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Molecular processes of transgenerational acclimation to a warming ocean

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

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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.

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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.

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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.

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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
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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.

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The authors declare no competing financial interests.

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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

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