Androdioecy in Caltha palustris (Ranunculaceae)
- Authors: Godin V.N.1
-
Affiliations:
- Central Siberian Botanical Garden SB RAS
- Issue: Vol 109, No 5 (2024)
- Pages: 446-459
- Section: COMMUNICATIONS
- URL: https://rjmseer.com/0006-8136/article/view/666563
- DOI: https://doi.org/10.31857/S0006813624050034
- EDN: https://elibrary.ru/QKFMYK
- ID: 666563
Cite item
Abstract
The article contains the first detailed report on androdioecy in Caltha palustris L., a short-rhizomatous, fibrous-rooted herbaceous perennial, based on the studies conducted in the Moscow Region from 2021 to 2023. C. palustris produces flowers of two types: perfect and staminate (remains of carpels with non-functioning stigmas are preserved). Most of the studied individuals had larger perfect flowers, and their elements were always larger than those of staminate flowers. The studied populations consisted of three types of individuals: ones with perfect flowers only, ones with both perfect and staminate flowers, and ones bearing staminate flowers only. The synflorescence of C. palustris is a closed thyrsus, its subunits are dichasia. In andromonoecious plants, perfect flowers take a terminal position on both the thyrsus axis and in the dichasia of the paracladia, while staminate flowers are formed exclusively on the lateral axes of the dichasia. Most plants in the studied populations had perfect flowers (from 87.3 to 95.0%). Over a three-year observation period, the individuals of different sexual forms showed no evidence of sex change, and the ratio of different kinds of plants remained stable with only minor fluctuations.
Keywords
Full Text

About the authors
V. N. Godin
Central Siberian Botanical Garden SB RAS
Author for correspondence.
Email: vn.godin@mpgu.su
Russian Federation, Zolotodolinskaya Str., 101, Novosibirsk, 630090
References
- Akimoto J., Fukuhara T., Kikuzawa K. 1999. Sex ratios and genetic variation in a functionally androdioecious species, Schizopepon bryoniaefolius (Cucurbitaceae). – Amer. J. Bot. 86(6): 880–886. https://doi.org/10.2307/2656708
- Barykina R.P., Chubatova N.V. Caltha palustris. – In: Biological flora of the Moscow region. Vol. 14. Мoscow. P. 87–100 (In Russ.).
- Bell G. 1985. On the function of flowers. – Proc. R. Soc. Lond. B. 224(1235): 223–265. http://doi.org/10.1098/rspb.1985.0031
- Burkill I.H. 1895. On some variations in the number of stamens and carpels. – Bot. J. Linn. Soc. 31(214): 216–245.https://doi.org/10.1111/j.1095-8339.1895.tb00805.x
- Charlesworth B., Charlesworth D. 1978. Model for evolution of dioecy and gynodioecy. – Amer. Nat. 112(988): 975–997. https://doi.org/10.1086/283342
- Charlesworth D. 1984. Androdioecy and the evolution of dioecy. – Biol. J. Linn. Soc. 22(4): 333–348. https://doi.org/10.1111/j.1095-8312.1984.tb01683.x
- Cieślak E. 2004. Morphological variability of the Caltha palustris L. complex (Ranunculaceae) in Poland. – Acta Soc. Bot. Poloniae. 73(3): 193–201. https://doi.org/10.5586/asbp.2004.026
- Cronk Q. 2022. The distribution of sexual function in the flowering plant: from monoecy to dioecy. – Phil. Trans. R. Soc. B 377: 20210486. https://doi.org/10.1098/rstb.2021.0486
- Cruden R.W., Lloyd R.M. 1995. Embryophytes have equivalent sexual phenotypes and breeding systems: why not a common terminology to describe them? – Amer. J. Bot. 82(6): 816–825. https://doi.org/10.2307/2445622
- Dagaeva V.K. 1929. About a flower anomaly in Caltha palustris L. – Izv. GBS SSSR. 28: 345–356 (In Russ.).
- Darwin C. 1877. The different forms of flowers on plants of the same species. London. 352 p.
- Delph L.F., Galloway L.F., Stanton M.L. 1996. Sexual dimorphism in flower size. – Amer. Nat. 148(2): 299–320. https://doi.org/10.1086/285926
- Demyanova E.I. 2013. On the sexual polymorphism of some androdioecious plants. – Bot. Zhurn. 98(9): 1139–1146 (In Russ.).
