ICES Journal
of Marine
Science,
54: 1009-1014.
1997
Past, present, and future of genetic improvement in salmon
aquaculture
0AP
H. M. Gjeren and H. B. Bentsen
Gjgen, H. M. and Bentsen,
ment in salmon aquaculture.
H. B. 1997. Past, present, and future of genetic improve- ICES Journal of Marine Science, 54: 1009-1014.
The farming of Atlantic salmon has become an important industry in several countries,
and breeding programmes have been implemented to improve genetic performance
and adaptation to farm environments. Founder stocks used in the Norwegian salmon
breeding programme have originated solely from Norwegian rivers and no extrinsic
genes have been introduced. The majority (more than 90%) of the additive genetic
variation in Norwegian populations of Atlantic salmon has been found within, and not
between, river strains. The Norwegian breeding programme comprises four subpopulations. In the event of reduced additive genetic variability due to random drift in
the closed breeding populations, crosses between the sub-populations could be made to
re-establish the variability. Selection in itself is not expected to reduce the additive
genetic variability as long as inbreeding is avoided. To date, seven different traits (body
weight at slaughter, age of sexual maturation, survival in challenge tests with
furunculosis and ISA, flesh colour, total fat content, and amount of fat tissues) have
been included in the breeding goal. The selection response obtained is about 10% per
generation for each of these traits. In the future, more traits are likely to be included.
The results of and prospects for selective breeding and the use of modern DNA
technology to improve genetic performance in aquatic species are discussed.
,c’1997 International Council for the Exploration of the Sea
Key words:
strains.
Atlantic
salmon,
breeding
programmes,
H. M. Gjoen and H. B. Bentsen: AKVAFORSK,
genetic
breeding
breeding
The Norwegian aquaculture industry started in the early
1970s and by 1995 the output from salmon and trout
farming was greater than the sum of the meat production from pig, cattle, and poultry (Anon, 1997a, b). An
experiment
presently
being conducted
by AKVAFORSK is comparing
a wild stock from the Namsen
river with salmon from the fourth generation
of the
national breeding programme (based mainly on Namsen
stock). Preliminary
results show that growth of the
selected fish until smolting was twice that of the wild
fish (T. Refstie, AKVAFORSK,
Sunndalsnra,
Norway,
pers. comm.), suggesting that genetic improvement
has
contributed
substantially
to the efficiency of salmon
aquaculture.
A general understanding
of additive genetic improvement through selection and knowledge of the selection
L.) is
programmes
for Atlantic salmon (S&no sub
essential when assessing the genetic interactions between
the wild stock and escaped farmed Atlantic salmon
(Bentsen, 1991). The aim of this paper is to present an
outline of some of the general principles of selective
$2.5.00/0/jm970299
selection,
PO Box 5010. 1432 Aas, Norway.
Introduction
105&3139/97/061009+06
variation,
and to describe
programme.
the
national
Norwegian
General principles of a breeding
programme
The most important
prerequisite
for genetic improvement through
selection is additive genetic variation
between individuals for the traits of interest. In practically all traits or characters
that can be measured in
nature, phenotypic variation can be found. Most studies
show that this variation is in part determined
by the
additive effect of the genes present in the population
(e.g. Gjedrem, 1983; Gjedrem et al., 1987; Gjerde et al,
1994). It is this additive genetic variation that makes
genetic improvement
by selection possible (see, e.g.,
Gjedrem, 1985; Bentsen, 1990).
The initial step in a breeding programme
is to select
the individuals with the best genetic performance
for the
trait of interest. Accurate estimates
of the breeding
values of the breeding
candidates
is important
for
the success of a breeding programme
(Bentsen and
0
1997 International
Council
for the Exploration
of the Sea
1010
IT. M. Gjeen and H. B. Bentsen
Gjerde, 1994). The simplest method is to use the
phenotypic value as the breeding value, whereas more
advanced breeding programmes utilize more precise
methods, methods that estimate the breeding values by
using information from all relatives of the breeding
candidate.
After selecting the superior individuals as parents to
produce the next generation, the selection response can
be measured in the offspring generation. It should
be noted that selection, after an initial two or three
generations, is not expected to reduce the additive
genetic variation in the offspring generation, either
phenotypically or genetically, compared to the parental
generation if inbreeding is avoided (Bulmer, 1971;
Falconer, 1989; Bentsen, 1994).
