Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Molecular processes of transgenerational acclimation to a warming ocean

Nature Climate Change volume 5, pages 1074–1078 (2015)Cite this article

Subjects

Abstract

Some animals have the remarkable capacity to acclimate across generations to projected future climate change1,2,3,4; however, the underlying molecular processes are unknown. We sequenced and assembled de novo transcriptomes of adult tropical reef fish exposed developmentally or transgenerationally to projected future ocean temperatures and correlated the resulting expression profiles with acclimated metabolic traits from the same fish. We identified 69 contigs representing 53 key genes involved in thermal acclimation of aerobic capacity. Metabolic genes were among the most upregulated transgenerationally, suggesting shifts in energy production for maintaining performance at elevated temperatures. Furthermore, immune- and stress-responsive genes were upregulated transgenerationally, indicating a new complement of genes allowing the second generation of fish to better cope with elevated temperatures. Other differentially expressed genes were involved with tissue development and transcriptional regulation. Overall, we found a similar suite of differentially expressed genes among developmental and transgenerational treatments. Heat-shock protein genes were surprisingly unresponsive, indicating that short-term heat-stress responses may not be a good indicator of long-term acclimation capacity. Our results are the first to reveal the molecular processes that may enable marine fishes to adjust to a future warmer environment over multiple generations.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Transgenerational experimental design and corresponding net aerobic scope measures.
Figure 2: Differentially expressed contigs, correlations to metabolic performance, and putative cellular function.
Figure 3: HSP contig expression pattern.

Similar content being viewed by others

References

  1. Donelson, J. M., Munday, P. L., McCormick, M. I. & Pitcher, C. R. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Clim. Change 2, 30–32 (2012).

    Article  Google Scholar 

  2. Miller, G. M., Watson, S-A., Donelson, J. M., McCormick, M. I. & Munday, P. L. Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nature Clim. Change 2, 858–861 (2012).

    Article  CAS  Google Scholar 

  3. Salinas, S. & Munch, S. B. Thermal legacies: Transgenerational effects of temperature on growth in a vertebrate. Ecol. Lett. 15, 159–163 (2012).

    Article  Google Scholar 

  4. Shama, L. N. S., Strobel, A., Mark, F. C. & Wegner, K. M. Transgenerational plasticity in marine sticklebacks: Maternal effects mediate impacts of a warming ocean. Funct. Ecol. 28, 1482–1493 (2014).

    Article  Google Scholar 

  5. Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nature Clim. Change 3, 919–925 (2013).

    Article  Google Scholar 

  6. Munday, P. L., Warner, R. R., Monro, K., Pandolfi, J. M. & Marshall, D. J. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16, 1488–1500 (2013).

    Article  Google Scholar 

  7. Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014).

    Article  CAS  Google Scholar 

  8. Munoz, N. J., Farrell, A. P., Heath, J. W. & Neff, B. D. Adaptive potential of a Pacific salmon challenged by climate change. Nature Clim. Change 5, 163–166 (2015).

    Article  Google Scholar 

  9. Nilsson, G. E., Crawley, N., Lunde, I. G. & Munday, P. L. Elevated temperature reduces the respiratory scope of coral reef fishes. Glob. Change Biol. 15, 1405–1412 (2009).

    Article  Google Scholar 

  10. Portner, H. O. & Farrell, A. P. Physiology and climate change. Science 322, 690–692 (2008).

    Article  Google Scholar 

  11. Portner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007).

    Article  Google Scholar 

  12. Johansen, J. L. & Jones, G. P. Increasing ocean temperature reduces the metabolic performance and swimming ability of coral reef damselfishes. Glob. Change Biol. 17, 2971–2979 (2011).

    Article  Google Scholar 

  13. Eliason, E. J. et al. Differences in thermal tolerance among sockeye salmon populations. Science 332, 109–112 (2011).

    Article  CAS  Google Scholar 

  14. Killen, S. S. et al. Aerobic scope predicts dominance during early life in a tropical damselfish. Funct. Ecol. 28, 1367–1376 (2014).

    Article  Google Scholar 

  15. Rummer, J. L. et al. Life on the edge: Thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Glob. Change Biol. 20, 1055–1066 (2014).

    Article  Google Scholar 

  16. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).

    Article  CAS  Google Scholar 

  17. Hazel, J. R. Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annu. Rev. Physiol. 57, 19–42 (1995).

    Article  CAS  Google Scholar 

  18. Kieffer, J. D., Alsop, D. & Wood, C. M. A respirometric analysis of fuel use during aerobic swimming at different temperatures in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 201, 3123–3133 (1998).

    Google Scholar 

  19. McClelland, G. B. Fat to the fire: The regulation of lipid oxidation with exercise and environmental stress. Comp. Biochem. Phys. B 139, 443–460 (2004).

    Article  Google Scholar 

  20. Kassahn, K. S., Crozier, R. H., Ward, A. C., Stone, G. & Caley, J. M. From transcriptome to biological function: Environmental stress in an ectothermic vertebrate, the coral reef fish Pomacentrus moluccensis. BMC Genom. 8, 358–374 (2007).

    Article  Google Scholar 

  21. Podrabsky, J. E. & Somero, G. N. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J. Exp. Biol. 207, 2237–2254 (2004).

