Abstract
The gills are the primary site of exchange in fishes. However, during early life-stages or in amphibious fishes, ionoregulation and gas-exchange may be primarily cutaneous. Given the similarities between larval and amphibious fishes, we hypothesized that cutaneous larval traits are continuously expressed in amphibious fishes across all life-stages to enable the skin to be a major site of exchange on land. Alternatively, we hypothesized that cutaneous larval traits disappear in juvenile stages and are re-expressed in amphibious species in later life-stages. We surveyed six species spanning a range of amphibiousness and characterized cutaneous ionocytes and neuroepithelial cells (NECs) as representative larval skin traits at up to five stages of development. We found that skin ionocyte density remained lower and constant in exclusively water-breathing, relative to amphibious species across development, whereas in amphibious species ionocyte density generally increased. Additionally, adults of the most amphibious species had the highest cutaneous ionocyte densities. Surprisingly, cutaneous NECs were only identified in the skin of one amphibious species (Kryptolebias marmoratus), suggesting that cutaneous NECs are not a ubiquitous larval or amphibious skin trait, at least among the species we studied. Our data broadly supports the continuous-expression hypothesis, as three of four amphibious experimental species expressed cutaneous ionocytes in all examined life-stages. Further, the increasing density of cutaneous ionocytes across development in amphibious species probably facilitates the prolonged occupation of terrestrial habitats.
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The datasets associated with this study have been placed in the University of Guelph Research Data Repository and upon publication will be available at https://doi.org/10.5683/SP3/1CJXC0 upon request.
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Acknowledgements
We thank Dr. Andreas Heyland for the use of his microscope and expertise, Dr. Andy Turko for valuable discussions and comments that have shaped and improved this work, Jodi Morrison at the University of Guelph histology suite for her time and guidance, Dr. Graham Scott for his comments on the study design, and Dr. Nicholas Bernier for the use of his dissecting scope. In addition, we thank Mike Davies, Matt Cornish and numerous undergraduates for assistance with animal care.
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This work was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grants to PAW (RGPIN- 2018-04218) and JMW (RGPIN-2014-04289) as well as a Canadian Foundation for Innovation (CFI) John R. Evans Leaders Fund (JELF; #32713) also to JMW. LT was awarded a NSERC graduate scholarship and an Ontario graduate scholarship.
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LT and PAW designed the experiments. LT conducted the experiments, analyzed the data, prepared figures, and wrote the draft manuscript. JMW trained LT on immunofluorescence techniques and provided guidance throughout. All authors reviewed and edited the manuscript and gave approval for submission.
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Tunnah, L., Wilson, J.M. & Wright, P.A. Retention of larval skin traits in adult amphibious killifishes: a cross-species investigation. J Comp Physiol B 192, 473–488 (2022). https://doi.org/10.1007/s00360-022-01436-7
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DOI: https://doi.org/10.1007/s00360-022-01436-7