Abstract
Monogonont rotifers typically undergo diapause to overpass adverse periods and often show within-population variation in diapause duration. Whether such variation corresponds to phenotypic plasticity, genetic polymorphism, or a bet-hedging strategy to cope with environmental unpredictability still remains unanswered. While bet hedging in diapause duration is often invoked in the rotifer literature, empirical evidence is scant and the description of a proximate mechanism responsible of the within-genotype variation required for bet hedging is still pending. We experimentally explored the role of maternal effects as responsible for the variability observed in the timing of resting egg hatching. By tracking the offspring of controlled crosses in clonal lineages of Brachionus plicatilis, we tested for differences in resting egg diapause duration due to (1) clone effect (controlling for genetic variability), (2) mother effect within clones, and (3) mother age and laying order (as candidate proximate factors explaining variability). We found a significant effect of laying order: the first eggs produced exhibited longer diapauses than eggs produced later. Finally, we critically discussed the idea that if rotifer mothers within a clone cannot anticipate the environment their offspring will experience, then they may produce resting eggs that vary in their timing of hatching via this maternal effect.
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Bates, D., M. Maechler & B. Bolker, 2009. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-31. http://lme4.r-forge.r-project.org/.
Becks, L. & A. F. Agrawal, 2012. The evolution of sex is favoured during adaptation to new environments. PLoS Biology. doi:10.1371/journal.pbio.1001317.
Campillo, S., E. M. García-Roger, M. J. Carmona & M. Serra, 2009. Selection on life-history traits and genetic population divergence in rotifers. Journal of Evolutionary Biology 22: 2542–2553.
Carmona, M. J., M. Serra & M. R. Miracle, 1994. Effect of population density and genotype on life-histroy traits in the rotifer Brachionus plicatilis O.F. Müller. Journal of Experimental Marine Biology and Ecology 182: 223–235.
Childs, D. Z., C. J. E. Metcalf & M. Rees, 2010. Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants. Proceedings of the Royal Society B: Biological Sciences 277: 3055–3064.
Crean, A. J. & D. J. Marshall, 2009. Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philosophical transactions of the Royal Society B: Biological Sciences 364: 1087–1096.
Domenich, T. & D. L. McFadden, 1975. Urban Travel Demand: A Behavioral Analysis. North-Holland Publishing Co, Amsterdam.
Evans, M. E. K. & J. J. Dennehy, 2005. Germ banking: bet hedging and variable release from egg and seed dormancy. The Quarterly Review of Biology 80: 431–451.
Fussmann, G. F., G. Kramer & M. Labib, 2007. Incomplete induction of mixis in Brachionus calyciflorus: patterns of reproduction at the individual level. Hydrobiologia 593: 111–119.
Gabaldón, C., J. Montero-Pau, M. Serra & M. J. Carmona, 2013. Morphological similarity and ecological overlap in two rotifer species. PLoS One. doi:10.1371/journal.pone.0057087.
García-Roger, E. M., M. J. Carmona & M. Serra, 2005. Deterioration patterns in diapausing egg banks of Brachionus (Müller, 1786) rotifer species. Journal of Experimental Marine Biology and Ecology 314(2): 149–161.
García-Roger, E. M., M. J. Carmona & M. Serra, 2006a. Patterns in rotifer diapausing egg Banks: density and viability. Journal of Experimental Marine Biology and Ecology 336(2): 198–210.
García-Roger, E. M., M. J. Carmona & M. Serra, 2006b. Hatching and viability of rotifer diapausing eggs collected from pond sediments. Freshwater Biology 51: 1351–1358.
García-Roger, E. M., M. Serra & M. J. Carmona, 2014. Bet-hedging in diapausing egg hatching of temporary rotifer populations—a review of models and new insights. International Review of Hydrobiology 98: 1–11.
Gremer, J. R. & D. L. Venable, 2014. Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecology Letters 17: 380–387.
Guillard, R. R. L., 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. L. & M. H. Chanley (eds), Culture of Marine Invertebrate Animals. Plenum Press, New York: 26–60.
Johnson, J. B. & K. S. Omland, 2004. Model selection in ecology and evolution. Trends in Ecology and Evolution 19: 101–108.
Kim, H. J. & A. Hagiwara, 2011. Effect of female aging on the morphology and hatchability of resting eggs in the rotifer Brachionus plicatilis Müller. Hydrobiologia 662: 107–111.
King, C. E., 1969. Experimental studies of aging in rotifers. Experimental Gerontology 4: 63–79.
King, C. E. & M. R. Miracle, 1980. A perspective on aging in rotifers. Hydrobiologia 73: 13–19.
Kotani, T., M. Ozaki, K. Matsuoka, T. W. Snell & A. Hagiwara, 2001. Reproductive isolation among geographically and temporally isolated marine Brachionus strains. Hydrobiologia 446(447): 283–290.
