
Knuth, P., Handbuch der Blütenbiologie, Leipzig, Bd. II, Teil II, 1899.
Knuth, P., Handbuch der Blütenbiologie, Leipzig, Bd. III, Teil I, 1904.
Kutschker, A., Revisión del género Valeriana (Valerianaceae) en Sudamérica austral, Gayana Bot., 2011, vol. 68, no. 2, pp. 244–296. https://doi.org/10.4067/S0717-66432011000200016
Ladley, J.J., Kelly, D., and Robertson, A.W., Explosive flowering, nectar production, breeding systems, and pollinators of New Zealand mistletoes (Loranthaceae), N. Z. J. Bot., 1997, vol. 35, no. 3, pp. 345–360.
Linnæi, C., Systema naturæ, sive regna tria naturæ systematice proposita per classes, ordines, genera, and species, Lugduni Batavorum, 1735.
Liston, A., Cronn, R., and Ashman, T., Fragaria: A genus with deep historical roots and ripe for evolutionary and ecological insights, Am. J. Bot., 2014, vol. 101, no. 10, pp. 1686–1699.
Loock, E.E.M., The carob or locust tree (Ceratonia siliqua L.), J. S. Afr. For. Ass., 1940, vol. 4, no. 1, pp. 78–80.
Maurice, S., Belhassen, E., Couvet, D., and Gouyon, P., Evolution of dioecy: Can nuclear-cytoplasmic interactions select for maleness?, Heredity, 1994, vol. 73, no. 4, pp. 346–354.
Maurice, S. and Fleming, T., The effect of pollen limitation on plant reproductive systems and the maintenance of sexual polymorphisms, Oikos, 1995, vol. 74, no. 1, pp. 55–60.
Mirski, P. and Brzosko, E., Are hermaphrodites better adapted to the colonization process in trioecious populations of Salix myrsinifolia?, Acta Soc. Bot. Pol., 2015, vol. 84, no. 2, pp. 167–175.
Morris, W.F. and Doak, D.F., Life history of the long-lived gynodioecious cushion plant Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices, Am. J. Bot., 1998, vol. 85, no. 6, pp. 784–793.
Neefus, C.D., Mathieson, A.C., Bray, T.L., and Yarish, C., The distribution, morphology, and ecology of three introduced asiatic species of Porphyra (Bangiales, Rhodophyta) in the northwestern Atlantic, J. Phycol., 2008, vol. 44, no. 6, pp. 1399–1414.
Nianhe, X. and Gilbert, M.G., Santalaceae, in Flora of China, 2003, vol. 5, pp. 208–219.
Norman, E.M., Buddlejaceae, in Flora Neotropica Monograph, New York, 2000, vol. 81.
Novara, L., Valerianaceae, Aportes Botanicos de Salta, Serie Flora, 2008, vol. 8, no. 8, pp. 1–22.
Ollerton, J., Johnson, S., and Hingston, A., Geographical variation in diversity and specificity of pollination systems, in Plant–Pollinator Interactions: From Specialization to Generalization, Univ. Chicago Press, 2006, pp. 283–308.
Ollerton, J., Winfree, R., and Tarrant, S., How many flowering plants are pollinated by animals?, Oikos, 2011, vol. 120, no. 3, pp. 321–326.
Palací, C.A., A systematic revision of the genus Catopsis (Bromeliaceae), PhD Dissertation, Laramie: Wyoming Univ., 1997.
Perrier de la Bathie, H., Anacardiaceae, in Flore de Madagascar et des Comores. Tananarive, 1946, pp. 1–85.
Perry, L.E., Pannell, J.R., and Dorken, M.E., Two’s company, three’s a crowd: experimental evaluation of the evolutionary maintenance of trioecy in Mercurialis annua (Euphorbiaceae), PLoS One, 2012, vol. 7, no. 4, p. e35597.
Pervukhina, N.V., Perianth of Angiosperms, Leningrad, 1979.
Quisumbing, E., Philippine Piperaceae, Philipp. J. Sci., 1930, vol. 43, no. 1, pp. 1–246.
Raunkiær, C., The Life Forms of Plants and Statistical Plant Geography, Oxford, 1934.
Rebman, J.P., The genus Echinocereus in Lower California, Mexico—taxonomy, rarity and reproductive biology, Cact. Succ. J. Am., 2003, vol. 75, pp. 194–196.
Rejmánek, M., Invasion of Rubus praecox (Rosaceae) is promoted by the native tree Aristotelia chilensis (Elaeocarpaceae) due to seed dispersal facilitation, Gayana Bot., 2015, vol. 72, no. 1, pp. 27–33.
Renner, S.S., The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database, Am. J. Bot., 2014, vol. 101, no. 10, pp. 1588–1596.
Richards, A.J., Plant Breeding Systems, Springer-Verlag, 1997.
Rosado, A., Vera-Velez, R., and Cota-Sanchez, J.H., Floral morphology and reproductive biology in selected maple (Acer L.) species (Sapindaceae), Braz. J. Bot., 2018, vol. 41, no. 2, pp. 361–374.
Rübsamen-Weustenfeld, T., Morphologische, embryologische, und systematische Untersuchungen an Triuridaceae, Bibl. Bot., 1991, vol. 140, pp. 1–113.
