Biodiversity Science ›› 2018, Vol. 26 ›› Issue (5): 519-526.doi: 10.17520/biods.2018038

• Original Papers • Previous Article     Next Article

Temporal variation of plant sexes in a wild population of Tulipa sinkiangensis over seven years

Juan Wang, Yaxin Zhai, Aiqin Zhang*()   

  1. College of Life Science and Technology, Xinjiang University, Urumqi 830046
  • Received:2018-02-05 Accepted:2018-04-26 Online:2018-09-11
  • Zhang Aiqin E-mail:zaql@sohu.com
  • About author:

    # Co-first authors

Understanding the variation in plant sexual strategies provides insights into the evolution of plant sexual systems. In hermaphrodite plants, floral gender is thought to be a plastic response that allows individuals to vary resource allocation to both female and male function under variable environmental conditions. Tulipa sinkiangensis is known to be hermaphroditic, early spring ephemeral plant, but our preliminary investigation showed that some populations had perfect flowers whereas other populations had staminate flowers. To understand correlates of occurrence and temporal variation of staminate flowers in T. sinkiangensis, we examined flower sex and its variation among individuals in a population of nearly 1,000 plants in Xinjiang, northwestern China from 2011 to 2017. (1) In the study population one-flower and two-flower plants comprised 74.5% (4,373) and 23.0% (1,358) of all flowering individuals (5,863), respectively. Sex differentiation was seen primarily in drier areas with shallow soils. Perfect and staminate flowers randomly occurred on different plants, constituting a hermaphroditic based population with some male and andromonoecious individuals. (2) Compared to perfect flowers, staminate flowers appeared later within individual plants and in the whole population during flowering. Staminate flowers were smaller and had aborted ovaries without visible ovules. However, pollen number and size, pollen morphology and fertility were not significantly different from perfect flowers when the two floral morphs were the same size. (3) During 2011 to 2014 of the study period, percentage of staminate flowers in the population declined from 23.4% to 3.1% but remained at stable (1.5% to 1.0%) from 2015 to 2017. The number of one-flower plants and two-flower plants fluctuated with time. (4) Our observations suggest that the production of staminate flowers in this endemic tulip flower was likely a plastic response to plant resource status, environmental conditions and other ecological factors.

Key words: Tulipa sinkiangensis, gender differentiation, staminate flowers, sex ratio, temporal variation

Fig. 1

The morphological and anatomy structure of staminate flower and perfect flower in Tulipa sinkiangensis. (A) Tulipa sinkiangensis plant with perfect flower; (B) Perfect flower with fertile ovary; (C) Staminate flower with sterile ovary; (D) Ovary crosscutting of perfect flower; (E) Ovary crosscutting of staminate flower; (F) Pollen grain morphology of perfect flower; (G) Ovary longitudinal cutting of perfect flower; (H) Ovary longitudinal cutting of staminate flower; (I) Pollen grain morphology of staminate flower. Ov1, Ovary; Ov2, Ovule; Pl, Placenta."

Fig. 2

Temporal variation of plant sexes in a wild population of Tulipa sinkiangensis. (A) The sex-ratio dynamic of staminate and perfect flower within plants from 2011 to 2017; (B) Annual changes in the proportion of staminate flowers at the level of population from 2011 to 2017. Different letters indicate significant difference at P = 0.05 level."

Table 1

Floral traits of perfect and staminate flowers in Tulipa sinkiangensis (mean ± SE, n = 20)"

