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Maternal effects on seed heteromorphism: a dual dynamic bet hedging strategy

Published online by Cambridge University Press:  05 July 2019

Li Jiang ,
Lei Wang Open the ORCID record for Lei Wang [Opens in a new window] ,
Carol C. Baskin ,
Changyan Tian  and
Zhenying Huang
Li Jiang
Affiliation:
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China
Lei Wang*
Affiliation:
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China
Carol C. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA
Changyan Tian
Affiliation:
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China
Zhenying Huang*
Affiliation:
State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, China
*
Author for correspondence: Lei Wang, Email: egiwang@ms.xjb.ac.cn and Zhenying Huang, Email: zhenying@ibcas.ac.cn
Author for correspondence: Lei Wang, Email: egiwang@ms.xjb.ac.cn and Zhenying Huang, Email: zhenying@ibcas.ac.cn
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Abstract

Maternal effects on offspring seeds are mainly caused by seed position on, and the abiotic environment of, the mother plant. Seed heteromorphism, a special form of position effect, is the production by an individual plant of morphologically distinct seed types, usually with different ecological behaviours. Seed heteromorphism is assumed to be a form of bet hedging and provides an ideal biological model to test theoretical predictions. Most studies of maternal effects on seeds have focused on abiotic environmental factors and changes in mean seed traits of offspring. Suaeda salsa is an annual halophyte that produces dimorphic seeds within the same inflorescence. We tested the hypothesis that plants grown from brown seeds of S. salsa have a higher offspring brown seed:black seed morph ratio and variance in seed size than plants from black seeds. Results from a pot experiment showed that plants grown from brown seeds had a higher brown seed:black seed ratio than plants grown from black seeds. This is the first layer of dynamic bet hedging. Brown seeds had higher size variation than black seeds, and seeds produced by plants from brown seeds also had higher seed size variation than plants grown from black seeds. This is the second layer of dynamic bet hedging. Thus, the maternal effect of seed heteromorphism is dual dynamic bet hedging. Furthermore, for seed traits we verified for the first time the theoretical prediction that an increase in offspring size variability induces an increase in the mean size of offspring.

Keywords

bet hedgingmaternal effectseed heteromorphismseed sizeSuaeda
Type
Short Communication
Information
Seed Science Research , Volume 29 , Issue 2 , June 2019 , pp. 149 - 153
Copyright
Copyright © Cambridge University Press 2019 

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References

Arshad, W, Sperber, K, Steinbrecher, T, Nichols, B, Jansen, VAA, Leubner-Metzger, G and Mummenhoff, K (2019) Dispersal biophysics and adaptive significance of dimorphic diaspores in the annual Aethionema arabicum (Brassicaceae). New Phytologist 221, 1434–1446.Google Scholar
Cheplick, GP and Quinn, JA (1983) The shift in aerial/subterranean fruit ratio in Amphicarpum purshii: causes and significance. Oecologia 57, 374–379.Google Scholar
Crean, AJ and Marshall, DJ (2009) Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philosophical Transactions of the Royal Society of London Series B - Biological Sciences 364, 1087–1096.Google Scholar
Doudová, J, Douda, J and Mandák, B (2017) The complexity underlying invasiveness precludes the identification of invasive traits: a comparative study of invasive and non-invasive heterocarpic Atriplex congeners. PloS ONE 12, e0176455.Google Scholar
El-Keblawy, A, Gairola, S and Bhatt, A (2016) Maternal salinity environment affects salt tolerance during germination in Anabasis setifera: a facultative desert halophyte. Journal of Arid Land 8, 254–263.Google Scholar
Galloway, LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytologist 166, 93–99.Google Scholar
Gutterman, Y and Fenner, M (2000) Maternal effects on seeds during development. In Seeds: The Ecology of Regeneration in Plant Communities (2nd edn), pp. 59–84. Wallingford, UK: CABI Press.Google Scholar
Hughes, PW (2018) Minimal-risk seed heteromorphism: proportions of seed morphs for optimal risk-averse heteromorphic strategies. Frontiers in Plant Science 9, 1412.Google Scholar
Imbert, E (2002) Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology Evolution and Systematics 5, 13–36.Google Scholar
Khan, MA, Gul, B and Weber, DJ (2001) Germination of dimorphic seeds of Suaeda moquinii under high salinity stress. Australian of Jouranl Botany 49, 185–192.Google Scholar
Kołodziejek, J (2017) Effect of seed position and soil nutrients on seed mass, germination and seedling growth in Peucedanum oreoselinum (Apiaceae). Scientific Reports 7, 1959.Google Scholar
Liu, RR, Wang, L, Tanveer, M and Song, J (2018) Seed heteromorphism: an important adaptation of halophytes for habitat heterogeneity. Frontiers in Plant Science 9, 1515.Google Scholar
Lu, JJ, Tan, DY, Baskin, JM and Baskin, CC (2012) Phenotypic plasticity and bet-hedging in a heterocarpic winter annual/spring ephemeral cold desert species of Brassicaceae. Oikos 121, 357–366.Google Scholar
Mandák, B and Pyšek, P (1999) Effects of plant density and nutrient levels on fruit polymorphism in Atriplex sagittata. Oecologia 119, 63–72.Google Scholar
Marshall, DJ and Uller, T (2007) When is a maternal effect adaptive? Oikos 116, 1957–1963.Google Scholar
Sadeh, A, Guterman, H, Gersani, M and Ovadia, O (2009) Plastic bet-hedging in an amphicarpic annual: an integrated strategy under variable conditions. Ecology and Evolution 23, 373–388.Google Scholar
Sendek, A, Herz, K, Auge, H, Hensen, I and Klotz, S (2015) Performance and responses to competition in two congeneric annual species: does seed heteromorphism matter? Plant Biology 17, 1203–1209.Google Scholar
Simons, AM (2011) Modes of response to environmental change and the elusive empirical evidence for bet hedging, Proceedings of the Royal Society B - Biological Sciences 278, 1601–1609.Google Scholar
Song, J and Wang, BS (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Annals of Botany 115, 541–553.Google Scholar
Venable, DL (1985) The evolutionary ecology of seed heteromorphism. American Naturalist 126, 577–595.Google Scholar
Wang, L, Baskin, JM, Baskin, CC, Cornelissen, JHC, Dong, M and Huang, ZY (2012) Seed dimorphism, nutrients and salinity differentially affect seed traits of the desert halophyte Suaeda aralocaspica via multiple maternal effects. BMC Plant Biology 12, 170.Google Scholar
Wang, F, Xu, Y, Wang, S, Shi, W, Liu, R, Feng, G and Song, J (2015) Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiology and Biochemistry 95, 41–48.Google Scholar
Yao, S, Lan, H and Zhang, F (2010) Variation of seed heteromorphism in Chenopodium album and the effect of salinity stress on the descendants. Annals of Botany 105, 1015–1025.Google Scholar