Genetic variance for growth in rainbow trout (Salmo gairdneri)

Aquaculture, 18 (1979) 123-134 o Elsevier Scientific Publishing Company,

GENETIC VARIANCE GAIRDNERI)*

Amsterdam

FOR GROWTH

- Printed

in The Netherlands

IN RAINBOW TROUT

123

(SALMO

R. KLIJPP Lehrstuhl ftir Tierzucht der Technischen stephan (Federal Republic of Germany) *Supported (Accepted

by the Deutsche

Universitiit Miinchen, D-8050 Freising- Weihen-

Forschungsgemeinschaft

12 April 1979)

ABSTRACT Klupp, R., 1979. Genetic culture. 18: 123-134.

variance

for growth

in rainbow

trout

(Salmo gairdneri). Aqua-

The possibilities of genetic improvement of growth of rainbow trout were investigated. Two half-diallel crossing experiments with three strains were performed. In the second experiment families within a strain or strain combinations could be identified. One hundred fish of each strain, strain cross or family were measured at five or four different ages. Differences between strains, crosses and between families within each of them were highly significant at all ages. In juvenile stages heterosis seemed to be present, although it was not statistically significant. Differences between strains became more pronounced as age advanced. Genetic variance within strains and strain crosses was large and appeared to increase with age. Genetic improvement by selection appears promising provided mass selection is not performed too early. The small flvalues of preliminary expt. 2 may indicate strong competition within each group which tends to increase residual variability.

INTRODUCTION

Compared to domestic animals, relatively little breeding work with fish has been reported. The interest of fish producers appears to be directed mainly towards improving management and nutrition. However, introduction of increasingly complex technology into fish production justifies increased attention to improvement, or adaptation, of the genetic level of a fish population to such conditions. In addition, new technologies permit standardization of environment and segregation of breeding groups and thus make breeding work possible on a larger scale. In the present report an attempt is made to add to the still scant knowledge of the genetics of growth in the rainbow trout (Salmo gairdneri). Lewis (1944) reported successful selection for earlier sexual maturity and increased adult weight of rainbow trout. The same was reported by Donaldson and Olson (1955) from a fairly long-term experiment (7-8 generations). Hayford and Embody (1930) succeeded in improving the growth rate of

124

salmonids by selection. Riggs and Sneed (1959) and Dollar and Katz (1964) also reported improved growth after selection in salmonids. In comparative performance tests of German trout strains, Tack (1958) found large differences in growth rate. In 1973 the same author pointed out that the growth improvement may have been caused, at least to some extent, by improved management and feed composition. Cordone and Nicola (1970) found differences in catch yield and growth among four rainbow trout strains. Von Limbach (1969) expected high heritability for growth traits in rainbow trout. Aulstad et al. (1972) estimated the components of variance caused by various factors and found heritability at a level which promised successful selection. Heritabilities appeared to increase with age. Gjedrem (1975) expressed the opinion that even short-term selection should yield improved growth. Savostyanova (1972) found large differences between strains from various European countries but little heterosis in crosses among them. She thought selection to be promising. Gall (1969) crossed wild and domesticated strains of rainbow trout and found heterosis in early growth which diminished with advancing age. Heritability of early growth was found to be around 50% while weight at 1 year of age had a heritability of 20% (Gall, 1965). Reichle (1974) reported similar results. Gall (1975) found a maternal effect in rainbow trout fry which disappeared after 75 days of age. Dzwillo (1962) thought domestication to be of consequence for growth. Fenderson and Carpenter (1971) found young wild salmon to be most aggressive at low stocking rates whereas hatchery-grown salmon showed most aggressiveness at high stocking rates. Vincent (1960) found that domesticated salmon grew better than wild salmon and Keenleyside and Yamamoto (1962) found the number of agonistic interactions to increase with the number of feedings. Size shows increased variability in densely stocked basins (Heland, 1971) mainly because the fish are unable to keep distance. In salmonids a social hierarchy is common (Brown, 1946; Newman, 1956). Moav et al. (1975) report genotyyje-environment interactions in carp and Gall (1969) found interactions between trout strains and stocking density. MATERIAL

