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Sexual reproduction of Daphnia in a deep temperate reservoir: the phenology and genetics of male formation

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Abstract

Long-term persistence of a Daphnia population is allowed by the production of dormant stages, produced mostly through sexual reproduction. We investigated the spatio-temporal dynamics of male production in a spring population of Daphnia galeata in the reservoir, and compared the genetic structure of three groups within this population: male-, female-producing females, and adult males. With a fine resolution sampling design and the use of highly variable microsatellite markers we revealed that: (1) the spring period of male offspring production was delimited in time with minimum interannual variation to about 3 weeks, and in space to the upper 5-m water layer; (2) there were no remarkable changes in the clonal composition of male-producing females within the period of male production; (3) overall certain clones exhibited a higher tendency to produce male offspring and therefore the clonal structure of male-producing lineages was significantly different from that of female-producing lineages; and (4) the clonal structure of male-producing females was not significantly different from that of adult males occurring later in the reservoir. This suggests that males were not subjected to any significant selective forces till maturity and the male-producing females confer a long-term fitness advantage over female-producing females.

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References

  • Alekseev, V. R. & W. Lampert, 2001. Maternal control of resting-egg production in Daphnia. Nature 414: 899–901.

    Article  CAS  PubMed  Google Scholar 

  • Banta, A. M., 1939. Studies on the physiology, genetics, and evolution of some Cladocera. Carnegie Institution of Washington, Washington, DC.

    Google Scholar 

  • Banta, A. M. & L. A. Brown, 1929. Control of sex in Cladocera. I. Crowding the mothers as a means of controlling male production. Physiological Zoology 2: 80–92.

    CAS  Google Scholar 

  • Berg, L. M., S. Palsson & M. Lascoux, 2001. Fitness and sexual response to population density in Daphnia pulex. Freshwater Biology 46: 667–677.

    Article  Google Scholar 

  • Brede, N., A. Thielsch, C. Sandrock, P. Spaak, B. Keller, B. Streit & K. Schwenk, 2006. Microsatellite markers for European Daphnia. Molecular Ecology Notes 6: 536–539.

    Article  CAS  Google Scholar 

  • Brewer, M. C., 1998. Mating behaviours of Daphnia pulicaria, a cyclic parthenogen: comparisons with copepods. Philosophical Transactions of the Royal Society of London B 353: 805–815.

    Article  Google Scholar 

  • Cáceres, C. E., 1998. Interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology 79: 1699–1710.

    Google Scholar 

  • Carvalho, G. R. & R. N. Hughes, 1983. The effect of food availability, female culture density and photoperiod on ephippia production in Daphnia magna Straus (Crustacea, Cladocera). Freshwater Biology 13: 37–46.

    Article  Google Scholar 

  • De Meester, L. & J. Vanoverbeke, 1999. An uncoupling of male and sexual egg production leads to reduced inbreeding in the cyclic parthenogen Daphnia. Proceedings of the Royal Society of London B 266: 2471–2477.

    Article  Google Scholar 

  • De Meester, L., A. Gomez, B. Okamura & K. Schwenk, 2002. The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologica: International Journal of Ecology 23: 121–135.

    Article  Google Scholar 

  • Ferrari, D. C. & P. D. N. Hebert, 1982. The induction of sexual reproduction in Daphnia magna: genetic differences between arctic and temperate populations. Canadian Journal of Zoology 60: 2143–2148.

    Article  Google Scholar 

  • Fitzsimmons, J. M. & D. J. Innes, 2006. Inter-genotype variation in reproductive response to crowding among Daphnia pulex. Hydrobiologia 568: 187–205.

    Article  CAS  Google Scholar 

  • Hamrová, E., J. Mergeay & A. Petrusek, 2011. Strong differences in the clonal variation of two Daphnia species from mountain lakes affected by overwintering strategy. BMC Evolutionary Biology 11: 231–240.

    Article  PubMed  Google Scholar 

  • Hobæk, A. & P. Larsson, 1990. Sex determination in Daphnia magna. Ecology 71: 2255–2268.

