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Mechanistic basis of adaptive maternal effects: egg jelly water balance mediates embryonic adaptation to acidity in Rana arvalis

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Abstract

Environmental stress, such as acidification, can challenge persistence of natural populations and act as a powerful evolutionary force at ecological time scales. The ecological and evolutionary responses of natural populations to environmental stress at early life-stages are often mediated via maternal effects. During early life-stages, maternal effects commonly arise from egg coats (the extracellular structures surrounding the embryo), but the role of egg coats has rarely been studied in the context of adaptation to environmental stress. Previous studies on the moor frog Rana arvalis found that the egg coat mediated adaptive divergence along an acidification gradient in embryonic acid stress tolerance. However, the exact mechanisms underlying these adaptive maternal effects remain unknown. Here, we investigated the role of water balance and charge state (zeta potential) of egg jelly coats in embryonic adaptation to acid stress in three populations of R. arvalis. We found that acidic pH causes severe water loss in the egg jelly coat, but that jelly coats from an acid-adapted population retained more water than jelly coats from populations not adapted to acidity. Moreover, embryonic acid tolerance (survival at pH 4.0) correlated with both water loss and charge state of the jelly, indicating that negatively charged glycans influence jelly water balance and contribute to embryonic adaptation to acidity. These results indicate that egg coats can harbor extensive intra-specific variation, probably facilitated in part via strong selection on water balance and glycosylation status of egg jelly coats. These findings shed light on the molecular mechanisms of environmental stress tolerance and adaptive maternal effects.

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Acknowledgments

We thank Beatrice Lindgren for invaluable help with the field and laboratory work, Baptiste Pasteur for help in collecting the frogs, and Yang Yue for help with the zeta potential measurement. The experiments were conducted under permissions from the Västra Götaland county board and the Ethical committee for animal experiments in Uppsala County. This study was supported by Swiss National Science foundation (to K.R.).

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Department of Aquatic Ecology, Eawag, 8600, Dübendorf, Switzerland

    Longfei Shu & Katja Räsänen

  2. Institute of Integrative Biology, ETH Zürich, 8092, Zürich, Switzerland

    Longfei Shu & Katja Räsänen

  3. Department of Environmental Toxicology, Eawag, 8600, Dübendorf, Switzerland

    Marc J.-F. Suter

  4. Department of Environmental Systems Science, ETH Zürich, 8092, Zurich, Switzerland

    Marc J.-F. Suter

  5. Animal Ecology/Department of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, 75236, Uppsala, Sweden

    Anssi Laurila

  6. Department of Biology, Washington University in St. Louis, St. Louis, MO, 63130, USA

    Longfei Shu

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  1. Longfei Shu
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  2. Marc J.-F. Suter
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  3. Anssi Laurila
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  4. Katja Räsänen
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Correspondence to Longfei Shu.

Additional information

Communicated by William J. Resetarits.

Research highlight:

This research increases our understanding of the ecological and evolutionary role of egg coats, which are maternally derived extracellular structures that surround the organism during early life stages. This study revealed that acid stress could cause severe water loss of egg jelly and likely imposed strong selection on water balance of egg jelly in amphibians by reduced embryonic hatching success. In addition, this study suggested that a “pH-jelly water balance” model, mediated via intra-specific glycan variability, may help explaining the molecular basis of embryonic adaptation to acid stress and egg-coat mediated adaptive maternal effects. Moreover, this model can be extended to other aquatic systems in both vertebrate and invertebrate taxa.

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Shu, L., Suter, M.JF., Laurila, A. et al. Mechanistic basis of adaptive maternal effects: egg jelly water balance mediates embryonic adaptation to acidity in Rana arvalis . Oecologia 179, 617–628 (2015). https://doi.org/10.1007/s00442-015-3332-4

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  • DOI: https://doi.org/10.1007/s00442-015-3332-4

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