Abstract
Maternal effects on the induction of defensive morphology are regarded as an adaptive strategy. For instance, a female can transmit environmental conditions related to predation risk to offspring of the same generation or succeeding generations. However, studies have presented limited information regarding such an adaptive maternal effect on monogonont rotifers. In the present study, the maternal effects on the spine development of rotifers were evaluated using Brachionus calyciflorus-Asplanchna models. Asplanchna can release soluble kairomones into the environments, thereby inducing B. calyciflorus to form defensive morphs (e.g., elongated posterolateral spines). Our empirical data supported the hypothesis that an amictic Brachionus-experienced Asplanchna kairomones could produce offspring with longer posterolateral spine in the current or succeeding generation than those of a non-experienced amictic female. On the basis of our data, we speculated that the maternal effect of B. calyciflorus may involve the transfer and dilution of inducers (e.g., hormone) within and between generations. On one hand, our results reinforced the within-generation maternal effects on induction of defensive morphology of rotifers; on the other hand, our results enhanced transgenerational inducible defense to other planktonic taxa that have been only observed in cladocera.
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Aránguiz-Acuňa, A., R. Ramos-Jiliberto, N. Sarma, S. S. S. Sarma, R. O. Bustamante & V. Toledo, 2010. Benefits, costs and reactivity of inducible defences: an experimental test with rotifers. Freshwater Biology 55: 2114–2122.
Agrawal, A. A., C. Laforsch & R. Tollrian, 1999. Transgenerational induction of defenses in animals and plants. Nature 401: 60–63.
Alekseev, V. & W. Lampert, 2001. Maternal control of resting-egg production in Daphnia. Nature 414: 899–901.
Bertani, S., S. Leonardi & G. Rossetti, 2013. Antipredator-induced trait changes in Brachionus and prey selectivity by Asplanchna in a large river under low-discharge conditions: evidence from a field study. Hydrobiologia 702: 227–239.
Ferrari, M. C. O., B. D. Wisenden & D. P. Chivers, 2010. Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology 88: 698–724.
Gilbert, J. J., 1966. Rotifer ecology and embryological induction. Science 151: 1234–1237.
Gilbert, J. J., 1999. Kairomone-induced morphological defenses in rotifers. In Tollrian, R. & C. D. Harvell (eds), The Ecology and Evolution of Inducible Defenses. Princeton University Press, New Jersey: 127–141.
Gilbert, J. J., 2007. Induction of mictic females in the rotifer Brachionus: oocytes of amictic females respond individually to population-density signal only during oogenesis shortly before oviposition. Freshwater Biology 52: 1417–1426.
Gilbert, J. J., 2009. Predator-specific inducible defenses in the rotifer Keratella tropica. Freshwater Biology 54: 1933–1946.
Gilbert, J. J., 2011. Induction of different defences by two enemies in the rotifer Keratella tropica: response priority and sensitivity to enemy density. Freshwater Biology 56: 926–938.
Gilbert, J. J., 2012. Predator-induced defense in rotifers: developmental lags for morph transformations, and effect on population growth. Aquatic Ecology 46: 475–486.
Gilbert, J. J., 2013. The cost of predator-induced morphological defense in rotifers: experimental studies and synthesis. Journal of Plankton Research 35: 461–472.
Gilbert, J. J. & M. A. McPeek, 2013. Maternal age and spine development in a rotifer: ecological implications and evolution. Ecology 94: 2166–2172.
Gilbert, J. J. & T. Schröder, 2007. Intraclonal variation in propensity for mixis in several rotifers: variation among females and with maternal age. Hydrobiologia 593: 121–128.
Gilbert, J. J. & J. K. Waage, 1967. Asplanchna, Asplanchna-substance, and posterolateral spine length variation of the rotifer Brachionus calyciflorus in a natural environment. Ecology 48: 1027–1031.
Hagiwara, A., Y. Kadota & A. Hino, 2005. Maternal effect by stem female in Brachionus plicatilis: effect of starvation on mixis induction in offspring. Hydrobiologia 546: 275–279.
