Skip to main content
Log in

Modes, mechanisms and evidence of bet hedging in rotifer diapause traits

  • ROTIFERA XIV
  • Review Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

In this contribution, we review our knowledge on bet-hedging strategies associated with rotifer diapause. First, we describe the ecological scenario under which bet hedging is likely to have evolved in three diapause-related traits in monogonont rotifer populations: (1) the timing of sex (because diapausing eggs are produced via sexual reproduction), (2) the sexual reproduction ratio (i.e. the fraction of sexually reproducing females) and (3) the timing of diapausing egg hatching. Then, we describe how to discriminate among bet-hedging modes and discuss which modes and mechanisms better fit the variability observed in these traits in rotifers. Finally, we evaluate the strength of the empirical evidence for bet hedging in the scarce studies available, and we call for the need of research at different levels of biological complexity to fully understand bet hedging in rotifer diapause.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Aparici, E., M. J. Carmona & M. Serra, 2001. Intrapopulation variability for mixis initiation in Brachionus plicatilis. Hydrobiologia 446/447: 45–50.

    Article  Google Scholar 

  • Cáceres, C. E. & A. J. Tessier, 2003. How long to rest: the ecology of optimal dormancy and environmental constraint. Ecology 84: 1189–1198.

    Article  Google Scholar 

  • Campillo, S., E. M. García-Roger, M. J. Carmona & M. Serra, 2011. Local adaptation in rotifer populations. Evolutionary Ecology 25: 933–947.

    Article  Google Scholar 

  • Carmona, M. J., A. Gómez & M. Serra, 1995. Mictic patterns of the rotifer Brachionus plicatilis Müller in small ponds. Hydrobiologia 313(314): 365–371.

    Article  Google Scholar 

  • Carmona, M. J., M. Serra & M. R. Miracle, 1994. Effect of population density and genotype on life-history traits in the rotifer Brachionus plicatilis O.F. Müller. Journal of Experimental Marine Biology and Ecology 182: 223–235.

    Article  Google Scholar 

  • Carmona, M. J., N. Dimas-Flores, E. M. García-Roger & M. Serra, 2009. Selection of low investment in sex in a cyclically parthenogenetic rotifer. Journal of Evolutionary Biology 22: 1975–1983.

    Article  CAS  PubMed  Google Scholar 

  • Carmona, M. J., N. Dimas-Flores, J. Montero-Pau & M. Serra, 2011. Effect of experimental methodology on estimation of density at sex initiation in cyclically parthenogenetic rotifers. Hydrobiologia 662: 131–139.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cohen, D., 1966. Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology 12: 119–129.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • De Meester, L. & H. De Jager, 1993. Hatching of Daphnia sexual eggs.1. Intraspecific differences in the hatching responses of Daphnia magna eggs. Freshwater Biology 30: 219–226.

    Article  Google Scholar 

  • Dumont, H. J. & A. J. Ali, 2004. Stage-specific cannibalism and spontaneous cyst hatching in the freshwater fairy shrimp Streptocephalus proboscideus Frauenfeld. Hydrobiologia 524: 103–113.

    Article  Google Scholar 

  • Einum, S. & I. A. Fleming, 2004. Environmental unpredictability and offspring size: conservative versus diversified bet-hedging. Evolutionary Ecology Research 6: 443–455.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gabaldón, C. & M. J. Carmona, 2015. Allocation patterns in modes of reproduction in two facultatively sexual cryptic rotifer species. Journal of Plankton Research 37: 429–440.

    Article  Google Scholar 

  • García-Roger, E. M., M. J. Carmona & M. Serra, 2006a. A simple model relating habitat features to a diapausing egg bank. Limnology and Oceanography 51: 1542–1547.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • García-Roger, E. M., M. J. Carmona & M. Serra, 2006c. Patterns in rotifer diapausing egg bank: density and viability. Journal of Experimental Marine Biology and Ecology 336: 198–210.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Gilbert, J. J., 1963. Contact chemoreception, mating behaviour, and sexual isolation in the rotifer genus Brachionus. Journal of Experimental Biology 40: 625–641.

    CAS  Google Scholar 

  • Gilbert, J. J., 1974. Dormancy in rotifers. Transcations of the American Microscopical Society 93: 490–513.

    Article  Google Scholar 

  • Gilbert, J. J., 2002. Endogenous regulation of environmentally induced sexuality in a rotifer: a multigenerational parental effect induced by fertilisation. Freshwater Biology 47: 1633–1641.

    Article  Google Scholar 

  • Gilbert, J. J., 2003. Environmental and endogenous control of sexuality in a rotifer life cycle: developmental and population biology. Evolution and Development 5: 19–24.

    Article  PubMed  Google Scholar 

  • Gilbert, J. J., 2007a. Timing of diapause in monogonont rotifers. In Alekseev, V., J. J. Gilbert & B. De Stasio (eds), Diapause in Aquatic Invertebrates: Theory and Human Use. Springer, Dordrecht: 11–27.

    Chapter  Google Scholar 

  • Gilbert, J. J., 2007b. 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.

