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

• Published in: Scientific reports Vol. 9; no. 1; pp. 16347 - 10
• Main Authors: Katayama, Yukitoshi, Takei, Yoshio, Kusakabe, Makoto, Sakamoto, Tatsuya
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 08.11.2019; Nature Publishing Group
• Subjects: 38; 38/77; 38/90; 631/181; 631/601/18; 82/51; Angiotensin; Angiotensin II; Angiotensin II - administration & dosage; Animals; Atrial Natriuretic Factor - administration & dosage; Atrial natriuretic peptide; Behavior; Biological Evolution; Cloning; Drinking behavior; Drinking Behavior - drug effects; Drinking Behavior - physiology; Drying; Ecosystem; Fish; Forebrain; Hindbrain; Hormones; Humanities and Social Sciences; Motivation; multidisciplinary; Osmoregulation; Peptides; Physiology; Prosencephalon - drug effects; Prosencephalon - physiology; Rhombencephalon - drug effects; Rhombencephalon - physiology; Science; Science (multidisciplinary); Skates, Fish; Skin; Swallowing; Thirst; Thirst - drug effects; Thirst - physiology; Vasoconstrictor Agents - administration & dosage; Vertebrates; Water-Electrolyte Balance - drug effects; Water-Electrolyte Balance - physiology
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-019-52870-7

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.