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Selection experiments with salmon. II. Proportion of Atlantic salmon smoltifying at 1 year of age
A~uuculture,
10 (1977) 231-242 o Elsevier Scientific ~blishing Company,
231 Amsterdam - Printed in The Netherlands
SELECTION EXPERIMENTS WITH SALMON. II. PROPORTION OF ATLANTIC SALMON SMOLT~FYING AT 1 YEAR OF AGE
TERJE REFSI’IE, TGRSTEIN Qepartment
A STEINE and T. GJEDREM
of Animal Genetics and Breeding, AgricuEtural University of Norway, k-NM4
As ~Nor~ay~ (Received 14 October 1976; revised IQ November 1976
ABSTRACT Refstie, T., Steine, T.k and Gjedrem, T, 1977. Selection experiments with salmon. II. Proportion of Atlantic salmon smoltifying at 1 year of age. Aquaculture, 10: 231-242. Salmon (Salmo sular) brood stock were taken from 37 localities in Norway for 4 consecutive years. Each year, after fertilization, the offspring in each family from each strain were reared in separate egg trays and fingerling tanks. The percentage of fish in each tank which smoltified at 1 year old was recorded, and environmental and genetic factors influencing the percentage smoltification were studied. Percentage smoltifieation was significantly affected by the number of fish held in a tank, or fish density (correlation co’ efficient 0.03-O. 27). Variation between locality of origin of brood stock and per cent smoltification was highly significant for each year class, and there was a high correlation fO.%Q-0.95) between smelt percentage and average weight of fish in a family. Heritabilities in per cent smoltification estimated by sire component from total data had a weighted average of 0.06 (range 0.16 to -0.01). From the dam component heritabilities ranged from 0.20 to 0.40 when tank effect was ignored, and 0.08-0.25 with tank effect taken into account. Variance eomponen~ for locality were two to three times as high as those for sires within localities, indicating that genetic variation is greater between than within localities. Highly significant interaction sire x dam was found, suggesting a considerable nonadditive genetic variance influencing the percentage of fish smoltifying at 1 year of age.
INTRODUCTION
Size is one of the most impo~~t factors determines the age at which salmon smoltify, and parr must reach a certain minimum size before the smoltification process can start (Elson, 1957; Parry, 1960; Koch, 1968; Sounders and Henderson, 1970; Johnston and Eales, 1970; Knutson and Grav, 1975). Parr which fail to reach this rni~rnu~ size in the spring or early summer of one year will remain parr, regardless of growth, until the following spring. In Scandinavian rivers salmon smoltify at 2-5 years old depending on variables such as water temperature, food supply and genetic factors. In commercial salmon farming age at smolti~cation is an important trait, since l-year-old smolts are cheaper to produce than 2-years-old or older fish.
232
In addition, Ritter (1975) found that fish which smoltify at the age of 1 year subsequently mature later than those smoltifying in 2 or 3 years. Early maturation is often undesirable in fish farms as it is accompanied by increased mortality and reduced meat quality. The purpose of this study was to examine the relative importance of genetic and environmental variation in determining the percentage of Atlantic salmon smoltifying at 1 year. MATERIALS
AND METHODS
Data from four year classes (1972-1975 inclusive) of salmon were used in this study. Brood fish were taken from 37 localities in different parts of Norway. For the purpose of this study, fish from a particular river, river system, or a fjord leading to a river or river system are regarded as being from a discrete “locality” or “strain”. Localities from which brood fish were taken were shown on a map by Gjedrem and Aulstad (1974), who also described the mating system used. Eggs from each full-sib family were hatched in separate trays. Subsequently, during the fry and parr stages of growth, fish of each family were reared separately in 2-m2 indoor fibre-glass tanks (Kanis et al., 1976). At the Fish Breeding Experimental Station, SunndalsBra, warm water from Aura hydroelectric power station is used to induce a high percentage of young salmon to smolt at 1 year old. Experience at Sunnda.ls@ra is that fish too big to pass a lo-mm grader by March will smoltify in spring of that year. Therefore, in the present study a smolt is defined as a young salmon not passing a lo-mm grader by March 15th. During late autumn and winter each year the fish in each indoor tank were graded two or three times. Parr not passing a lo-mm grader were counted, weighed, freeze-branded, and transferred to outside concrete ponds. In March the parr which passed the grader in each tank were counted and weighed. Table I shows the number .of sires and dams used as brood fish, the number of localities from which they were taken, and the total number of young salmon each year from which observations were included in statistical analyses. Data from localities represented by only one or two families were excluded from the analyses. TABLE
I
Number of localities, sires, dams and total number of young salmon for the year classes used in statistical analyses 1972 Number of localities Number of sires Number of dams Total number of young salmon
1974
1973 14 52 119
106 254
23 39 66 71608
1975 11 35 94
8 62 149
224 139
114 267
233
For a detailed investigation of the effect of environmental factors on the percentage of salmon smoltifying at 1 year old the data from 1974 were used. The following sources of variation were included in a least squares model. Modes I Yij = /.I+ ai + b, (Xl ii-X 1) + bz (Xzij -X2)
+ b,(X,ij-xs)
+ b4 (X4,-X4)
+ bS (X,ij-X,)
+ eij
where 5.j P ai X, x2
= percentage one year old smolt per group, ith locality and jth tank. = least squares mean. = effect of ith locality. = average hatching date. = average date of first feed. K = average number of days from hatching to recording of smolt percentage. xe = average number of days from first feed to recording of smelt percentage,
x5 = average number of fish per group. e., = random effect for the ijth recording. The”b’s are partial regression coefficients of Y on the respective cated by their suffix.
X’s as indi-
To study the relationship between percentage of l-year-old smelt, fish density and average weight of all fish in the group, the following model was used. Model II Yij = /A+ ai + bl (Xl ij -r,)
+ bz (X2 ij-rz
) + eij
where yij
= actual observation, percentage smelt per group or average weight, ith location and jth tank. = least square mean. = effect of ith locality. = mean value of total number per tank. = mean value of X1 squared.
!J ai “K -K = random effect for the ijth recording. eij bl and b2 are partial regression coefficients of Y on X, and X2, respectively. Correlation between the traits were also calculated. To demonstrate calities individual
differences observations
in percentages of fish smoltifying between lowere used, smoltification being treated as an
234
“all-or-none” trait. A smolt was given the code value 1, and a non-smolt value 0. The following model was used.
the
Model III
Yij = P
+
ai + b (Xii-~)
+ eii
where
x
= the actual observation, 1 or 0. = least square mean. = effect of the ith locality. = partial regression coefficient of smelt/non-smolt of fish per tank. = mean value of total number of fish per tank.
eij
=
yij
c1 ai
b
random
on the total number
effect for the ijth record.
In the analysis of relations between smolt percentage and other charateristics, the regression coefficient of smolt percentage on the total number of fish per tank squared was not significant and hence this element was ignored in the above model. For fish of the 1972 year class matings were made in a factorial way within sets. Each locality could have several sets. However, some groups died before final registration so that an ordinary cross-classified analysis of variance was unsatisfactory for estimating variance components of sires and dams and interaction between sire and dam. Harvey (1964) has given a method where the variance components found by two nested models can be used to find the correct variance components for sire and dams, and interaction between them. Therefore, the two following analyses of variance were applied. ANOVA
I
Source Total Locality
d.f. N-l r-l
0; + I h &
Sire/locality
s-r
u: + 1 kz o&S + I k3 0s”
Dam/sire/locality
q-s
u; 4 1 B1 u&
Individual/dam/sire/locality
N-q
ui
d.f. N-l r-l
Expectation
u; + 2k4u2 s,d +
q-r
us +?k2u2
ANOVA II Source Total Locality Dam/locality
Expectation
of mean square + lkS us”+ 1 k2 u;
of mean square 2 ks
s/d +2+
fJ;
+
2 k6
0;
235
Sire/dam/locality
s-q
0; +*kl
Individual/sire/dam/locality
N-s
uz
The estimate
of interaction
CJ2
u2sd, can be obtained
s/d
from the equation
E (Okd ) = u; + u2sd which gives (-32 zu2 sd s/d -
‘s
2zu2
s/d
+u2
d
A common mating system was used to produce fish of the 1973,1974 and 1975 year classes, whereby sperm from one male fertilized the eggs of three females. Therefore, the results from these three year classes were analysed by a regular hierarchical method with dams nested within sires. This analysis of variance (ANOVA III) included all fish groups for each year class. In 1973, and more frequently in 1974 and 1975, some full-sib groups were divided into ttio tanks. This makes it possible to estimate the variance components due to tank differences and to remove this source of variation when estimating genetic components of variance. The following analysis of variance was applied. ANOVA IV Source Total Locality
d.f. N-l r-l
u: + k,u; f ksu;/,
+ k,u; + k10 of
Sire/locality
s-r
u: + k4u; + k5u;,s
+ k6u;
Dam/sire/locality
q--a
Tank/dam/sire/locality
t-q
u: + kzu; + k 3u2d/s u: + kluf
Individual/tank/dam/sire/ locality
N-t
U2 e
Expectatidn
of mean square
When using this model full-sib groups without replicates were excluded. The heritabilities were calculated by using the sire components (hi) and by using the dam components (hi). Their standard errors were calculated according to the procedure described by Becker (1967). RESULTS
Density The effect of fish density (number of fish per tank at first grading) on the percentage of fish smoltifying at 1 year of age was investigated in several ways.
236
TABLE
II
Average smelt percentage, correlations (r) between smelt percentage and number of fish per tank, regression coefficients (b) of smolt percentage on number of fish per tank, average number of fish per tank and average weight of the fish (g) 1973
1972
Average smelt percentage : Average number per tank Average weight fish (g)
-
17.5 +O.l 0.002+0.0003 0.03
1055k1.3 5.7
to.54
-
1974
67.1 to.2 0.26 0.018+0.0004 1 267+2.3 19.6
t2.56
-
1975
40.5 to.2 0.27 0.018+0.0001 1800*1.5 12.8
i0.36
-
78.4 rO.l 0.14 0.02+0.0004 876il.l 23.3
to.52
By applying Model II it was found that the coefficient of regression for the number of fish squared was not significant, and it was therefore assumed that the regression of smolt percentage on density was linear. The average number of fish per tank for each year class is shown in Table II. By applying Model III the coefficients of regression shown in Table II were obtained. Regression coefficients for the last three year classes of fish were similar, and indicated that there is a reduction of about 2% in the number of fish smolting in 1 year for a rise in fish density of 100 individuals per tank. The effect of density found in the results from the 1972 year class can partly be ex. plained by the low number of fish per tank and low average weight of fish from that year. The effect of fish density on the percentage of fish smoltifying in 1 year was highly significant, and accounted for 0.04, 3.5, 5.6 and 2.5% of the total variance for the 1972, 1973, 1974 and 1975 year classes, respectively. Similar results were obtained by Refstie and Kittelsen (1976).
