Advertisement

Hydrobiologia

, Volume 715, Issue 1, pp 113–123 | Cite as

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

  • Jiří Macháček
  • Ivana Vaníčková
  • Jaromir Seda
  • Mathilde Cordellier
  • Klaus Schwenk
CLADOCERA

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.

Keywords

Daphnia Reservoir population Male induction Clonal structure Microsatellite 

Notes

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).

References

  1. Alekseev, V. R. & W. Lampert, 2001. Maternal control of resting-egg production in Daphnia. Nature 414: 899–901.CrossRefPubMedGoogle Scholar
  2. Banta, A. M., 1939. Studies on the physiology, genetics, and evolution of some Cladocera. Carnegie Institution of Washington, Washington, DC.Google Scholar
  3. 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.Google Scholar
  4. Berg, L. M., S. Palsson & M. Lascoux, 2001. Fitness and sexual response to population density in Daphnia pulex. Freshwater Biology 46: 667–677.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. Cáceres, C. E., 1998. Interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology 79: 1699–1710.Google Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Fitzsimmons, J. M. & D. J. Innes, 2006. Inter-genotype variation in reproductive response to crowding among Daphnia pulex. Hydrobiologia 568: 187–205.CrossRefGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. Hobæk, A. & P. Larsson, 1990. Sex determination in Daphnia magna. Ecology 71: 2255–2268.CrossRefGoogle Scholar
  15. Innes, D. J., 1997. Sexual reproduction of Daphnia pulex in a temporary habitat. Oecologia 111: 53–60.CrossRefGoogle Scholar
  16. Innes, D. J. & R. L. Dunbrack, 1993. Sex allocation variation in Daphnia pulex. Journal of Evolutionary Biology 6: 559–575.CrossRefGoogle Scholar
  17. 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
  18. 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.PubMedGoogle Scholar
  19. Keller, B. & P. Spaak, 2004. Nonrandom sexual reproduction and diapausing egg production in a Daphnia hybrid species complex. Limnology and Oceanography 49: 1393–1400.CrossRefGoogle Scholar
  20. Kleiven, O. T., P. Larsson & A. Hobæk, 1992. Sexual reproduction in Daphnia magna requires three stimuli. Oikos 65: 197–206.CrossRefGoogle Scholar
  21. Korpelainen, H., 1986. The effects of temperature and photoperiod on life history parameters of Daphnia magna (Crustacea: Cladocera). Freshwater Biology 16: 615–620.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. Pietrzak, B., A. Bednarska & M. Grzesiuk, 2010. Longevity of Daphnia magna males and females. Hydrobiologia 643: 71–75.CrossRefGoogle Scholar
  27. Ruthová, Š., 2008. Daphnia hybridization in canyon-shaped reservoirs. M.Sc. thesis. Charles University in Prague, Viničná: 60 p.Google Scholar
  28. 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
  29. 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.Google Scholar
  30. 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
  31. Spaak, P., 1995. Sexual reproduction in Daphnia: interspecific differences in a hybrid species complex. Oecologia 104: 501–507.CrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. Straškraba, M., 1998. Limnological differences between deep valley reservoirs and deep lakes. International Review of Hydrobiology 83: 1–12.CrossRefGoogle Scholar
  35. 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.Google Scholar
  36. Tessier, A. J. & C. E. Cáceres, 2004. Differentiation in sex investment by clones and populations of Daphnia. Ecology Letters 7: 695–703.CrossRefGoogle Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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
  40. Yampolsky, L. Y., 1992. Genetic variation in the sexual reproduction rate within a population of a cyclic parthenogen, Daphnia magna. Evolution 46: 833–837.CrossRefGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. Zaffagnini, F., 1987. Reproduction in Daphnia. In Peters, R.H. & R. de Bernardi (eds), Daphnia. Memorie dell’Istituto Italiano di Idrobiologia 45: 245–284.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Jiří Macháček
    • 1
  • Ivana Vaníčková
    • 1
    • 2
  • Jaromir Seda
    • 1
  • Mathilde Cordellier
    • 3
    • 5
  • Klaus Schwenk
    • 4
  1. 1.Biology Centre of the Academy of Sciences of the Czech RepublicInstitute of HydrobiologyCeske BudejoviceCzech Republic
  2. 2.Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  3. 3.Department of Biology IIUniversity of Munich (LMU)Planegg-MartinsriedGermany
  4. 4.Molecular Ecology, Institute of Environmental SciencesUniversity of Koblenz-LandauLandau/PfalzGermany
  5. 5.Biodiversity and Climate Research CentreFrankfurt am MainGermany

Personalised recommendations