The Emerging Scientific Debate on Frankenfish

Subject: Will souped up salmon sink or swim?
Nature 06 July 2000 (UK)
Tony Reichhardt writes from Washington for Nature

A company in Massachusetts is seeking permission to market salmon
genetically modified to grow faster than normal. Tony Reichhardt explores
the potential ecological risks, should the fish escape from salmon farms.

Michael Roggo/Still pictures and aqua bounty farms

Scaled up: the effects of growth-hormone genes (right) may find use in fish
farms (above).

A few years ago, when Garth Fletcher's office telephone rang, it was
usually another scientist wanting to talk about aquaculture or fish
genetics. Nowadays, it is just as likely to be a news reporter asking
barbed questions about 'Frankenfish'. "We're getting hit every day in the
press," he says.

Fletcher is president of the Canadian arm of Aqua Bounty Farms, a company
based in Waltham, Massachusetts, that hopes to bring genetically modified
(GM) salmon to the dinner plates of North America. At the company's
experimental hatchery on Canada's Prince Edward Island, its aquaculturists
are raising Atlantic salmon (Salmo salar) modified to carry a
growth-hormone gene from the Pacific chinook salmon (Oncorhynchus
tshawytscha), which is hooked to a powerful promoter sequence. This boosts
the fishes' growth rate, so that they reach market size quicker(1).

Aqua Bounty Farms, formerly a subsidiary of the company A/F Protein, has
applied to the US Food and Drug Administration (FDA) for permission to
market its salmon. And ever since this application was picked up by the
media, the company has been plunged into the thick of the controversy
surrounding GM foods ó which, after a slow start compared with the furore
in Europe, is now beginning to register in North America. Some ecologists
have even warned that transgenic salmon could wipe out natural populations
of related fish should they escape into the wild.

So far, the only things that have been wiped out are the business plans of
two companies that licensed A/F Protein's gene-insertion technology in the
1990s. Both Otter Ferry Salmon in Scotland and the New Zealand King Salmon
Company scrapped their GM salmon research after unfavourable publicity. But
with Aqua Bounty Farms still pressing ahead, ecologists warn that the
current state of scientific knowledge is inadequate to provide a full
assessment of the risks posed by the company's fish. "There's just so much
speculation compared to the amount of data," says Robert Devlin, a
researcher with Canada's Department of Fisheries and Oceans, based in West
Vancouver. Much of the research only started in the past decade. Because it
can take 10 years to produce a stable line of transgenic salmon, says
Devlin, the dearth of experimental studies is hardly surprising.

Research on transgenic strains is currently under way for some 35 species
of fish worldwide, including Pacific salmon such as the chinook and coho (
Oncorhynchus kisutch), various other members of the salmonid family, and
other economically important fish including catfish and tilapia. Most of
the work is being done by commercial fisheries and involves growth-hormone
genes.

The one certainty is that conventionally farmed salmon, typically raised in
netted pens in shallow coastal waters, will escape. Where there are salmon
farms, farmed fish tend to turn up in salmon streams ó in some cases
outnumbering their wild counterparts. In western Canada and in Washington
state, south of the US border, ecologists are becoming particularly
concerned about the effects of escaping Atlantic salmon ó which number
tens, if not hundreds, of thousands ó on already declining Pacific salmon
populations.

The salmon run.
Whether transgenic salmon pose a special risk is uncertain, but the
potential problems are clear enough. One worry is that escaped GM fish will
breed with their wild counterparts and release their added growth-hormone
genes into wild populations, with unpredictable consequences. Proponents of
the technology counter that it is possible to make the transgenic fish
sterile ó and if Aqua Bounty Farms' Atlantic salmon were farmed off the
Pacific coast of British Columbia and the northwest United States, they
would be unlikely to breed successfully with native Pacific salmon species.

Even if fast-growing GM fish do not spread their genes to their wild
counterparts, they could disrupt the ecology of salmon streams by competing
with native fish for resources. The consequences will depend on many
factors, including the health of the local population, the number and
specific genetic strain of the escaped fish, and the local environment.

WILLIAM MUIR

Trojan genes: Muir's research has raised fears that wild salmon may be
decimated by GM fish.

On the question of interbreeding, alarming results have come from
laboratory studies conducted by William Muir and Richard Howard of Purdue
University in West Lafayette, Indiana. Using the fast-breeding Japanese
medaka (Oryzias latipes) as an experimental model, Muir and Howard looked
at the role of size in mating success, and found that big medaka males had
a fourfold advantage over their smaller competitors.

