Aquaculture

ELSEVIER

Aquaculture

158 (1997) 277-288

Genetic correlations between survival of Atlantic

salmon in challenge and field tests
Hans Magnus Gj@en

*,

Terje Refstie, Ottar Ulla , Bjarne Gjerde

AKVAFORSK (Institute ofAquaculture Research), P.O. Box 5010, Aas N-1432, Norway
Accepted

1 September

1997

Abstract
Four sub-samples of 171 full-sib groups of Atlantic salmon presmolts (the offspring of 96 sires
and 171 dams) were tested for survival after challenge with the pathogenic bacteria Areomonas
salmonicida,
Vibrio salmonicida,
Vibrio anguillarum
and the viral disease Infectious Salmon
Anaemia (ISA). Another sub-sample of 123 of the full-sib groups was tested as postsmolts at a
marine test-site (field test) where infection with A. salmonicida prevailed causing high mortality
during a two-month summer period. A full-sib group mean MINQUE model was used to estimate
the variance and covariance components
for survival in each test environment.
Estimated
heritabilities on the underlying liability scale for survival in the challenge test with A. salmonicida
was 0.53 (at 50% survival) and in the field test 0.38 (at 65% survival). The genetic correlation
between survival in the two tests was 0.95. Thus, the results give good prospects for genetic
improvement of resistance to furunculosis when survival data from challenge tests of presmolts
are used as the selection criterion. The results also indicate a positive genetic correlation between
resistance to each of the bacterial diseases, but a weak negative genetic correlation between
resistance to the viral disease ISA and resistance to each of the bacterial diseases. 0 1997 Elsevier
Science B.V.
Keywords: Genetics; Areomonas salmonicida; Vibrio salmonicida; Vibrio anguillarum; Infectious
Anaemia; Salmo salar

* Corresponding
author.
hans.magnus.gjoen@akvaforsk.nlh.no.
NFA, N-7200 Kyrksaterora.

Tel.:

+ 47-64-96-95-12;

fax:

00448486/97/$17.00
0 1997 Elsevier Science B.V. All rights reserved.
PII SOO44-8486(97)00203-2

+ 47-64-94-95-02;

Salmon

e-mail:

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1. Introduction
Reducing the economic loss due to diseases is considered to be one of the major
goals of the aquaculture industry in Norway. Disease problems have abated due to
improved management (Wheatley et al., 1995), improved feed mixtures and vaccines,
and this has reduced the total consumption of medicated feed. Vaccination has prevented
big losses caused by the main bacterial diseases, but in order to make vaccination
superfluous
and to decrease the risk of any possible future epizootic or enzootic
diseases, it will still be beneficial to select for increased resistance to diseases. In mice,
selection for increased genetic resistance also improved the response to vaccination
(Biozzi et al., 1982; Gavora, 1990). Public concern about extended and excessive use of
antibiotics is growing, both because of the risk of developing resistant bacteria and also
because of possible residues in the product. This calls for increased effort to improve the
genetic resistance against diseases in farmed fish.
Different terms may be used to describe resistance against a specific disease. An
animal may be resistant to a disease because it has high tolerance, i.e., it is clinically
unaffected by an infection; or it may be resistant because it is less susceptible to the
disease, i.e., it is not infected when challenged. In most instances, it is difficult, or too
expensive, to determine if the surviving animal is infected or not, and the only record
that is made is the number of animals surviving the challenge test. Hereafter, the term
resistance is used, and it is not considered whether this resistance is due to low
susceptibility or due to high tolerance.
The classic experiments by Biozzi et al. (1982) showed that selecting for antibody
production gave a selection response. Moreover, it also improved disease resistance to a
group of infectious diseases with antibody dependent immunity,
but it decreased
resistance against diseases with macrophage dependent immunity. In poultry, selection
response has been obtained when selecting against fowl typhoid, avian lymphomatosis,
Newcastle Disease and Mareks disease, using survival after natural or artificial infection as a selection criterion (Gavora, 1990). As an example, Cole (1968) used survival of
a sample of progeny, after inoculation with Mareks disease virus, as the criterion for
selection, and obtained a difference between the high and low selected groups of 88%
after two generations. In a dairy cattle, a response of 2.2% units per sire generation was
obtained when selecting against mastitis with an average frequency of 20% (Solbu and
Lie, 1990).
In fish, genetics of disease resistance has lately been reviewed by Chevassus and
Dorson (1990) and Fjalestad et al. (1993). Many studies have focused on the genetic
variation in immunological
and physiological parameters presumably related to diseases,
and many new candidates have recently been reported (Fevolden et al., 1992; Reed et
al., 1992; Fjalestad, 1993; Reed et al., 1993a,b; Wiegertjes et al., 1994). Genetic
variation in resistance to specific diseases have also been shown (Amend and Nelson,
1977; Bailey, 1986; Gjedrem et al., 1991; Gjedrem and Gjoen, 1995). Genetic associations between immune parameters and disease resistance are in some studies significant
(Salte et al., 1993; Hollebecq et al., 1995), but not always too easy to explain (Lund et
al., 1995), and some are not too evident (Eide et al., 1994; Zarnecki et al., 1994). Even
for the studies showing significant correlations, the ratio of the total variation in survival