- Diels L. 1912. Plantae Chinenses Forrestianae. – Notes Roy. Bot. Gard. Edinburgh. 5(25): 161–308.
- Duan Y., Li W., Zheng S., Sylvester S.P., Li Y., Cai F., Zhang C., Wang X. 2019. Functional androdioecy in the ornamental shrub Osmanthus delavayi (Oleaceae). – PLoS ONE. 14(9): e0221898 https://doi.org/10.1371/journal.pone.0221898
- Emms S.K. 1993. Andromonoecy in Zigadenus paniculatus (Liliaceae): spatial and temporal patterns of sex allocation. – Amer. J. Bot. 80(8): 914–923. https://doi.org/10.1002/j.1537-2197.1993.tb15312.x
- Endress P.K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge. 511 p.
- Endress P.K. 1995. Floral structure and evolution in Ranunculanae. – In: Systematics and Evolution of the Ranunculiflorae. Springer. Vol. 9. P. 47–61. https://doi.org/10.1007/978-3-7091-6612-3_5
- Fedorov Al.A., Artyushenko Z.T. 1975. Organographia illustrata plantarum vascularum. Flos. Leningrad. 351 p. (In Russ.).
- Gertz O. 1913. Om variationen i antalet kalkblad hos Caltha palustris L. – Bot. Notis. P. 281–289.
- Godin V.N., Perkova T.V. 2017. Flowering biology and sexual polymorphism in the Apiaceae species (Moscow region). – Bot. Zhurn. 102(1): 35–47 (In Russ.). https://doi.org/10.1134/S0006813617010033
- Godin V.N., Arkhipova T.V., Tagieva A.N. 2021. Andromonoecy and its manifestation in inflorescences of Chaerophyllum aromaticum (Apiaceae) in Moscow region. – Bot. Zhurn. 106(4): 382–396 (In Russ.). https://doi.org/10.31857/S0006813621040049
- Godin V.N., Arkhipova T.V., Vetlova M.A., Kuranova N.G. 2022. Andromonoecy and floral protandry of Oenanthe aquatica (Apiaceae). – Tomsk State University Journal of Biology. 58: 96–112. https://doi.org/10.17223/19988591/58/5
- Godin V.N. 2024. Androdioecy in Ranunculus ficaria ssp. ficaria (Ranunculaceae). – Bot. Zhurn. 109(2): 176–187. (In Russ.). https://doi.org/10.31857/S0006813624020058
- Hagerup O. 1950. Rain-pollination. – Det Kgl. Danske Videnskabernes Selskab. Biol Medd. 18(5): 1–19.
- Han Y., He Y., Yue S., Guo B., Zhu Q., Zhang H., Hai X., Shang F. 2023. Floral bud differentiation and mechanism underlying androdioecy of Osmanthus fragrans. – Ornamental Plant Research. 3(1): 11. https://doi.org/10.48130/OPR-2023-0011
- Haughn G.W., Somerville C.R. 1988. Genetic control of morphogenesis in Arabidopsis. – Developmental Genet. 9(2): 73–89. https://doi.org/10.1002/dvg.1020090202
- Hegi G. 1912. Caltha L. – In: Illustrierte Flora von Mittel-Europa. B. 3. T. 1. München. P. 457–459.
- Hill A.W. 1918. The Genus Caltha in the Southern Hemisphere. – Ann. Bot. 32(3): 421–435. https://doi.org/10.1093/oxfordjournals.aob.a089683
- Husse L., Billiard S., Lepart J., Vernet P., Saumitou-Laprade P. 2013. A one-locus model of androdioecy with two homomorphic self-incompatibility groups: expected vs. observed male frequencies. – J. Evol. Biol. 26(6): 1269–1280. https://doi.org/10.1111/jeb.12124
- Kartashova N.N. 1965. Stroenie i funktsii nektarnikov tsvetka dvudol'nykh rasteniy [Structure and functions of flower nectaries of dicotyledonous plants]. Tomsk. 194 p. (In Russ.).
- Kleopov Yu.D. 1990. Analiz flory shirokolistvennykh lesov Yevropeyskoy chasti SSSR [Analysis of the flora of broad-leaved forests of the European part of the USSR]. Kiev. 352 p. (In Russ.).