AND METHODS

The data originate from a diallel crossing experiment whose design is outlined in Table I. The first part of the experiment involved three pure strains and three crosses on one side, the second part two pure strains and the three reciprocal crosses. In the first part the fish were derived from 4-5 females and 5-6 males, in the second part the fish were offspring of single-pair matings. The fish were grown in warm effluent water of a dairy plant. It was used only once and its heat utilized only to control the temperature of the incoming water. The operation involved a hatchery with eight troughs, a growing house and a laboratory. The growing house contained 36 tanks (2 X 2 X 0.6 m)

125 TABLE I Experimental

design

IA

d

B

C

A

AA

2”

4**

B

AB

BB 2*

4**

C

AC

BC

CC 4**

Letters refer to experiment 1, numbers to experiment 2. * 2 families with identical dam (e.g., B,A,, B,A,). **4 families from two sires and two dams in all combinations (e.g., C,A,, C,A,, C,A,, C,A, where C, denotes dam 1 of strain C).

each having its own water and air supply. For hygienic reasons, sperm had to be transported for fertilization. It was collected in test tubes and stored in melting ice where it remained fully fertile. After fertilization, eggs were transported immediately to the hatchery. Until the fry reached the eye-point stage they were treated twice weekly with malachite. After hatching, the fry were placed in troughs and later in hatching trays. When the fry started to eat they were put into the tanks (Expt. 1) and when they reached 20 g they were transferred to a seine. In Expt. 2 the transfer was later and the fish came into seines at 35 g weight. Four families, identified by fin marking, were put into one seine. Feeding was performed at first with a “Scharfling” apparatus which permitted control of intake, and later with a pendulum automatic feeder (ad. lib.). TABLE II Preliminary experiments for testing differences between tanks Prel. expt. 1 (golden trout)*

Prel. expt. 2**

Weight

Weight

8.3 2.051 2.1

4.0 0.196 1.3

Length

Head length

Height

Width

6.9 0.74 0.533

1.5 0.13 0.928

1.4 0.19 0.384

0.83 0.10 0.491

_ Mean ;

*df 2, 265; **df 5, 534. (J standard deviation within tank. F tank/residual.

126

A sample of 100 fish was measured from each tank. Date and age of measurements are given in Tables III and IV (width was not measured at time 1). For the statistical analysis the following general model was assumed. Y = p + Ul + bij + eijk’ =

observed measurement, = population mean (where all groups are equally frequent), = effect of genetic type (pure strain or cross), ai bli = effect of strain or strain cross within genetic type, = residual. eijk Expt. 2 permitted the analysis of differences within strain and strain crosses and for that purpose the above model was extended by an effect (cijk’) to account for families. For estimating, separately, paternal (sl) and maternal (mi) effects and their interaction (Smli), the data for the two strains and three strain crosses of Expt. 2 were analysed by a factorial model: Y

/J

y = I-1+ si + “j + (sm)ij + f?ijk Possible differences between tanks were investigated in preliminary experiments firstly by adding 90 golden trout to each of the three groups of Expt. 1 and secondly by growing trout of one strain in each tank. TABLE

III

Analysis of variance of Expt.

1 Weight

Source A&days):

SO

Head length 100

df Genetic types Lines CrlXSeS Residual

1 2 2 694

1.34 0.02 1.82 0.03

149.3 21.6 50.6 3.3

160 MS

216

282*

1 26 582 32

17662 47064 1664 448

50

100

160

216

282

7.04 12.69 0.04 0.10

3.0 14.3 0.3 0.2

MS 1221 23649 69896 2426

0.192 0.026 0.265 0.007

0.30 1.42 0.27 0.04

0.01 0.03 0.33 0.05

* x 10’ ; MS, mean square.

TABLE Analysis

IV of variance

of Expt.

2

Source

A&days):

68

df Genetic types

Lines(L) Crosses(C) Families/L Families/C Residual

Headlength

Weight 184

334

88

125 184 MS

334

11 233 4833 906 8826 54

23835 27879 50078 4619 15768 219

0.34 0.16 1.01 0.06 0.41 0.003

0.21 0.02 3.17 0.17 1.27 0.01

2.48 1.92 6.35 1.20 2.81 0.05

MS 1

1 2 4 1 1680

MS. mean square.

