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Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution

Thirst has evolved for vertebrate terrestrial adaptation. We previously showed that buccal drying induced a series of drinking behaviours (migration to water–taking water into the mouth–swallowing) in the amphibious mudskipper goby, thereby discovering thirst in ray-finned fish. However, roles of di...

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Autores principales: Katayama, Yukitoshi, Takei, Yoshio, Kusakabe, Makoto, Sakamoto, Tatsuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6841719/
https://www.ncbi.nlm.nih.gov/pubmed/31705012
http://dx.doi.org/10.1038/s41598-019-52870-7
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author Katayama, Yukitoshi
Takei, Yoshio
Kusakabe, Makoto
Sakamoto, Tatsuya
author_facet Katayama, Yukitoshi
Takei, Yoshio
Kusakabe, Makoto
Sakamoto, Tatsuya
author_sort Katayama, Yukitoshi
collection PubMed
description Thirst has evolved for vertebrate terrestrial adaptation. We previously showed that buccal drying induced a series of drinking behaviours (migration to water–taking water into the mouth–swallowing) in the amphibious mudskipper goby, thereby discovering thirst in ray-finned fish. However, roles of dipsogenic/antidipsogenic hormones, which act on the thirst center in terrestrial tetrapods, have remained unclear in the mudskipper thirst. Here we examined the hormonal effects on the mudskipper drinking behaviours, particularly the antagonistic interaction between angiotensin II (AngII) and atrial natriuretic peptide (ANP) which is important for thirst regulation in mammalian ‘forebrain’. Expectedly, intracerebroventricular injection of ANP in mudskippers reduced AngII-increased drinking rate. ANP also suppressed the neural activity at the ‘hindbrain’ region for the swallowing reflex, and the maintenance of buccopharyngeal water due to the swallowing inhibition may attenuate the motivation to move to water. Thus, the hormonal molecules involved in drinking regulation, as well as the influence of buccopharyngeal water, appear to be conserved in distantly related species to solve osmoregulatory problems, whereas hormonal control of thirst at the forebrain might have been acquired only in tetrapod lineage during evolution.
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spelling pubmed-68417192019-11-14 Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution Katayama, Yukitoshi Takei, Yoshio Kusakabe, Makoto Sakamoto, Tatsuya Sci Rep Article Thirst has evolved for vertebrate terrestrial adaptation. We previously showed that buccal drying induced a series of drinking behaviours (migration to water–taking water into the mouth–swallowing) in the amphibious mudskipper goby, thereby discovering thirst in ray-finned fish. However, roles of dipsogenic/antidipsogenic hormones, which act on the thirst center in terrestrial tetrapods, have remained unclear in the mudskipper thirst. Here we examined the hormonal effects on the mudskipper drinking behaviours, particularly the antagonistic interaction between angiotensin II (AngII) and atrial natriuretic peptide (ANP) which is important for thirst regulation in mammalian ‘forebrain’. Expectedly, intracerebroventricular injection of ANP in mudskippers reduced AngII-increased drinking rate. ANP also suppressed the neural activity at the ‘hindbrain’ region for the swallowing reflex, and the maintenance of buccopharyngeal water due to the swallowing inhibition may attenuate the motivation to move to water. Thus, the hormonal molecules involved in drinking regulation, as well as the influence of buccopharyngeal water, appear to be conserved in distantly related species to solve osmoregulatory problems, whereas hormonal control of thirst at the forebrain might have been acquired only in tetrapod lineage during evolution. Nature Publishing Group UK 2019-11-08 /pmc/articles/PMC6841719/ /pubmed/31705012 http://dx.doi.org/10.1038/s41598-019-52870-7 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Katayama, Yukitoshi
Takei, Yoshio
Kusakabe, Makoto
Sakamoto, Tatsuya
Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
title Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
title_full Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
title_fullStr Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
title_full_unstemmed Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
title_short Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
title_sort hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6841719/
https://www.ncbi.nlm.nih.gov/pubmed/31705012
http://dx.doi.org/10.1038/s41598-019-52870-7
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