- Knuth P. 1898. Handbuch der Blütenbiologie. Bd. II. T. I. Leipzig. 697 S.
- Kordyum E.L., Glushchenko G.I. 1976. Tsitoembriologicheskie aspekty problemy pola pokrytosemennykh [Cytoembryological aspects of the problem of sex of angiosperms]. Kiev. 197 p. (In Russ.).
- Laugier F., Saumitou-Laprade P., Vernet P., Lepart J., Cheptou P.-O., Dufay M. 2023. Male fertility advantage within and between seasons in the perennial androdioecious plant Phillyrea angustifolia. – Ann. Bot.: mcad169. https://doi.org/10.1093/aob/mcad169
- Lecoq H. 1855. Étude sur la géographie botanique de l'Europe et, en particulier, sur la végétation du plateau central de la France. Paris. T. 4. 536 p.
- Liston A., Rieseberg L., Elias T. 1990. Functional androdioecy in the flowering plant Datisca glomerata. – Nature. 343: 641–642. https://doi.org/10.1038/343641a0
- Liu J., Li C.-Q., Dong Y., Yang X., Wang Y.-Z. 2018. Dosage imbalance of B- and C-class genes causes petaloid-stamen relating to F1 hybrid variation. – BMC Plant Biol. 18(1): 341. https://doi.org/10.1186/s12870-018-1562-4
- Lloyd D.G. 1975. The maintenance of gynodioecy and androdioecy in angiosperms. – Genetica. 45(3): 325–339. https://doi.org/10.1007/BF01508307
- Loew E. 1894. Blütenbiologische Floristik des mittleren und nördlichen Europa sowie Grönlands. Systematische Zusammenstellung des in den letzten zehn Jahren veröffentlichten Beobachtungsmaterials. Stuttgart. 424 S.
- Maltseva T.A., Savinykh N.P. 2008. Biomorphology of Caltha palustris L. – Bulletin of Chelyabinsk State Pedagogical University. 12: 257–271 (In Russ.).
- Manicacci D., Després L. 2001. Male and hermaphrodite flowers in the alpine lily Lloydia serotina. – Can. J. Bot. 79(9): 1107–1114. https://doi.org/10.1139/b01-087
- Mucina L., Bültmann H., Dierßen K., Theurillat J.-P. et al. 2016. Vegetation of Europe: hierarchical floristic classification system of vascular plant, bryophyte, lichen, and algal communities. – Appl. Veg. Sci. 19(S1): 3–264.https://doi.org/10.1111/avsc.12257
- Pannell J. 1997. Mixed genetic and environmental sex determination in an androdioecious population of Mercurialis annua. – Heredity. 78(1): 50–56. https://doi.org/10.1038/hdy.1997.6
- Pannell J.R. 2002. The evolution and maintenance of androdioecy. – Ann. Rev. Ecol. Syst. 33: 397–425. https://doi.org/10.1146/annurev.ecolsys.33.010802.150419
- Pannell J.R., Eppley S.M., Dorken M.E., Berjano R. 2014. Regional variation in sex ratios and sex allocation in androdioecious Mercurialis annua. – J. Evol. Biol. 27(7): 1467–1477. https://doi.org/10.1111/jeb.12352
- Philbrick C.T. 1983. Contributions to the reproductive biology of Panax trifolium L. (Araliaceae). – Rhodora. 85(841): 97–113.
- POWO. 2023. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. http://www.plantsoftheworldonline.org/
- Ronse de Craene L.P. 2010. Floral diagrams. An aid to understanding flower morphology and evolution. Cambridge. 441 p.
- Ross M.D. 1982. Five evolutionary pathways to subdioecy. – Amer. Nat. 119(3): 297–318. https://doi.org/10.1086/283911
- Sakio H., Nirei T. 2022. Is the high proportion of males in a population of the self-incompatible Fraxinus platypoda (Oleaceae) Indicative of true androdioecy or cryptic-dioecy? – Plants. 11(6): 753. https://doi.org/10.3390/plants11060753
- Saumitou-Laprade P., Vernet P., Vassiliadis C., Hoareau Y., Magny G., Dommée B., Lepart J. 2010. A self-incompatibility system explains high male frequencies in an androdioecious plant. – Science. 327(5973): 1648–1650. https://doi.org/10.1126/science.1186687
- Schuettpelz E., Hoot S.B. 2004. Phylogeny and biogeography of Caltha (Ranunculaceae) based on chloroplast and nuclear DNA sequences. – Amer. J. Bot. 91(2): 247–253. https://doi.org/10.3732/ajb.91.2.247
- Schulz A. 1890. Beiträge zur Kenntniss der Bestäubungseinrichtungen und der Geschlechtsvertheilung bei den Pflanzen. II. – Bibliotheca Botanica. 17: 1–224.