125

0.36 0.18 8.48 0.59 3.43 0.02

2.5 4.0 458.7 21.4 133.5 1.6

1.31 4.62 4.18 0.13 2.20 0.04

127

6

24

g

22

1

68

days

9

140

1

g

240

14

I

125 days

184 days

384

days

9

I;Gd 6

10

3

0.9

4

08 0.7 6:6# K&M,

68 days

Fig. 1. Growth performance.

-8 c&%2

125 days

164 days

i%g$

334

days

(a) Expt. 1, (b) Expt. 2, (c) families of strain C.

RESULTS

As is evident from Table II, none of the differences between tanks was significant. Since water temperature, flow rate, depth of water and aeration of the tanks were closely controlled this result appears plausible. Therefore it can be safely assumed that differences between genetic groups were due to inborn differences and were unconfounded with tank effects. However, even though not significant, the F-value of preliminary expt. 1 is fairly large. It is probably caused by an interaction between the golden trout and the various groups they were associated with. The small F-values of preliminary expt. 2 may indicate

128

strong competition within each group which tends to increase residual variability. Weights at various ages are given in Fig. 1, weight growth curves in Fig. 2 a. It is interesting that, in particular in Expt. 1, crosses were superior at younger ages while strain B expressed its superiority only after 5 months of age. In addition to weight, measurements were made of body length, head length, height and width at each age given in Table III. However, since these measures are closely correlated (Table VII) the results of the analysis of variance (AoV) are given for weight and head length only. In the AoV the mean square (MS) “genetic types” was tested against the combined MS strains and strain crosses, the latter each against the pooled error MS. At 100 days of age, differences between crosses and strains were significant for height and width only. At later ages most of the MS’s for strains and crosses were highly significant. However, it is evident that F-values for crosses tend to be larger at earlier ages while later on F-values for strains surpass those of

Weight

Weight(g) 250

(g)

1001

1

184

304

6

1

c 2i6 5

4

I I :i’

I

GenotypesAA-BB----C- _..........AB .-.-._ AC---_ BC-_.__

(a)

Genotypes

BBcc __-m

._.._. CA-.-._ CB---

Famclfes

21Ol2102

.._..._..

2201----2202_._._._

(b)

Fig. 2. Growth curves. (a) Expt. 1, (b) Expt. 2, (c) families of strain C.

Cc)

129 TABLE V Heterosis* for weight (Expt. 1) Age (days)

%

50 100 150 216 282

24 32 0.5 -14 -2

*Measured as deviation of all crosses from respective parental means. TABLE VI Analysis of variance of family differences in weight (Expt. 2) Source

df

Age(days):

68

125

184

334

MS Sire Dam Sire X dam Residual

3* 3 3 1180

Sire Residual

2** 400

1.13 5.77 0.17 0.02

129.0 111.9 5.9 1.5

1920 3212 1034 55

12171 15516 1789 190

2.59 0.18

139.0 0.31

5937 49

20059 304

* 4 families; ** 2 families. MS, mean square. TABLE VII Correlation

Weight Length Head length Height

(X

lo*) between traits at 282 days of age Length

Head length

Height

Width

92

84 88

92 90 83

87 84 76 91

crosses. It appears that differences between crosses are more important in the juvenile stage whereas strains become more diverse as age advances. Weights from Expt. 2 for three ages are included in Fig. 1, and weight growth curves in Fig. 2b. In contrast to Expt. 1, differences between the two pure strains did not surpass those of the crosses at later ages even though they did become more pronounced. This is also evident from the AoV where the Fvalue for crosses remains higher than the corresponding value for the strains (Table IV). The reason for this appears to be the much better performance of

