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Thesis.Pdf (8.850Mb) Faculty of Biosciences, Fisheries and Economics Photoperiodic history-dependent preadaptation of the smolting gill Novel players and SW immediate response as markers of growth and welfare Marianne Iversen A dissertation for the degree of Philosophiae Doctor, December 2020 Photoperiodic history-dependent preadaptation of the smolting gill Novel players and SW immediate response as markers of growth and welfare Marianne Iversen A dissertation for the degree of Philosophia Doctor December 2020 UiT - The Arctic University of Norway Faculty of Biosciences, Fisheries and Economics Department of Arctic and Marine Biology Arctic Chronobiology and Physiology Research Group Front page image: Juvenile salmon showing the transition from parr (bottom) to smolt (top). Photo by Barbara Tomotani. List of contents I. Acknowledgements ......................................................................................................................... I II. Thesis Abstract ................................................................................................................................ II III. List of papers.................................................................................................................................. III IV. Abbreviations ................................................................................................................................. IV 1. Introduction .................................................................................................................................... 1 1.1 The Atlantic salmon –evolution and life history ...................................................................... 2 1.1.1 The salmonid-specific whole genome duplication .......................................................... 3 1.1.2 Evolution of anadromy and species radiation ................................................................. 4 1.1.3 Life history of Atlantic salmon ......................................................................................... 6 1.2 Chronobiology of fishes ........................................................................................................... 9 1.2.1 Biological clocks ............................................................................................................. 10 1.2.2 Circannual rhythms ....................................................................................................... 10 1.2.3 The light-brain-pituitary axis of teleosts ....................................................................... 13 1.3 Gill function in FW and SW –opposing forces ....................................................................... 15 1.3.1 Gill physiology................................................................................................................ 17 1.3.2 Osmoregulation in freshwater ...................................................................................... 18 1.3.3 Osmoregulation in saltwater ......................................................................................... 19 1.3.4 Osmosensing and responses to osmotic stress ............................................................. 20 1.4 Photoperiodic and hormonal control of smolting ................................................................. 24 1.4.1 The light-brain-pituitary axis during smoltification ....................................................... 25 1.4.2 General physiological changes during smoltification .................................................... 28 1.4.3 Structural and cellular changes to gill physiology during smoltification ....................... 30 2. Aims of the study .......................................................................................................................... 33 3. Summary of papers ....................................................................................................................... 34 4. Transcriptomics data can provide further insight into smolting .................................................. 38 5. Discussion of main findings .......................................................................................................... 43 5.1 Novel genes linked to smolting ............................................................................................. 43 5.2 Role of photoperiodic history-dependence in smolting and adaptation of the gill .............. 45 5.3 Diversified clock genes involved in the regulation of smolting and SW adaptation ............. 47 5.4 Regulation of NKA activity ..................................................................................................... 48 5.4.1 Regulation of NKA and its constituents during smolting ............................................... 48 5.4.2 Are deiodinases a part of the NKA regulatory system? ................................................ 49 5.5 Experimental design .............................................................................................................. 51 5.6 Future perspectives ............................................................................................................... 52 5.7 Concluding remarks ............................................................................................................... 53 6. References .................................................................................................................................... 54 7. Appendix ....................................................................................................................................... 82 I. Acknowledgements Finally, it is done. It’s been a long and winding road where I have experienced and learned a lot, both about salmon and about myself. I’d like to thank those communities that I have been part of during this time. My friends and colleagues at UiT, both new and old. The professors, researchers, post-docs, technicians and fellow phd-students that I shared my time with at the Arctic Chronobiology and Physiology research group deserve a special mention, you are all brilliant! Thank you to my friends found around various UiT departments and research institutions. You have provided interesting discussion about all and nothing during those occasional long lunch breaks. Thank you to the sporting dog communities in Tromsø, for making me focus solely on my dog during training, providing that much needed thesis- free space. Thank you to my always-up-for-fun-dog Kajsa for providing relaxing hikes and bringing enthusiasm to everything we do. Thank you to my family, my parents, and my wonderful husband for always being there for me, patient, understanding and loving. I would like to make a special dedication to my aunt Arna, whom sadly passed this December. Since I moved to Tromsø as a young student we became very close, and I will surely miss her a lot. Finally, to my supervisors David and Even, thank you for seeing this through with me. I II. Thesis Abstract This thesis presents a rich introduction to the evolution, life history and physiology of Atlantic salmon, with a special emphasis on the developmental transitions (termed smolting) juvenile salmon pass through has they prepare to migrate from their native freshwater habitat to the sea. The introduction provides a comprehensive background on chronobiology and osmoregulation in fishes and links this to the process of smolting as it has been described in literature. Further, this thesis contributes three papers to the standing literature on Atlantic salmon, salmonids and smolting. Paper I focuses on the role of photoperiod history for smolting and pre-adaptation to saltwater to occur in a coordinated and organized manner, and presents results showing photoperiod history ultimately influences saltwater growth. The paper presents data on previously unstudied genes in the context of salmonids and pre-adaptation to saltwater indicating that they could be important for predicting SW-tolerance in juvenile salmon. Paper II further illustrates the importance of photoperiod stimuli to drive smolting and preadaptation to saltwater. The data presented in paper II show clear differences in the response to saltwater between different photoperiod treatments. Not only in the number of responsive genes but also in the group of genes whose expression was influenced by saltwater exposure. Saltwater-responsive genes in the two treatments designed not to bring forth a saltwater-adapted juvenile were enriched for promoter motifs linked with a general stress response and osmoregulatory stress. The third paper focused on the temporal and spatial expression of the so-called clock genes in salmon, also smolting. One of the main findings of this paper is that many clock genes derived from the fourth salmon specific whole genome duplication have tissue-specific expression profiles, and that their regulation in the gill correlates with smolting. The main findings of these papers are presented and discussed together with insights from literature and unpublished data derived from the same datasets presented in the papers. II III. List of papers Paper I RNA profiling identifies novel, photoperiod-history dependent markers associated with enhanced saltwater performance in juvenile Atlantic salmon Marianne Iversen1, Teshome Mulugeta2, Børge Gellein Blikeng1#, Alexander West1, Even Jørgensen1, Simen Rød Sandven3 and David Hazlerigg 1 1Department of Arctic and Marine Biology, UiT -The Arctic University of Norway, Tromsø NO-9037, Norway, 2Department of Animal and Aquaculture
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