Serebryakov, I.G., Ecological Morphology of Plants, Moscow, 1962.
Shamsutdinova, E.Z., Biology of flowering, diversity of sexual types and seed production in Salsola orientalis S.G. Gmel, Agric. Biol., 2016, vol. 51, no. 6, pp. 951–960. https://doi.org/10.15389/agrobiology.2016.6.951rus
Silva, C.A., Oliva, M.A., Vieira, M.F., and Fernan-des, G.W., Trioecy in Coccoloba cereifera Schwacke (Polygonaceae), a narrow endemic and threatened tropical species, Braz. Arch. Biol. Technol., 2008, vol. 51, no. 5, pp. 1003–1010.
Sokal, R.R. and Rohlf, F.J., Biometry: the Principles and Practice of Statistics in Biological Research, New York, 2012.
Soreng, R. and Peterson, P.M., Revision of Poa L. (Poaceae, Pooideae, Poeae, Poinae) in Mexico: new records, re-evaluation of P. ruprechtii, and two new species, P. palmeri and P. wendtii, PhytoKeys, 2012, vol. 15, no. 15, pp. 1–104.
Soriano, A.M., Salazar, G.A., and Dávila, P.D., Phylogenetic relationships in Zeugites (Poaceae: Centothecoideae) inferred from plastid and nuclear DNA sequences and morphology, Syst. Bot., 2007, vol. 32, no. 4, pp. 722–730. https://doi.org/10.1043/06-75.1
Staudt, G., Die Genetik und Evolution der Heterözie in der Gattung Fragaria. I. Untersuchungen an Fragaria orientalis, Z. Pflanzenzuchtung, 1967, vol. 58, no. 3, pp. 245–277.
Storey, W.B., Genetics of papay, J. Hered., 1953, vol. 44, no. 2, pp. 70–78.
Sultangaziev, O., Schueler, S., and Geburek, T., Morphometric traits and sexual dimorphisms do not strongly differentiate populations of Zeravshan juniper (Juniperus seravschanica Kom.) in Kyrgyzstan, Flora, 2010, vol. 205, no. 8, pp. 532–539.
Takhtajan, A.L., The Floristic Regions of the World, Berkeley: UC Press, 1986.
Tandon, R., Shivanna, K.R., and Mohan Ram, H.Y., Reproductive biology of some gum-producing Indian desert plants, in Desert Plants, Springer-Verlag, 2010, pp. 177–195.
Tseng, Y.-H., Hsieh, C.-F., and Hu, J.-M., Incidences and ecological correlates of dioecious angiosperms in Taiwan and its outlying Orchid Island, Bot. Stud., 2008, vol. 49, no. 3, pp. 261–276.
Vary, L.B., Gillen, D.L., Randrianjanahary, M., Lowry II, P.P., Sakai, A.K., and Weller, S.G., Dioecy, monoecy, and their ecological correlates in the littoral forest of Madagascar, Biotropica, 2011, vol. 43, no. 5, pp. 582–590.
Vitale, J.J. and Freeman, D.C., Partial niche separation in Spinacia oleracea L.: an examination of reproductive allocation, Evolution, 1986, vol. 40, no. 2, pp. 426–430.
Warfa, A.M., Cordia (Boraginaceae) in NE Tropical Africa and Tropical Arabia, Acta Univ. Ups., 1988.
Warming, M.E., Sur la structure et le procédé présumé de pollination chez quelques fleurs groenlandaises, Bulletin de l’Académie royale des sciences et des lettres de Danemark, 1886, pp. 25–33.
Weberling, F. and Stützel, Th., Morphological and anatomical investigations of Aretiastrum magellanicum (Hombr. and Jacq.) Skottsb., Wulfenia, 2006, vol. 13, pp. 193–205.
Willson, M.F., Irvine, A.K., and Walsh, N.G., Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons, Biotropica, 1989, vol. 21, no. 2, pp. 133–147.
Xia, F., Cheng, F., Liu, Z., Lin, L., Wang, H., and Wang, G., Sexual system and ecological links of flowering plants in Changbai Mountain, Russ. J. Ecol., 2020, vol. 51, no. 4, pp. 345–350.
Zenil-Ferguson, R., Burleigh, J.G., Freyman, W.A., Igić, B., Mayrose, I., and Goldberg, E.E., Interaction among ploidy, breeding system and lineage diversification, New Phytol., 2019, vol. 224, no. 3, pp. 1252–1265.
Yampolsky, C. and Yampolsky, H., Distribution of sex forms in the phanerogamic flora, Bibl. Genet., 1922, vol. 3, pp. 1–62.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests. The author declares that he has no conflicts of interest.
This article does not contain any studies involving animals or human subjects performed by the author.
Additional information
In memoriam Evgeniya Ivanovna Demyanova (1936–2020), my teacher in the field of plant sexual polymorphism
Translated by T. Tkacheva
Rights and permissions
About this article
Cite this article
Godin, V.N. Trioecy in Flowering Plants. Dokl Biol Sci 507, 301–311 (2022). https://doi.org/10.1134/S0012496622060023
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0012496622060023