Skip to main content
SpringerLink
Log in

Heritability, Environmental Effects, and Genetic and Phenotypic Correlations of Oxidative Stress Resistance-Related Enzyme Activities During Early Life Stages in Atlantic Salmon

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Oxidative stress (OS) may pose important physiological constraints on individuals, affecting trade-offs between growth and reproduction or ageing and survival. Despite such evolutionary and ecological importance, the results from studies on the magnitude of individual variation in OS resistance and the underlying causes of this variation such as genetic, environmental, and maternal origins, remain inconclusive. Using a high throughput methodology, we investigated the activity levels in three OS resistance-related enzymes (superoxide dismutase, SOD; glutathione reductase, GR; glutathione S-transferase, GST) during the early life stages of 1000 individuals from 50 paternal half-sib families in two populations of Atlantic salmon. Using animal mixed models, we detected the presence of narrow-sense heritability for SOD and GST; that for GST differed between populations due to differences in environmental variance. We found support for the presence of common environmental variation, including maternal effects, for only GR. Using a bivariate animal model, we detected a positive environmental correlation between activity levels of SOD and GST but were unable to detect an additive genetic correlation. Our results complement previous heritability findings for levels of reactive oxygen species or OS resistance by demonstrating the presence of heritability for OS-related enzyme activities. Our findings provide a foundation for future work, such as investigations on the evolutionary importance of variation in enzyme activities. In addition, our findings emphasise the importance of accounting for developmental stage, environmental variance, and kin relationships when investigating the OS-response at the enzyme activity level.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., & Sorci, G. (2004). Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecology Letters, 7(5), 363–368.

    Article  Google Scholar 

  • Beacham, T. D., & Murray, C. B. (1985). Effect of female size, egg size, and water temperature on developmental biology of chum salmon (Oncorhynchus keta) from the Nitinat River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences, 42(11), 1755–1765.

    Article  Google Scholar 

  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological, 57(1), 289–300.

    Google Scholar 

  • Bize, P., Devevey, G., Monaghan, P., Doligez, B., & Christe, P. (2008). Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology, 89(9), 2584–2593.

    Article  PubMed  Google Scholar 

  • Butler DG, Cullis BR, Gilmour AR, Gogel BJ. (2009). Mixed models for S language environments ASReml-R reference manual. Brisbane: Queensland Department of Primary Industries and Fisheries, NSW Department of Primary Industries.

  • Carney Almroth, B., Johansson, A., Forlin, L., & Sturve, J. (2010). Early-age changes in oxidative stress in brown trout, Salmo trutta. Comparative Biochemistry and Physiology Part B, Biochemistry and Molecular Biology, 155(4), 442–448.

    Article  PubMed  Google Scholar 

  • Costantini, D., & Dell’Omo, G. (2006). Environmental and genetic components of oxidative stress in wild kestrel nestlings (Falco tinnunculus). Journal of Comparative Physiology B, 176(6), 575–579.

    Article  CAS  Google Scholar 

  • Costantini, D., Monaghan, P., & Metcalfe, N. B. (2013). Loss of integration is associated with reduced resistance to oxidative stress. Journal of Experimental Biology, 216(12), 2213–2220.

    Article  CAS  PubMed  Google Scholar 

  • Dennery, P. A. (2010). Oxidative stress in development: Nature or nurture? Free Radical Biology and Medicine, 49(7), 1147–1151.

    Article  CAS  PubMed  Google Scholar 

  • Einum, S. (2003). Atlantic salmon growth in strongly food-limited environments: Effects of egg size and paternal phenotype? Environmental Biology of Fishes, 67(3), 263–268.

    Article  Google Scholar 

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics (p. 464). Harlow: Longman. xv.

    Google Scholar 

  • Finkel, T., & Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature, 408(6809), 239–247.

    Article  CAS  PubMed  Google Scholar 

  • Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130–7139.

    CAS  PubMed  Google Scholar 

  • Halliwell, B., & Gutteridge, J. (2007). Free radicals in biology and medicine. Oxford: Oxford University Press.

    Google Scholar 

  • Heinimaa, S., & Heinimaa, P. (2004). Effect of the female size on egg quality and fecundity of the wild Atlantic salmon in the sub-arctic River Teno. Boreal Environment Research, 9(1), 55–62.

    Google Scholar 

  • Hõrak, P., & Cohen, A. (2010). How to measure oxidative stress in an ecological context: Methodological and statistical issues. Functional Ecology, 24(5), 960–970.

    Article  Google Scholar 

  • Isaksson, C., Sheldon, B. C., & Uller, T. (2011). The challenges of integrating oxidative stress into life-history biology. BioScience, 61(3), 194–202.