This improvement of the population mean of a given
trait is determined strictly by parameters that can be
measured in the population. The improvement, AG, is
given by:
AG=i . op. h2
where i is the selection intensity; or, is phenotypic
standard deviation, which is the sum of the genetic and
environmental variation; and h2 is the heritability, which
is determined by the proportion of the phenotypic
variation that is caused by additive gene effects
(Falconer, 1989). The validity of this equation has been
proved through hundreds of experiments in a variety of
species. The principles of the equation will also apply to
more complex selection procedures, such as combined
selection and multi-trait selection (e.g. Cunningham,
1969).
This means that if selection programmes are to
generate continuous genetic progress, they will have to
be managed so that the additive genetic variation is
maintained in every generation (Gjerde et al., 1996;
Villanueva et al., 1996). This can be achieved by controlling inbreeding (Meuwissen and Woolliams, 1994;
Meuwissen et al., 1995). In the Norwegian national
breeding programme records are kept of the pedigree of
all the breeding candidates, and the mating scheme is
designed in a way that minimizes any increase in
inbreeding. Simulation studies and experiments have
shown that maintaining
additive genetic variation
through generations of selection is possible, both in
fish and other animals (e.g. Falconer, 1989; Toro
and Perez-Enciso, 1990; Gjerde et al., 1996). This is
in contrast to a common assumption that selective
breeding will necessarily make a population genetically
homogeneous.
The great advantage of selecting for additive genetic
improvement is that new genetic gain can be accumulated in each generation and may then be maintained
in the population. This will result in stepwise and
long-term genetic progress.
Current breeding programmes
The Norwegian breeding programme for Atlantic
salmon
Origin and gene flow
The base populations of the Norwegian breeding programme were formed in the years 1971 to 1974 (Gjedrem
et al., 1991a). In order to obtain a broad genetic base,
AKVAFORSK collected fertilized eggs from 40 out of
about 400 rivers that had stocks of Atlantic salmon. The
breeding programme is designed with full-sib groups as
the basic unit. The goal was to collect about 12 full-sib
groups from each river, but the number of such groups
from each river varied.
Owing to a four-year generation interval in Atlantic
salmon in Norway, four populations of different genetic
origin were formed in order to provide stock for the
farming industry each year (Gjedrem, 1979; Gjedrem
et al., 1987). In each new generation, broodstock is
selected according to a ranking of all breeding candidates. This ranking is based on the individual’s breeding
values for the traits described in the breeding goal,
which will be outlined later. At present the programme is
in the 6th generation.
In 1989, the strain or stock composition of the
Norwegian
breeding
populations
was estimated
(Gjedrem et al., 1991a). Figure 1 shows the results from
population 1 as an example. In the base population,
generation 0, when the eggs were collected from the
different rivers, there was a fairly even distribution
among a number of river stocks. After only a few
generations, however, one of the strains dominated the
population. This may be explained by the findings from
comparative studies of strains (Gjerde and Refstie,
1984). Most of the genetic variation for a given trait was
found within river-strains, between and within families.
Only a small fraction, less than 5-10% of the total
variation, was explained by the river of origin. This
agrees well with studies based on the allelic variation of
enzymes (Stahl and Hindar, 1988). Thus, because of the
rather small sample sizes from each river stock in the
base populations, samples from some rivers could by
chance include a larger proportion of superior individuals. Consequently, this strain would also contribute
more to the next generation. If a larger proportion of the
genetic variability had been associated with the riverstrains, measures could have been taken to secure a
more equal genetic representation of the strains in the
future gene pool. This would, however, require at least
two generations (i.e. 8 years) of strain crossing with
severe restrictions on the selection, and consequently
limited genetic progress.
Figure 2 shows the pattern of gene-flow from the
river-strains to the eight populations currently in the
Norwegian breeding programme for Atlantic salmon.
Past, present, and future of genetic improvement in salmon aquaculture
Figure 1. Frequency of river strains in population 1 in the Norwegian breeding programmes. gen. 0 0;
gen. 3 (El).
1011
gen. 1 (B)); gen. 2 (0;
River strains
Pop. 2
Pop. 3
Pop. 4
1986 NFA
Figure 2. Gene-flow in the Norwegian breeding programme.
