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

Lead Research Organisation: Zoological Soc London Inst of Zoology
Department Name: Institute of Zoology

Abstract

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 buy 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 competitiveness: 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. Public understanding of science: 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.

Publications

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Graystock, P (2014) The genetic basis of migration behaviour in Atlantic salmon - RADseq analyses. in iEOS2014 Omics Annual Conference

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Warren, I (2013) The genetic basis of migration behaviours in the Atlantic salmon in Population Genetics Annual Meeting

Related Projects

Project Reference Relationship Related To Start End Award Value
BB/H007105/1 01/03/2010 31/03/2013 £567,587
BB/H007105/2 Transfer BB/H007105/1 01/04/2013 31/12/2014 £256,162
 
Description Genome-wide and local gene duplication events have contributed to the ability of salmon to produce alternating phenotypes from the same genome. This study provides insights into the mechanism that facilitate migration and maintain its life history.
Exploitation Route These findings provide important fundamental science on the mechanisms underpinning the important, and sensitive life history of this economically important species.
Sectors Environment