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279

that could be explained by the immune parameters were considered too low to be useful
as selection criteria. Performing indirect selection on immune or physiological parameters for resistance have given varied results (Cipriano and Heartwell, 1986; Fevolden et
al., 1992). However, several studies show that direct selection for resistance to a specific
disease gives evident response (Ehlinger, 1964, 1977; Kirpichnikov et al., 1979, 1993;
Hollebecq et al., 1995).
Earlier studies of field data, recorded either in freshwater tanks or in sea-cages, with
outbreak of diseases, have shown genetic variation in survival (Gjedrem and Aulstad,
1974; Gjerde, 1981; Standal and Gjerde, 1987; Rye et al., 1990). Standal and Gjerde
(1987) analysed survival records from the sea-rearing period for three-year classes
(1980-1982)
for which cold water vibriosis (Haemorrhagic syndrome) was believed to
be the major cause of high mortality. Their pooled estimate of heritability,
after
transformation
to the assumed underlying liability scale (Dempster and Lerner, 1950)
was 0.17 for survival in the life periods studied.
Gavora (1990) (p. 827) has clearly stated the importance of carrying out selection
against diseases. If such testing and selection is not performed, the fate of resistance
would then depend on its genetic correlation with traits under selection. From 1989,
increased resistance to Areomonas salmonicida and, in addition from 1991, Infectious
Salmon Anaemia (ISA) have been included in the selection criteria of the breeding
programme run by the Norwegian Salmon Breeding. Selection for increased resistance is
based on challenge test survival data obtained on two independent sub-samples of all
full-sib groups tested in the programme each year. The value of this test depends to a
large extent on the magnitude of the genetic correlation between survival in the
challenge test and survival recorded in a field test. The aim of this study is to investigate
the genetic relationship between survival in field test and in challenge test for furunculosis in the Atlantic salmon population of the Norwegian Salmon Breeding. This correlation will indicate the possibility
of obtaining genetic gain in survival in a field
environment
when selecting for survival in challenge tests. It was also considered
important to estimate the genetic parameters for survival after challenge test with Vibrio
salmonicida,
V. anguillarum
and Infectious Salmon Anaemia, and to estimate the
genetic correlation between the diseases.

2. Materials

and methods

2.1. Fish
Survival data were obtained from 171 full-sib groups of Atlantic salmon produced in
November 1990 in the Norwegian breeding programme (Refstie, 1990). One hundred
twenty-three of the groups (the offspring of 66 sires and 123 dams) were produced at the
breeding station at Kyrkszterora,
whereas 48 groups (the offspring of 30 sires and 48
dams) were produced at the breeding station at AKVAFORSK,
Sunndalsora. On both
breeding stations, a hierarchical mating design was used with, on average, two dams per
sire. Each family is marked by fin-clipping
and cold-branding
(Gunnes and Refstie,
1980). In November 1991, four sub-samples of, on average, 34 presmolts from each

