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The smoke rising from smouldering rainforests and the stark skeleton
of the long-dead dodo are potent symbols of the impact the human race can
have on the biosphere. Less obvious, but perhaps just as important, are
the effects we have on what survives. While we are destroying natural ecosystems
and driving some species to extinction, we are also moulding the evolution
of the survivors. Some of these unwitting selection experiments are well
documented: the evolution of resistance to insecticides in our insect pests,
the widespread evolution of resistance to antibiotics in the microbial world
and the rapid spread of fungal pathogens on new varieties of cereal crops
bred to resist such attack.

Not all of our unplanned selection experiments are so well recognised
or understood. One of these is the change we are forcing upon natural fish
stocks by the way we exploit them. It requires no special insight to appreciate
that harvesting these natural resources could have some effect on their
evolution. If you ask a farmer what he would expect to happen if he continually
sold his largest cattle and kept the smaller ones for breeding, he would
tell you that the individuals in later generations would be smaller. In
effect, this is what the fishing fleets often do to fish stocks: they remove
the larger individuals and leave the smaller ones. In principle, we might
expect a similar evolutionary response.

The extent of the selection process depends on the kind of fishery.
Trawl nets, for instance, remove larger fish, with the size of the mesh
controlling the minimum size at which an individual can be caught. This
is easy to demonstrate by placing a fine-meshed cover behind the cod-end
of the trawl net. The fine net will collect the small fish that pass through
the trawl. Gill nets are more discriminating, and remove fish of a more
particular size: small fish swim straight through the net and large fish
are too big to be caught by their gills (although they sometimes become
entangled).

Even if the gear itself was not selective, fishing would probably still
tend to select by size because fish stocks are not evenly mixed in the sea,
and fishermen would undoubtedly concentrate their activities where the fish
are of the most saleable and profitable size.

However, fishing will exert a substantial selection pressure on a stock
only if there is an appreciable difference between the characteristics of
individuals before selection and those of the survivors after selection.
This depends on how many fish in the stock are killed by fishing. Removal
of, say, 100 large individuals would have a much greater impact on the mean
size of the survivors if there were only 110 large individuals in the first
place than if there were 10 000. It is important to understand that in heavily
exploited stocks, such as cod, haddock and plaice in the North Sea, the
fishing kills many more fish than any natural causes, once fish are large
enough to be included in the fishery. To put it another way, a cod that
has reached a size at which it could be caught is much more likely to end
up as part of a fish supper or to be discarded (dead) by a fisherman than
to die for all other reasons put together. This bears witness to the remarkable
efficiency with which we exploit these resources. But such high mortality
suggests that fishing can exert substantial selection pressure on natural
stocks of fish.

What are these selection pressures? All other things being equal, the
survivors of a bout of trawling, for example, should be smaller on average
than those present before fishing. But this simple picture is complicated
by the fact that all other things are unlikely to be equal. We are ultimately
concerned with how many offspring the survivors leave to subsequent generations
and this depends on how many eggs they produce as well as their ability
to evade capture. If heavy fishing begins at sizes well before sexual maturation,
fast-growing fish which minimise the length of time during which they can
be caught before they can reproduce would be at an advantage. At the same
time, such fishing could put pressure on the fish to mature earlier, while
the fish are still small. The equation governing the selection pressure
is complex and depends on details of the lives of the fish concerned. An
interesting consequence of this is that fishing does not inexorably push
a stock towards smallness. Fishermen, if they manage their activities carefully,
can control the selection, driving the fish towards larger size or smaller
size as required.

The amount of selection applied to the fish is measured as the difference
in the mean size of a given age before selection and the mean size of the
survivors after selection (this is known as the selection differential).
How large this is is immaterial unless the offspring of the survivors differ
on average from the rest of the population: the difference must be inherited
if there is to be evolution. No one knows much about the heritability of
traits such as the size of a fish at a certain age in natural fish stocks,
but fish farmers who take their fish from the wild and breed them in captivity
are beginning to acquire some information. The upshot of these breeding
experiments with captive fish is that we can expect a genetic response to
selection (that is, a heritable change) in many traits, roughly of the order
of 10 per cent per generation of the selection differential applied.

Direct extrapolation from these experiments to fisheries is dangerous
because both the environmental conditions experienced by the fish and the
kind of selection practised are different in the wild. Nonetheless, the
experiments make it increasingly difficult to deny the possibility of evolution
in fisheries on the grounds that there is no genetic variation on which
selective fishing could act.

