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An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish

Nature Ecology & Evolution volume 2, pages 334–342 (2018)Cite this article

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Abstract

The impacts of ocean acidification will depend on the ability of marine organisms to tolerate, acclimate and eventually adapt to changes in ocean chemistry. Here, we use a unique transgenerational experiment to determine the molecular response of a coral reef fish to short-term, developmental and transgenerational exposure to elevated CO2, and to test how these responses are influenced by variations in tolerance to elevated CO2 exhibited by the parents. Within-generation responses in gene expression to end-of-century predicted CO2 levels indicate that a self-amplifying cycle in GABAergic neurotransmission is triggered, explaining previously reported neurological and behavioural impairments. Furthermore, epigenetic regulator genes exhibited a within-generation specific response, but with some divergence due to parental phenotype. Importantly, we find that altered gene expression for the majority of within-generation responses returns to baseline levels following parental exposure to elevated CO2 conditions. Our results show that both parental variation in tolerance and cross-generation exposure to elevated CO2 are crucial factors in determining the response of reef fish to changing ocean chemistry.

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Fig. 1: Experimental design of the study.
Fig. 2: Global differential gene expression patterns between treatments.
Fig. 3: Functional enrichment analysis of differentially expressed genes across CO2 rearing treatments that were significant in both differential gene expression models (control, acute, developmental and transgenerational) and different behavioural parental phenotypes (tolerant and sensitive).
Fig. 4: The GABA (γ-aminobutyric acid) signalling pathway in the synapse between a pre- and postsynaptic neuron.
Fig. 5: Expression patterns of histone-related transcripts across all CO2 treatments.

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Acknowledgements

This study was supported by the Office of Competitive Research Funds OSR-2015- CRG4-2541 from the King Abdullah University of Science and Technology (T.R., P.L.M., C.S. and J.L.R.), the Australian Research Council (ARC) and the ARC Centre of Excellence for Coral Reef Studies (P.L.M. and J.L.R.) and the University of Oslo (G.E.N.). We thank the Marine and Aquaculture Research Facilities Unit (JCU), Integrative Systems Biology Laboratory (KAUST) and Biosciences Core Laboratory (KAUST) for support and assistance. Figures 1 to 4 were produced by X. Pita, scientific illustrator at King Abdullah University of Science and Technology (KAUST).

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Authors and Affiliations

  1. KAUST Environmental Epigenetic Program (KEEP), Division of Biological and Environmental Sciences & Engineering, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia

    Celia Schunter & Timothy Ravasi

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

    Megan J. Welch, Jodie L. Rummer & Philip L. Munday

  3. Section for Physiology and Cell Biology, Department of Biosciences, University of Oslo, Oslo, Norway

    Göran E. Nilsson

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  1. Celia Schunter
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  2. Megan J. Welch
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  5. Philip L. Munday
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Contributions

M.J.W. and P.L.M. designed and managed the fish rearing experiments. M.J.W. performed the adult fish behavioural phenotyping. C.S. prepared the samples for RNA sequencing and analysed transcriptome expression data and performed quantitative real-time PCR expression validation. G.E.N. and J.L.R. assisted in interpreting the expression data. C.S., P.L.M. and T.R. wrote the paper, and all authors read, revised and approved the final manuscript.

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Correspondence to Philip L. Munday or Timothy Ravasi.

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Schunter, C., Welch, M.J., Nilsson, G.E. et al. An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish. Nat Ecol Evol 2, 334–342 (2018). https://doi.org/10.1038/s41559-017-0428-8

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