Genotype × environment interactions, stoichiometric food quality effects, and clonal coexistence in Daphnia pulex

Abstract

The role of stoichiometric food quality in influencing genotype coexistence and competitive interactions between clones of the freshwater microcrustacean, Daphnia pulex, was examined in controlled laboratory microcosm experiments. Two genetically distinct clones of D. pulex, which show variation in their ribosomal (r)DNA structure, as well as differences in a number of previously characterized growth-rate-related features (i.e., life-history features), were allowed to compete in two different arenas: (1) batch cultures differing in algal food quality (i.e., high vs. low carbon:phosphorus (C:P ratio) in the green alga, Scenedesmus acutus); (2) continuous flow microcosms receiving different light levels (i.e., photosynthetically active radiation) that affected algal C:P ratios. In experiment 1, a clear genotype × environment interaction was determined with clone 1 out-competing clone 2 under high nutrient (i.e., low food C:P) conditions, while the exact opposite pattern was observed under low nutrient (i.e., high C:P) conditions. In experiment 2, clone 1 dominated over clone 2 under high light (higher C:P) conditions, but clonal coexistence was observed under low light (low C:P) conditions. These results indicate that food (nutrient) quality effects (hitherto an often overlooked factor) may play a role in microevolutionary (genotypic) responses to changing stoichiometric conditions in natural populations.

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Notes

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    we report here only the carbon and phosphorus data given that the N:P ratio ensured P-limitation—as explained in the above text.

References

  1. Akimoto S (1990) Local adaptation and host race formation of a gall-forming aphid in relation to environmental heterogeneity. Oecologia 83:162–170

    Article  Google Scholar 

  2. Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, Berkeley

  3. Bell G (1991) The ecology and genetics of fitness in Chlamydomonas. III. Genotype-by-environment interactions within strains. Evolution 45:668–679

    Article  Google Scholar 

  4. Berenbaum M (1983) Coumarins and caterpillars: a case for coevolution. Evolution 37:163–179

    Article  CAS  Google Scholar 

  5. De Barro PJ, Sherratt TN, David O, Maclean N (1995) An investigation of the differential performance of clones of the aphid Sitobion avenae on two host species. Oecologia 104:379–385

    Article  Google Scholar 

  6. Diehl S, Berger S, Ptacnik R, Wild A (2002) Phytoplankton, light, and nutrients in a gradient of mixing depths: field experiments. Ecology 83:399–411

    Google Scholar 

  7. Elser JJ, Dobberfuhl D, MacKay NA, Schampel JH (1996) Organism size, life-history, and N:P stoichiometry: towards a unified view of cellular and ecosystem processes. BioScience 46:674–684

    Article  Google Scholar 

  8. Elser JJ, Dowling T, Dobberfuhl DA, O’Brien J (2000a) The evolution of ecosystem processes: ecological stoichiometry of a key herbivore in temperate and arctic habitats. J Evol Biol 13:845–853

    Article  Google Scholar 

  9. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000b) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Article  Google Scholar 

  10. Elser JJ, Hayakawa K, Urabe J (2001) Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82:898–903

    Google Scholar 

  11. Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  12. Epp GT (1996) Clonal variation in the survival and reproduction of Daphnia pulicaria under low-food stress. Freshwat Biol 35:1–10

    Article  Google Scholar 

  13. Futuyma DJ, Leipertz SL, Mitter C (1981) Selective factors affecting clonal variation in the fall cankerworm, Alsophila pometaria (Lepidoptera: Geometridae). Heredity 47:161–172

    Google Scholar 

  14. Geedey CK, Tessier AJ, Machledt K (1996) Habitat heterogeneity, environmental change and the clonal structure of Daphnia populations. Funct Ecol 10:613–621

    Article  Google Scholar 

  15. Glazier DS (1992) Effects of food, genotype, and maternal size and age on offspring investment in Daphnia magna. Ecology 73:910–926