Halbach, U., 1970. Die Ursachen der Temporalvariation von Brachionus calyciflorus Pallas (Rotatoria). Oecologia 4: 262–318.
Holeski, L. M., G. Jander & A. A. Agrawal, 2012. Transgenerational defense induction and epigenetic inheritance in plants. Trends in Ecology and Evolution 27: 618–626.
Kilham, S. S., D. A. Kreeger, S. G. Lynn, C. E. Goulden & L. Herrera, 1998. COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377: 147–159.
Lamontagne, J. M. & E. Mccauley, 2001. Maternal effects in Daphnia: what mothers are telling their offspring and do they listen? Ecology Letter 4: 64–71.
Lass, S. & P. Spaak, 2002. Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491: 221–239.
Lynch, M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnology and Oceanography 24: 253–272.
Marshall, D. J. & T. Uller, 2007. When is a maternal effect adaptive? Oikos 116: 1957–1963.
Mikulski, A. & J. Pijanowska, 2009. Maternal experience can enhance production of resting eggs in Daphnia exposed to the risk of fish predation. Archiv für Hydrobiologie 174: 301–305.
Mikulski, A. & J. Pijanowska, 2010. When and how can Daphnia prepare their offspring for the threat of predation? Hydrobiologia 643: 21–26.
Mousseau, T. A. & C. W. Fox, 1998. The adaptive significance of maternal effects. Trends in Ecology and Evolution 13: 403–407.
Sarma, S. S. S., R. A. L. Resendiz & S. Nandini, 2011. Morphometric and demographic responses of brachionid prey (Brachionus calyciflorus Pallas and Plationus macracanthus (Daday)) in the presence of different densities of the predator Asplanchna brightwellii (Rotifera: Asplanchnidae). Hydrobiologia 662: 179–187.
Stemberger, R. S., 1990. Food limitation, spination, and reproduction in Brachionus calyciflorus. Limnology and Oceanography 35: 33–44.
Schröder, T. & J. J. Gilbert, 2004. Transgenerational plasticity for sexual reproduction and diapause in the life cycle of monogonont rotifers: intraclonal, intraspecific and interspecific variation in the response to crowding. Functional Ecology 18: 459–466.
Schröder, T. & J. J. Gilbert, 2009. Maternal age and spine development in the rotifer Brachionus calyciflorus: increase of spine length with birth orders. Freshwater Biology 54: 1054–1065.
Sun, D. & C. J. Niu, 2012. Maternal crowding can enhance the propensity of offspring to produce mictic females in the rotifer Brachionus calyciflorus. Journal of Plankton Research 34: 732–737.
Tollrian, R. & C. D. Harvell, 1999. The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton.
Van Donk, E., 2007. Chemical information transfer in freshwater plankton. Ecological Informatics 2: 112–120.
Yin, X. W., P. F. Liu, S. S. Zhu & X. X. Chen, 2010. Food selectivity of herbivore Daphnia magna (Cladocera) and its impact on competition outcome between two freshwater green algae. Hydrobiologia 655: 15–23.
Yin, X. W. & C. J. Niu, 2008. Polymorphism in stem females and successive parthenogenetic generations in Brachionus calyciflorus Pallas. Aquatic Ecology 42: 415–420.
Yin, X. W., B. B. Tan, Y. C. Zhou & W. Liu. Developmental time of male and female in rotifers with sexual size dimorphism. Hydrobiologia (In revision).
Zar, J. H., 1999. Biostatistical Analysis. Prentice-Hall, Illinois, USA.
Acknowledgments
We thank two anonymous reviewers for constructive comments that improve our manuscript greatly. This study was supported by the National Natural Science Foundation of China (31000218; 51079123; 41206110), the Program for Liaoning Excellent Talents in University (LJQ2011079), and the Natural Science Foundation of Dalian (2012J21DW013).
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Yin, X.W., Zhao, N.X., Wang, B.H. et al. Transgenerational and within-generational induction of defensive morphology in Brachionus calyciflorus (Rotifera): importance of maternal effect. Hydrobiologia 742, 313–325 (2015). https://doi.org/10.1007/s10750-014-1995-1
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DOI: https://doi.org/10.1007/s10750-014-1995-1