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

Abstract

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.

The Physicochemical Characteristics of Gelam Honey and Its Outcome on the Female Reproductive Tissue of Sprague–Dawley Rats: A Preliminary Study

“…Honey is known to affect dipsogenic hormones and cause an anti-dipsogenic effect. Angiotensin II and serotonin are dipsogenic hormones that are able to increase thirst perception, resulting in an increased water intake [9,29]. However, in the present study, the rats receiving higher doses of GH experienced anti-dipsogenic effects and ultimately reduced their water intake.…”

Introducing the Amphibious Mudskipper Goby as a Unique Model to Evaluate Neuro/Endocrine Regulation of Behaviors Mediated by Buccal Sensation and Corticosteroids

“…Indeed, we recently demonstrated that artificial removal (e.g., by piercing holes in the opercula) of buccal water stored on land by the mudskipper resulted in a strong behavioral preference for a water environment, suggesting the presence of thirst (defined as a conscious sensation of a need for water and a desire to drink, which is followed by a search for water in terrestrial animals such as mammals [ 29 , 30 ]) in fish [ 17 ]. Furthermore, administration of the most potent dipsogenic hormone known in many vertebrate species, angiotensin II [ 31 , 32 , 33 ], resulted in a swallowing action of water held in the buccal cavity of the mudskipper that was regulated by the area postrema (AP) in the hindbrain, as in aquatic fish ( Figure 3 a,b; [ 17 , 24 ]). Migration of the mudskipper to water following the loss of buccal water by swallowing is indicative of the seeking behavior exhibited by tetrapods in a local thirst (dry mouth) response [ 16 , 17 ].…”

“…Plastic mesh on the land area facilitates drainage of water. Water in the tank is constantly aerated[17,[24][25][26].…”

Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin

“…modestus store water in the buccal and opercular cavities as a source of drinking water when on land [ 6 ]. Furthermore, our comparison of hormonal regulation of drinking behaviours among the Periophthalmus mudskipper and mammals suggested repeated evolution of thirst in distant taxa of vertebrates [ 6 , 7 ]. As well as thirst regulated by hormones, postprandial thirst serves to prevent systemic dehydration in tetrapods [ 8 , 9 ].…”

“…This implies that buccal sensation of food or drying motivates mudskippers to move to water for drinking. Because mudskippers cannot absorb water through the cutaneous skin, unlike ‘cutaneous drinking’ in amphibians [ 14 ], analyses of their migration have been used as an index of their desire for water [ 6 , 7 ]. Although the migration is triggered by many behavioural/physiological requirements [ 5 ], this index can allow examination of whether postprandial drinking has been acquired during terrestrialisation of ray-finned fish as an anticipatory response to potential dehydration.…”