A more critical question is how fast such evolution takes place. For
those who see evolution as a process observable over geological eras rather
than years or decades, there would seem to be more pressing matters for
fisheries biologists to consider. However, we know that evolution can be
rapid, particularly under conditions where human activities are responsible
for generating heavy selection pressures, as with the evolution of resistance
to pesticides by insects.

In fish stocks selection caused by exploitation is substantially less
than that caused by chemicals used to control pests, and the generation
times of fish are considerably longer than those of insects. But a selection
differential of 5 centimetres acting on a length-at-age 2 years, say, gives
a 0.5 centimetre change in the trait each generation when the heritability
is 10 per cent. With a mean generation time of 3 years, the average length-at-age
should decrease by roughly 5 centimetres over 30 years. In the medium term,
over decades, changes of this magnitude would have important effects on
yield.

Is it really evolution?

If exploitation is driving evolution this fast, studies of particular
stocks over decades should reveal any changes in traits such as size-at-age.
However, these traits also respond readily to environmental changes, so
it is hard to see what exactly is causing the changes. For instance, irrespective
of any heritable change, fish grow more in years of plentiful food than
when food is scarce; so we are likely to find ourselves searching for an
evolutionary signal beneath a lot of environmental noise. To make matters
worse, exploitation may itself increase the amount of food available-because
there are fewer fish left to eat the food. This does not mean that evolution
is not taking place but it does mean that it is difficult to measure and
monitor in exploited fish stocks.

Despite this seemingly impossible tangle of factors, there are some
cases in which changes are best explained as a consequence of evolution
driven by exploitation. Some of the best documented examples are those described
in 1978 by William Ricker of the Department of Fisheries in Canada and his
colleagues on the Pacific salmon species. They looked at catch data for
five species of salmon in a large number of river systems in British Columbia
and Alaska. The data on the pink salmon (Oncorhynchus gorbuscha) are particularly
straightforward to interpret because, unusually, this species is almost
always ‘biennial’. This means that when the fish are caught as they return
to their rivers to spawn they are approaching their second birthday, so
that the sizes recorded in the catch data are approximately size-at-age
2. The animals’ natural history also means that rivers usually support two
populations, one spawning in even years and the other in odd years.

Ricker and his colleagues examined the mean weight of fish caught between
1951 and 1975, distinguishing between those caught by gill nets, trolling
and seines, and treating the even-year fish separately from those of odd
years. In 57 of the 97 data sets for pink salmon there was a significant
decrease in weight, as much as 30 per cent in some cases, and enough to
be of serious concern for management of the fishery. The biologists could
not account for this decline in terms of any environmental effects on the
salmon’s growth rate: size, for instance, was not generally correlated with
the number of fish of that year, an indication that food supply might be
involved. Neither could Ricker find an association between body size and
the salinity of the ocean, although there was some evidence that the salmon
grew bigger in years when the surface waters were warmer.

In the absence of a clear association between growth and the environment,
the researchers turned to the selection generated by fishing. About 80 per
cent of the fish returning to spawn were being caught, so fishing had the
potential to exert substantial selection pressure on the salmon. Of the
three main types of fisheries in operation, gill nets and trolling removed
individuals larger on average than seine fisheries. But, in 1945 there was
a change from selling fish by the individual to sale by the pound. This
placed a premium on the total weight of the catch rather than the total
number of individuals, encouraging the use of gill nets with larger mesh
which would catch the larger fish. The upshot of Ricker’s calculations is
that, if about 30 per cent of the variation in size is inherited, selection
brought about by fishing is enough to account for all of the decline in
size that he and his colleagues observed.

Another quite different case is the Northeast Arctic cod (Gadus morhua),
one of the largest of all the North Atlantic cod stocks. These fish spawn
close to the Norwegian coast, mostly near the Lofoten Islands. The eggs
and larvae drift in the ocean currents northwards to the Barents Sea and
the seas around Spitsbergen. Here the fish grow until they reach sexual
maturity, when they migrate annually to the spawning grounds.