Dates of hatching and first feed for different families varied both within and between year classes. There were also differences in the number of days from hatching and first feed to the date on which smolt percentage was recorded. Fish of the 1974 year class showed the widest range in hatching date, and this year class was therefore ,used to study the effect of hatching date on the percentage of l-year-old smolt by the application of Model I. Hatching and first feeding dates were found to have no significant effect on the percentage of smolts produced or on the average weight of fish in a tank. The number of days from hatching and first feed to the recording date did have a significant effect on both smolt percentage and average weight of fish. However, these two factors accounted for only 1.3 and 1.5% of the total
237
variance in the traits smolt percentage and average weight of fish per tank, respectively, so it was decided not to adjust the data for these age effects. Locality of origin or strain Model III was used to estimate the effect of strain difference on the percentage of salmon smoltifying in their first year. There was a large difference in smolt percentages between year classes (Table II), possibly because of differences in winter water temperature. In view of these large year-class differences and the fact that few strains were sampled repeatedly over several years, it was decided to estimate the effect of strain on smolt percentage for each year class separately. Deviation from the average smoltification for each year class is shown in Fig.1. The localities are shown in theeorder they appear on a map of the coast of Norway, without trying to take into account differences in latitude. Localities which may include several river systems, those from which farmed brood stock were used, and the Swedish strain Lule?i , are listed separately.
.
- 1972 ymr
A -1973
-;,-
0 -197Y
-I-
.
-‘I-
-1975
da55
Fig.1. Differences between localities for smoltification, expressed by fitting constants for smoltification registered as an all-or-none trait. The specific localities, except LuleP (Sweden), are ranked according to northern latitude.
Differences in percentage of l-year-old smolt between localities were highly significant for each year class. Localities in western Norway seemed to produce the highest percentage of smolts( (Fig.1). Locality variance was estimated by Model III to be 3.7, 7.9, 4.2 and 1.5% of the total variance for the year classes 1972, 1973, 1974 and 1975, respectively. The strain variance is partly genetic and partly environmental, but the size
238
of the genetic variance cannot be calculated from these data. The environmental variance is due to differing qualities of eggs coming from brood stock which lived in different environments before stripping. After fertilization, environmental differences’were removed, i.e. all eggs and fry received the same treatment in the hatchery. It is considered probable that the greater part of the strain variance in l-year-old smolt percentage is genetic. correlation between smelt percentage and weight of fish
The estimated correlations between percentage of fish smoltifying at 1 year of age and the average weight of fish in a tank were 0.89,0.91, 0.95 and 0.95 for the year classes 1972, 1973, 1974 and 1975, respectively. These correlations are highly significant. Tank effect
For the year classes 1973,1974 and 19’75 each full-sib group was hatched in one tray and fed in one 2-m2 plastic tank. Some of the groups were, however, divided into two groups in separate tanks to make it possible to estimate tank effect and ANOVA IV, was used for this purpose. As shown in Table V, the tank effect on smolt percentage was significant for each of the year classes. The variance component represented only 2,5--6.4% of the total variance, which is in good agreement with the results obtained by Aulstad et al. (1972) for rainbow trout fingerlings. Genetic parameters
Before genetic analyses were carried out the figures for smolt percentage were adjusted for differences in fish density by applying the regression coefficients given in Table II. Variance components and h~tab~ity estimates for fish of the 1972 year class are shown in Table III. The estimates were obtained by using ANOVA I and II. All classifications are highly significant. The heritabilities estimated from the sire and dam components are comparable, assuming that there is no maternal effect which would be included in the dam component. Maternal effect, therefore, seems to be of little importance in determining percentage of smolt at 1 year. According to Aulstad et al. (1972), the expected composition of the interaction sire X dam is where 0; @iA
= variance due to dominance. = additive X additive gene interaction.
239
and
= additive
Gn
= dominance
TABLE
X dominance
gene interaction.
X dominance
gene interaction.
III
Variance components and heritabilities for smolt percentage estimated for the 1972 year class Source
d.f.
Variance comnonents
-~ Locality Sire Dam Interaction sire x dam Residual
11 51 46
0.0044** 0.0055** 0.0043**
2 346 106 253
0.0026** 0.1235
Heritabilities
0.16~0.05 0.13*0.09
**p < 0.01.
Assuming that oiD = ub/4, and that the other components are zero, the percentage of variance due to dominance would be 0.07. For the 1972 yearclass the dominance deviation is about half the magnitude of the additive variance and should be taken into account. The variance components for the 1973-1975 year classes estimated by applying ANOVA III are given in Table IV. Only for some of the data could the tank effect be estimated using ANOVA IV, and the results are presented in Table V. The heritabilities estimated from the sire components should not be influenced by non-additive variance and the tank effect seems to have little influence on the sire components (Tables IV and V). The estimated heritabilities for smolt percentage are all small and the sire component is only significant for the 1974 year class. Aulstad et al. (1972) found higher estimates of heritability for weight and length of rainbow trout fingerlings, while Naevdal et al. (1975) and Lindroth (1972) found very high heritabilities for length and weight of salmon Parr, respectively. Moav and Wolfarth (1966), however, found very low heritability estimates for growth in carp. The dam component given in Table IV includes additive genetic variance as well as non-additive variance, maternal effect and tank effect. All heritabilities estimated by means of the dam component are higher than estimates for the sire. The dam components are highly significant for all year classes. By including tank effect in the model, the dam component is reduced from h* = 0.27 to h* = 0.14. DISCUSSION
The results presented
above show that there is considerable
variation
be-
Variance components
0.0071* 0.0020 0.0115** 0.1897
d. f.
22 16 27 71 542
1973
V
0.04+0.09 0.23kO.03
G
0.0049* 0.0037* 0.0097** 0.1911
10 24 59 224 045
Variance components 0.0042* 0.0022 0.0050** 0.0055** 0.2066
d. f.