    Article  CAS  Google Scholar 

  22. Bly, J. E., Grimm, A. S. & Morris, I. G. Transfer of passive immunity from mother to young in a teleost fish: Haemagglutinating activity in the serum and eggs of plaice, Pleuronectes platessa L. Comp. Biochem. Phys. A 84, 309–313 (1986).

    Article  CAS  Google Scholar 

  23. Lemke, H. & Lange, H. Is there a maternally induced immunological imprinting phase a la Konrad Lorenz? Scand. J. Immunol. 50, 348–354 (1999).

    Article  CAS  Google Scholar 

  24. Bonga, S. E. W. The stress response in fish. Physiol. Rev. 77, 591–625 (1997).

    Article  Google Scholar 

  25. Xiong, X., He, H. & Sun, Y. Ribosomal protein S27-like and S27 interplay with p53-MDM2 axis as a target, a substrate and a regulator. Oncogene 30, 1798–1811 (2011).

    Article  CAS  Google Scholar 

  26. Zeldin, D. C. Epoxygenase pathways of arachidonic acid metabolism. J. Biol. Chem. 276, 36059–36062 (2001).

    Article  CAS  Google Scholar 

  27. Yang, B. et al. Overexpression of cytochrome P450 protects against hypoxia-reoxygenation injury in cultured bovine aortic endothelial cells. J. Pharmacol. Exp. Ther. 60, 310–320 (2001).

    CAS  Google Scholar 

  28. Chen, G. et al. CYP2J2 overexpression attenuates nonalcoholic fatty liver disease induced by high-fat diet in mice. Am. J. Physiol. Endocrinol. Metab. 308, E97–E110 (2015).

    Article  CAS  Google Scholar 

  29. Feder, M. E. & Hofmann, G. E. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243–282 (1999).

    Article  CAS  Google Scholar 

  30. Lukash, T. O., Turkivska, H. V., Negrutskii, B. S. & El’skaya, A. V. Chaperone-like activity of mammalian elongation factor eEF1A: Renaturation of aminoactyl-tRNA synthetases. Int. J. Biochem. Cell Biol. 36, 1341–1347 (2004).

    Article  CAS  Google Scholar 

  31. Basu, N. et al. Heat shock protein genes and their functional significance in fish. Gene 295, 173–183 (2002).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Australian Research Council (ARC) and the ARC Centre of Excellence for Coral Reef Studies (P.L.M. and W.L.), the Competitive Research Funds OCRF-2014-CRG3-62140408 from the King Abdullah University of Science and Technology (T.Ravasi, M.L.B., T.Ryu, L.S., and Y.G.), the Australian Coral Reef Society (H.D.V.), and a GBRMPA Science for Management Award (H.D.V.). This project was completed under JCU Ethics A1233 and A1415. We thank J. L. Rummer for comments on the manuscript and members of the Molecular Ecology and Evolution Laboratory (JCU), Marine and Aquaculture Research Facilities Unit (JCU), Integrative Systems Biology Laboratory (KAUST), and Biosciences Core Laboratory (KAUST) for support and assistance.

Author information

Author notes

  1. Heather D. Veilleux and Taewoo Ryu: These authors contributed equally to this work.

Authors and Affiliations

  1. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia

    Heather D. Veilleux, William Leggat & Philip L. Munday

  2. College of Marine and Environmental Sciences, James Cook University, Townsville, Queensland 4811, Australia

    Heather D. Veilleux, Jennifer M. Donelson, Lynne van Herwerden & Philip L. Munday

  3. Division of Biological and Environmental Sciences & Engineering, Division of Applied Mathematics and Computer Sciences, KAUST Environmental Epigenetic Program (KEEP), King Abdullah University of Science and Technology, 23955-6900 Thuwal, Kingdom of Saudi Arabia

    Taewoo Ryu, Loqmane Seridi, Yanal Ghosheh & Timothy Ravasi

  4. School of Life Sciences, University of Technology Sydney, PO Box 123 Broadway, New South Wales 2007, Australia,

    Jennifer M. Donelson

  5. Centre for Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland 4811, Australia

    Lynne van Herwerden

  6. Division of Biological and Environmental Sciences and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia

    Michael L. Berumen

  7. College of Medical, Veterinary and Biomedical Sciences, James Cook University, Townsville, Queensland 4811, Australia

    William Leggat

Authors
  1. Heather D. Veilleux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Taewoo Ryu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer M. Donelson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lynne van Herwerden
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loqmane Seridi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yanal Ghosheh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael L. Berumen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. William Leggat
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Timothy Ravasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Philip L. Munday
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.M.D. and P.L.M. designed and managed the fish rearing experiments. J.M.D. performed metabolism experiments. H.D.V. prepared samples for sequencing. T.Ryu assembled transcriptome. T.Ryu, T.Ravasi, L.S. and Y.G. analysed expression and assessed assembly quality. H.D.V. performed quantitative real-time-PCR expression validation. H.D.V. analysed the data. H.D.V., P.L.M., T.Ryu, J.M.D., L.v.H., M.L.B., W.L. and T.Ravasi wrote the paper and all authors read and approved the manuscript.

Corresponding authors

Correspondence to Timothy Ravasi or Philip L. Munday.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Veilleux, H., Ryu, T., Donelson, J. et al. Molecular processes of transgenerational acclimation to a warming ocean. Nature Clim Change 5, 1074–1078 (2015). https://doi.org/10.1038/nclimate2724

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2724

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing