Molecular processes of transgenerational acclimation to a warming ocean

Journal name:
Nature Climate Change
Volume:
5,
Pages:
1074–1078
Year published:
DOI:
doi:10.1038/nclimate2724
Received
Accepted
Published online

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.

At a glance

Figures

  1. Transgenerational experimental design and corresponding net aerobic scope measures.
    Figure 1: Transgenerational experimental design and corresponding net aerobic scope measures.

    a, Experimental design tree showing the three temperature treatments (+0.0 °C, +1.5 °C and +3.0 °C) at which three generations (F0, F1 and F2) of Acanthochromis polyacanthus were reared. Temperature treatments are colour coded and experimental duration for each generation is shown in the vertical grey bars to the right. Fish in the F2 generation representing control, developmental and transgenerational temperature treatments are indicated by horizontal grey bars. b, Net aerobic scope (NAS) of fish in control, developmental and transgenerational F2 treatments (mean ± s.e.m.). Lower case letters above bars indicate significant differences (P < 0.05) among treatments. Number of fish used to measure NAS for each treatment is shown beneath the grey bars.

  2. Differentially expressed contigs, correlations to metabolic performance, and putative cellular function.
    Figure 2: Differentially expressed contigs, correlations to metabolic performance, and putative cellular function.

    ac, Heatmap (left) of differentially expressed contigs (adjusted P < 0.05) from Acanthochromis polyacanthus, comparing +1.5 °C and +3.0 °C developmental (devel.) and transgenerational (transgen.) treatments with control (+0.0 °C). On the basis of expression patterns, contigs were separated into three groups (ac). The associated cellular functions for each group are presented as pie charts (middle), with each contig represented by two functions with the exception of those that were uncharacterized. Numbers within pie chart sections represent the total number of contigs that correspond to that function. Venn diagrams (right) indicate the proportion of contigs with expression that positively (blue) or negatively (red) correlated to metabolic data (NAS: net aerobic scope, MMR: maximum metabolic rate, and RMR: routine metabolic rate). Purple text indicates negative NAS and positive RMR.

  3. HSP contig expression pattern.
    Figure 3: HSP contig expression pattern.

    Heatmap of HSP expression from Acanthochromis polyacanthus, comparing +1.5 °C and +3.0 °C developmental (devel.) and transgenerational (transgen.) treatments with control (+0.0 °C). There were no significant differences in expression (adjusted P < 0.05). Expression values correspond to the contig with the best match (E-value < 10−27) to HSP genes within our transcriptome.

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Author information

  1. These authors contributed equally to this work.

    • Heather D. Veilleux &
    • Taewoo Ryu

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. KAUST Environmental Epigenetic Program (KEEP), Division of Biological and Environmental Sciences & Engineering, Division of Applied Mathematics and Computer Sciences, 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. Red Sea Research Center, Division of Biological and Environmental Sciences and Engineering, 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

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.

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The authors declare no competing financial interests.

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