7 17 28 53 158 181
Variance components
0.0099 0.0039 0.0044 0.0140** 0.1879
d. f.
6 2 11 11 25 369
0.07to.14 0.08+0.09
i22
1974
1973
*P < 0.05; **p < 0.01.
Locality Sire Dam Tank Fish
Source
0.06+0.05 0.20+0.02
iz
0.0093** -0.0001 0.0214** 0.1844
7 54 87 114 120
0.04+0.05 0.09*0.05
i;a
Variance components 0.0111* -0.0078 0.0122* 0.0051** 0.1835
d. f.
2 8 2 13 21 239
1975
year classes
Variance components
year classes
d.f.
Effect of tank calculated, 1973-1975
Variance components
1975
Effect of tank ignored, 1973-1975
d.f.
1974
Estimates of variance components and heritabilities for smoltification.
TABLE
*P < 0.05; ** P < 0.01.
Locality Sire Dam Fish
Source
Estimates of variance components and heritabilities for smoltification.
TABLE IV
-0.04~0.09 0.25kO.43
G
-0.01~0.03 0.40+0.09
AZ
-0.01 0.14
Pooled estimate of G
0.02 0.27
Pooled estimate of i2
241
tween strains, or the offspring of brood fish taken from different localities, in the percentage of salmon smoltifying at 1 year of age under hatchery conditions. Also, the percentage smoltifying at 1+ differs from one year class to another; in the present study the range was 23-45%. Although these differ,ences represent less than 10% of the total phenotypic variance, they do show the importance of selecting the better strains for future breeding work. The ranking of salmon strains for performance in the trait “smoltifi~ation at 1 year old” presented here is based on a limited number of brood fish from each strain. It would be desirable to collect further information from more brood stock in the future, especially from those of strains which showed most promise but were represented by few indi~duals in the present study. The estimates of additive genetic variance are very low (Tables III, IV and V), indicating that a selection programme to increase the percentage of fish smoltifying in 1 year may be expected to give only small ,progress by phenotypic selection alone. The best chance for improvement in this trait is to apply family selection. The figures for sire and dam interaction (Table III) and the fact that the dam variance component was consistently higher than the sire component (Tables IV and V) indicate that there is a significant non-additive genetic variance for the trait smoltification at 1 year old. To take advantage of this, a programme of cross-breeding between the best strains of fish has already been started at the Fish Breeding experiments Station, Sunndals~ra, Norway, using brood stock reared in captivity from the 1972 year class.
REFERENCES Aulstad, D., Gjedrem, T. and Skjervold, H., 1972, Genetic and environmental sources of variation in length and weight of rainbow trout (Salmo gair~~e~i). J. Fish. Res. Board Can., 29: 237-241. Becker, W.A., 1967. Manual of Procedures in Quantitative Genetics. Washington State University Press, Wash., 130 pp. Elson, P.F., 1957. The importance of size in the change from parr to smolt in Atlantic salmon. Can. Fish Cult., 21: 1-6. Gjedrem, T. and Aulstad, D., 1974. Selection experiments with salmon. I. Differences in resistance to vibrio disease of salmon parr (S&no sabr). Aquaculture, 3: 51-59. Harvey, W. R., 1964. Computing Procedures for a Generalized Least Square Analysis Program. Paper presented at the Analysis of Variance Conference, Colorado State University, Fort Collins, Colo., 50 pp., mimeographed. Johnston, C.E. and Eales, J.G., 1970. Influence of body size on silvering of Atlantic salmon (S&no salar ) at parr-smolt transformation. J. Fish. Res. Board Can., 27: 983-987. Kanis, E., Refstie, T. and Gjedrem, T., 1976. A genetic analysis of egg, alevin and fry martality in salmon (Salmo saiar) sea trout (Salmo frufta) and rainbow trout (SaEmo gairdneri) Aqua~ulture, 8:259-268. Knutson, S. and Grav, T., 1975. Seawater adoption in Atlantic salmon (Salmo salarf at different experimental temperatures and photoperiods. Int. Comic. Explor. Sea, Comm. Meet. 20. Anadromous and Catadromous Fish Committee. Fisheries Improvement, 24 pp. Koch, H.J.A., 1968. Perspectives in Endocrinology Hormones in the Lives of Lower Vertebrates. Academic Press, London, New York, N.Y., 305-349.
242
Lindroth, A., 1972. Heritability estimates of growth in fish. Aguilo, Ser. Zool., 13: 77-80. Moav, R. and Wohlfarth, G.W., 1966. Genetic improvement of yield in carp. FAO World Symp. Warm-water Pond Fish Cult., Rome, 18-25 May 1966. FAO, Rome, 17 pp. Naevdal, G., Holm, M., M$ller, D. and f&thus, O.D., 1975. Experiments with selective breeding of Atlantic salmon. Int. Count. Explor. Sea, Comm. Meet., 22. Anadromous and Catadromous Fish Committee. Fisheries Improvement, 9 pp. Parry, G., 1960. The development of salinity tolerance in the salmon, Salmo salar (L) and some related species. J. Exp. Biol., 37: 425-434. Refstie, T. and Kittelsen, A., 1976. Effect of density on growth and survival of artificially reared Atlantic salmon. Aquaculture, 8: 319-326. Ritter, J.A., 1975. Relationships of Smolt Size and Age with Age at First Maturity in Atlantic Salmon. Tech. Rep. Ser. No. MAR/T-76-5, Resource Development Branch, Maritimes Region, 7 pp. Sounders, R.L. and Henderson, E.B., 1970. Influence of photoperiod on smolt development and growth of Atlantic salmon (Salmo salar). J. Fish. Res. Board Can., 27: 1295-1311.