The researchers then compared the viability of normal medaka with another
group to which they had added a human growth-hormone gene. Under aquarium
conditions, the fast-growing GM fish were 30% more likely to die before
reaching sexual maturity. The final step was to plug these and other
results into a computer to model to see what would happen when 60
transgenic fish were introduced into a population of 60,000 wild medaka.
The results were disturbing. It took only 40 generations for the GM fish,
which mated more successfully but produced offspring that did not survive
as well, to drive the population to extinction. Muir and Howard called it
the "Trojan gene effect"(2).

The Purdue researchers stressed that their results should be treated with
caution. Among other things, the dire prediction of population extinction
assumed that mature transgenic fish would be bigger than their wild
counterparts ó whereas the human growth-hormone gene only increased the
medaka's juvenile growth rate, and produced adult fish no bigger than
average. Muir has since been experimenting with the gene for a salmon
growth hormone and has found that it can make adult medaka grow up to 50%
larger than normal. The viability of these fish was even worse ó their
survival to sexual maturity was reduced by as much as 78% compared with
wild-type medaka, which suggests that they could wipe out a wild population
very quickly. These results have yet to be published, but make the Trojan
gene seem like a real threat if the techniques used to make GM fish sterile
prove less than 100% reliable.

Shock treatment
Creating sterile salmon is relatively simple. If salmon eggs are subjected
to a heat or pressure shock shortly after fertilization, they retain an
extra set of chromosomes, ending up with three sets, rather than the normal
two. The resulting 'triploid' fish do not develop normal sexual
characteristics, and the females are sterile. It is also possible to raise
female salmon as fertile males by treating them with male sex hormones. So
by using these 'sex reversed' males ó which will be able to produce only
female offspring ó as breeding stock, and applying a pressure shock to the
eggs that they fertilize, it should be possible to raise GM salmon that
consist entirely of sterile, triploid females.

Fletcher argues that skilled aquaculturists can apply this method
unerringly, but other scientists are less confident. "Even when you're
pretty good at it, you get a lot of batch to batch variation," argues Anne
Kapuscinski, a specialist in biotechnology and aquaculture at the
University of Minnesota in St Paul.

A growing problem?
But even if sterility cannot be guaranteed, will Aqua Bounty Farms' salmon
grow into oversized adults that have an advantage in the mating game? That
is the "million dollar question", says Kapuscinski. Commercial fish farmers
are only interested in having salmon that grow to market size faster, and
Fletcher says the company's studies have found "zero evidence" that the
transgenic salmon are bigger after they reach sexual maturity. But other
scientists point out that these results have not been published in the
peer-reviewed literature. "No one outside of their circle has seen those
data,' complains Eric Hallerman, a fisheries biologist at the Virginia
Polytechnic Institute in Blacksburg.

Devlin, who has raised growth-enhanced transgenic coho salmon in the lab,
finds that they are about 50% larger at sexual maturity than their wild
counterparts. But that may in part reflect the difference between cosy lab
conditions and the harsh natural environment. The key test is to grow
transgenic and wild-type fish under identical conditions. When scientists
at the Center for Genetic Engineering and Biotechnology in Havana, Cuba,
conducted such experiments with GM tilapia, the genetically engineered fish
grew up to twice as large at maturity as non-transgenic fish(3). So far, no
one has published this type of experiment with salmon.

Studies addressing the ability of transgenic salmon to disrupt ecosystems
irrespective of their ability to interbreed with wild populations have
yielded similarly inconclusive results. Devlin and his colleagues, for
instance, have found that growth-enhanced transgenic coho salmon eat nearly
three times as much food as their natural counterparts under laboratory
conditions(4) their elevated growth-hormone levels appear to make them
hungrier. Whether this would hold true in the wild is uncertain. But if so,
the transgenic fish, which also mature faster, could be foraging ravenously
at times when natural food availability in a particular stream is low,
which could seriously disrupt its ecology.

Arnold Sutterlin of Aqua Bounty Farms, working with Mark Abrahams of the
University of Manitoba in Winnepeg, has conducted similar experiments with
growth-enhanced Atlantic salmon. Again, the fish were hungrier, but they
were also less careful about avoiding predators ó judged by experiments in
which young fish had to get their food from a portion of a tank containing
a large trout(5). This, together with the observation that young transgenic
Atlantic salmon appear to have less effective camouflage, should mean that
they are less likely to survive in the wild, minimizing the ecological
damage that escaping fish might cause.

Devlin and his colleagues also report that their transgenic coho are slower
swimmers(6). But Aqua Bounty Farms' scientists have found that the GM
Atlantic salmon appear more active than the wild-type fish(5), (7). These
varying results may reflect the different species being studied, or just
the strain-to-strain variations caused by the vagaries of transgenic
technology. Depending on where exactly the extra genes are incorporated
into the fish genome, they can exert subtly different effects. For example,
although Muir's experiments with a salmon growth-hormone gene in medaka
showed that survival to sexual maturity was depressed by up to 78%, in some
strains the figure was only 40%. To conduct an accurate environmental risk
assessment for GM fish, he says, you need to evaluate each genetic line
individually. "We're not sure of all the reasons why," says Muir, "but
every transgenic founder is unique."