    Article  Google Scholar 

  • Gilbert, J. J., 2010. Effect of food concentration on the production and viability of resting eggs of the rotifer Brachionus: implications for the timing of sexual reproduction. Freshwater Biology 54: 2437–2446.

    Article  Google Scholar 

  • Gilbert, J. J. & D. K. Schreiber, 1998. Asexual diapause induced by food limitation in the rotifer Synchaeta pectinata. Ecology 79: 1371–1381.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gilbert, J. J. & M. C. Dieguez, 2010. Low crowding threshold for induction of sexual reproduction and diapause in a patagonian rotifer. Freshwater Biology 55: 1705–1718.

    Article  Google Scholar 

  • Gillespie, J. H., 1974. Natural selection for within-generation variance in offspring number. Genetics 76: 601–606.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hairston, N. G. & W. R. Munns, 1984. The timing of copepod diapause as an evolutionary stable strategy. American Naturalist 123: 733–751.

    Article  Google Scholar 

  • Hairston, N. G. & E. J. Olds, 1984. Population differences in the timing of diapause in a spatially heterogeneous environment. Oecologia 61: 42–48.

    Article  PubMed  Google Scholar 

  • Hildrew, A. G., 1985. A quantitative study of the life-history of a fairy shrimp (Branchiopoda, Anostraca) in relation to the temporary nature of its habitat, a Kenyan rainpool. Journal of Animal Ecology 54: 99–110.

    Article  Google Scholar 

  • Hino A. & R. Hirano, 1977. Ecological studies on the mechanism of bisexual reproduction in the rotifer Brachionus plicatilis—II. Effects of cumulative parthenogenetic generation on the frequency of bisexual reproduction. Bull. Jpn. Soc. Sci. Fish. 43: 1147–1155.

    Article  Google Scholar 

  • Kabay, M. E. & J. J. Gilbert, 1977. Polymorphism and reproductive mode in the rotifer, Asplanchna sieboldi: relationship between meiotic oogenesis and shape of body-wall outgrowths. Journal of Experimental Zoology 201: 21–28.

    Article  CAS  PubMed  Google Scholar 

  • Marshall, D. J. & T. Uller, 2007. When is a maternal effect adaptive? Oikos 116: 1957–1963.

    Article  Google Scholar 

  • Martínez-Ruiz, C. & E. M. García-Roger, 2015. Being first increases the probability of long diapause in rotifer resting eggs. Hydrobiologia 745: 111–121.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Philippi, T. & J. Seger, 1989. Hedging one’s evolutionary bets, revisited. Trends in Ecology and Evolution 4: 41–44.

    Article  CAS  PubMed  Google Scholar 

  • Philipi, T., M. A. Simovich, E. T. Bauder & J. A. Moorad, 2001. Habitat ephemerality and hatching fractions of a diapausing anostracan (Crustacea: Branchiopoda). Israel Journal of Zoology 47: 387–395.

    Article  Google Scholar 

  • Pourriot, R. & P. Clément, 1975. Influence de la durée de l’éclairement quotidien sur le taux de femelles mictiques chez Notommata copeus Ehr. (rotifère). Oecologia 22: 67–77.

    Article  PubMed  Google Scholar 

  • Pourriot, R. & C. Rougier, 1976. Influence de l’âge des parents sur la production de femelles mictiques chez Brachionus calyciflorus (Pallas) et B. rubens Ehr. (Rotifères). Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences Série D 283: 1497–1500.

    Google Scholar 

  • Pourriot, R. & C. Rougier, 1986. Rhythmes de production de femelles sexuées chez le rotifère Brachionus calyciflorus, en élevage à température constante. Bulletin de la Societé Zoologique de France 111: 203–209.

    Google Scholar 

  • Rees, M., D. Z. Childs, K. E. Rose & P. J. Grubb, 2004. Evolution of size dependent flowering in a variable environment: partitioning the effects of fluctuating selection. Proceedings of the Royal Society B: Biological Sciences 271: 471–475.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rees, M., C. Jessica, E. Metcalf & D. Z. Childs, 2010. Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proceedings of the Royal Society B: Biological Sciences 277: 1149–1151.

    Article  PubMed  Google Scholar 

  • Ricci, C., 2001. Dormancy patterns in rotifers. Hydrobiologia 446(447): 1–11.

    Article  Google Scholar 

  • Rougier, C. & R. Pourriot, 1977. Aging and control of the reproduction in Brachionus calyciflorus (Pallas) (Rotatoria). Experimental Gerontology 12: 137–151.

    Article  CAS  PubMed  Google Scholar 

  • Saiah, H. & N. Perrin, 1990. Autumnal vs spring hatching in the fairy shrimp Siphonophanes grubii (Dybowski) (Crustacea, Anostraca) – diversified-bet hedging strategy. Functional Ecology 4: 769–775.

    Article  Google Scholar 

  • Schröder, T., 1999. Lebenszyklusstrategien planktischer Rotatorien (Monogononta, Rotifera) im Zusammenhang mit den saisonalen Überflutungen in der Flussaue des Unteren Odertals. Ph.D. Dissertation. Freie Universität Berlin, 183 pp.