10 (1977) 231-242 o Elsevier Scientific ~blishing Company,
231 Amsterdam - Printed in The Netherlands
SELECTION EXPERIMENTS WITH SALMON. II. PROPORTION OF ATLANTIC SALMON SMOLT~FYING AT 1 YEAR OF AGE
TERJE REFSI’IE, TGRSTEIN Qepartment
A STEINE and T. GJEDREM
of Animal Genetics and Breeding, AgricuEtural University of Norway, k-NM4
As ~Nor~ay~ (Received 14 October 1976; revised IQ November 1976
ABSTRACT Refstie, T., Steine, T.k and Gjedrem, T, 1977. Selection experiments with salmon. II. Proportion of Atlantic salmon smoltifying at 1 year of age. Aquaculture, 10: 231-242. Salmon (Salmo sular) brood stock were taken from 37 localities in Norway for 4 consecutive years. Each year, after fertilization, the offspring in each family from each strain were reared in separate egg trays and fingerling tanks. The percentage of fish in each tank which smoltified at 1 year old was recorded, and environmental and genetic factors influencing the percentage smoltification were studied. Percentage smoltifieation was significantly affected by the number of fish held in a tank, or fish density (correlation co’ efficient 0.03-O. 27). Variation between locality of origin of brood stock and per cent smoltification was highly significant for each year class, and there was a high correlation fO.%Q-0.95) between smelt percentage and average weight of fish in a family. Heritabilities in per cent smoltification estimated by sire component from total data had a weighted average of 0.06 (range 0.16 to -0.01). From the dam component heritabilities ranged from 0.20 to 0.40 when tank effect was ignored, and 0.08-0.25 with tank effect taken into account. Variance eomponen~ for locality were two to three times as high as those for sires within localities, indicating that genetic variation is greater between than within localities. Highly significant interaction sire x dam was found, suggesting a considerable nonadditive genetic variance influencing the percentage of fish smoltifying at 1 year of age.
INTRODUCTION
Size is one of the most impo~~t factors determines the age at which salmon smoltify, and parr must reach a certain minimum size before the smoltification process can start (Elson, 1957; Parry, 1960; Koch, 1968; Sounders and Henderson, 1970; Johnston and Eales, 1970; Knutson and Grav, 1975). Parr which fail to reach this rni~rnu~ size in the spring or early summer of one year will remain parr, regardless of growth, until the following spring. In Scandinavian rivers salmon smoltify at 2-5 years old depending on variables such as water temperature, food supply and genetic factors. In commercial salmon farming age at smolti~cation is an important trait, since l-year-old smolts are cheaper to produce than 2-years-old or older fish.
232
In addition, Ritter (1975) found that fish which smoltify at the age of 1 year subsequently mature later than those smoltifying in 2 or 3 years. Early maturation is often undesirable in fish farms as it is accompanied by increased mortality and reduced meat quality. The purpose of this study was to examine the relative importance of genetic and environmental variation in determining the percentage of Atlantic salmon smoltifying at 1 year. MATERIALS
AND METHODS
Data from four year classes (1972-1975 inclusive) of salmon were used in this study. Brood fish were taken from 37 localities in different parts of Norway. For the purpose of this study, fish from a particular river, river system, or a fjord leading to a river or river system are regarded as being from a discrete “locality” or “strain”. Localities from which brood fish were taken were shown on a map by Gjedrem and Aulstad (1974), who also described the mating system used. Eggs from each full-sib family were hatched in separate trays. Subsequently, during the fry and parr stages of growth, fish of each family were reared separately in 2-m2 indoor fibre-glass tanks (Kanis et al., 1976). At the Fish Breeding Experimental Station, SunndalsBra, warm water from Aura hydroelectric power station is used to induce a high percentage of young salmon to smolt at 1 year old. Experience at Sunnda.ls@ra is that fish too big to pass a lo-mm grader by March will smoltify in spring of that year. Therefore, in the present study a smolt is defined as a young salmon not passing a lo-mm grader by March 15th. During late autumn and winter each year the fish in each indoor tank were graded two or three times. Parr not passing a lo-mm grader were counted, weighed, freeze-branded, and transferred to outside concrete ponds. In March the parr which passed the grader in each tank were counted and weighed. Table I shows the number .of sires and dams used as brood fish, the number of localities from which they were taken, and the total number of young salmon each year from which observations were included in statistical analyses. Data from localities represented by only one or two families were excluded from the analyses. TABLE
I
Number of localities, sires, dams and total number of young salmon for the year classes used in statistical analyses 1972 Number of localities Number of sires Number of dams Total number of young salmon
1974
1973 14 52 119
106 254
23 39 66 71608
1975 11 35 94
8 62 149
224 139
114 267
233
For a detailed investigation of the effect of environmental factors on the percentage of salmon smoltifying at 1 year old the data from 1974 were used. The following sources of variation were included in a least squares model. Modes I Yij = /.I+ ai + b, (Xl ii-X 1) + bz (Xzij -X2)
+ b,(X,ij-xs)
+ b4 (X4,-X4)
+ bS (X,ij-X,)
+ eij
where 5.j P ai X, x2
= percentage one year old smolt per group, ith locality and jth tank. = least squares mean. = effect of ith locality. = average hatching date. = average date of first feed. K = average number of days from hatching to recording of smolt percentage. xe = average number of days from first feed to recording of smelt percentage,
x5 = average number of fish per group. e., = random effect for the ijth recording. The”b’s are partial regression coefficients of Y on the respective cated by their suffix.
