Abstract
When amphibious fishes are on land, gill function is reduced or eliminated and the skin is hypothesized to act as a surrogate site of ionoregulation. Skin ionocytes are present in many fishes, particularly those with amphibious life histories. We used nine closely related killifishes spanning a range of amphibiousness to first test the hypothesis that amphibious killifishes have evolved constitutively increased skin ionocyte density to promote ionoregulation on land. We found that skin ionocyte densities were constitutively higher in five of seven amphibious species examined relative to exclusively water-breathing species when fish were prevented from leaving water, strongly supporting our hypothesis. Next, to examine the scope for plasticity, we tested the hypothesis that skin ionocyte density in amphibious fishes would respond plastically to air-exposure to promote ionoregulation in terrestrial environments. We found that air-exposure induced plasticity in skin ionocyte density only in the two species classified as highly amphibious, but not in moderately amphibious species. Specifically, skin ionocyte density significantly increased in Anablepsoides hartii (168%) and Kryptolebias marmoratus (37%) following a continuous air-exposure, and only in K. marmoratus (43%) following fluctuating air-exposure. Collectively, our data suggest that highly amphibious killifishes have evolved both increased skin ionocyte density as well as skin that is more responsive to air-exposure compared to exclusively water-breathing and less amphibious species. Our findings are consistent with the idea that gaining the capacity for cutaneous ionoregulation is a key evolutionary step that enables amphibious fishes to survive on land.
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The datasets associated with this study have been placed in the University of Guelph Research Data Repository and are available at https://doi.org/10.5683/SP3/KGT8NE upon request.
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Acknowledgements
The authors thank Dr. Andreas Heyland for the use of his microscope. Dr. Graham Scott for the donation of Fundulus heteroclitus and suggestions on study design, and Dr. Jonathan Wilson for guidance with histological analyses. In addition, we thank Mike Davies, Matt Cornish, and numerous undergraduates for assistance with animal care.
Funding
This work was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant to PAW (RGPIN-2018-04218). LT was awarded an NSERC graduate scholarship and an Ontario graduate scholarship. AJT was supported by an NSERC postdoctoral fellowship.
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All authors contributed to study conceptualization. LT conducted the experiments, analyzed the data (with phylogenetic statistical assistance from AJT), prepared figures, and wrote the draft manuscript. All authors edited the manuscript.
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Tunnah, L., Turko, A.J. & Wright, P.A. Skin ionocyte density of amphibious killifishes is shaped by phenotypic plasticity and constitutive interspecific differences. J Comp Physiol B 192, 701–711 (2022). https://doi.org/10.1007/s00360-022-01457-2
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DOI: https://doi.org/10.1007/s00360-022-01457-2