The physiological and genomic basis to the timing of life history transitions in the Atlantic salmon

Lead Research Organisation: University of Aberdeen
Department Name: Inst of Biological and Environmental Sci


In migratory Atlantic salmon, the process whereby young fish born in freshwater streams (parr) become migratory 'smolts' and go to sea represents a crucial life-history transition, involving complex behavioural and physiological changes. Most mysterious amongst these is the acquisition of an olfactory 'imprint' of the natal stream, prior to smolt migration, upon which return as adults later depends. Similarly the neural and neuroendocrine events governing the precise spring timing of the parr-smolt transition (PST) are also very poorly understood. Hence practical definition of the smolt phenotype is largely based on behaviour or unreliable gross traits such as 'silverness', manifest long after the process has been initiated. Molecular physiological and genetic understanding of these processes is potentially of major value for management of wild and farmed Atlantic populations. This project will take a multi-pronged approach to address this problem, capitalising on a unique combination of expertises and resources. Using parr reared in semi-natural conditions at the Scottish Office, Fisheries Research Services (FRS) facility at Almondbank & in dedicated photoperiod / temperature controlled aquaria at the University of Aberdeen, we will (a) assess the expression patterns of key elements of the neuroendocrine system recently shown to play a key role in driving seasonal changes in physiology in other vertebrate groups, but so far unexplored in fish and (b) use new generation ultra-high throughput sequencing methods to generate genome wide profiles of gene expression in the hypothalamus/pituitary and the olfactory epithelium during the PST. Together these approaches will yield candidate genes for upstream regulators of key neural aspects of PST, and begin to address the question of extent to which changes in the neuroendocrine system drive or parallel changes in the olfactory epithelium. In further experiments, the expression of these genes will be assessed during PST in fish from high and lowland streams, which show distinctive timing of PST. This will allow us to define the molecular events in both the neuroendocrine and olfactory systems through which differential timing of migratory behaviour and physiology develops. Collectively these studies will greatly advance understanding of the neurobiology of PST.

Technical Summary

The control of the timing of the life history transition of juvenile salmon from a non-migratory form (parr) to smolts which migrate to the sea is under photoperiodic and genetic control. Different populations of salmon show variable timing of this parr-smolt transition (PST), with ecologically important consequences. The process of PST depends crucially on changes in the neuroendocrine and olfactory systems, which remain poorly understood. We will examine transcriptional responses in both the hypothalamus and olfactory epithelium in juvenile salmon held artificial and semi-artificial conditions. Under Objective 1, using in situ hybridisation and neuroanatomical procedures, we will test the explicit hypothesis that local changes in hypothalamic deiodinase expression, analogous to those in birds and mammals, are intrinsic to photoperiodic induction of PST. Under Objective 2 we will use Roche 454 and Illumina SOLEXA sequencing to perform a transcriptomic analysis of hypothalamic and olfactory changes in gene expression in juvenile salmon transferred from short to long photoperiods. This and subsequent qPCR or in situ hybridisation experiments will build a list of candidate timing genes for the control of PST, and will allow us to resolve whether changes in olfactory epithelial function run in parallel or subsequent to changes in the neuroendocrine system. Under Objective 3 we will apply this list to a comparative experiment in which early and late migrating lines of salmon are exposed to progressively increasing photoperiods under controlled conditions. Hence we will identify genes whose differential expression underlies differential timing of PST. These experiments will provide new insights into photoperiodic timing mechanisms in teleosts in general, and will form a foundation, along with the pending completion of the salmon genome, to improve management strategies for wild and farmed populations.

Planned Impact

The Atlantic salmon is the most mysterious fish inhabiting the UK waters and for generations has intrigued both academic and general public alike. The wild salmon fishery whilst still of high economic importance to the Scottish economy has been superseded by the salmon aquaculture industry which now is second only to beef for agricultural export from Scotland. This project will impact on 4 major stakeholder groups. Wild fish interests: The salmon that migrate back to fresh water in the spring described as spring salmon have shown a major decrease in abundance in recent decades, these are the most valued part of the salmon stock with regard to the tourism industry. This project will help understand how different populations of salmon uniquely adapted to their environment. Our findings will give insights that allow hatchery rearing of fish for restocking that are better matched to stream environments into which they are released. Aquaculture interests: The control of life history changes is central to the efficient production of salmon, although sea water tolerance can be achieved by photoperiod manipulation the underlying mechanisms are poorly understood. We anticipate that the fundamental genetic mechanisms underlying these influences will in part be common to those controlling smolting, and that by characterising these we may provide new foci for selection and management strategies to maximise the efficiency of farmed fish production. Further, these insights are likely to extend to many other important aquaculture species. UK Scientific community: The UK currently supports several world-leading groups working on timing mechanisms in mammals and birds, but is relatively weak in other vertebrate groups. Broadening the UK portfolio to encompass the teleosts will further enhance UK scientific competitiveness in the general area of timing, and increase capacity to consider this subject from evolutionary and environmental perspectives. The General Public: The wider public community will be engaged through links between the PI's and charitable foundations including the Atlantic Salmon Trust, the Salmon and Trout Association and Scottish Natural Heritage.