    Article  Google Scholar 

  16. Gorokhova E, Dowling TE, Weider LJ, Crease TJ, Elser JJ (2002) Functional and ecological significance of rDNA IGS variation in a clonal organism under divergent selection for production rate. P R Soc Lond B 269:2373–2379

    Article  CAS  Google Scholar 

  17. Goulden CE, Henry LL, Tessier AJ (1982) Body size, energy reserves and competitive ability in three species of Cladocera. Ecology 63:1780–1789

    Article  Google Scholar 

  18. Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis: a practical handbook. Helena Laboratories, Beaumont

    Google Scholar 

  19. Hietala J, Laurén-Määttä C, Walls M (1997) Sensitivity of Daphnia to toxic cyanobacteria: effects of genotype and temperature. Freshwat Biol 37:299–306

    Article  Google Scholar 

  20. Hill J (1975) Genotype-environment interactions—a challenge for plant breeding. J Agric Sci 85:477–493

    Article  Google Scholar 

  21. Hochstädter S (2000) Seasonal changes of C:P ratios of seston, bacteria, phytoplankton and zooplankton in a deep, mesotrophic lake. Freshwat Biol 44:453–463

    Article  Google Scholar 

  22. Jokela J, Lively CM, Fox JA, Dybdahl MF (1997) Flat reaction norms and “frozen” phenotypic variation in clonal snails (Potamopyrgus antipodarum). Evolution 51:1120–1129

    Article  Google Scholar 

  23. Kause A, Saloniemi I, Morin J-P, Haukioja E, Hanhimäki S, Ruohomäki K (2001) Seasonally varying diet quality and the quantitative genetics of development time and body size in birch feeding insects. Evolution 55:1992–2001

    PubMed  CAS  Google Scholar 

  24. Kilham SS, Kreger DA, Lynn SG, Goulden CE, Herrara L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159

    Article  CAS  Google Scholar 

  25. Laurén-Määttä C, Hietala J, Walls M (1997) Responses of Daphnia pulex populations to toxic cyanobacteria. Freshwat Biol 37:635–647

    Article  Google Scholar 

  26. Loaring JM, Hebert PDN (1981) Ecological differences among clones of Daphnia pulex (Leydig). Oecologia 51:162–168

    Article  Google Scholar 

  27. Mitter L, Futuyma DJ, Schneider JC, Hare DJ (1979) Genetic variation and host plant relations in a parthenogenetic moth. Evolution 33:777–790

    Article  Google Scholar 

  28. Pani SN, Lasley JF (1972) Genotype × environment interactions in animals. Res. Bull. Agri. Exp. Sta., Univ. Missouri No. 992

  29. Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221

    CAS  Google Scholar 

  30. Repka S (1997) Effects of food type on the life history of Daphnia clones from lakes differing in trophic state. I. Daphnia galeata feeding on Scenedesmus and Oscillatoria. Freshwat Biol 37:675–683

    Article  Google Scholar 

  31. Repka S (1998) Effects of food type on the life history of Daphnia clones from lakes differing in trophic state. II. Daphnia cucullata feeding on mixed diets. Freshwat Biol 38:685–692

    Article  Google Scholar 

  32. Rhomberg LR, Joseph S, Singh RS (1985) Seasonal variation and clonal selection in cyclically parthenogenetic rose aphids (Macrosiphum rosae). Can J Genet Cytol 27:224–232

    Google Scholar 

  33. Service PM, Lenski RE (1982) Aphid genotypes, plant phenotypes and genetic diversity: a demographic analysis of experimental data. Evolution 36: 1276–1282

    Article  Google Scholar 

  34. Snell TW (1980) Blue-green algae and selection in rotifer populations. Oecologia 46:343–346

    Google Scholar 

  35. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  36. Sterner RW, Hessen DO (1994) Algal nutrient limitation and the nutrition of aquatic herbivores. Ann Rev Ecol Syst 25:1–29