Logan, M., 2010. Biostatistical Design and Analysis Using R: A Practical Guide. Blackwell Publishing, Oxford.
Marcus, N. H., R. Lutz, W. Burnett & P. Cable, 1994. Age, viability and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnology & Oceanography 39: 154–158.
Marshall, D. J. & T. Uller, 2007. When is a maternal effect adaptive? Oikos 116: 1957–1963.
Menu, F. & E. Desouhant, 2002. Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132: 167–174.
Oloffson, H., J. Ripa & N. Jonzen, 2009. Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proceedings of the Royal Society B: Biological Sciences 276: 2963–2969.
Philippi, T. & J. Seger, 1989. Hedging one’s evolutionary bets, revisited. Trends in Ecology and Evolution 4: 41–44.
Pinceel, T., B. Vanschoenwinkel, J. Uten & L. Brendonck, 2013. Mechanistic and evolutionary aspects of light-induced dormancy termination in a temporary pond crustacean. Freshwater Science 32: 517–524.
Pinheiro, J. C. & D. M. Bates, 2000. Mixed-Effects Models in S and S-PLUS. Springer, New York.
R Development Core Team, 2011. The R Project for Statistical Computing. R Foundation for statistical computing, Vienna.
Scheuerl, T. & C.-P. Stelzer, 2013. Patterns and dynamics of rapid local adaptation and sex in varying habitat types in rotifers. Ecology and Evolution. doi:10.1002/ece3.781.
Schröder, T., 2005. Diapause in monogonont rotifers. Hydrobiologia 181: 291–306.
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: 458–466.
Serra, M., E. Aparici & M. J. Carmona, 2008. When to be sexual: sexual allocation theory and population density-dependent induction of sex in cyclical parthenogens. Journal of Plankton Research 30: 1207–1214.
Simons, A. M., 2009. Fluctuating natural selection accounts for the evolution of diversification bet-hedging. Proceedings of the Royal Society B: Biological Sciences 276: 1987–1992.
Simons, A. M., 2011. Modes of response to environmental change and the elusive empirical evidence of bet-hedging. Proceedings of the Royal Society B: Biological Sciences 278: 1601–1609.
Simons, A. M. & M. O. Johnston, 1997. Developmental instablility as a bet hedging strategy. Oikos 80: 401–406.
Simons, A. M. & M. O. Johnston, 2003. Suboptimal timing of reproduction in Lobelia inflate may be a conservative bet-hedging strategy. Journal of Evolutionary Biology 16: 233–243.
Simons, A. M. & M. O. Johnston, 2006. Environmental and genetic sources of diversification in the timing of seed germination: implications for the evolution of bet hedging. Evolution 60: 2280–2292.
Snell, T. W. & M. Childress, 1987. The effect of age on male and female fertility in the rotifer Brachionus plicatilis. Hydrobiologia 147: 329–334.
Snell, T. & B. L. Garman, 1986. Encounter probabilities between male and female rotifers. Journal of Experimental Marine Biology and Ecology 97: 221–230.
Snell, T. W., J. Kubanek, W. Carter, A. B. Payne, J. Kim, M. K. Hicks & C.-P. Stelzer, 2006. A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Marine Biology 149: 763–773.
Stelzer, C. P. & T. W. Snell, 2003. Induction of Sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by a density-dependent chemical cue. Limnology & Oceanography 48: 939–943.
Therneau, T. M., 2014. Package ‘survival’. R package version 2.37-7. http://r-forge.r-project.org/.
Tortajada, A. M., M. J. Carmona & M. Serra, 2009. Does haplodiploidy purge inbreeding depression in rotifer populations? PLoS One 4(12): e8195.
Van Dooren, T. J. M. & L. Brendonck, 1998. The hatching pattern of Branchipodopsis wolfi (Crustacea: Anostraca): phenotypic plasticity, additive genetic and maternal effects. Archiv für Hydrobiologie 52: 219–227. (Special Issues on Advanced Limnology).
Vanoberbeke, J. & L. De Meester, 2009. Within season short-term hatching delays suggest risk-spreading behavior in populations of the freshwater cladoceran Daphnia. Écoscience 16: 441–451.
Acknowledgments
We thank R. Ortells, J. Montero-Pau, M.J. Carmona and M. Serra for helpful comments on the manuscript. Two anonymous reviewers contributed to improve the final version of the manuscript. C. Gabaldón kindly provided the studied rotifer clones from her own collection. This research was supported by funds from the projects UV-INV-PRECOMP12-80525 (University of València) and CGL2012-30779 (Spanish Ministry of Economy and Competitivity, co-financed by FEDER).
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Martínez-Ruiz, C., García-Roger, E.M. Being first increases the probability of long diapause in rotifer resting eggs. Hydrobiologia 745, 111–121 (2015). https://doi.org/10.1007/s10750-014-2098-8
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DOI: https://doi.org/10.1007/s10750-014-2098-8