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Description During the parr smolt transformation, when you salmon are preparing to migrate to the ocean the thyroid system is activated. Central to this is the conversion of inactive thyroxine (T4) to active T3, this occurs by removal of an iodine molecule by enzymes called deiodinases. We showed that two genes are present in salmon that encode the deiodinase 2 gene. One of these is expressed in the brain and responds to photoperiod changes, whereas the second copy is activated in the gill tissue following transfer to saltwater. This has led to greater insights to seasonal biology in vertebrates, as this is first time such changes have been observed in fish.
Exploitation Route 1. The basic finding of set the scene for future research to define the life history strategies of salmon from different regions of their natural range.
2. The information can be utilised by the aquaculture industry to ensure the salmon are fully prepared for transfer from fresh to salt water.
Sectors Agriculture, Food and Drink,Environment

Description A follow on grant to this has been fund by the Norwegian Research Council "Light and salt". University of Aberdeen are partners on this project and will be directly involved in determining how anadromous and non anadromous species of salmonids have genetically diverged, especially in genes relating to migration and sea water adapation. The parr smolt transformation is a key phase in the farmingof Atlantic salmon. In recent years there have been many changes in the production of salmon smolts, in parallel to this there have been increasing problems with gill health in salmon during the marine phase of farming. The outputs of this project are now being applied to new research projects more directly related to aquaculture production.
First Year Of Impact 2018
Sector Agriculture, Food and Drink,Environment
Impact Types Societal

Description ROBUST-SMOLT Impact of early life history in freshwater Recirculation Aquaculture Systems on A. salmon robustness and susceptibility to disease at sea
Amount £200,000 (GBP)
Funding ID BB/S004270/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 01/2019 
End 12/2021
Title Microarray for Atlantic salmon 
Description We have used microarray for gene expression in Atlantic salmon to understand the gen expression responses between different life history stages. We have fully reannaotated the microarray to make down stream data analysis much better. To do this we associated each gene feature on the microarray with a human protein identifier, allowing programs such as DAVID and KEGG analysis to be used. 
Type Of Material Biological samples 
Year Produced 2011 
Provided To Others? Yes  
Impact papers in preparation 
Title RNAseq 
Description We have used RNAseq to examine the differences in gene expression during early life history changes in Atlantic salmon. We have preformed RNAseq on both pituitary and hypothalamus from salmon smolts. Analysis for this is still underway. 
Type Of Material Biological samples 
Provided To Others? No  
Impact We have been developing a comprehensive Atlantic salmon transcriptome which will be of use for others working in the field, but it is not fully completed. 
Title Atlantic salmon transcriptome for brain, pituitary and olfactory epithelium 
Description We carried out a transcriptome analysis of tissues in salmon believed to be important in decision making for migration. We used juvenile Atlantic salmon and performed a 454 sequencing approach. All sequences are deposited in NCBI database and a paper has been published. 
Type Of Material Database/Collection of data 
Year Produced 2014 
Provided To Others? Yes  
Impact This will be further used when annotating the recently released Atlantic salmon genome. 
Description Dr Aleksei Krasnov 
Organisation NOFIMA Ås
Country Norway 
Sector Private 
PI Contribution Development of tools for assessment of the immune competence of Atlantic salmon smolts and growers (Forskerprosjekt - HAVBRUK2)
Collaborator Contribution Development of tools for assessment of the immune competence of Atlantic salmon smolts and growers (Forskerprosjekt - HAVBRUK2
Impact Project just started no outputs yet
Start Year 2017
Description Professor D Hazlerigg 
Organisation University of Tromso
Country Norway 
Sector Academic/University 
PI Contribution Prof Hazlerigg was PI on the grant until November 2013 when he relocated to University of Tromso. We have continued to work together on the grant and Prof Hazlerigg has provided additional biological material for research directly on the grant.
Collaborator Contribution Data analysis and manuscript preparation.
Impact No Outcomes to date
Start Year 2013
Description European Aquaculture Society, Aquaculture Europe, 20-23rd September 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Oral Conference presentation
E. Antonopoulou, K. A. Kormas, S. Chatzifotis, G. Piccolo, L. Gasco, SAM. Martin and E. Mente
European Aquaculture Society, Aquaculture Europe, 20-23rd September 2016
Year(s) Of Engagement Activity 2016
Description Rivers and Angling Trusts of Scotrland 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Rivers and Angling Trusts for Scotland help manage many river systems in Scotland with emphasis on biological diversity of the river catchments. Our BBSRC project is targeted at understanding the control of migration of Atlantic salmon from Freshwater to salt water environment. We have discussed our finding from the project with various river trusts and also at a more international level.

Potential future projects / studentsips
Year(s) Of Engagement Activity 2011