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Genomics and the Mystery of the Fraser River Sockeye

The Fraser River sockeye salmon is a denizen of two very different worlds. The first year of its four-year life cycle is spent in its freshwater birthplace, after which the salmon migrates out to sea to roam the deep ocean and grow to maturity. Then the salmon returns to its freshwater home, fighting its way upstream against tremendous odds, so that it can spawn and die.

There are about 90 spawning populations of sockeye in the Fraser, and each population faithfully returns to its birthplace to spawn at the same time every year (spring, early summer, summer, or fall). This phenomenon has occurred like precision clockwork for thousands of years with, in a good year, about fifteen million salmon returning to spawn in the Fraser and its tributaries.

One of the most important migrations is the late-run (fall) salmon, which historically re-enter the river in late September – all two to five million of them. In the past decade, however, there has been a worrisome shift in their return migration schedules. In some years, the late-run salmon have entered the Fraser a full four to six weeks earlier than usual, making their migration up the river during periods of peak water temperatures that they are not adapted to, with as many as 95% dying before spawning. This has had a devastating effect on fish conservation and fish stock management in the Fraser. Predicting fish numbers to set quotas, which is done on a stock-by-stock basis using all sorts of variables, is a challenging task at the best of times. Changing conditions make it even more difficult.

Given that the Fraser is one of the world’s most significant salmon rivers and that it supports an economically important fishery, there was an understandable urgency attached to getting to the bottom of this mystery of shifting migration schedules and mass mortality. As well, there was a clear need, in light of the mounting evidence of global warming, to develop tools that would help fishery managers do their job under changing conditions. Little wonder then that a team of scientists has been bringing an array of research to bear on these problems for almost a decade – and, since 2003, they have included genomics techniques that are so cutting edge that they are practically being invented on the spot.

Kristi Miller, a research scientist with Fisheries and Oceans Canada (DFO), is part of the team. Other members come from universities (British Columbia and Carleton), other sections of DFO, and industry (LGL Ltd., and Kintama Research), with funding from CBS Genomics, the Pacific Salmon Commission and NSERC. Miller heads the Molecular Genetics group at DFO’s Pacific Biological Station in Nanaimo, British Columbia, and they are working to develop and apply genetic and genomic tools in ways that aid and support conservation-based fisheries management. As Miller explains, “Genetic tools have been in use for about 15 years and are in high demand, but genomics is the new area and it is really booming. Why? Because while genetics research allows you to look at a few different markers at a time, genomics lets you look at thousands.” To illustrate the immensity of scale possible, the DFO group works with genomic salmon microarrays, which are microscope slides each containing an incredible 16,000 genes spotted onto their surface, and this capability is growing.

Microarrays, contrary to their name, are immense data sets, currently able to hold 16,000 gene transcripts for wild salmon. They were originally developed with human genes to classify sarcoma types in humans.

Deciphering the mystery of the Fraser River salmon deaths and migration schedule shift has been no easy task, but new technologies that enable a broad-scale, genome-wide profiling have helped put together a detailed understanding of the physiological changes and constraints associated with spawning migration. The salmon basically have to reconfigure themselves at the molecular level for freshwater conditions, and late-run sockeye have historically spent three to six weeks sitting off the mouth of the Fraser while this happens. To study the transformation in action, Miller looked at gene expression in brain, liver and gill tissue samples from salmon at various stages of this retooling process. She says the results from the brain tissue were as clear-cut as if someone had flipped a switch. The brain is the control centre for a vast array of physiological processes, but in migratory salmon, the control of reproductive maturation, cognitive memory for homing, and sensory development are of primary interest, and these processes are changing simultaneously as salmon migrate.

Late-run sockeye salmon stop feeding anywhere between 600 to 1,000 km before they reach the Fraser. They must digest their own tissue for the energy needed for the remaining one to two months before they spawn and die – and some run out of energy before they make it to spawning grounds. The metabolic shifts associated with starvation can be observed by profiling gene expression in the liver such that individual fish can be energetically evaluated and classified. However, unlike brain and liver, gill tissue can be sampled without killing the fish, which makes this the most valuable tissue of all. Gill tissue is the first to respond to environmental changes, including salinity, pathogens, toxins and oxygen. Researchers can combine the evaluation of gill physiology and migration fate by tracking the movement of fish, which have been caught, sampled and fitted with a radio transmitting tag in the ocean, all the way back to their spawning grounds. It is the gill tissue that has provided valuable insights linking freshwater preparedness in the ocean to survival in the river.

The end result is that the team has been able to confirm that many of the early migrating fish that died before reaching their spawning grounds had not completed their cellular remodelling to prepare for freshwater prior to entering the river, thus making them more prone to stress and disease. The double whammy was that their early entry time meant river temperatures were up to five degrees higher than they would normally experience, thus increasing their stress levels, energetic demands and impacts of freshwater pathogens and parasites. The environmental triggers, however, that pushed the fish up the river ahead of schedule are still not fully understood.

A really important outcome of the research is the identification of a number of fitness predictive biomarkers for the salmon. Indeed, Miller sees physiology and fitness as becoming key factors in stock assessment models of the future. The development of predictive biomarkers is going to be extremely valuable. They will potentially enable fishery managers to predict freshwater entry timing of fish undergoing spawning migrations and to forecast fish with poor fitness characteristics, and, as a result, to determine those more predisposed to die en route to their spawning grounds, given adverse river conditions. All in all, this means they will be able to make more confident decisions about opening or closing the fishery.

And what about the future? DNA provides accurate, reliable and precise estimates of stock composition, and Miller’s group can currently carry out this analysis on an 18-hour turnaround. But these are still early days. She predicts that a wave of new genomics tools are going to be developed that will change dramatically the way we understand, predict and manage our wild resources, especially in the context of global warming changes. Happily, we are very much at the forefront of the wave. As it stands, Canada is the only country in the world already managing its fisheries using genetic tools in a real-time context.

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