X’s as indi-
To study the relationship between percentage of l-year-old smelt, fish density and average weight of all fish in the group, the following model was used. Model II Yij = /A+ ai + bl (Xl ij -r,)
+ bz (X2 ij-rz
) + eij
where yij
= actual observation, percentage smelt per group or average weight, ith location and jth tank. = least square mean. = effect of ith locality. = mean value of total number per tank. = mean value of X1 squared.
!J ai “K -K = random effect for the ijth recording. eij bl and b2 are partial regression coefficients of Y on X, and X2, respectively. Correlation between the traits were also calculated. To demonstrate calities individual
differences observations
in percentages of fish smoltifying between lowere used, smoltification being treated as an
234
“all-or-none” trait. A smolt was given the code value 1, and a non-smolt value 0. The following model was used.
the
Model III
Yij = P
+
ai + b (Xii-~)
+ eii
where
x
= the actual observation, 1 or 0. = least square mean. = effect of the ith locality. = partial regression coefficient of smelt/non-smolt of fish per tank. = mean value of total number of fish per tank.
eij
=
yij
c1 ai
b
random
on the total number
effect for the ijth record.
In the analysis of relations between smolt percentage and other charateristics, the regression coefficient of smolt percentage on the total number of fish per tank squared was not significant and hence this element was ignored in the above model. For fish of the 1972 year class matings were made in a factorial way within sets. Each locality could have several sets. However, some groups died before final registration so that an ordinary cross-classified analysis of variance was unsatisfactory for estimating variance components of sires and dams and interaction between sire and dam. Harvey (1964) has given a method where the variance components found by two nested models can be used to find the correct variance components for sire and dams, and interaction between them. Therefore, the two following analyses of variance were applied. ANOVA
I
Source Total Locality
d.f. N-l r-l
0; + I h &
Sire/locality
s-r
u: + 1 kz o&S + I k3 0s”
Dam/sire/locality
q-s
u; 4 1 B1 u&
Individual/dam/sire/locality
N-q
ui
d.f. N-l r-l
Expectation
u; + 2k4u2 s,d +
q-r
us +?k2u2
ANOVA II Source Total Locality Dam/locality
Expectation
of mean square + lkS us”+ 1 k2 u;
of mean square 2 ks
s/d +2+
fJ;
+
2 k6
0;
235
Sire/dam/locality
s-q
0; +*kl
Individual/sire/dam/locality
N-s
uz
The estimate
of interaction
CJ2
u2sd, can be obtained
s/d
from the equation
E (Okd ) = u; + u2sd which gives (-32 zu2 sd s/d -
‘s
2zu2
s/d
+u2
d
A common mating system was used to produce fish of the 1973,1974 and 1975 year classes, whereby sperm from one male fertilized the eggs of three females. Therefore, the results from these three year classes were analysed by a regular hierarchical method with dams nested within sires. This analysis of variance (ANOVA III) included all fish groups for each year class. In 1973, and more frequently in 1974 and 1975, some full-sib groups were divided into ttio tanks. This makes it possible to estimate the variance components due to tank differences and to remove this source of variation when estimating genetic components of variance. The following analysis of variance was applied. ANOVA IV Source Total Locality
d.f. N-l r-l
u: + k,u; f ksu;/,
+ k,u; + k10 of
Sire/locality
s-r
u: + k4u; + k5u;,s
+ k6u;
Dam/sire/locality
q--a
Tank/dam/sire/locality
t-q
u: + kzu; + k 3u2d/s u: + kluf
Individual/tank/dam/sire/ locality
N-t
U2 e
Expectatidn
of mean square
When using this model full-sib groups without replicates were excluded. The heritabilities were calculated by using the sire components (hi) and by using the dam components (hi). Their standard errors were calculated according to the procedure described by Becker (1967). RESULTS
Density The effect of fish density (number of fish per tank at first grading) on the percentage of fish smoltifying at 1 year of age was investigated in several ways.
236
TABLE
II
Average smelt percentage, correlations (r) between smelt percentage and number of fish per tank, regression coefficients (b) of smolt percentage on number of fish per tank, average number of fish per tank and average weight of the fish (g) 1973
1972
Average smelt percentage : Average number per tank Average weight fish (g)
-
17.5 +O.l 0.002+0.0003 0.03
1055k1.3 5.7
to.54
-
1974
67.1 to.2 0.26 0.018+0.0004 1 267+2.3 19.6
t2.56
-
1975
40.5 to.2 0.27 0.018+0.0001 1800*1.5 12.8
i0.36
-
78.4 rO.l 0.14 0.02+0.0004 876il.l 23.3
to.52
By applying Model II it was found that the coefficient of regression for the number of fish squared was not significant, and it was therefore assumed that the regression of smolt percentage on density was linear. The average number of fish per tank for each year class is shown in Table II. By applying Model III the coefficients of regression shown in Table II were obtained. Regression coefficients for the last three year classes of fish were similar, and indicated that there is a reduction of about 2% in the number of fish smolting in 1 year for a rise in fish density of 100 individuals per tank. The effect of density found in the results from the 1972 year class can partly be ex. plained by the low number of fish per tank and low average weight of fish from that year. The effect of fish density on the percentage of fish smoltifying in 1 year was highly significant, and accounted for 0.04, 3.5, 5.6 and 2.5% of the total variance for the 1972, 1973, 1974 and 1975 year classes, respectively. Similar results were obtained by Refstie and Kittelsen (1976).
