Abstract
The sexual system of Aruncus aethusifolius (Amygdaloideae, Rosaceae), which is endemic to Korean, remains poorly understood. Here, we investigate the sexual system of A. aethusifolius based on a detailed morphological, micromorphological, and anatomical study. The natural population of this endemic species is restricted to Hallasan Mountain on Jeju Island. We found two types of plants in the natural population: hermaphrodite and female plants. Each sexual morph exhibited different floral traits, showing a modest form of sexual dimorphism. Significant quantitative differences were detected in the investigated organs (i.e., petal, sepal, ovary, stamen, nectary, and follicle). For example, hermaphroditic floral organs (i.e., petal, sepal, stamen and nectary) were larger than those of the female flowers (P < 0.001), but the ovary and follicle were relatively larger in female flowers than in hermaphrodites (P < 0.001). The fruit-setting rate (proportion of matured fruits/flowers) in female individuals (approximately 79.29%) was, on an average, more than twice that of hermaphroditic ones (approximately 34.41%). In addition, female flowers produced more seeds per follicle. Usually, 5–6 seeds per follicle developed in female flowers, whereas 3–4 seeds were produced in the hermaphroditic flowers. Accordingly, A. aethusifolius is another example of a gynodioecious species of flowering plants with clear sexual dimorphism.
Similar content being viewed by others
References
Ashman TL, Stanton ML (1991) Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72:993–1003. https://doi.org/10.2307/1940599
Ashman C, Khanna SN, Pederson MR (2000) Structure and isomerization in alkali halide clusters. Phys Status Solidi b 217:323–334
Bacha MA, Ali MA, Farahat FA (1997) Chemical composition of pollen grains of some date palm males grown in Riyadh, Saudi Arabia. Arab Gulf J Sci Res 15:783–803
Baker HG (1948) Corolla-size in gynodioecious and gynomonoecious species of flowering plants. Proc Leeds Philos Lit Soc (Sci Sect II) 5:136–139
Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284. https://doi.org/10.1038/nrg776
Barrett SCH, Hough J (2013) Sexual dimorphism in flowering plants. J Exp Bot 64:67–82. https://doi.org/10.1093/jxb/ers308
Bawa KS (1980) Evolution of dioecy in flowering plants. Annual Rev Ecol Syst 11:15–39
Bawa KS, Beach JH (1981) Evolution of sexual systems in flowering plants. Ann Missouri Bot Gard 68:254–274. http://www.jstor.org/stable/2398798
Bawa KS, Opler PA (1975) Dioecism in tropical forest trees. Evolution 29:167–179. http://www.jstor.org/stable/2407150v
Bell G (1985) On the function of flowers. Proc R Soc Lond B 224:223–265. http://www.jstor.org/stable/36033
Benevides CR, Haddad IVN, Barreira NP, de Rodarte ATA, Galetto L, de Santiago-Fernandes LDR, de Lima HA (2013) Maytenus obtusifolia Mart. (Celastraceae): a tropical woody species in a transitional evolutionary stage of the gynodioecy–dioecy pathway. Pl Syst Evol 299:1693–1707. https://doi.org/10.1007/s00606-013-0826-6
Bond TET (1962) On bisexual flowers in Aruncus sylvester. Baileya 10:89–91
Budar F, Pelletier G (2001) Male sterility in plants: occurrence, determinism, significance and use. Compte Rend Acad Sci Ser III 324:543–550. https://doi.org/10.1016/S0764-4469(01)01324-5
Chang SM (2006) Female compensation through the quantity and quality of progeny in a gynodioecious plant, Geranium maculatum (Geraniaceae). Amer J Bot 93:263–270. https://doi.org/10.3732/ajb.93.2.263
Charlesworth D (2006) Evolution of plant breeding systems. Curr Biol 16:726–735. https://doi.org/10.1016/j.cub.2006.07.068
Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Amer Naturalist 112:975–997. http://www.jstor.org/stable/2460344
Darwin CR (1877) The different forms of flowers on plants of the same species. Murray, London
De Melo MC, Borba EL, Paiva EAS (2010) Morphological and histological characterization of the osmophores and nectaries of four species of Acianthera (Orchidaceae: Pleurothallidinae). Pl Syst Evol 286:141–151. https://doi.org/10.1007/s00606-010-0294-1
Delph LF (1996) Flower size dimorphism in plants with unisexual flowers. In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, pp 217–237
Delph LF (1999) Sexual dimorphism in life history. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 149–173
Delph LF, Lively CM (1992) Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos 63:161–170. http://www.jstor.org/stable/3545374
Delph LF, Lloyd DG (1991) Environmental and genetic control of gender in the dimorphic shrub Hebe subalpina. Evolution 45:1957–1964. http://www.jstor.org/stable/2409844
Delph LF, Galloway LF, Stanton ML (1996) Sexual dimorphism in flower size. Amer Naturalist 148:299–320. http://www.jstor.org/stable/2463456
Dormer KJ (1961) The crystals in the ovaries of certain Compositae. Ann Bot (Oxford) 25:241–254