花型
Floral morph
外轮Outer (cm) 内轮Inner (cm) 雄蕊Stamen (cm) 雌蕊Pistil (cm) 花粉量
No. of
pollen
grains per
flower
败育率
Abortin
ratio
(%)
花瓣长
Petal
length
花瓣宽
Petal width
花瓣长
Petal
length
花瓣宽
Petal
width
花丝长
Filament length
花药长
Anther length
子房直径 Ovary
diameter
雌蕊长
Pistil length
两性花
Perfect flower
2.31 ± 0.050 0.81 ± 0.035 2.14 ± 0.042 0.97 ± 0.042 0.52 ±
0.009
0.57 ± 0.013 0.22 ± 0.011 0.82 ± 0.039 101,000 ± 7,007 3.16 ± 0.99
雄花
Staminate flower
2.20 ± 0.039 0.59 ± 0.023 1.99 ± 0.040 0.84 ± 0.034 0.50 ±
0.010
0.51 ± 0.015 0.08 ± 0.010 0.56 ± 0.045 95,055 ± 10,249 3.47 ± 0.91
t 1.79 5.38 2.64 2.38 1.35 3.52 8.75 4.39 0.48 0.22
P 0.080 2.15*10-6 0.011 0.021 0.18 0.0010 4.77*10-7 0.0010 0.64 0.83
1 Anderson GJ, Symon DE (1989) Functional dioecy and andromonoecy in Solanum. Evolution, 43, 204-219.
2 Abdusalam A, Tan DY, Tahan O (2012) Effects of vegetative growth, plant size and flowering order on sexual reproduction allocation of Tulipa sinkiangensis. Biodiversity Science, 20, 391-399. (in Chinese with English abstract)
[艾沙江·阿不都沙拉木, 谭敦炎, 吾买尔夏提·塔汉 (2012) 新疆郁金香营养生长、个体大小和开花次序对繁殖分配的影响. 生物多样性, 20, 391-399.]
3 Abdusalam A, Tan DY (2014) Contribution of temporal floral closure to reproductive success of the spring-flowering Tulipa iliensis. Journal of Systematics and Evolution, 52, 186-194.
4 Bertin RI (1982) The evolution and maintenance of andromonoecy. Evolutionary Theory, 6, 25-32.
5 Charnov EL (1982) The Theory of Sex Allocation. Princeton University Press, Princeton.
6 Charlesworth D (1999) Theories of the evolution of dioecy. In: Gender and Sexual Dimorphism in Flowering Plants (eds Geber MA, Dawson TE, Delph LF), pp. 33-60. Springer, Berlin.
7 Chen JR (1991) The review and application of plant sporopollen dyeing technology. In: Botanical Research (ed. Institute of Botany, Chinese Academy of Sciences), pp. 269-276. Science Press, Beijing. (in Chinese)
[陈家瑞 (1991) 植物孢粉染色技术综述及其应用. 植物学集刊(中国科学院植物研究所编). 科学出版社, 北京.]
8 Dai C, Galloway LF (2012) Male flowers are better fathers than hermaphroditic flowers in andromonoecious Passiflora incarnate. New Phytologist, 193, 787-796.
9 Darwin C (1877) The Different Forms of Flowers on Plants of the Same Species. John Murray, London.
10 Delesalle VA (1989) Year-to-year changes in phenotypic gender: A monoecious cucurbit Apodanthera undulata. American Journal of Botany, 76, 30-39.
11 Diggle PK (1993) Developmental plasticity, genetic variation, and the evolution of andromonoecy in Solanum hirtum (Solanaceae). American Journal of Botany, 80, 967-973.
12 Elle E (1999) Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). I. Female success. American Journal of Botany, 86, 278-286.
13 Emms SK (1993) Andromonoecy in Zigadenus paniculatus (Liliaceae): Spatial and temporal patterns of sex allocation. American Journal of Botany, 80, 914-923.
14 Freeman DC, Harper KT, Charnov EL (1980) Sex change in plants: Old and new observations and new hypotheses. Oecologia, 47, 222-232.
15 Han B, Wang XF, Huang SQ (2011) The production of male flowers does not decrease with plant size in insect-pollinated Sagittaria trifolia, contrary to predictions of size-dependent sex allocation. Journal of Systematics and Evolution, 49, 379-385.
16 Hanzawa FM, Kalisz S (1993) The relationship between age, size, and reproduction in Trillum grandiflorum (Liliaceae). American Journal of Botany, 80, 405-410.
17 Heslop-Harrison J (1958) The unisexual flower: A reply to criticism. Phytomorphology, 8, 117-184.
18 Huang SQ (2003) Flower dimorphism and the maintenance of andromonoecy in Sagittaria guyanensis ssp. lappula (Alismataceae). New Phytologist, 157, 357-364.
19 Huang SQ, Guo YH (2000) Advances in the research of pollination biology. Chinese Science Bulletin, 45, 225-237. (in Chinese)
[黄双全, 郭友好 (2000) 传粉生物学的研究进展. 科学通报, 45, 225-237.]
20 Huang SQ, Sun SG, Takahashi Y, Guo YH (2002) Gender variation of sequential inflorescences in a monoecious plant Sagittaria trifolia (Alismataceae). Annals of Botany, 90, 613-622.
21 Irwin RE (2000) Morphological variation and female reproductive success in tow sympatric Trillium species: Evidence for phenotypic selection in Trillium erectum and Trillium grandiflorum (Liliaceae). American Journal of Botany, 87, 205-214.
