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Comparative transcriptomics across populations offers new insights into the evolution of thermal resistance in marine snails

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Abstract

Adaptation to thermal conditions in intertidal ectotherms involves tolerating and surviving frequent and often extreme variations in environmental temperatures. Modulation of gene expression plays an important role in the adaptive evolution of thermal tolerance. To understand such patterns, we investigated the thermal tolerance among three Asian populations (from Xiamen, Hong Kong, and Singapore) of the marine littorinid snail Echinolittorina malaccana and examined gene expression profiles in these populations before, during, and after heat stress using an Illumina RNA-sequencing platform. Analysis of transcriptomic changes between different conditions revealed that a proportion of the differentially expressed genes showed similar expression profiles across all three populations, including many classic molecular chaperones such as HSP70 and HSP90 that may constitute the core of the thermal stress response machinery in marine snails. Meanwhile, population-specific transcriptomic responses to heat stress were also detected. A few genes in particular showed more analogous expression profiles in the more thermally tolerant Hong Kong and Singapore populations, and these genes are likely to contribute, at least in part, to the enhanced thermal tolerance of these populations. We argue that repression of a subset of metabolic genes including several cytochrome P450 gene family members, to minimize energy expenditure and control reactive oxygen species turnover, may underpin the enhanced thermal resistance in these two populations. As such, these findings offer new insights into how marine snails cope with thermal stress and their potential evolutionary trajectory toward adapting to a warming climate.

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Acknowledgments

We would like to thank Prof. Y. W. Dong of Xiamen University and Dr. Neil Hutchinson of James Cook University Singapore for their assistance in sample collection. We are grateful to two anonymous reviewers for their constructive suggestions on an earlier version of this manuscript. The present study was substantially supported by a grant from the Research Grants Council (RGC), Hong Kong (HKU782011), and grants under the Group Research and Direct Grant Schemes of The Chinese University of Hong Kong.

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  1. Wei Wang

    Present address: Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, USA

Authors and Affiliations

  1. Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Wei Wang, Jerome H. L. Hui & Ka Hou Chu

  2. Partner State Key Laboratory of Agrobiotechnology, Center of Soybean Research, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Jerome H. L. Hui

  3. The Swire Institute of Marine Science, The University of Hong Kong, Hong Kong SAR, China

    Gray A. Williams & Stephen R. Cartwright

  4. School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China

    Gray A. Williams & Stephen R. Cartwright

  5. Institute of Marine Biology, National Taiwan Ocean University, Keelung, Taiwan

    Ling Ming Tsang

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  1. Wei Wang
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Correspondence to Ka Hou Chu.

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Wang, W., Hui, J.H.L., Williams, G.A. et al. Comparative transcriptomics across populations offers new insights into the evolution of thermal resistance in marine snails. Mar Biol 163, 92 (2016). https://doi.org/10.1007/s00227-016-2873-3

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