Dufay M, Billard E (2012) How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Ann Bot (Oxford) 109:505–519. https://doi.org/10.1093/aob/mcr062
Dufay M, Champelovier P, Käfer J, Henry JP, Mousset S, Marais GAB (2014) An angiosperm-wide analysis of the gynodioecy-dioecy pathway. Ann Bot (Oxford) 114:539–548. https://doi.org/10.1093/aob/mcu134
Eckhart VM (1991) Floral investment and the mating system of Phacelia linearis (Hydrophyllaceae). PhD Thesis, University of Utah, Utah
Eckhart VM (1999) Sexual dimorphism in flowers and inflorescences. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 123–148
Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annual Rev Pl Biol 56:41–71. https://doi.org/10.1146/annurev.arplant.56.032604.144106
Galen C, Newport MEA (1987) Bumblebee behavior and selection on flower sizein the sky pilot, Polemonium viscosum. Oecologia 74:20–23. https://doi.org/10.1007/BF00377340
Gębura J, Winiarczyk K (2016) A study on calcium oxalate crystals in Tinantia anomala (Commelinaceae) with special reference to ultrastructural changes during anther development. J Pl Res 4:685–695. https://doi.org/10.1007/s10265-016-0812-5
Gu C, Alexander C (2003) Aruncus L. In: Wu ZY, Raven PH (eds) Flora of China, vol. 9. Pittosporaceae through Connaraceae. Science Press, Beijing, pp 74–75
Harder L, Barrett S (1992) The energy cost of bee pollination for Pontederia cordata (Pontederiaceae). Funct Ecol 6:226–233. http://www.jstor.org/stable/2389759
Hong SP, Moon HK (2003) Gynodioecy in Lycopus maackianus Makino (Lamiaceae) in Korea: floral dimorphism and nutlet production. Flora 198:461–467. https://doi.org/10.1078/0367-2530-00119
Horner HT (1977) A comparative light- and electron-microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile sunflower (Helianthus annuus). Amer J Bot 64:745–759. http://www.jstor.org/stable/2441727
Horovitz A, Galil J (1972) Gynodioecism in East Mediterranean Hirschfeldia incana. Cruciferae. Bot Gaz 133:127–131. https://doi.org/10.1086/336625
Hutchinson J (1964) The genera of flowering plants, vol. 1. Dicotyledons. Clarendon Press, Oxford
Ikeda H (2001) Aruncus L. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan, vol. IIb. Angiospemae dicotyledoneae archichlamydeae(b). Kodansha, Tokyo, pp 101–102
Jang TS, Moon HK, Hong SP (2015) Sex expression, population structure, and floral dimorphism in a gynodioecious herb, Agastache rugosa (Lamiaceae) in Korea. Flora 215:23–32. https://doi.org/10.1016/j.flora.2015.06.004
Johnson SG, Delph LF, Elderkin CL (1995) The effect of petal-size manipulation on pollen removal, seed set, and insect-visitor behavior in Campanula americana. Oecologia 102:174–179. https://doi.org/10.1007/BF00333249
Kalkman C (2004) Rosaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol. 6. Flowering plants-dicotyledons: celastrales, oxalidales, rosales, cornales, ericales. Springer, Berlin, pp 343–386
Kawakubo N (1994) Gynodioecy in Cirsium chikushiense koidz. (Compositae). Ann Bot (Oxford) 74:357–364
Lee ST (2007) Aruncus L. In: Flora of Korea Editorial Committee (ed) The genera of vascular plants of Korea. Academy Publishing Co, Seoul, pp 541–542
Levin DA (1973) The role of trichomes in plant defense. Quart Rev Biol 48:3–15. http://www.jstor.org/stable/2822621
Li J, Koski MH, Ashman TL (2012) Functional characterization of gynodioecy in Fragaria vesca ssp. bracteata (Rosaceae). Ann Bot (Oxford) 109:545–552. https://doi.org/10.1093/aob/mcr279
Lloyd D (1975) The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45:325–339. https://doi.org/10.1007/BF01508307
Marciniuk J, Marciniuk P, Rymuza K (2010) Effects of site conditions on sexual dimorphism and sex ratio in lowland populations of Aruncus sylvestris Kostel. (Rosaceae). Polish J Ecol 58:249–257
McCauley DE, Bailey MF (2009) Recent advances in the study of gynodioecy: the interface of theory and empiricism. Ann Bot (Oxford) 104:611–620. https://doi.org/10.1093/aob/mcp141
Mellichamp TL (1976) A comparative study of Aruncus (Rosaceae) and Astilbe (Saxifragaceae), and the problem of their relationships. PhD Thesis, University of Michigan, Michigan
Mellichamp TL (2014) Aruncus L. In: Flora of North America Editorial Committee (ed) Flora of North America, vol. 9. Oxford University Press, New York, pp 422–424
Meric C (2009) Calcium oxalate crystals in some species of the Tribe Inuleae (Asteraceae). Acta Biol Cracov Bot 51:105–110
Meric C, Dane F (2004) Calcium oxalate crystals in floral organs of Helianthus annuus L. and H. tuberosus L. (Asteraceae). Acta Biol Szeged 48:19–23
Moon HK, Hong SP (2015) Morphological traits of gynodioecious Persicaria amphibia (Polygonaceae). Phytotaxa 219:133–143. https://doi.org/10.11646/phytotaxa.219.2.3
Nepi M (2007) Nectary structure and ultrastructure. In: Nicolson S, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 129–166
Ohwi J (1965) Flora of Japan. Smithsonian Institution, Washington, D.C.