    Article  Google Scholar 

  • Jones, D. P. (2006). Redefining oxidative stress. Antioxidants & Redox Signaling, 8(9–10), 1865–1879.

    Article  CAS  Google Scholar 

  • Jones, A. G., Small, C. M., Paczolt, K. A., & Ratterman, N. L. (2010). A practical guide to methods of parentage analysis. Molecular Ecology Resources, 10(1), 6–30.

    Article  PubMed  Google Scholar 

  • Kamler, E. (2002). Ontogeny of yolk-feeding fish: An ecological perspective. Reviews in Fish Biology and Fisheries, 12(1), 79–103.

    Article  Google Scholar 

  • Kamler, E. (2005). Parent–egg–progeny relationships in teleost fishes: An energetics perspective. Reviews in Fish Biology and Fisheries, 15(4), 399–421.

    Article  Google Scholar 

  • Kamler, E. (2008). Resource allocation in yolk-feeding fish. Reviews in Fish Biology and Fisheries, 18(2), 143–200.

    Article  Google Scholar 

  • Kane, T. R. (1988). Relationship of temperature and time of initial feeding of Atlantic salmon. Progressive Fish-Culturist, 50(2), 93–97.

    Article  Google Scholar 

  • Kaplan, R. H. (1987). Developmental plasticity and maternal effects of reproductive characteristics in the frog, Bombina orientalis. Oecologia, 71(2), 273–279.

    Article  Google Scholar 

  • Kenward, M. G., & Roger, J. H. (1997). Small sample inference for fixed effects from restricted maximum likelihood. Biometrics, 53(3), 983–997.

    Article  CAS  PubMed  Google Scholar 

  • Kim, S.-Y., Noguera, J. C., Morales, J., & Velando, A. (2010a). Heritability of resistance to oxidative stress in early life. Journal of Evolutionary Biology, 23(4), 769–775.

    Article  PubMed  Google Scholar 

  • Kim, S. Y., Velando, A., Sorci, G., & Alonso-Alvarez, C. (2010b). Genetic correlation between resistance to oxidative stress and reproductive life span in a bird species. Evolution, 64(3), 852–857.

    Article  CAS  PubMed  Google Scholar 

  • Kruuk, L. E., & Hadfield, J. D. (2007). How to separate genetic and environmental causes of similarity between relatives. Journal of Evolutionary Biology, 20(5), 1890–1903.

    Article  CAS  PubMed  Google Scholar 

  • Limon-Pacheco, J., & Gonsebatt, M. E. (2009). The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutation Research, 674(1–2), 137–147.

    Article  CAS  PubMed  Google Scholar 

  • Livingstone, D. R. (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42(8), 656–666.

    Article  CAS  PubMed  Google Scholar 

  • Losdat, S., Helfenstein, F., Blount, J. D., & Richner, H. (2014). Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird. Journal of Evolutionary Biology, 27(9), 1990–2000.

    Article  CAS  PubMed  Google Scholar 

  • Lundström, J., Carney, B., Amcoff, P., Pettersson, A., Börjeson, H., Förlin, L., & Norrgren, L. (1999). Antioxidative systems, detoxifying enzymes and thiamine levels in Baltic salmon (Salmo salar) that develop M74. Ambio, 28(1), 24–29.

    Google Scholar 

  • Mari, M., Morales, A., Colell, A., Garcia-Ruiz, C., & Fernandez-Checa, J. C. (2009). Mitochondrial glutathione, a key survival antioxidant. Antioxidants & Redox Signaling, 11(11), 2685–2700.

    Article  CAS  Google Scholar 

  • Metcalfe, N. B., & Alonso-Alvarez, C. (2010). Oxidative stress as a life-history constraint: The role of reactive oxygen species in shaping phenotypes from conception to death. Functional Ecology, 24(5), 984–996.

    Article  Google Scholar 

  • Monaghan, P., Metcalfe, N. B., & Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: Mechanisms, measurements and interpretation. Ecology Letters, 12(1), 75–92.

    Article  PubMed  Google Scholar 

  • Noguera, J. C., Lores, M., Alonso-Álvarez, C., & Velando, A. (2011). Thrifty development: Early-life diet restriction reduces oxidative damage during later growth. Functional Ecology, 25(5), 1144–1153.

    Article  Google Scholar 

  • Olsson, M., Wilson, M., Uller, T., Mott, B., Isaksson, C., Healey, M., & Wanger, T. (2008). Free radicals run in lizard families. Biology Letters, 4(2), 186–188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pamplona, R., & Costantini, D. (2011a). Molecular and structural antioxidant defenses against oxidative stress in animals. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 301, R843–R863.