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1.58 (1997) 277-288

full-sib group, weighing 20-40 g, were brought to Vikan AkvaVet, Namsos. Here, each
subgroup was infected with either A. salmonicida, the bacterium causing furunculosis,
V. salmonicida, the bacterium causing cold water vibriosis (Nordmo et al., 1995) V.
anguillarum, the bacterium causing vibriosis, or Infectious Salmon Anaemia (ISA),
which recently has been classified as a viral disease (Dannevig et al., 1995). Infection
with A. salmonicida was by means of cohabitation, whereas for the other diseases, fish
were infected by means of intraperitoneal
(ip.) injection. ISA infection was accomplished with homogenised and filtered tissue from liver, kidney, and spleen from fish
with typical ISA symptoms.
For each of the 123 full-sib groups produced at KyrksEterora, 40 individuals were
tagged with Passive Implemented Transponders (PIT-tags) injected into the abdominal
cavity. On May 19, 1992, when the fish had an average weight of 72 g, they were
stocked in one 500 m3 net-cage at the sea-unit at Kyrksaeterora. In late July, the fish
started to die due to infection of A. salmonicida, which were isolated from kidneys of
dead fish. Dead fish, which all showed clear evidence of furunculosis, were collected
and their tag-numbers recorded, every day until September 15, 1992 when the test was
terminated. At that time, 35% of the fish had died. The records used in the analysis are
the total number of fish tagged and the mean survival rate in each family.

3. Statistical methods
The (co)variance component estimates for the survival traits were obtained by the
MINQUE (minimum
norm quadratic unbiased estimation)
(Rao, 1971) algorithms
derived by Simianer and Gjerde (1991) and Gjoen et al. (1997). This method uses the
mean and total number in each full-sib group as the observation vectors, but yields
variance and covariance estimates equivalent to those obtained from individual records.
In this study, the individual records were binary (dead or alive), i.e., they are not
normally distributed. Consequently, the estimated (co)variance components are MINQUE
estimates and not MIVQUE (minimum variance quadratic unbiased estimation) estimates.
The method permits the use of unequal number of full-sib groups for the two traits. In
this study, there were 171 full-sib groups with observations
in the challenge test,
whereas there were only 123 full-sib groups tested in the field. The model includes
additive genetic effects and residual effects for each trait and the additive genetic
covariance. This is obtained via the dispersion matrices which contains information from
the additive genetic relationship matrix. The dispersion matrices are set up according to
the rules given by Simianer and Gjerde (1991) and Gjoen et al. (1997). For each disease,
the fish from all groups were stocked in the same tank in the challenge test, and in the
same net-cage at the sea-site. Thus, no corrections for fixed effects were required.
Because the true parameter values are not known, nor the ratios between them, some
values of best choice have to be used as priors for the first run of the MINQUE model.
The estimates of variance components for all traits converged within eight rounds of
iteration, except for analysis including resistance to V. salmonicida. The convergence
criterion was that the variance component estimates of the round were identical to those

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281

of the previous round to five decimal places. The estimates thus obtained are equivalent
to REML estimates provided they are within the parameter space and that the data are
normally distributed. But the normality assumption is not met in the present data.
The heritability
for each trait was obtained in a single trait analysis, and the
covariance analyses were performed for two traits at a time. The residual covariance was
not included in the model because the observations in each trait were made on separate
subgroups of the full-sib groups in different test environments.
Consequently,
it is
assumed that no effects, other than the additive genetic, influence both subdivided
full-sib groups. When calculating the heritabilities,
estimates of total variance were
obtained as p( 1 - p), where p is the mean survival rate in the test. This is done because
the present full-sib group mean MINQUE model has a low efficiency, compared with an
individual model, when calculating the residual variance component (Gjoen et al., 1997).
The transformation
from the observed to the assumed underlying liability scale are
calculated in accordance with Dempster and Lemer (1950). Because genetic correlations
are shown to be equal on the observed and the underlying liability scale (Hijschele,
1986; Gjoen et al., 1997) there is no need to transform the present estimate of the
genetic correlation to the underlying liability scale.
The variance of the estimates are obtained from the information matrix which is
given by twice the inverted left hand side of the MINQUE equation. These are biased
estimates of the (co)variances of the variance components unless the data are normally
distributed, which is obviously not the case here. The standard deviation (S.D.) and
standard error (S.E.) of the estimates are nevertheless presented because they may be
used as a measure of accuracy when comparing the variance and covariance component
100

90

!
7

30

60

Day
Fig. 1. Cumulative
mortality in Atlantic salmon presmolts challenge tested with A. salmonicida,
V.
sahonicida,
V. anguillarum and Infectious Salmon Anaemia (ISA). The field test represents a marine
farm-site (field test) where an outbreak of A. salmonicida caused high mortality. Day 1 is the day of challenge
in the challenge test, and the first day that A. salmonicida are detected in dead fish in the field test.