After three to four generations of selection at AKVAFORSK’s research station at Sunndalserra, a second
breeding station, the Norwegian Fish Farmers’ Breeding
Station, was established at KyrksEtersra
(Norske
Fiskeoppdretteres
Avlsstasjon, NFA). Between 1986
and 1989, parallels of full-sib groups from AKVAFORSK were transferred to NFA. Transfer of eyed eggs
between the two breeding stations has continued on a
regular basis with 10 to 15 full-sib groups exchanged
annually between the two stations.
In addition to the national breeding programme,
private hatcheries have produced their own stocks for
farming since 1971, based on fry originating from the
national breeding programme or from Norwegian rivers.
Two of these private hatcheries, Jakta and Bolaks, also
supplied full-sib groups from their own populations to
1012
H. A4. Gjgen and H. B. Bentsen
NFA between 1986 and 1989. These groups are no
longer represented in the NFA breeding populations,
since they did not compete with the National breeding
programme’s original broodstock for the traits included
in the breeding goal (Fig. 2).
The total number of breeding populations in Norway,
both national and private breeding programmes, is
between 8 and 15, depending on how many of the
private programmes are classed as breeding populations.
Division of a population into several sub-populations is
a recommended strategy to counteract loss of genetic
variability due to genetic drift (e.g. Falconer, 1989). The
random allelic loss is expected to be divergent in different sub-populations, and full variability may thus be
restored by crossing of sub-populations. This possibility
has not yet been exploited in Norwegian farmed salmon,
but could be used if loss of genetic variability is detected
in the future. Furthermore, genetic variability may be
restored or introduced by using broodstock from outside
the breeding programme. Since it is likely that such
introductions will perform less well than the selected
broodstock, a separate operation will be needed to
preserve and upgrade the introduced germplasm by
relaxed selection and controlled crossing with top breeders from the breeding programme. This may require
several generations.
Organization
of the breeding programme
The breeding programme comprises two breeding centres located on the north-west coast of Norway. Each
breeding centre has four test stations located along the
coast to ensure testing under different farming conditions. The mating system used is hierarchical, such that
each male is mated to two or three females (Refstie,
1990). When the fish are large enough to be tagged
(about 20 g in weight), the 120 best ranked full-sib
groups are mixed together in the same tank to avoid
systematic errors in the test due to common environmental effects influencing each full-sib group. At smolting the fish are transferred to sea cages. One hundred
fish from each full-sib group are evenly distributed
among the test stations and an additional 150 fish from
each full-sib group are reared at the breeding centre’s sea
unit as breeding candidates.
In 1992, AKVAFORSK
transferred the breeding
activity to a separate unit, AkvaGen. Both NFA
and AkvaGen were then organized under a new
mother company, Norwegian Salmon Breeding (Norsk
Lakseavl, NLA), which now operates both breeding
centres.
Breeding goal
Over the 20 years of the programme, the breeding goal
has been expanded to cover an increasing number of
traits (Table 1). The first trait selected for was growth
performance, which is measured as body weight at
Table 1. Breeding goal in the Norwegian breeding programme.
Year
1975
1981
1993
1994
1995
Trait
Growth (G)
G+Age sexual maturation (SM)
G+SM + Disease resistance (DR)
G+SM+DR+Flesh
colour (C)
G+SM+DR+C+Body
composition
slaughter.
In 1981, age at sexual maturation
was
included as the second trait, since maturation of fish
after 1 year in the sea was a problem for the industry. At
that time, the fish reached market size only after 2 years
in sea cages. Breeding values for growth and age at
sexual maturation are computed based on records collected at the breeding centres as well as from the
relatives at the test stations.
In 1990, the first experiments with challenge tests to
determine resistance against the bacterial disease furunculosis were carried out (Gjedrem et al., 1991b), and this
information was utilized in the breeding programme in
1993. The following year, resistance in challenge tests
with the viral disease Infectious Salmon Anaemia, ISA,
was included in the breeding goal. The challenge tests
are carried out with parallel groups from the full-sib
groups at the breeding centres in a carefully designed
closed test station. The test fish are destroyed after
testing and the records are used to select among their
relatives at the breeding centres.
Flesh quality is considered important when marketing
Atlantic salmon, but there has been a lack of good
methods to measure it, and of exact definitions of the
trait(s). Flesh colour, measured optically by a Minolta
spectrophotometer, was included in the breeding goal in
1994. In 1995, the second quality trait, body composition or fat content in the meat, was included. This
trait consists of two different measurements,
total
fat content and amount of fat tissue, recorded in a
computer tomograph. Carcass traits are recorded on
fish slaughtered at the test stations, and the records are
used to select among their relatives at the breeding
centres.