    Article  Google Scholar 

  • Innes, D. J., 1997. Sexual reproduction of Daphnia pulex in a temporary habitat. Oecologia 111: 53–60.

    Article  Google Scholar 

  • Innes, D. J. & R. L. Dunbrack, 1993. Sex allocation variation in Daphnia pulex. Journal of Evolutionary Biology 6: 559–575.

    Article  Google Scholar 

  • Innes, D. J. & D. R. Singleton, 2000. Variation in allocation to sexual and asexual reproduction among clones of cyclically parthenogenetic Daphnia pulex (Crustacea: Cladocera). Biological Journal of the Linnean Society 71: 771–787.

    Google Scholar 

  • Jankowski, T. & D. Straile, 2004. Allochronic differentiation among Daphnia species, hybrids and backcrosses: the importance of sexual reproduction for population dynamics and genetic architecture. Journal of Evolutionary Biology 17: 312–321.

    CAS  PubMed  Google Scholar 

  • Keller, B. & P. Spaak, 2004. Nonrandom sexual reproduction and diapausing egg production in a Daphnia hybrid species complex. Limnology and Oceanography 49: 1393–1400.

    Article  Google Scholar 

  • Kleiven, O. T., P. Larsson & A. Hobæk, 1992. Sexual reproduction in Daphnia magna requires three stimuli. Oikos 65: 197–206.

    Article  Google Scholar 

  • Korpelainen, H., 1986. The effects of temperature and photoperiod on life history parameters of Daphnia magna (Crustacea: Cladocera). Freshwater Biology 16: 615–620.

    Article  Google Scholar 

  • Montero-Pau, J., A. Gomez & J. Munoz, 2008. Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography: Methods 6: 218–222.

    Article  CAS  Google Scholar 

  • Olmstead, A. W. & G. A. LeBlanc, 2002. Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. Journal of Experimental Zoology 293: 736–739.

    Article  CAS  PubMed  Google Scholar 

  • Peakall, R. & P. E. Smouse, 2006. GENALEX 6: genetic analysis in excel population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.

    Article  Google Scholar 

  • Peakall, R., P. E. Smouse & D. R. Huff, 1995. Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss Buchloe dactyloides. Molecular Ecology 4: 135–147.

    Article  CAS  Google Scholar 

  • Pietrzak, B., A. Bednarska & M. Grzesiuk, 2010. Longevity of Daphnia magna males and females. Hydrobiologia 643: 71–75.

    Article  Google Scholar 

  • Ruthová, Š., 2008. Daphnia hybridization in canyon-shaped reservoirs. M.Sc. thesis. Charles University in Prague, Viničná: 60 p.

  • Seda, J., 1989. Main factors affecting spring development of herbivorous Cladocera in the Římov reservoir (Czechoslovakia). Archiv für Hydrobiologie Beihefte Ergebnisse der Limnologie 33: 619–630.

    Google Scholar 

  • Seda, J. & J. Macháček, 1998. The effect of flow-through regimes on zooplankton densities in a canyon-shaped dam reservoir. In Straškrabová, V. & J. Vrba (eds), Proceedings of the 3rd International Conference on Reservoir Limnology and Water Quality, České Budějovice, Czech Republic, August 11–15, 1997. International Review of Hydrobiology 83: 477–484.

  • Sommer, U., Z. M. Gliwicz, W. Lampert & A. Duncan, 1986. The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv für Hydrobiologie 106: 433–471.

    Google Scholar 

  • Spaak, P., 1995. Sexual reproduction in Daphnia: interspecific differences in a hybrid species complex. Oecologia 104: 501–507.

    Article  Google Scholar 

  • Spaak, P. & M. Boersma, 2001. The influence of fish kairomones on the induction and vertical distribution of sexual individuals of the Daphnia galeata species complex. Hydrobiologia 442: 185–193.

    Article  Google Scholar 

  • Spaak, P., A. Denk, M. Boersma & L. J. Weider, 2004. Spatial and temporal patterns of sexual reproduction in a hybrid Daphnia species complex. Journal of Plankton Research 26: 625–635.