-. .

zy

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277-288

estimates with each other. The left hand side of the MINQUE equations for the four
challenge tests are identical, except for the priors. The SE. of the heritabilities
are
calculated by Taylor series approximation of the variance of a ratio.

4. Results
The cumulative mortality curves for the challenge tests and the field tests are shown
in Fig. 1. The progress in mortality in the challenge test with furunculosis is similar to
that observed in earlier tests (Gjedrem et al., 1991; Gjedrem and Gjoen, 1995). In the
field test, the outbreak of furunculosis was more moderate, probably due to less intense
contagion. The estimates of he&abilities and genetic correlations presented in Table 1,
are those obtained at a certain point of time which corresponds to an average mortality
of 50% in the challenge tests, whereas final mortality (35%) was used for the field test.

1.2

Convergence

0.2

!0

i
0.2

0.4

0.6

0.8

Prior correlation
Fig. 2. MINQUE-estimates
of genetic correlation between survival in challenge test and field test for
furunculosis for a range of prior values of the genetic correlation. The estimated correlations were obtained
after one round of iteration. The other priors are fixed.

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H&l. Gj@en et al./Aquaculture 158 (1997)277-288

An average mortality of 50% was chosen to obtain maximum variance and symmetric
distribution of the observations.
The estimated he&abilities for survival after challenge and field test with furunculosis were both medium to high, and the genetic correlation between the two traits was
very high (Table 1). The low SD. of the genetic covariance between survival in
challenge and field test indicates that this covariance is substantial.
Fig. 2 displays MINQUE-estimates
of genetic correlation between survival in challenge test and field test for furunculosis
obtained after one round of iteration for
different prior values of the genetic correlation. The results show that, for the present
data, the MINQUE model is robust when it comes to choice of priors.
Table 1 also shows that the heritability for V. salmonicidu and V. anguillarum are
high, but as can be seen from the very large S.E., not significantly different from zero.
Heritability for ISA was medium to low, but had a much smaller S.E. compared with V.
salmonicida and V. anguillarum. The genetic correlations among the bacterial diseases
are all positive, whereas the correlations of the viral disease (ISA) with each of the
bacterial diseases were all slightly negative (Table 1). The genetic correlation between
the challenge test results for V. salmonicida and V. anguillarum was very high.

5. Discussion
The heritability for survival after challenge with furunculosis is similar to previous
results found in Atlantic salmon (Gjedrem et al., 1991; Gjedrem and Gjoen, 1995) and
of the same magnitude as the present estimate obtained from the field test. The high
genetic correlation between survival in the two test environments indicates that genetic
improvement
of resistance to furunculosis
may be obtained based on survival data
recorded in either of the environments.
However, the factors which influence survival
under farming conditions will be multiform, and it may be difficult to trace the exact
cause of mortality. Furthermore, to let the selection rely on field tests, implies practical
difficulties and a greater risk of failure as the test would depend on a disease outbreak at
the site. In addition, the veterinarian responsible at a site would generally not allow an
outbreak of the disease to proceed without medicating and, thus, less information would
be available. It may, therefore, be argued that challenge tests are the most accurate and
proper measure when resistance to a specific disease is included in the breeding goal.
Results from challenge tests are also easier to evaluate precisely because the test can be
standardised. Challenge tests on presmolts are also economically beneficial due to lower
cost per individual compared with postsmolts which have to be used in a field test.
Falconer (1989) (pp. 320-322) has discussed the merit of indirect selection relative to
direct selection, and has deduced a ratio between indirect and direct selection given the
genetic correlation, the selection intensities, and the he&abilities of the two traits. For
the present data, indirect selection, based on challenge tests, will accordingly slightly
outdo direct selection. This is due to the higher heritability for the challenge test and the
high genetic correlation between the two traits.
The prospects of obtaining selection response for improved resistance to furunculosis
should thus be good in salmon due to the high fecundity which allows much information