Dates of hatching and first feed for different families varied both within and between year classes. There were also differences in the number of days from hatching and first feed to the date on which smolt percentage was recorded. Fish of the 1974 year class showed the widest range in hatching date, and this year class was therefore ,used to study the effect of hatching date on the percentage of l-year-old smolt by the application of Model I. Hatching and first feeding dates were found to have no significant effect on the percentage of smolts produced or on the average weight of fish in a tank. The number of days from hatching and first feed to the recording date did have a significant effect on both smolt percentage and average weight of fish. However, these two factors accounted for only 1.3 and 1.5% of the total
237
variance in the traits smolt percentage and average weight of fish per tank, respectively, so it was decided not to adjust the data for these age effects. Locality of origin or strain Model III was used to estimate the effect of strain difference on the percentage of salmon smoltifying in their first year. There was a large difference in smolt percentages between year classes (Table II), possibly because of differences in winter water temperature. In view of these large year-class differences and the fact that few strains were sampled repeatedly over several years, it was decided to estimate the effect of strain on smolt percentage for each year class separately. Deviation from the average smoltification for each year class is shown in Fig.1. The localities are shown in theeorder they appear on a map of the coast of Norway, without trying to take into account differences in latitude. Localities which may include several river systems, those from which farmed brood stock were used, and the Swedish strain Lule?i , are listed separately.
.
- 1972 ymr
A -1973
-;,-
0 -197Y
-I-
.
-‘I-
-1975
da55
Fig.1. Differences between localities for smoltification, expressed by fitting constants for smoltification registered as an all-or-none trait. The specific localities, except LuleP (Sweden), are ranked according to northern latitude.
Differences in percentage of l-year-old smolt between localities were highly significant for each year class. Localities in western Norway seemed to produce the highest percentage of smolts( (Fig.1). Locality variance was estimated by Model III to be 3.7, 7.9, 4.2 and 1.5% of the total variance for the year classes 1972, 1973, 1974 and 1975, respectively. The strain variance is partly genetic and partly environmental, but the size
238
of the genetic variance cannot be calculated from these data. The environmental variance is due to differing qualities of eggs coming from brood stock which lived in different environments before stripping. After fertilization, environmental differences’were removed, i.e. all eggs and fry received the same treatment in the hatchery. It is considered probable that the greater part of the strain variance in l-year-old smolt percentage is genetic. correlation between smelt percentage and weight of fish
The estimated correlations between percentage of fish smoltifying at 1 year of age and the average weight of fish in a tank were 0.89,0.91, 0.95 and 0.95 for the year classes 1972, 1973, 1974 and 1975, respectively. These correlations are highly significant. Tank effect
For the year classes 1973,1974 and 19’75 each full-sib group was hatched in one tray and fed in one 2-m2 plastic tank. Some of the groups were, however, divided into two groups in separate tanks to make it possible to estimate tank effect and ANOVA IV, was used for this purpose. As shown in Table V, the tank effect on smolt percentage was significant for each of the year classes. The variance component represented only 2,5--6.4% of the total variance, which is in good agreement with the results obtained by Aulstad et al. (1972) for rainbow trout fingerlings. Genetic parameters
Before genetic analyses were carried out the figures for smolt percentage were adjusted for differences in fish density by applying the regression coefficients given in Table II. Variance components and h~tab~ity estimates for fish of the 1972 year class are shown in Table III. The estimates were obtained by using ANOVA I and II. All classifications are highly significant. The heritabilities estimated from the sire and dam components are comparable, assuming that there is no maternal effect which would be included in the dam component. Maternal effect, therefore, seems to be of little importance in determining percentage of smolt at 1 year. According to Aulstad et al. (1972), the expected composition of the interaction sire X dam is where 0; @iA
= variance due to dominance. = additive X additive gene interaction.
239
and
= additive
Gn
= dominance
TABLE
X dominance
gene interaction.
X dominance
gene interaction.
III
Variance components and heritabilities for smolt percentage estimated for the 1972 year class Source
d.f.
Variance comnonents
-~ Locality Sire Dam Interaction sire x dam Residual
11 51 46
0.0044** 0.0055** 0.0043**
2 346 106 253
0.0026** 0.1235
Heritabilities
0.16~0.05 0.13*0.09
**p < 0.01.
Assuming that oiD = ub/4, and that the other components are zero, the percentage of variance due to dominance would be 0.07. For the 1972 yearclass the dominance deviation is about half the magnitude of the additive variance and should be taken into account. The variance components for the 1973-1975 year classes estimated by applying ANOVA III are given in Table IV. Only for some of the data could the tank effect be estimated using ANOVA IV, and the results are presented in Table V. The heritabilities estimated from the sire components should not be influenced by non-additive variance and the tank effect seems to have little influence on the sire components (Tables IV and V). The estimated heritabilities for smolt percentage are all small and the sire component is only significant for the 1974 year class. Aulstad et al. (1972) found higher estimates of heritability for weight and length of rainbow trout fingerlings, while Naevdal et al. (1975) and Lindroth (1972) found very high heritabilities for length and weight of salmon Parr, respectively. Moav and Wolfarth (1966), however, found very low heritability estimates for growth in carp. The dam component given in Table IV includes additive genetic variance as well as non-additive variance, maternal effect and tank effect. All heritabilities estimated by means of the dam component are higher than estimates for the sire. The dam components are highly significant for all year classes. By including tank effect in the model, the dam component is reduced from h* = 0.27 to h* = 0.14. DISCUSSION
The results presented
above show that there is considerable
variation
be-
Variance components
0.0071* 0.0020 0.0115** 0.1897
d. f.
22 16 27 71 542
1973
V
0.04+0.09 0.23kO.03
G
0.0049* 0.0037* 0.0097** 0.1911
10 24 59 224 045
Variance components 0.0042* 0.0022 0.0050** 0.0055** 0.2066
d. f.