    Article  Google Scholar 

  • Straškraba, M., 1998. Limnological differences between deep valley reservoirs and deep lakes. International Review of Hydrobiology 83: 1–12.

    Article  Google Scholar 

  • Stross, R. G., 1987. Photoperiodism and phased growth in Daphnia populations: coactions in perspective. In Peters, R. H. & R. de Bernardi (eds), Daphnia. Memorie dell’Istituto Italiano di Idrobiologia 45: 413–437.

  • Tessier, A. J. & C. E. Cáceres, 2004. Differentiation in sex investment by clones and populations of Daphnia. Ecology Letters 7: 695–703.

    Article  Google Scholar 

  • Thielsch, A., N. Brede, A. Petrusek, L. De Meester & K. Schwenk, 2009. Contribution of cyclic parthenogenesis and colonization history to population structure in Daphnia. Molecular Ecology 18: 1616–1628.

    Article  PubMed  Google Scholar 

  • Vanoverbeke, J. & L. De Meester, 2010. Clonal erosion and genetic drift in cyclical parthenogens—the interplay between neutral and selective processes. Journal of Evolutionary Biology 23: 997–1012.

    Article  CAS  PubMed  Google Scholar 

  • Winsor, G. L. & D. J. Innes, 2002. Sexual reproduction in Daphnia pulex (Crustacea: Cladocera): observations on male mating behaviour and avoidance of inbreeding. Freshwater Biology 47: 441–450.

    Google Scholar 

  • Yampolsky, L. Y., 1992. Genetic variation in the sexual reproduction rate within a population of a cyclic parthenogen, Daphnia magna. Evolution 46: 833–837.

    Article  Google Scholar 

  • Yin, M., A. Petrusek, J. Seda & J. Wolinska, 2012. Fine-scale genetic analysis of Daphnia host populations infected by two virulent parasites—strong fluctuations in clonal structure at small temporal and spatial scales. International Journal for Parasitology 42: 115–121.

    Article  PubMed  Google Scholar 

  • Zaffagnini, F., 1987. Reproduction in Daphnia. In Peters, R.H. & R. de Bernardi (eds), Daphnia. Memorie dell’Istituto Italiano di Idrobiologia 45: 245–284.

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Acknowledgments

The authors thank to two anonymous reviewers for helpful comments on an earlier versions of the manuscript and D. W. Hardekopf for the linguistic revision of the text. The study was supported by Czech Science Foundation grant 206/09/1325. I. Vaníčková was also supported by the Grant Agency of the University of South Bohemia (project no. 142/2010/P) and Erasmus Programme (EU).

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Authors and Affiliations

  1. Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Hydrobiology, Na Sadkach 7, Ceske Budejovice, 37005, Czech Republic

    Jiří Macháček, Ivana Vaníčková & Jaromir Seda

  2. Faculty of Science, University of South Bohemia, Branisovska 31, Ceske Budejovice, 37005, Czech Republic

    Ivana Vaníčková

  3. Department of Biology II, University of Munich (LMU), Grosshaderner Str. 2, 82152, Planegg-Martinsried, Germany

    Mathilde Cordellier

  4. Molecular Ecology, Institute of Environmental Sciences, University of Koblenz-Landau, 76829, Landau/Pfalz, Germany

    Klaus Schwenk

  5. Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325, Frankfurt am Main, Germany

    Mathilde Cordellier

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  1. Jiří Macháček
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  2. Ivana Vaníčková
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  3. Jaromir Seda
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  4. Mathilde Cordellier
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  5. Klaus Schwenk
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Correspondence to Jiří Macháček.

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Guest editors: Marina Manca & Piet Spaak / Cladocera: Proceedings of the 9th International Symposium on Cladocera

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Macháček, J., Vaníčková, I., Seda, J. et al. Sexual reproduction of Daphnia in a deep temperate reservoir: the phenology and genetics of male formation. Hydrobiologia 715, 113–123 (2013). https://doi.org/10.1007/s10750-012-1419-z

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  • DOI: https://doi.org/10.1007/s10750-012-1419-z

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