    Article  Google Scholar 

  37. Sterner RW, Hagemeier DD, Smith WL, Smith RF (1993) Phytoplankton nutrient limitation and food quality for Daphnia. Limnol Oceanogr 38:857–871

    Article  Google Scholar 

  38. Sterner RW, Elser JJ, Fee EJ, Guildford SJ, Chrzanowski TH (1997) The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. Am Nat 150:663–684

    Article  PubMed  CAS  Google Scholar 

  39. Tessier AJ, Consolati NL (1989) Variation in offspring size in Daphnia and consequences for individual fitness. Oikos 56:269–276

    Article  Google Scholar 

  40. Tezuka Y (1990) Bacterial regeneration of ammonium and phosphate as affected by the carbon:nitrogen:phosphorus ratio of organic substrates. Microb Ecol 19:227–238

    Article  CAS  Google Scholar 

  41. Urabe J, Sterner RW (1996) Regulation of herbivore growth by the balance of light and nutrients. Proc Natl Acad Sci USA 93:8465–8469

    PubMed  Article  CAS  Google Scholar 

  42. Urabe J, Watanabe Y (1992) Possibility of N or P limitation for planktonic cladocerans: an experimental test. Limnol Oceanogr 37:244–251

    CAS  Google Scholar 

  43. Urabe J, Clasen J, Sterner RW (1997) Phosphorus-limitation of Daphnia: is it real? Limnol Oceanogr 42:1436–1443

    CAS  Article  Google Scholar 

  44. Urabe J, Elser JJ, Kyle M, Yoshida T, Sekino T, Kawabata Z (2002a) Herbivorous animals can mitigate unfavourable ratios of energy and material supplies by enhancing nutrient recycling. Ecol Lett 5:177–185

    Article  Google Scholar 

  45. Urabe J, Kyle M, Makino W, Yoshida T, Andersen T, Elser JJ (2002b) Reduced light increases herbivore production due to stoichiometric effects of light:nutrient balance. Ecology 83:619–627

    Article  Google Scholar 

  46. Vanni MJ (1987) Colonization dynamics and life history traits of seven Daphnia pulex genotypes. Oecologia 72:263–271

    Article  Google Scholar 

  47. Vrijenhoek RC (1978) Coexistence of clones in a heterogeneous environment. Science 199:549–553

    PubMed  Article  CAS  Google Scholar 

  48. Vrijenhoek RC (1979) Factors affecting clonal diversity and coexistence. Amer Zool 19:787–797

    Google Scholar 

  49. Weider LJ (1985) Spatial and temporal genetic heterogeneity in a natural Daphnia population. J Plankton Res 7:101–123

    Article  Google Scholar 

  50. Weider LJ, Glenn KL, Kyle M, Elser JJ (2004) Associations among ribosomal (r)DNA intergenic spacer length variation, growth rate, and C:N:P stoichiometry in the genus Daphnia. Limnol Oceanogr 49:1417–1423

    CAS  Article  Google Scholar 

  51. Winder M, Boersma M, Spaak P (2003) On the cost of vertical migration: are feeding conditions really worse at greater depths? Freshwat Biol 48:383–393

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Science Foundation (US, Grant no. 9977047) and a Grant-in-Aid for Scientific Research B (no. 12440218) from MEXT, Japan. We thank S. Ishida, T. Ishikawa, T. Iwata, N. Kuwae, J. Togari, and C. Yoshimizu for laboratory assistance. All experiments were in compliance with applicable laws of the US and Japan. We thank S. Kohler and two anonymous reviewers for their comments.

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Correspondence to Lawrence J. Weider.

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Communicated by Steve Kohler

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Weider, L.J., Makino, W., Acharya, K. et al. Genotype × environment interactions, stoichiometric food quality effects, and clonal coexistence in Daphnia pulex . Oecologia 143, 537–547 (2005). https://doi.org/10.1007/s00442-005-0003-x

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Keywords

  • Nutrients
  • Elemental ratios
  • Daphniids
  • Competition
  • Clones