7 17 28 53 158 181
Variance components
0.0099 0.0039 0.0044 0.0140** 0.1879
d. f.
6 2 11 11 25 369
0.07to.14 0.08+0.09
i22
1974
1973
*P < 0.05; **p < 0.01.
Locality Sire Dam Tank Fish
Source
0.06+0.05 0.20+0.02
iz
0.0093** -0.0001 0.0214** 0.1844
7 54 87 114 120
0.04+0.05 0.09*0.05
i;a
Variance components 0.0111* -0.0078 0.0122* 0.0051** 0.1835
d. f.
2 8 2 13 21 239
1975
year classes
Variance components
year classes
d.f.
Effect of tank calculated, 1973-1975
Variance components
1975
Effect of tank ignored, 1973-1975
d.f.
1974
Estimates of variance components and heritabilities for smoltification.
TABLE
*P < 0.05; ** P < 0.01.
Locality Sire Dam Fish
Source
Estimates of variance components and heritabilities for smoltification.
TABLE IV
-0.04~0.09 0.25kO.43
G
-0.01~0.03 0.40+0.09
AZ
-0.01 0.14
Pooled estimate of G
0.02 0.27
Pooled estimate of i2
241
tween strains, or the offspring of brood fish taken from different localities, in the percentage of salmon smoltifying at 1 year of age under hatchery conditions. Also, the percentage smoltifying at 1+ differs from one year class to another; in the present study the range was 23-45%. Although these differ,ences represent less than 10% of the total phenotypic variance, they do show the importance of selecting the better strains for future breeding work. The ranking of salmon strains for performance in the trait “smoltifi~ation at 1 year old” presented here is based on a limited number of brood fish from each strain. It would be desirable to collect further information from more brood stock in the future, especially from those of strains which showed most promise but were represented by few indi~duals in the present study. The estimates of additive genetic variance are very low (Tables III, IV and V), indicating that a selection programme to increase the percentage of fish smoltifying in 1 year may be expected to give only small ,progress by phenotypic selection alone. The best chance for improvement in this trait is to apply family selection. The figures for sire and dam interaction (Table III) and the fact that the dam variance component was consistently higher than the sire component (Tables IV and V) indicate that there is a significant non-additive genetic variance for the trait smoltification at 1 year old. To take advantage of this, a programme of cross-breeding between the best strains of fish has already been started at the Fish Breeding experiments Station, Sunndals~ra, Norway, using brood stock reared in captivity from the 1972 year class.
REFERENCES Aulstad, D., Gjedrem, T. and Skjervold, H., 1972, Genetic and environmental sources of variation in length and weight of rainbow trout (Salmo gair~~e~i). J. Fish. Res. Board Can., 29: 237-241. Becker, W.A., 1967. Manual of Procedures in Quantitative Genetics. Washington State University Press, Wash., 130 pp. Elson, P.F., 1957. The importance of size in the change from parr to smolt in Atlantic salmon. Can. Fish Cult., 21: 1-6. Gjedrem, T. and Aulstad, D., 1974. Selection experiments with salmon. I. Differences in resistance to vibrio disease of salmon parr (S&no sabr). Aquaculture, 3: 51-59. Harvey, W. R., 1964. Computing Procedures for a Generalized Least Square Analysis Program. Paper presented at the Analysis of Variance Conference, Colorado State University, Fort Collins, Colo., 50 pp., mimeographed. Johnston, C.E. and Eales, J.G., 1970. Influence of body size on silvering of Atlantic salmon (S&no salar ) at parr-smolt transformation. J. Fish. Res. Board Can., 27: 983-987. Kanis, E., Refstie, T. and Gjedrem, T., 1976. A genetic analysis of egg, alevin and fry martality in salmon (Salmo saiar) sea trout (Salmo frufta) and rainbow trout (SaEmo gairdneri) Aqua~ulture, 8:259-268. Knutson, S. and Grav, T., 1975. Seawater adoption in Atlantic salmon (Salmo salarf at different experimental temperatures and photoperiods. Int. Comic. Explor. Sea, Comm. Meet. 20. Anadromous and Catadromous Fish Committee. Fisheries Improvement, 24 pp. Koch, H.J.A., 1968. Perspectives in Endocrinology Hormones in the Lives of Lower Vertebrates. Academic Press, London, New York, N.Y., 305-349.
242
Lindroth, A., 1972. Heritability estimates of growth in fish. Aguilo, Ser. Zool., 13: 77-80. Moav, R. and Wohlfarth, G.W., 1966. Genetic improvement of yield in carp. FAO World Symp. Warm-water Pond Fish Cult., Rome, 18-25 May 1966. FAO, Rome, 17 pp. Naevdal, G., Holm, M., M$ller, D. and f&thus, O.D., 1975. Experiments with selective breeding of Atlantic salmon. Int. Count. Explor. Sea, Comm. Meet., 22. Anadromous and Catadromous Fish Committee. Fisheries Improvement, 9 pp. Parry, G., 1960. The development of salinity tolerance in the salmon, Salmo salar (L) and some related species. J. Exp. Biol., 37: 425-434. Refstie, T. and Kittelsen, A., 1976. Effect of density on growth and survival of artificially reared Atlantic salmon. Aquaculture, 8: 319-326. Ritter, J.A., 1975. Relationships of Smolt Size and Age with Age at First Maturity in Atlantic Salmon. Tech. Rep. Ser. No. MAR/T-76-5, Resource Development Branch, Maritimes Region, 7 pp. Sounders, R.L. and Henderson, E.B., 1970. Influence of photoperiod on smolt development and growth of Atlantic salmon (Salmo salar). J. Fish. Res. Board Can., 27: 1295-1311.