Drinking by amphibious fish

Convergent evolution of thirst mechanisms during vertebrate terrestrialization

Yukitoshi Katayama, Tatsuya Sakamoto, Kazuhiro Saito, Hirotsugu Tsuchimochi, Hiroyuki Kaiya, Taro Watanabe, James T. Pearson, Yoshio Takei

Research output: Contribution to journalArticleResearchpeer-review

4 Citations (Scopus)

Abstract

Thirst aroused in the forebrain by angiotensin II (AngII) or buccal drying motivates terrestrial vertebrates to search for water, whereas aquatic fish can drink surrounding water only by reflex swallowing generated in the hindbrain. Indeed, AngII induces drinking through the hindbrain even after removal of the whole forebrain in aquatic fish. Here we show that AngII induces thirst also in the amphibious mudskipper goby without direct action on the forebrain, but through buccal drying. Intracerebroventricular injection of AngII motivated mudskippers to move into water and drink as with tetrapods. However, AngII primarily increased immunoreactive c-Fos at the hindbrain swallowing center where AngII receptors were expressed, as in other ray-finned fish, and such direct action on the forebrain was not found. Behavioural analyses showed that loss of buccal water on land by AngII-induced swallowing, by piercing holes in the opercula, or by water-absorptive gel placed in the cavity motivated mudskippers to move to water for refilling. Since sensory detection of water at the bucco-pharyngeal cavity like 'dry mouth' has recently been noted to regulate thirst in mammals, similar mechanisms seem to have evolved in distantly related species in order to solve osmoregulatory problems during terrestrialization.

Original languageEnglish
Article number625
Number of pages10
JournalScientific Reports
Volume8
Issue number1
DOIs
Publication statusPublished - 12 Jan 2018
Externally publishedYes

Keywords

  • animal behaviour
  • animal physiology

Cite this

Katayama, Y., Sakamoto, T., Saito, K., Tsuchimochi, H., Kaiya, H., Watanabe, T., ... Takei, Y. (2018). Drinking by amphibious fish: Convergent evolution of thirst mechanisms during vertebrate terrestrialization. Scientific Reports, 8(1), [625]. https://doi.org/10.1038/s41598-017-18611-4
Katayama, Yukitoshi ; Sakamoto, Tatsuya ; Saito, Kazuhiro ; Tsuchimochi, Hirotsugu ; Kaiya, Hiroyuki ; Watanabe, Taro ; Pearson, James T. ; Takei, Yoshio. / Drinking by amphibious fish : Convergent evolution of thirst mechanisms during vertebrate terrestrialization. In: Scientific Reports. 2018 ; Vol. 8, No. 1.
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abstract = "Thirst aroused in the forebrain by angiotensin II (AngII) or buccal drying motivates terrestrial vertebrates to search for water, whereas aquatic fish can drink surrounding water only by reflex swallowing generated in the hindbrain. Indeed, AngII induces drinking through the hindbrain even after removal of the whole forebrain in aquatic fish. Here we show that AngII induces thirst also in the amphibious mudskipper goby without direct action on the forebrain, but through buccal drying. Intracerebroventricular injection of AngII motivated mudskippers to move into water and drink as with tetrapods. However, AngII primarily increased immunoreactive c-Fos at the hindbrain swallowing center where AngII receptors were expressed, as in other ray-finned fish, and such direct action on the forebrain was not found. Behavioural analyses showed that loss of buccal water on land by AngII-induced swallowing, by piercing holes in the opercula, or by water-absorptive gel placed in the cavity motivated mudskippers to move to water for refilling. Since sensory detection of water at the bucco-pharyngeal cavity like 'dry mouth' has recently been noted to regulate thirst in mammals, similar mechanisms seem to have evolved in distantly related species in order to solve osmoregulatory problems during terrestrialization.",
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Drinking by amphibious fish : Convergent evolution of thirst mechanisms during vertebrate terrestrialization. / Katayama, Yukitoshi; Sakamoto, Tatsuya; Saito, Kazuhiro; Tsuchimochi, Hirotsugu; Kaiya, Hiroyuki; Watanabe, Taro; Pearson, James T.; Takei, Yoshio.

In: Scientific Reports, Vol. 8, No. 1, 625, 12.01.2018.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Katayama, Yukitoshi

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