Pannell J (2002) The evolution and maintenance of androdioecy. Annu Rev Ecol Evol Syst 33:397–425. https://doi.org/10.1146/annurev.ecolsys.33.010802.150419
Plack A (1957) Sexual dimorphism in Labiatae. Nature 180:1218–1219. https://doi.org/10.1038/1801218a0
Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 101:1588–1596. https://doi.org/10.3732/ajb.1400196
Richards AJ (1997) Plant breeding systems. Chapman & Hall, London
Robertson KR (1974) The genera of Rosaceae in the southeastern United States. J Arnold Arbor 55:303–332
Ross MD (1978) The evolution of gynodioecy and subdioecy. Evolution 32:174–188. http://www.jstor.org/stable/2407418
Schemske DW (1978) Evolution of reproductive characteristics in Impatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Ecology 59:596–613. https://doi.org/10.2307/1936588
Schultz ST (2003) Sexual dimorphism in gynodioecious Sidalcea hirtipes (Malvaceae). I. Seed, fruit, and ecophysiology. Int J Pl Sci 164:165–173. https://doi.org/10.1086/344550
Shykoff JA, Kolokotronis SO, Collin CL, López-Villavicencio M (2003) Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135:1–9. https://doi.org/10.1007/s00442-002-1133-z
Song JH, Oak MK, Hong SP (2016) Morphological traits in an androdioecious species, Chionanthus retusus (Oleaceae). Flora 223:129–137. https://doi.org/10.1016/j.flora.2016.05.009
Spigler RB, Ashman TL (2012) Gynodioecy to dioecy: are we there yet? Ann Bot (Oxford) 109:531–543. https://doi.org/10.1093/aob/mcr170
Thiers B (2017) [continuously updated] Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at: http://sweetgum.nybg.org/ih/. Accessed 10 July 2017
Tilton VR, Horner HT Jr (1980) Calcium oxalate raphide crystals and crystalliferous idioblasts in the carpels of Ornithogalum caudatum. Ann Bot (Oxford) 46:533–539. https://doi.org/10.1093/oxfordjournals.aob.a085951
Torrices R, Méndez M, Gómez JM (2011) Where do monomorphic sexual systems fit in the evolution of dioecy? Insights from the largest family of angiosperms. New Phytol 190:234–248
Tutin TG (1968) Aruncus L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora europaea, vol. 2. Rosaceae to umbelliferae. Cambridge University Press, Cambridge, pp 3–6
Webb CJ (1999) Empirical studies: evolution and maintenance of dimorphic breeding systems. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 61–95
Werker E (1993) Function of essential oil-secreting glandular hairs in aromatic plans of Lamiaceae-a review. Flav Frag J 8:249–255. https://doi.org/10.1093/aob/mcr170
Williams CF, Kuchenreuther MA, Drew A (2000) Floral dimorphism, pollination, and self-fertilization in gynodioecious Geranium richardsonii (Geraniaceae). Amer J Bot 87:661–669
Willson MF (1990) Sexual selection in plants and animals. Trends Ecol Evol 5:210–214. https://doi.org/10.1016/0169-5347(90)90133-X
Wolfe LM, Shmida A (1997) The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology 78:101–110. http://www.jstor.org/stable/2265982
Yampolsky C, Yampolsky H (1922) Distribution of sex forms in the phanerogamic flora. Bibliogr Genet 3:4–62
Yun N, Suh HJ, Oh SH (2017) Sexuality of Aruncus aethusifolius (Rosaceae). Korean J Pl Taxon 47:189–195. https://doi.org/10.11110/kjpt.2017.47.3.189
Yuzepchuk SV (1939) Aruncus. In: Komarov VL (ed) Flora of the U.S.S.R., vol. 4, Rosales and Sarraceniales. Izdatel’’stvo Akademii Nauk SSSR. Moscow, Leningrad. Pub. by Israel Program for Scientific Translations Ltd., Jerusalem, pp 238–240
Acknowledgements
We would like to thank the directors of the herbaria of KB, KH, KHUS, KYO, NY, and TI for permitting the examination of specimens through loans. We are also grateful to our colleagues Dr. H.-K. Moon, S.-Y. Kim, and M.-J. Kong for helping us in various ways. Moreover, three anonymous reviewers and the handling editor Dr. Louis P. Ronse De Craene, whose comments and corrections improved the work, are also acknowledged. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Sciences and Technology (NRF-2012R1A1A2004149) to S.-P. Hong.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Louis P. Ronse De Craene.
Rights and permissions
About this article
Cite this article
Oak, MK., Song, JH. & Hong, SP. Sexual dimorphism in a gynodioecious species, Aruncus aethusifolius (Rosaceae). Plant Syst Evol 304, 473–484 (2018). https://doi.org/10.1007/s00606-018-1493-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-018-1493-4