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The development of the O2-sensing system in an amphibious fish: consequences of variation in environmental O2 levels

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Abstract

Proper development of the O2-sensing system is essential for survival. Here, we characterized the development of the O2-sensing system in the mangrove rivulus (Kryptolebias marmoratus), an amphibious fish that transitions between hypoxic aquatic environments and O2-rich terrestrial environments. We found that NECs formed in the gills and skin of K. marmoratus during embryonic development and that both NEC populations are retained from the embryonic stage to adulthood. We also found that the hyperventilatory response to acute hypoxia was present in embryonic K. marmoratus, indicating that functional O2-sensing pathways are formed during embryonic development. We then exposed embryos to aquatic normoxia, aquatic hyperoxia, aquatic hypoxia, or terrestrial conditions for the first 30 days of embryonic development and tested the hypothesis that environmental O2 availability during embryonic development modulates the development of the O2-sensing system in amphibious fishes. Surprisingly, we found that O2 availability during embryonic development had little impact on the density and morphology of NECs in the gills and skin of K. marmoratus. Collectively, our results demonstrate that, unlike the only other species of fish in which NEC development has been studied to date (i.e., zebrafish), NEC development in K. marmoratus is largely unaffected by environmental O2 levels during the embryonic stage, indicating that there is interspecies variation in O2-induced plasticity in the O2-sensing system of fishes.

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Acknowledgements

We thank Dr. Andreas Heyland for the use of his microscope, Drs. Nicholas Bernier and Beren Robinson for advice on study design and data interpretation, and Nicole Carpenter, Mike Davies, and Matt Cornish for assistance with animal care.

Funding

Funding was provided by Natural Sciences and Engineering Research Council of Canada (NSERC) and Ontario Graduate scholarships to P.V.C. and a NSERC discovery grant to P.A.W.

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Authors and Affiliations

  1. Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Paige V. Cochrane & Patricia A. Wright

  2. Department of Biology, University of Ottawa, Ottawa, ON, K1N 6N5, Canada

    Michael G. Jonz

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Contributions

PVC and PAW conceived the study and designed the experiments. PVC conducted the experiments, analyzed the data, and wrote the draft manuscript. MGJ trained PVC on immunohistochemical techniques and aided in the interpretation of images. All authors reviewed and revised the manuscript, and gave final approval for publication.

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Correspondence to Paige V. Cochrane.

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Communicated by B. Pelster.

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Cochrane, P.V., Jonz, M.G. & Wright, P.A. The development of the O2-sensing system in an amphibious fish: consequences of variation in environmental O2 levels. J Comp Physiol B 191, 681–699 (2021). https://doi.org/10.1007/s00360-021-01379-5

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