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Involvement of Kisspeptin and Melatonin in the Seasonal Entrainment of Reproduction in European Sea Bass (Dicentrarchus Labrax)

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Involvement of Kisspeptin and Melatonin in the Seasonal Entrainment of Reproduction in European Sea Bass (Dicentrarchus Labrax) Involvement of kisspeptin and Melatonin in the seasonal entrainment of reproduction in European sea bass (Dicentrarchus labrax) RANIA FAHMY KHEDR ISMAIL JULY 2011 A THESIS SUBMITTED TO THE DEGREE OF DOCTOR OF PHILOSOPHY Institute of Aquaculture University of Stirling Declaration This thesis has been composed in its entirety by the candidate. Except where specifically acknowledged, the work described in this thesis has been conducted independently and has not been submitted for any other degree. Candidate name: ……………………………………………… Signature: ………………………………………………. Date: ……………………………………………… Supervisor name: ……………………………………………… Signature: ……………………………………………… Date: ……………………………………………… i Rania Ismail Abstract Abstract Aquaculture is an essential developing sector for world food production however one of the major bottlenecks for the sustainability of the aquaculture industry is the ability to control fish reproduction in captivity and to produce high quality seeds. European sea bass is a one of most commercially important species for the European fish farming industry. If broodstock management under captivity is well established, problems remain in hatcheries where survival can be low and deformity prevalence high as well as in on growing sites where fish reach puberty early especially with skewed sex ratio towards males. Sea bass displays strong seasonality in its physiology and is therefore an excellent candidate for the study of the photo-neuroendocrine control of reproduction and growth. The overall aims of this thesis were to better understand the molecular and endocrine drivers that control the Brain-Pituitary-Gonad axis in repeat spawner sea bass, and expand our knowledge of sea bass light and temperature regulation of melatonin production. First, this PhD project investigated the seasonal expression of kisspeptin, GnRH and gonadotropin genes in relation to the gonadal development throughout a reproductive cycle in male repeat spawning sea bass (Chapter 3). A partial sequence for the receptor kissr4 was isolated and described showing similarity to all other teleost species sequences available to date. QPCR molecular assays were validated to mesure the expression of a suite of genes along the BPG axis including kisspeptin related genes (Kiss1 and Kiss2 and its receptor kissr4) over a full reproductive cycle (12 months) in adult male European sea bass. Brain Kisspeptin mRNA expression levels (kiss1, 2 and kissr4) showed clear seasonal profiles and correlated well to other BPG markers (GnRHs, fshβ and lhβ), supporting a possible involvement of kisspeptin genes in the seasonal control of reproduction in repeat ii Rania Ismail Abstract spawning sea bass. Moreover, clear seasonal patterns were observed for expression of the genes encoding for pituitary mRNA expression of lhβ and fshβ, with a significant correlation between expression of both subunits and GSI and steroids levels. However, no clear seasonal profiles in brain GnRHs gene expression were observed with the exception to some peaks in GnRH1 and GnRH2. The second part of this PhD project investigated the potential direct effect of the two kisspeptin core peptides (kiss1 and kiss2) on the pituitary gonadotropin gene expression (Chapter 4). The aim of this work was to better understand the mechanism by which kisspeptin acts on the BPG axis. This was done by testing the kisspeptin decapeptide core sequences on the lhβ and fshβ transcript expression in primary culture of sea bass pituitary cells using QPCR technique. The findings, as a whole, provided evidence that kisspeptin can act directly on the pituitary gonadotroph cells and modulate fshß and lhß mRNA expression in sea bass although effects were limited and not uniform. Of note, kissr4 gene expression was also detected in the sea bass pituitary. The third part of this PhD project focused on the effects of environmental signals (photoperiod and temperature) on melatonin production (Chapter 5). Environmental manipulation is routinely used in the aquaculture industry with the purpose of enhancing growth and manipulating the timing of reproduction in seasonal fish species like sea bass. Melatonin, known as the light perception and time keeping hormone, has been suggested to play key roles in the synchronisation of most physiological functions in vertebrates, although the mechanisms by which melatonin controls reproduction, growth and behaviour are still not fully understood in fish. The studies performed aimed .to determine the synergistic effects of both temperature and photoperiod on the daily phase and amplitudinal changes in melatonin production through both in