, Volume 742, Issue 1, pp 267–278 | Cite as

Stress tolerance and population stability of rock pool Daphnia in relation to local conditions and population isolation

  • Yi-Fan Liao
  • Leanne K. Faulks
  • Örjan Östman
Primary Research Paper


Small fragmented populations can lose genetic variability, which reduces population viability through inbreeding and loss of adaptability. Current and previous environmental conditions can also alter the viability of populations, by creating local adaptations that determine responses to stress. Yet, most studies on stress tolerance usually consider either the effect of genetic diversity or the local environment, missing a more holistic perspective of the factors contributing to stress tolerance among natural populations. Here, we studied how salinity stress affects population growth of Daphnia longispina, Daphnia magna, and Daphnia pulex from rock pools with varying degrees of population isolation and salinity conditions. Standing variation of in situ rock pool salinity conditions explained more variation in salt tolerance than the standing variation of population isolation or genetic diversity, in both a pulse and a press disturbance experiment. This indicates that the level of stress, which these natural populations experience, influences their response to that stress, which may have important consequences for the conservation of fragmented populations. However, long-term population stability in the field decreased with population isolation, indicating that natural populations experience a variety of stresses; thus, population isolation and genetic diversity may stabilize population dynamics over larger spatiotemporal scales.


AFLP Biodiversity Population genetics Zooplankton Saline waters 



We are grateful to Jacob Höglund who improved an earlier version of this manuscript. Financial support was given to LKF from the Carl Trygger’s Foundation and to ÖÖ from the Swedish Research Council. The authors declare no interest or relationship, financial, or otherwise, which might be perceived as a potential source of conflict of interest influencing our objectivity.

Supplementary material

10750_2014_1990_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)