To Devlin, the catalogue of scientific uncertainties shows why more
research is desperately needed. And it will not come cheap. "These are not
small experiments," he says. "When you're talking about raising a family of
transgenic fish, it's not a vial. It's large tanks." Muir would start by
conducting aquarium experiments to test how transgenic fish compare with
normal fish over a range of parameters related to their biological
'fitness'. In the manner of his medaka experiments, he would then generate
a computer model to consider the likely impact of the fish in wild
populations. To this Devlin would add laboratory studies that simulate
stream conditions. Even better, says ecologist Jeff Hutchings of Dalhousie
University in Halifax, Nova Scotia, would be to conduct tests in the wild,
blocking off a portion of a stream to prevent fish escaping into a larger
aquatic system. Whether it would be feasible to isolate streams in this way
is unclear ó and any experiment involving the deliberate environmental
release of a transgenic animal is likely to prove highly controversial.

The FDA is still considering Aqua Bounty Farms' application to market its
transgenic salmon, and has yet to clarify the experiments it wants to see
conducted before deciding whether to approve the fish. The FDA's main task
is to examine whether transgenic salmon are fit for human consumption, and
whether the fishes' own welfare is compromised by the addition of
growth-hormone genes. But the agency is also charged with assessing the
environmental impact of the fish, and so it is consulting with two other US
government agencies, the Fish and Wildlife Service and the National Marine
Fisheries Service.

Given the uncertainties, many ecologists argue that a 'safety first'
approach is essential. Kapuscinski would even go so far as to demand that
transgenic salmon should be raised in isolated artificial ponds, so they
cannot escape to the wild.

Swimming against the tide
Still pictures and BBC natural history

Coming ashore: concerns about damage to wild salmon (left) may force fish
farms inland (above).

For salmon farmers, such measures would impose economic penalties. Because
they reach market size faster, Aqua Bounty Farms has touted its GM fish as
being superior in terms of 'feed conversion' ó how much it costs to feed
them while they are being raised. But Fletcher is cautious about putting
any firm figures on this. And the advantage would have to be large to
counter the costs of the measures suggested by Kapuscinski.

Aqua Bounty Farms is assuming that the FDA will demand it raises only
sterile, female triploid fish. Individual screening for sterility is
relatively cheap, costing only 20 cents per fish, claims Kapuscinski. But
any regulations preventing GM salmon from being raised in coastal waters
would pose problems. Production of Atlantic salmon is presently conducted
almost exclusively in sea pens. Unless the performance of transgenic salmon
becomes truly remarkable, Fletcher believes it is unlikely that a sizeable
portion of the industry would switch to contained land-based, pumped
systems given their high capital and operating costs.

But Elliot Entis, chief executive officer of Aqua Bounty Farms, takes a
more sanguine view. Even if the FDA imposed a ban on the rearing of
growth-enhanced GM salmon in coastal net pens, he believes the transgenic
fish could become a viable economic proposition in the long term. The UN
Food and Agriculture Organization predicts that global aquacultural
production will more than double over the coming decade. Given that coastal
aquaculture is already causing ecological damage, by spreading fish
diseases, modifying habitats, causing nutrient pollution, and through the
escape of exotic farmed fish (8), Entis believes regulators may eventually
demand that fish farms move from coastal pens to contained ponds. "A lot of
salmon farming is going to move inland regardless," he says. If so, argues
Entis, fast-growing transgenic salmon might be just what the industry needs
to remain economically competitive.

References 1. Hew, C. L., Fletcher, G. L. & Davies, P. L. J. Fish Biol.
Suppl. A 47, 1-19 (1995).
2. Muir, W. M. & Howard, R. D. Proc. Natl Acad. Sci. USA 96, 13853-13856
(1999). Links
3. de la Fuente, J., Guillen, I., Martinez, R. & Estrada, M. P. Genet.
Anal. Biomol. Eng. 15, 85-90 (1999).
4. Devlin, R. H. et al. Aquaculture Res. 30, 479-482 (1999).
5. Abrahams, M. V. & Sutterlin, A. Anim. Behav. 58, 933-942 (1999). Links
6. Farrell, A. P., Bennet, W. & Devlin, R. H. Can. J. Zool. 75, 335-337
(1997).
7. Stevens, E. D., Sutterlin, A. & Cook, T. J. Can. J. Fisheries Aquat.
Sci. 55, 2028-2035 (1998).
8. Naylor, R. L. et al. Nature 405, 1017-1024 (2000).
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