  • Schröder, T., 2001. Colonizing strategies and diapause of planktonic rotifers (monogononta, rotifera) during aquatic and terrestrial phases in a floodplain (Lower Oder valley, Germany). International Review of Hydrobiology 86: 635–660.

    Article  Google Scholar 

  • Schröder, T., 2005. Diapause in monogonont rotifers. Hydrobiologia 181: 291–306.

    Article  Google Scholar 

  • Schröder, T., S. Howard, M. L. Arroyo & E. J. Walsh, 2007. Sexual reproduction and diapause of Hexarthra sp. (Rotifera) in short-lived ponds in the Chihuahuan Desert. Freshwater Biology 52: 1033–1042.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Schröder, T. & E. J. Walsh, 2007. Cryptic speciation in the cosmopolitan Epiphanes senta complex (Monogononta, Rotifera) with the description of new species. Hydrobiologia 593: 129–140.

    Article  Google Scholar 

  • Seger, J. & H. J. Brockmann, 1987. What is bet hedging? In Harvey, P. H. & L. Partridge (eds), Oxford Surveys in Evolutionary Biology. Oxford University Press, Oxford: 182–211.

    Google Scholar 

  • Serra, M. & C. E. King, 1999. Optimal rates of bisexual reproduction in cyclical parthenogens with density-dependent growth. Journal of Evolutionary Biology 12: 263–271.

    Article  Google Scholar 

  • Serra, M. & T. W. Snell, 2009. Sex loss in monogonont rotifers. In Schön, Isa, Koen Martens & Peter Van Dijk (eds), Lost Sex. Springer, Berlin.

    Google Scholar 

  • Serra, M., T. W. Snell & C. E. King, 2004. The timing of sex in rotifers. In Moya, A. & E. Font (eds), Evolution from Molecules to Ecosystems. Oxford University Press, New York: 135–146.

    Google Scholar 

  • Serra, M., T. W. Snell & J. J. Gilbert, 2005. Delayed mixis in rotifers: an adaptive response to the effects of density-dependent sex on population growth. Journal of Plankton Research 27: 37–45.

    Article  Google Scholar 

  • Simons, A. M., 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Simons, A. M. & M. O. Johnston, 2003. Suboptimal timing of reproduction in Lobelia inflata may be a conservative bet-hedging strategy. Journal of Evolutionary Biology 16: 233–243.

    Article  CAS  PubMed  Google Scholar 

  • Simovich, M. A. & S. A. Hathaway, 1997. Diversified bet-hedging as a reproductive strategy of some ephemeral pool anostracans (Branchiopoda). Journal of Crustacean Biology 17: 38–44.

    Article  Google Scholar 

  • Slobodkin, L. B. & H. L. Sanders, 1969. On the contribution of environmental predictability to species diversity. Brookhaven Symposium of Biology 22: 82–95.

    CAS  Google Scholar 

  • Snell, T. W. & E. M. Boyer, 1988. Thresholds for mictic female production in the rotifer Brachionus plicatilis (Müller). Journal of Experimental Marine Biology and Ecology 124: 73–85.

    Article  Google Scholar 

  • Starrfelt, J. & H. Kokko, 2012. Bet-hedging – a triple trade-off between means, variances and correlations. Biological Reviewvs 87: 742–755.

    Article  Google Scholar 

  • Vanoverbeke, J. & L. De Meester, 2009. Within season short-term hatching delays suggest risk-spreading behaviour in populations of the freshwater cladoceran Daphnia. Ecoscience 16: 441–451.

    Article  Google Scholar 

  • Vanschoenwinkel, B., M. Seaman & L. Brendonck, 2010. Hatching phenology, life history and egg bank size of fairy shrimp Branchiodopsis spp. (Branchiopoda, Crustacea) in relation to the ephemerality of their rock pool habitat. Aquatic Ecology 44: 771–780.

    Article  Google Scholar 

  • Walsh, E. J., H. A. Smith & R. L. Wallace, 2014. Rotifers of temporary waters. International Review of Hydrobiology 99: 3–19.

    Article  Google Scholar 

  • Wilbur, H. M. & V. H. W. Rudolf, 2006. Life-history evolution in uncertain environments: bet hedging in time. American Naturalist 168: 398–411.

    PubMed  Google Scholar 

Download references

Acknowledgments

The research presented in this study was supported by funds from the projects UV-INV-PRECOMP12-80525 (University of València, Spain) and CGL2012-30779 (Spanish Ministry of Economy and Competitiveness, co-financed by UE-FEDER).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eduardo M. García-Roger.

Additional information

Guest editors: M. Devetter, D. Fontaneto, C. D. Jersabek, D. B. Mark Welch, L. May & E. J. Walsh / Evolving rotifers, evolving science

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Roger, E.M., Carmona, M.J. & Serra, M. Modes, mechanisms and evidence of bet hedging in rotifer diapause traits. Hydrobiologia 796, 223–233 (2017). https://doi.org/10.1007/s10750-016-2869-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2869-5

Keywords

Navigation