  1. Allen, M. R., R. A. Thum & C. E. Cáceres, 2010. Does local adaptation to resources explain genetic differentiation among Daphnia populations? Molecular Ecology 19: 3076–3087.PubMedCrossRefGoogle Scholar
  2. Armbruster, P. & D. H. Reed, 2005. Inbreeding depression in benign and stressful environments. Heredity 95: 235–242.PubMedCrossRefGoogle Scholar
  3. Bengtsson, J., 1986. Life histories and interspecific competition between three Daphnia species in rockpools. Journal of Animal Ecology 55: 641–655.CrossRefGoogle Scholar
  4. Bengtsson, J., 1993. Interspecific competition and determinants of extinction in experimental populations of three rockpool Daphnia species. Oikos 67: 451–464.CrossRefGoogle Scholar
  5. Bijlsma, R. & V. Loeschcke, 2011. Genetic erosion impedes adaptive responses to stressful environments. Evolutionary Applications 5: 117–129.PubMedCentralCrossRefGoogle Scholar
  6. Bijlsma, R., J. Bundgaard & W. F. Van Putten, 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology 12: 1125–1137.CrossRefGoogle Scholar
  7. Bonin, A., D. Ehrich & S. Manel, 2007. Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Molecular Ecology 16: 3737–3758.PubMedCrossRefGoogle Scholar
  8. Coors, A., J. Vanoverbeke, T. De Bie & L. De Meester, 2009. Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquatic Toxicology 95: 71–79.PubMedCrossRefGoogle Scholar
  9. De Meester, L., A. Gomez, B. Okamura & B. Schwenk, 2002. The monopolization hypothesis – gene flow paradox in aquatic organisms. Acta Oecologia 23: 121–135.CrossRefGoogle Scholar
  10. Denver, R. J., 1997. Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Hormones and Behavior 31: 169–179.PubMedCrossRefGoogle Scholar
  11. Ebert, D., 2006. Artificial Daphnia medium: ADaM (Aachener Daphnien Medium). . 23 November 2013.
  12. Ebert, D., C. Haag, M. Kirkpatrick, M. Riek, J. W. Hottinger & V. I. Pajunen, 2002. A selective advatage to immigrant genes in a Daphnia metapopulation. Science 295: 485–488.PubMedCrossRefGoogle Scholar
  13. Ehrich, D., 2006. AFLPdat: a collection of R functions for convenient handling of AFLP data. Molecular Ecology Notes 6: 603–604.CrossRefGoogle Scholar
  14. Fahrig, L., 2003. Effect of habitat fragmentation on biodiversity. Annual Review in Ecology, Evolution and Systematics 34: 487–515.CrossRefGoogle Scholar
  15. Grantham, T. E., A. M. Merenlender & V. H. Resh, 2010. Climatic influences and anthropogenic stressors: an integrated framework for streamflow management in Mediterranean-climate California. USA. Freshwater Biology 55(Suppl. 1): 188–204.CrossRefGoogle Scholar
  16. Haag, C. R., J. W. Hottinger, M. Riek & D. Ebert, 2002. Strong inbreeding depression in a Daphnia metapopulation. Evolution 56: 518–526.PubMedCrossRefGoogle Scholar
  17. Haag, C. R., M. Riek, J. W. Hottinger, V. I. Pajunen & D. Ebert, 2006. Founder events as determinants of within-island and among-island genetic structure of Daphnia metapopulations. Heredity 96: 150–158.PubMedCrossRefGoogle Scholar
  18. Hanski, I., 1994. A practical model of metapopulation dynamics. Journal of Animal Ecology 63: 151–162.CrossRefGoogle Scholar
  19. Keller, L. F. & D. M. Waller, 2002. Inbreeding effects in wild populations. TRENDS in Ecology and Evolution 17: 230–241.CrossRefGoogle Scholar
  20. Kristensen, T. N., M. R. Knudsen & V. Loeschcke, 2011. Slow inbred lines of Drosophila melanogaster express as much inbreeding depression as fast inbred lines under semi-natural conditions. Genetica 139: 441–451.PubMedCrossRefGoogle Scholar
  21. Lande, R., 1988. Genetic and demography in biological conservations. Science 241: 1455–1460.PubMedCrossRefGoogle Scholar
  22. Latta, L. C., L. J. Weider, J. K. Colbourne & M. E. Pfrender, 2012. The evolution of salinity tolerance in Daphnia: a functional genomics approach. Ecology Letters 15: 794–802.PubMedCrossRefGoogle Scholar
  23. Loureiro, C., B. B. Castro, A. P. Cuco, M. A. Pedrosa & F. Gonçalves, 2013. Life-history responses of salinity-tolerant and salinity-sensitive lineages of a stenohaline cladoceran do not confirm clonal differentiation. Hydrobiologia 702: 73–82.CrossRefGoogle Scholar
  24. McLaughlin, O.B., M.C. Emmerson & E.J. O’Gorman, 2013. Habitat isolation reduces the temporal stability of island ecosystems in the face of flood disturbance. In: Woodward, G. & E.J. O’Gorman (eds), Advances in ecological research: Global change in multispecies system. Advances in Ecological Research 48: 225–284.Google Scholar
  25. Nevo, E., 2001. Evolution of genome-phenome diversity under environmental stress. Proceedings of the National Academy of Science USA 98: 6233–6240.CrossRefGoogle Scholar
  26. Nislow, K. H., M. Hudy, B. H. Letcher & E. P. Smith, 2011. Variation in local abundance and species richness of stream fishes in relation to dispersal barriers: implications for management and conservation. Freshwater Biology 56: 2135–2144.CrossRefGoogle Scholar
  27. Nilsson, C., R. Jansson & U. Zinko, 1997. Long-term responses of river-margin vegetation to water-level regulation. Science 276: 798–800.PubMedCrossRefGoogle Scholar
  28. Orsini, L., K. I. Spanier & L. De Meester, 2012. Genomic signature of natural and anthropogenic stress in wild populations of the waterflea Daphnia magna: validation in space, time and experimental evolution. Molecular Ecology 21: 2160–2175.PubMedCrossRefGoogle Scholar
  29. Orsini, L., J. Mergeay, J. Vanoverbeke & L. De Meester, 2013. The role of selection in driving landscape genomic structure of the waterflea Daphnia magna. Molecular Ecology 22: 583–601.PubMedCrossRefGoogle Scholar
  30. Östman, Ö., 2011a. Interspecific competition affects genetic structure but not genetic diversity of Daphnia magna. Ecosphere 2: art34.Google Scholar
  31. Östman, Ö., 2011b. Abundance-occupancy relationships in metapopulations: examples of rock pool Daphnia. Oecologia 165: 687–697.PubMedCrossRefGoogle Scholar
  32. Pfrender, M. E., K. Spitze, J. Hicks, K. Morgan, L. Latta & L. Lynch, 2000. Lack of concordance between genetic diversity estimates at the molecular and quantitative-trait levels. Conservation Genetics 1: 263–269.CrossRefGoogle Scholar
  33. Ranta, E., 1979. Niche of Daphnia species in rockpools. Archive für Hydrobiologia 87: 205–223.Google Scholar
  34. Sandin, L. & A. G. Solimini, 2009. Freshwater ecosystem structure-function relationships: from theory to application. Freshwater Biology 54: 2017–2024.CrossRefGoogle Scholar
  35. Scoville, A. G. & M. E. Pfrender, 2010. Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proceedings of the National Academy of Science 107: 4260–4263.CrossRefGoogle Scholar
  36. Taft, H. R. & D. A. Roff, 2012. Do bottlenecks increase additive genetic variance? Conservation Genetics 13: 333–342.CrossRefGoogle Scholar
  37. Vanoverbeke, J., K. Fe Gelas & L. De Meester, 2007. Habitat size and the genetic structure of a cyclical parthenogen, Daphnia magna. Heredity 98: 419–426.PubMedGoogle Scholar
  38. Vekemans, X., 2002. AFLP-SURV version 1.0. Distributed by the author. Laboratoire de Genetique et Ecologie Vegetale, Universite Libre de Bruxelles, Belgium.Google Scholar
  39. Ventura, M., A. Petrusek, A. Miró, E. Hamrová, D. Bũnay, L. De Meester & J. Mergeay, 2014. Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential. Molcular Ecology 23: 1014–1027.CrossRefGoogle Scholar
  40. Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van de Lee, M. Hornes, A. Frijters, J. Pot, J. Peleman, M. Kulper & M. Zabeau, 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23: 4407–4414.PubMedCentralPubMedCrossRefGoogle Scholar
  41. Walsh, P., D. Metzger & R. Higuchi, 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing of forensic material. BioTechniques 10: 506–513.PubMedGoogle Scholar
  42. Whitlock, R., H. Hipperson, M. Mannarelli, R. Butlin & T. Burke, 2008. An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Molecular Ecology Research 8: 725–735.CrossRefGoogle Scholar
  43. Willi, Y., J. V. Buskirk & A. A. Hoffmann, 2006. Limits to the adaptive potential of small populations. Annual Review in Ecology, Evolution and Systematics 37: 433–458.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Yi-Fan Liao
    • 1
    • 2
  • Leanne K. Faulks
    • 1
  • Örjan Östman
    • 1
  1. 1.Department of Ecology and Genetics/Population Biology and Conservation BiologyUppsala UniversityUppsalaSweden
  2. 2.Taiwan Green Productivity FoundationTaipei CityTaiwan

Personalised recommendations