Photic Entrainment and onset of puberty in Nile tilapia Oreochromis niloticus niloticus

Abstract

Despite teleosts being the largest and most diverse group of vertebrates, fish models currently used to study photoperiodic effects on fish physiology have been limited to a few species, most of which are temperate seasonal breeders. The overall aim of this work was to expand our knowledge on circadian biology and environmental physiological effects in Nile tilapia (Oreochromis niloticus niloticus), a continuous breeding species of tropical-subtropical origin. The circadian light axis of Nile tilapia is described with regards to melatonin production. Circadian melatonin profiles of fish under 12L:12D photoperiods were observed to be low at day and high at night, suggesting melatonin to be an entraining signal as observed in all other vertebrates. When constant light (LL) was used, such day and night fluctuations where abolished. However when fish where exposed to constant darkness (DD) a strong robust endogenous melatonin rhythm was found, suggesting the presence of circadian oscillators in this species. Importantly, this endogenous rhythm was observed to be maintained for at least three weeks under darkness and proved to be circadian in nature. Moreover, although the melatonin system was able to produce day and night melatonin rhythms when exposed to a different (6L:6D) photocycle, the oscillator appeared to not be entrainable to such a short photo cycle when exposed to DD, as melatonin levels remained high. When comparing the circadian organization of different teleost species including Nile tilapia, preliminary studies showed at least three divergent circadian light organizations in teleosts. Nile tilapia was characterised by a pineal gland far less sensitive than in other fish species as demonstrated through in vitro studies. Furthermore, pineal melatonin production was clearly dependent on the light perceived by the eyes as ophthalmectomy resulted in basal plasma melatonin levels during the dark period. These findings are the first to be reported in a teleost and could be comparable to the circadian light organization of higher vertebrates such as mammals. The onset of puberty of Nile tilapia was studied with regards to the newly discovered Kiss1/GPR54 system. Such a system has recently been discovered in mammals and found to be the primary switch of the brain-pituitary-gonadal (BPG) axis. The results of this study not only suggest a link between the Kiss1/GPR54 system and the onset of III puberty in this tropical batch spawning teleost, that would be a highly conserved feature across vertebrates, but also that the transcriptional mechanisms regulating GPR54 expression could be directly or indirectly influenced by light. Finally, a study was conducted on the effects of different intensities of continuous light (LL) on the growth and sexual development of Nile tilapia up to first maturation. The results showed a significant growth response of fish in all LL treatments compared to control fish. Importantly, this confirmed that LL enhances growth in this species and suggests that it is the light regime more than the intensity which is having an effect. This work thus provides important basic knowledge of the light entrainment pathway and circadian melatonin rhythms in Nile tilapia. Of special importance is the discovery of a strong endogenous melatonin oscillator and a novel circadian organization in fish which would seem to be homologous to that observed in higher vertebrates. Moreover, this work provides evidence that the newly discovered Kiss1/GPR54 system has a similar role in fish as has been found in mammals and that such a system could be directly or indirectly regulated by light. If so, Nile tilapia and other fish species could become important models in the chronobiology and reproduction fields. Finally, this work not only increases our basic and applied knowledge of this species, but also broadens our understanding of the circadian light axis in teleosts and its mediatory effects on reproduction.