Over the past 50 years the pattern of exploitation of the Northeast
Arctic cod has changed significantly. Previously, fishing boats concentrated
on adults on the spawning grounds but, with the development of fleets of
distant water trawlers in the 1930s, the fish are now heavily exploited
on their feeding grounds. Before this fishery developed, an immature individual
had roughly a 40 per cent probability of surviving from age 3 to 8 years;
since then, its chances have fallen to about 2 per cent. Such a large change
in the mortality imposed by fishing generates a big selection pressure for
early maturation, irrespective of any change in size-at-age. The changes
observed in the stock match this prediction: the age at maturation has decreased
from between 9 and 11 years from the 1920s to the 1950s to about 7 or 8
years today. This change could be the result of increased growth if more
food becomes available as the stock was depleted by fishing (maturation
depends on body size), but no one has yet shown such density-dependent change
in this stock.

Evolution of the kind suggested by the pink salmon and the cod has important
implications for future fisheries and the size of the yield which fish stocks
will support. One possible outcome is evident from a laboratory experiment
carried out by Michael Edley at the University of York. Edley set up several
populations of water fleas (Daphnia magna) as an experimental ‘fishery’,
harvesting large individuals in some populations and small individuals in
others. After about five months, the populations showed large heritable
differences-the result of the contrasting patterns of exploitation. Most
importantly, the survivors in populations from which large individuals were
removed tended to grow slowly so that they were much older before they were
liable to be caught. As the experiment progressed, there were fewer and
fewer individuals in the vulnerable size range, and the yield declined correspondingly.
Taken to its extreme, such evolution would produce growth so slow that no
individuals would ever reach a size at which they could be caught by a fishing
fleet.

Orchestrating evolution

Other outcomes are possible, however. Given the right conditions, harvesting
could select for increased growth. More-over, quite apart from its dependence
on growth, the sustainable yield depends on the capacity of the fish to
leave offspring. All other things being equal, you would expect to obtain
a larger yield from a stock in which a female produced an average of 100
offspring that survived to a fishable size, than from a stock in which this
figure was only 10. The immediate effect of selection is likely to be an
increase in the rate of population renewal, the ‘turnover’, although the
consequences in the longer term also depend on the way in which population
density interacts with renewal. Evidently the way in which the yield of
a fishery evolves is complicated and depends on details of the fishery under
consideration.

To estimate how much evolutionary change in yield could be expected
in a fishery, David Grey at the University of Sheffield and I have done
some calculations on the Northeast Arctic cod. These estimate the total
catch one might expect each year after evolution caused by the present-day
fisheries on both the spawning and feeding grounds, and compare this with
the catch after evolution under the pre-1930 conditions when fishing was
concentrated on the spawning fish. Underlying the calculations is an assumption
that the growth of a fish represents a compromise between resources allocated
to muscle and other body tissue and those allocated to reproduction. The
present-day fisheries with their selection pressure in favour of early maturation
tilt the balance towards reproduction at the expense of growth; the result
is that after evolution the catch is only about 20 per cent of that selected
by the pre-1930 fishery. We would not want to argue that this gives an exact
measure of the relative effects of the fisheries, but it does suggest that
the evolutionary effects of exploitation on the catch could be far from
trivial.

Taking this train of thought a step further, if the way in which we
exploit a fishery causes different yields to evolve, might it be possible
to manage such evolution? Fishermen have the means, in theory at least,
to control the sizes at which fish are caught, to control how many fish
are killed by fishing and, in cases such as the Northeast Arctic cod, they
also have the capacity to harvest selectively individuals at different stages
of development. Could we not control these properties of fisheries so that
the stock evolves the properties we want, such as the capacity to sustain
high yields? This is what we might call ‘evolutionary management’, along
the lines of cattle breeding and plant breeding. Obviously it is a much
less powerful tool than those available to animal and plant breeders, but
it does take advantage of the only real point of contact with the species
we exploit in the wild.

There is a real possibility that we could manage fisheries and other
natural resources in this way. But before we do, we need to know a lot more
about the resources. For instance, we need to know what selection pressures
we are applying to our heavily exploited fish stocks. This is relatively
straightforward to do and could be a standard part of the monitoring of
any fishery. We also need to know a great deal more about the genetics of
characters which will respond to the selective effects of fishing, such
as size-at-age and the age at sexual maturity. With such information at
their disposal, biologists would be in a position to examine the paths of
evolution that stem from different patterns of exploitation. From there,
they could determine those which select the desired properties and work
out how management of evolution can help to maintain these exploited natural
resources.

Dr Richard Law is a lecturer in biology at the University of York.