vivo and in vitro trials. The results iii Rania Ismail Abstract confirmed the diel melatonin rhythm in sea bass as previously reported in many teleost species with “high at night” and “low at day” melatonin profiles. Temperature showed clear effects on the amplitude of the melatonin production under both in vivo and in vitro conditions for both long day and short day photoperiods. Furthermore, no endogenous melatonin production was found under constant darkness in both in vivo and in vitro conditions. These results suggested a lack of intrapineal (or located elsewhere such as retina and/or deep brain) oscillators in sea bass, contrasting with previous reports. These results further enhance our knowledge of light perception and circadian rhythmicity in sea bass, while the circadian system remains to be characterised in sea bass and teleosts as a whole. Overall, this doctoral work broadened our understanding on the photoneuroendocrine control of reproduction in a seasonal fish species, sea bass. New knowledge gained and tools developed from this work should help to develop/optimise husbandry techniques for the sea bass farming industry with the view to increase production and profitability and thus promoting the sustainable expansion of the sea bass aquaculture in Europe. It has also the potential to help the fishery sector in the modelling of wild sea bass populations. iv Rania Ismail Acknowledgments Acknowledgments I would like to gratefully acknowledge the source of funding that made my PhD research possible. I was funded by a governmental scholarship from the Ministry of Higher Education and State for Scientific Research in Egypt. I would like to give my sincere thanks to my principal supervisor, Dr. Herve Migaud, for his supervision, guidance, help and for the thorough revision of my thesis. Dr. Andrew Davie has been an excellent second supervisor throughout the time of the present research. He was always eager to help when I encountered difficulties. I really think this work could have not been the same without their guidance and motivation. My sincere thanks are also due to Dr. John Taylor for his sincere help and essential lab training, statistical guidance and constructive comments. A very special ‘Thank You’ goes to Mrs. Fiona Muir, for her effective help and guidance during the time of the in vitro experiment. The invaluable cooperation from the staff at Machrihanish Marine Environmental Research Laboratory was highly appreciated. The hard times I faced while carrying out this research are heartily memorised and deeply appreciated, as these have added a lot to my practical experience. My stay in Scotland has been made enjoyable due to a lot of friends at the Institute of Aquaculture, University of Stirling. My warm and sincere thanks go to Eric Leclercq, Jan Heumann, Matteo Minghetti, Sean Monaghan, Sophie Fridman, and to all others with whom I shared hours in the office. A sincere and a very special ‘Thank You’ goes to Carlos Cristian Martinez for his effective help during the initial experimental steps of this research, to Mairi Cowan for her sincere cooperation during the sampling process and v Rania Ismail Acknowledgments in memory of hours on the road to and from Machrihanish, and finally to Amy Rajaee for her continuous support and encouragement. Above all, I feel a deep sense of gratitude to my parents and my sisters in Egypt. During more than four years of work my family gave me endless support and encouragement in order to attain, write and finish this research. Finally special thanks must go to my husband, Tarek, for his support and encouragement and help during the whole journey of my PhD specially the final stages of this work. vi Rania Ismail Contents Table of Contents Declaration ………………………………………………………………............. i Abstract ………………………………………………………………………….. ii Acknowledgements ……………………………………………………………… v Table of Contents ………………………………………………………………... vii List of Abbreviations ….…………………………………………………………. xii List of Species …………………………………………………………………… xiii List of Figures ……………………………………………………........................ xiv List of Tables …………………………………………………………….............. xix 1. General Introduction ……………………………………………………… 1 1.1. Overview of Sea bass life history and commercial exploitation……... 2 1.1.1. Taxonomy of European sea bass ……………………………….. 2 1.1.2. Life cycle of European sea bass …………………………........... 3 1.1.3. Geographical distribution and Commercial exploitation of sea bass ……………………………………………………………... 4 1.2. Environmental control of physiology in fish …………....................... 7 1.2.1. Photoperiod …………………………………………………….. 7 1.2.2. Temperature ……………………………………………………. 12 1.2.3. Food availability ………………………………………………... 12 1.2.4. Other factors ……………………………………………………. 13 1.3. The circadian axis: How light entrains physiology? …………............ 13 1.3.1. Melatonin synthesis and regulation …………………………….. 18 1.3.2. Melatonin biosynthesis and diel profile
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