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285

to be obtained through challenge testing sub-samples of large full-sib groups at a low

cost. This enables high accuracy of the estimated breeding values.
In a breeding programme aiming at improving disease resistance, effort should be
made to monitor the genetic improvement
over time. This may be accomplished by
producing some full-sib groups by use of cryopreserved milt from previous generations
and record the survival of all groups both in the challenge tests and at the marine test
sites. It is thus possible to approximately
estimate the genetic improvement
of the
population. At the test sites, it may be important to quantify the mortality caused by the
different disease agents.
The estimate of the additive genetic variation in survival after challenge testing with
V. salmonicida did not converge, but the present data indicates that such variation exists.
Earlier results from a challenge test (Gjedrem and Gjoen, 1995) and from a field test
(Standal and Gjerde, 1987), both showed substantial additive genetic variation for
resistance against this disease and so give evidence for genetic variation in this trait. The
present test results also indicate substantial additive genetic variation in resistance to V.
anguillarum, which is in accordance with a study by Gjedrem and Aulstad (1974).
In the present challenge tests, infection with V. salmonicida and V. anguillarum were
by means of i.p. injection, whereas infection with A. salmonicida was performed by
cohabitation. The latter is likely to be an appropriate model of natural infection, whereas
injection allows the pathogen to bypass a number of important barriers to infection. This
is illustrated in Fig. 1 by what appears to be a very short incubation time and also by the
steep mortality curve for V. anguillarum
and V. salmonicidu.
The i.p. infection
procedure is probably also a cause of the large standard errors of the heritability for
survival after challenge with these diseases (Table 1). Likewise, the very high genetic
correlation between challenge test with V. salmonicida and V. anguillarum, in contrast
to the low genetic correlation these diseases show with A. salmonicida, may also
indicate that the test procedure plays a major role, as would a lack of convergence when
estimating the genetic parameters, as was the case with resistance to V. salmonicida.
Recent developments
of the infection procedures at Vikan AkvaVet have made it
possible to also challenge fish with V. salmonicida and V. anguillarum by cohabitation
(Nordmo, personal communication);
the effect of this improved procedure on the
estimated genetic parameters should be investigated.
The present study confirms earlier results that indicate positive genetic correlation
between resistance to different bacterial diseases (Gjedrem and Gjoen, 1995). But results
indicate that there are unfavourable genetic correlations between resistance to ISA and
resistance to each of the bacterial diseases. Such a negative correlation was perhaps to
be expected because viruses rely on other pathogenic
mechanisms
than bacteria.
However, the magnitude of these correlations should easily allow genetic gain in both
traits. Based on these findings, the Norwegian Salmon Breeding has decided to select for
increased survival after challenge test with furunculosis and ISA. By selecting candidates superior for more than one disease, it may be ascertained that the selection is not
too disease specific.
In poultry, similar challenge tests, field tests, and also selection experiments have
been performed. Here, large variation among estimates of heritability for survival traits
are found. For example, Gavora (1990) found estimates ranging from 0.06 to 0.67 for

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Mareks disease. Some of these differences are due to the association between variance
and frequency in binary traits (Gjoen et al., 1997). The correlation between family mean
survival in a natural outbreak and a challenge test with Mareks disease has been
estimated as 0.56 f 0.18 in an experiment where the total mean survival was 10% in the
natural outbreak and 7.9% in the challenge test (Biggs et al., 1968). Negative genetic
correlations between test with viral diseases and test with bacterial diseases have also
been found in poultry (Gavora, 1990; pp. 828-829).
Further studies on disease resistance in Atlantic salmon should focus on obtaining
more reliable estimates of genetic variances and covariances for mortality caused by the
diseases studied here. There is also a need to verify whether the high genetic correlation
between challenge and field tests with furunculosis also applies to the other bacterial
diseases, and to obtain an estimate of the genetic correlation between survival in
challenge and field tests for the viral disease ISA. In the Norwegian breeding programme, there is also other traits subject to selection: growth rate, early sexual maturity,
colour and fat content of the muscle. An unfavourable genetic correlation between any
of these traits and the disease traits may slow down the total genetic response to
selection. These correlations have to be known if correct expected genetic gain is to be
predicted.

Acknowledgements
This work was financed by the Regional Development
Fund and the Norwegian
Salmon Breeding Company Ltd. Vikan AkvaVet is acknowledged for the challenge tests
of the respective diseases.

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