- Sennikov A.N. 2001. Genus 2. Caltha L. – In.: Flora of Eastern Europe. Vol. 10. Saint Petersburg. P. 43–44 (In Russ.).
- Shwe E., Wu B., Huang S.Q. 2020. Both small and large plants are likely to produce staminate (male) flowers in a hermaphrodite lily. – Plant Divers. 42(3): 142–147. https://doi.org/10.1016/j.pld.2020.01.004
- Skipworth J.P. 1970. Floral anatomy of Helleborus niger and Caltha palustris and its bearing on the gonophyll theory. – Phytomorphology. 20(3): 222–228.
- Smets E.F., Cresens E.M. 1988. Types of floral nectaries and the concepts ‘character’ and ‘character-state’ – a reconsideration. – Acta Bot. Neerl. 37(1): 121–128. https://doi.org/10.1111/j.1438-8677.1988.tb01586.x
- Smit P.G. 1973. A revision of Caltha (Ranunculaceae). – Blumea. 21(1): 119–150.
- Sokal R.R., Rohlf F.J. 2012. Biometry: the principles and practice of statistics in biological research. 4th edition. New York. 937 p.
- Solomon B.P. 1986. Sexual allocation and andromonoecy, resource investment in male and hermaphrodite flowers of Solanum carolinense (Solanaceae). – Amer. J. Bot. 73(8): 1215–1221. https://doi.org/10.1002/j.1537-2197.1986.tb08568.x
- Song J.-H., Oak M.-K., Hong S.-P. 2016. Morphological traits in an androdioecious species, Chionanthus retusus (Oleaceae). – Flora. 223: 129–137. https://doi.org/10.1016/j.flora.2016.05.009
- Sukaczev V.N. 1919. About Caltha palustris L. var. Stebutiana m. in connection with the question of the variability of its and typical form. – J. Soc. Bot. Russ. 4(1–4): 111–132 (In Russ.).
- Tamura M. 1993. Ranunculaceae. – In: The families and genera of vascular plants. II. P. 563–583. Springer. https://doi.org/10.1007/978-3-662-02899-5_67
- Tedder A., Helling M., Pannell J.R., Shimizu-Inatsugi R., Kawagoe T., van Campen J., Sese J., Shimizu K.K. 2015. Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae). – Ann. Bot. 115(5): 763–776. https://doi.org/10.1093/aob/mcv006
- Theißen G. 2001. Development of floral organ identity: stories from the MADS house. – Curr. Opin. Pl. Biol. 4(1): 75–85. https://doi.org/10.1016/S1369-5266(00)00139-4
- Troll W. 1969 Die Infloreszenzen: Typologie und Stellung im Aufbau des Vegetationskörpers. Bd. II. Jena. 630 S.
- Vassiliadis C., Saumitou-Laprade P., Lepart J., Viard F. 2002. High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia. – Evolution. 56(7): 1362–1373. https://doi.org/10.1111/j.0014-3820.2002.tb01450.x
- Woodell S.R., Kootin-Sanwu M. 1971. Intraspecific variation in Caltha palustris L. – New Phytol. 70(1): 173–186. https://doi.org/10.1111/j.1469-8137.1971.tb02522.x
- Zhang Z.-Q., Zhu X.-F., Sun H., Yang Y.-P., Barrett S.C.H. 2014. Size-dependent gender modification in Lilium apertum (Liliaceae): does this species exhibit gender diphasy? – Ann. Bot. 114(3): 441–453. https://doi.org/10.1093/aob/mcu140
- Ziman S.N. Ecological and morphological analysis of the family Ranunculaceae. – Bot. Zhurn. 65(8): 1120–1130 (In Russ.).
Supplementary files