    Article  CAS  PubMed  Google Scholar 

  • Pamplona, R., & Costantini, D. (2011b). Molecular and structural antioxidant defenses against oxidative stress in animals. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 301(4), R843–R863.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria ISBN: 3-900051-07-0: R Foundation for Statistical Computing.

  • Rizzo, A. M., Adorni, L., Montorfano, G., Rossi, F., & Berra, B. (2007). Antioxidant metabolism of Xenopus laevis embryos during the first days of development. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 146(1), 94–100.

    Article  Google Scholar 

  • Rubolini, D., Romano, M., Bonisoli Alquati, A., & Saino, N. (2006). Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks. Journal of Evolutionary Biology, 19(5), 1571–1584.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675.

    Article  CAS  PubMed  Google Scholar 

  • Smith, I. K., Vierheller, T. L., & Thorne, C. A. (1988). Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis(2-nitrobenzoic acid). Analytical Biochemistry, 175(2), 408–413.

    Article  CAS  PubMed  Google Scholar 

  • Timme-Laragy, A. R., Goldstone, J. V., Imhoff, B. R., Stegeman, J. J., Hahn, M. E., & Hansen, J. M. (2013). Glutathione redox dynamics and expression of glutathione-related genes in the developing embryo. Free Radical Biology and Medicine, 65, 89–101.

    Article  CAS  PubMed  Google Scholar 

  • Tvenning, H. (1985). Fiskeoppdrett. Oslo: H. Aschehoug & Co.

    Google Scholar 

  • Ukeda, H., Kawana, D., Maeda, S., & Sawamura, M. (1999). Spectrophotometric assay for superoxide dismutase based on the reduction of highly water-soluble tetrazolium salts by xanthine-xanthine oxidase. Bioscience, Biotechnology, and Biochemistry, 63(3), 485–488.

    Article  CAS  Google Scholar 

  • van der Leeden R, Busing FM, Meijer E. (1997). Bootstrap methods for two-level models. In Multilevel conference (p. 26). Amsterdam, Netherlands.

  • Vuori, K. A. M., & Nikinmaa, M. (2007). M74 syndrome in Baltic salmon and the possible role of oxidative stresses in its development: Present knowledge and perspectives for future studies. AMBIO: A Journal of the Human Environment, 36(2), 168–172.

    Article  CAS  Google Scholar 

  • Wilson, A. J., Reale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., et al. (2010). An ecologist’s guide to the animal model. Journal of Animal Ecology, 79(1), 13–26.

    Article  PubMed  Google Scholar 

  • Wolak, M. E. (2012). nadiv: An R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods in Ecology and Evolution, 3(5), 792–796.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Põlula Fish Rearing Centre for creating and maintaining animals and logistic support; L. Maran, L. Pukk, K. Pai, I. Tallerman and M. Aid for hatchery assistance; T. Pajula, PM. Maravi, N. Vuori, M. Kanerva and K. Sõstar for laboratory assistance. For initial analyses and manuscript improvements we greatly thank M. Bruneaux. Sylvain Losdat and three anonymous reviewers are thanked for improving an earlier version of the manuscript. This study was funded by the SA Archimedes Foundation, Emil Aaltosen Säätiö and Oskar Öflunds Stiftelse to SK, the Estonian Science Foundation (Grant Numbers 6802, 8215) and the Estonian Ministry of Education and Research (institutional research funding project IUT8-2) to AV and the Academy of Finland to AV, J-PV and KV.

Author information

Author notes

    Authors and Affiliations

    1. Department of Biology, University of Turku, Pharmacity 7th Floor, Itäinen Pitkäkatu 4, 20520, Turku, Finland

      Siim Kahar, Paul V. Debes, Kristina A. M. Vuori, Juha-Pekka Vähä & Anti Vasemägi

    2. Department of Biology, Concordia University, Montreal, Canada

      Paul V. Debes

    3. Department of Aquaculture, Estonian University of Life Sciences, Tartu, Estonia

      Anti Vasemägi

    4. Kevo Subarctic Research Institute, University of Turku, Turku, Finland

      Juha-Pekka Vähä

    Authors
    1. Siim Kahar
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Paul V. Debes
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Kristina A. M. Vuori
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Juha-Pekka Vähä
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Anti Vasemägi
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Siim Kahar.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    Siim Kahar and Paul V. Debes have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 32 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Kahar, S., Debes, P.V., Vuori, K.A.M. et al. Heritability, Environmental Effects, and Genetic and Phenotypic Correlations of Oxidative Stress Resistance-Related Enzyme Activities During Early Life Stages in Atlantic Salmon. Evol Biol 43, 215–226 (2016). https://doi.org/10.1007/s11692-016-9368-5

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11692-016-9368-5

    Keywords

    Search

    Navigation