Genetic gain
Estimates from 1994 indicate approximately 8-10% genetic gain per generation for growth rate, age at maturation and flesh pigmentation (B. Gjerde AKVAFORSK,
As, Norway, pers. comm.). The highest gain has been
achieved for growth rate. Since this is the only trait that
can be measured on the breeding candidate itself, a
higher selection intensity is achieved than for the other
traits which are selected based on information from
relatives only.
Past, present, and future of genetic improvement in salmon aquaculture
Future additions to the breeding goal
Methods by which to measure the texture of the flesh are
under evaluation. A mechanical procedure which has
been shown to give similar scores to those given by a
trained sensorial test panel has been investigated. The
preliminary results are promising, and a heritability of
0.2 has been estimated. NLA is likely to include this trait
in the breeding goal in 1997.
The next quality trait which is likely to be included in
the breeding goal is body shape. Rapid growth in
Atlantic salmon is associated with deeper body shape,
which is undesirable for marketing reasons since it is
different from most wild fish. This can be counteracted
by selecting for slimmer fish. The trait may be measured
by the traditional condition factor or by developing
other related measurements.
Some traits may be discontinued if they cease to be of
economic importance. For example, as growth rate has
been improved, an increasing proportion of the farmed
salmon in Norway will reach market size within 1 year
of transfer to sea-cages. Delaying sexual maturation
through the breeding programme may then become less
important than it was some years ago.
Breeding programmes
other countries
for Atlantic
salmon
1013
from Scotland and Newfoundland, via Australia. Since,
1996 a breeding programme with selection based on full
and half-sib information has been established.
The future
Genetic
engineering
During recent years, much attention and many resources
have been allocated to research efforts on genetic engineering (e.g. gene transfer). To date, such techniques
have not been considered as acceptable tools in the
national breeding programme in Norway, or to the fish
farmers, to the general public, or to the consumers. The
results so far have been of limited value to the industry.
One of the main problems when applying these techniques to enhance performance is the incorporation of
the introduced gene in a way that results in a wellbalanced organism, able to benefit from the superior
gene effect without major disturbances of other biological processes. If transgenic farmed fish become more
acceptable or offer benefits in the future, the testing of
such individuals and the incorporation of the new gene
into the population, are best achieved in an ongoing
breeding programme utilizing additive genetic effects.
in
In Iceland, the main focus of Atlantic salmon production since 1960 has been sea ranching. Initially, the
programme utilized (natural) selection for return rate by
using recaptured fish as broodstock. In the years 1988 to
1993, a large-scale breeding programme funded by the
Nordic Council was conducted at Kollafiordur breeding
station near Reykjavik (Jonasson, 1993, 1996). An
increased return rate was observed as a result of selective
breeding based on family information (Jonasson, 1994).
Owing to a general decrease in return rates, the programme was terminated in 1993. In 1995, however, a
breeding programme in support of salmon farming
was initiated based on broodstock imported from
private breeding programmes in Norway.
In Canada, the Atlantic salmon Federation
in
St Andrews, New Brunswick, has conducted a breeding
programme since 1984 based on Atlantic salmon captured in the St John River (Friars et al., 1995). The
design of the programme is similar to the Norwegian
national breeding programme, and the improved stocks
are used by the salmon farming industry.
Fish from the national breeding programme in
Norway were used as base populations in a breeding
programme
in the Faeroe Islands. The breeding
programme was established in 1992 and is based on
records from full and half-sib groups.
From its beginning in the early 198Os, the Chilean
Atlantic salmon farming industry has been based on
imported broodstock, mainly from Norway, but also
Microsatellite
loci
Currently available tagging systems represent a major
economic and practical limitation for further development of selection programmes based on pedigree information. In such programmes, family groups have to be
reared separately until individuals are large enough
for tagging. This requires costly multi-tank facilities and
also introduces systematic environmental effects common to sibs that may lead to bias in the estimated
breeding values. The detection and use of microsatellite
loci for family identification purposes may, therefore,
represent a milestone in selective breeding of aquatic
species. These techniques enable family groups to be
reared in a common environment post-fertilization, and
the number of families included in the test may be
increased considerably.
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