22 Kamenetsky R (1994) Life cycle, flower initiation, and propagation of the desert geophytes Allium rothii. International Journal of Plant Sciences, 49, 603-609.
23 Kawano S, Hiratsuka A, Hayashi K (1982) Life history characteristics and survivorship of Erythronium japonicum. Oikos, 38, 129-149.
24 Kawano S, Masuda J, Hayashi K (2008) Life-history monographs of Japanese plants. 10: Friitillaria koidzumiana Ohwi (Liliaceae). Plant Species Biology, 23, 51-57.
25 Liao WJ, Zhang QG, Zhang DY (2003) A preliminary study on the reproductive features of Nigrum along an altitudinal gradient. Acta Phytoecologica Sinica, 27, 240-248. (in Chinese with English abstract)
[廖万金, 张全国, 张大勇 (2003)不同海拔藜芦种群繁殖特征的初步研究. 植物生态学报, 27, 240-248.]
26 Lloyd DG (1982) Selection of combined versus separate sexes in seed plants. The American Naturalist, 120, 571-585.
27 Lloyd DG, Bawa KS (1984) Modification of the gender of seed plants in varying conditions. Evolutionary Biology, 17, 255-338.
28 Mamut J, Xiong YZ, Tan DY, Huang SQ (2014) Pistillate flowers experience more pollen limitation and less geitonogamy than perfect flowers in a gynomonoecious herb. New Phytologist, 201, 670-677.
29 Mamut J, Xiong YZ, Tan DY, Huang SQ (2017) Flexibility of resource allocation in a hermaphrodite-gynomonoecious herb through deployment of female and male resources in perfect flowers. American Journal of Botany, 104, 461-467.
30 Mao ZM (1984) The research of Tulipa L. plants. Arid Zone Research, 1(2), 39-43. (in Chinese)
[毛祖美 (1984) 新疆郁金香属植物的研究. 干旱区研究, 1(2), 39-43.]
31 Pannell JR, Ojeda F (2000) Patterns of flowering and sex-ratio variation in the Mediterranean shrub Phillyrea angustifolia (Oleaceae): Implications for the maintenance of males with perfects. Ecology Letters, 3, 495-502.
32 Primack RB, Lloyd DG (1980) Andromonoecy in the New- Zealand montane shrub manuka, Leptospermum scoparium (Myrtaceae). American Journal of Botany, 67, 361-368.
33 Shimizu T, Hatanaka Y, Zentoh H, Yashima T, Kinoshita E, Watano Y, Shimizu T (1998) The role of sexual and clonal reproduction in maintaining population in Fritillaria camtschatcensis (L.) Ker-Gawl. (Liliaceae). Ecological Research, 13, 27-39.
34 Sinclair JP, Kameyama Y, Shibata A, Kudo G (2016) Male- biased hermaphrodites in a gynodioecious shrub, Daphne jezoensis. Plant Biology, 18, 859-867.
35 Stócklin J, Pavre P (1994) Effects of plant size and morphological constraints on variation in reproductive components in two related species of Epilobium. Journal of Ecology, 82, 735-746.
36 Traveset A (1995) Reproductive ecology of Cneorum tricoccon L. (Cneoraceae) in the Balearic-Islands. Botanical Journal of the Linnean Society, 117, 221-232.
37 Weiner J (1988) The influence of competition on plant reproduction. In: Plant Reproductive Ecology: Patterns and Strategies (eds Lovett DJ, Lovett DL), pp. 228-245. Oxford University Press, New York.
38 Zhang DY (2004) Life History Evolution and Reproductive Ecology in Plants. Science Press, Beijing. (in Chinese)
[张大勇 (2004) 植物生活史进化与繁殖生态学. 科学出版社, 北京.]
39 Zhang ZC, Tan DY (2012) Floral sex allocation and flowering pattern in the andromonocious Soranthus meyeri (Apiaceae). Chinese Journal of Plant Ecology, 36, 63-71. (in Chinese with English abstract)
[张振春, 谭敦炎 (2012) 雄全同株植物簇花芹花期性别分配与开花式样. 植物生态学报, 36, 63-71.]
40 Zhang ZQ, Zhu XF, Sun H, Yang YP, Barrett SCH (2014) Size-dependent gender modification in Lilium apertum (Liliaceae): Does this species exhibit gender diphasy? Annals of Botany, 114, 441-453.
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[5] Qiu-Shi YU, Qian WANG, Ai-Lan WANG, Gui-Li WU,Jian-Quan LIU. Interspecific delimitation and phylogenetic origin of Pugionium (Brassicaceae)[J]. J Syst Evol, 2010, 48(3): 195 -206 .
[6] ZHANG Qi,YUAN Xiu-Liang,CHEN Xi,LUO Ge-Ping,LI Long-Hui. Vegetation change and its response to climate change in Central Asia from 1982 to 2012[J]. Chin J Plan Ecolo, 2016, 40(1): 13 -23 .
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