Drinking by amphibious fish: convergent evolution of thirst mechanisms during vertebrate terrestrialization

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.

The Amphibious Mudskipper: A Unique Model Bridging the Gap of Central Actions of Osmoregulatory Hormones Between Terrestrial and Aquatic Vertebrates

“…AT1 receptors have been cloned in teleosts including mudskippers ( Nishimura, 2017 ) although no expression study has demonstrated a calcium signal in the recombinant receptors ( Russell et al, 2001 ). AT1-like mRNA was not detected in the OVLT-like region of mudskippers, while many nuclei in the AP expressed the mRNA ( Katayama et al, 2018 ). AT2 receptors have been cloned in teleosts ( Nishimura, 2017 ), but AT2 mRNA was not detected in the eel brain ( Wong and Takei, 2013 ).…”

“…From the comparative point of view, it is intriguing to examine whether amphibious mudskippers have the mechanism inducing thirst as a motivation for drinking. Our recent study showed that peripheral or central administration of Ang II motivates the fish to move to water and to increase the volume of water ingested ( Katayama et al, 2018 ). An OVLT-like structure has been found histologically in the parvocellular preoptic nucleus (PP) of the mudskipper ( Hamasaki et al, 2016 ), but our histochemical study did not support the direct action of Ang II on this region.…”

“…Thus, AT1, not AT2, appears to mediate Ang II-induced drinking behavior also in teleosts. In mudskippers, Ang II, through its action on the AP, induced swallowing of buccal water, which is stored on land, and the loss of buccal water motivated mudskippers to move to water ( Figure 2B ; Katayama et al, 2018 ). Although regulation of the renin-angiotensin system has not been examined when mudskippers are on land, Ang II appears to induce drinking naturally in teleosts since an inhibitor of the renin-angiotensin system (captopril) attenuates spontaneous drinking ( Okawara et al, 1987 ; Perrott et al, 1992 ; Kobayashi and Takei, 1996 ).…”

“…Mudskippers, which evolved from the aquatic teleosts to invade the terrestrial environment ( You et al, 2014 ; Ord and Cooke, 2016 ), have developed the thirst-inducing mechanism by local sensation, in addition to the hormonal/anticipatory regulation of swallowing at the medulla oblongata observed in totally aquatic fishes ( Figures 2B,C ). Phylogenetically distant vertebrates (ray-finned fish and tetrapods) appear to have acquired the thirst sensation that elicits a series of drinking behaviors when they are exposed to a desiccating environment ( Katayama et al, 2018 ). From the evolutionary point of view, it is intriguing to examine possible thirst mechanisms of amphibious lungfish, which belong to the class Sarcopterygii and are recognized as the closest living relatives of tetrapods ( Brinkmann et al, 2004 ).…”

Neural populations for maintaining body fluid balance

“…Interestingly, studies in aquatic amphibious fishes revealed a unique system of Ang II-related thirst regulation. In mudskipper, Ang II stimulates the area postrema (AP), a hindbrain nucleus, to induce swallowing action [17,18]. Recent studies with contemporary neural manipulation tools have expanded our knowledge of thirst circuits at a finer resolution.…”