130

the C strain in Expt. 2 than in Expt. 1. In Expt. 2, B strain trout established their superiority only at about 1 year of age. Differences between families were all highly significant. As examples, weights and growth curves of C strain families are shown in Figs. 1 and 2c, respectively. Heterosis was estimated as superiority of the crossbreds relative to mid-parent averages. None of the MS’s due to genetic types were significant. Thus, neither were the differences attributable to heterosis significant. However, some heterosis was discernible in the juvenile stage (Table V). It diminished with advancing age and finally became negative. The same trend occurred in Expt. 2 (BC and parent strains B and C, Figs. 1,2b). The results of the factorial and of the halfsib analysis are given in Table VI. All MS’s are highly significant. The MS for dams decreased relative to the sire MS with advancing age, indicating a decline of the maternal influence. The interaction MS is also highly significant. Taken at face value, it indicates the importance of dominance and epistatic effects for growth of fish, phenomena which can lead to “nicking” and which, for their eventual full exploitation, would demand some kind of cross-breeding. Nevertheless, the sire and dam MS, reflecting mainly additive effects, are considerably greater than the interaction MS. Correlations between various measures are given in Table VII. All are quite high, indicating that they reflect mainly a general size factor. ESTIMATION

OF GENETIC

VARIANCE

Even though only few strains and crosses and few families have been studied, it is quite evident that considerable genetic variability is present. In view of the scarcity of estimates of genetic variance in trout, it appears desirable to analyse these results in this respect and to attempt to quantify the importance of the genotype. For this purpose the expected composition of “between families” MS (Table IV) in terms of genetic variance components was derived: E(MS) =R +fG/2=-

R f” n

= = = =

residual additive number number

S

=&es

s-1 f-l

m-l n G/4 = -n f-l

G/4

variance genetic variance full-sib families within strain or strain cross = s X m full sibs/family

m = dams The composition differs depending in each strain or cross (Table I):

on whether

there were two or four families 100 +-G 3

4families:

f=4,s=2,m=2,n=lOO

E(MS)=R

2 families:

f = 2, s = 2, m = 1, n = 100

E(MS)=R+-G

100 4

131 TABLE VIII Heritabilities* for growth traits

Age (days)

Weight

68 125 184 334

0.73 1.06 0.74 0.82

f f * *

Head length 0.35 0.49 0.34 0.38

1.05 0.99 0.65 0.76

f + * t

0.60 0.47 0.32 0.40

*Estimated from full-sib or maternal half-sib (within sire) covariances. Standard errors were estimated as given by Dickerson (1963).

As is evident from the composition of the (MS), only additive genetic effects were considered in the estimate and all others - maternal, dominance, epistasis - were neglected. However, in view of the very restricted numbers of families which could be analysed, only a rough estimate of genetic variance is justified and any further sophistication would have to await new experiments. As shown in Table VIII, the genetic variance is quite large relative to the total variance. The standard errors of this ratio were estimated according to Dickerson (1963). Thus there are indications that selection should be successful. DISCUSSION

The number of genetic groups was quite small and the results obtained are strictly valid for this material only. However, the three strains are typical representatives of trout stock used in the Federal Republic of Germany. Therefore it appears that the results, in particular those from “between family” analysis, later experiments not withstanding, can be extrapolated to the German trout population. Any breeding experiments demand that environmental differences between genetic groups be either avoided or taken into account. So far, most breeding experiments with trout have been performed in ponds which are quite variable so that it is difficult to get valid results, in particular since replication is often not possible. Also very often the growth rate is too slow to have results within one year. One way to take account of environmental differences is the use of a control strain as mentioned by Probst (1949) and suggested also by Klupp (1976). However, since fish populations form social hierarchies (Brown, 1946; Zamecki, 1964; Heland, 1971), interactions between the control and the experimental strains are possible and differences between control strains in different tanks will not necessarily indicate only environmental differences. In domestic fish, low stocking density and good nutrition can diminish such interactions (Fenderson and Carpenter, 1971; Klupp, 1976). Warm-water-fed tank systems can be tested for differences by a uniformity trial, as was done in preliminary expt. 2. The low F-values of this trial are caused probably by competition in the densely stocked basins. In contrast, the

132 golden trout of preliminary expt. 1 gave larger (though still insignificant) Fvalues. It could be observed during feeding that golden fish were at the lower end of the social hierarchy, coming to feed only in the evening hours. This is similar to the observations of Keenleyside and Yamamoto (1962). In this connection it should be mentioned that individual solitary fish were observed even in densely stocked basins (4000 fish) which successfully defended their place, being obviously at the top of the hierarchy. The study of such behavior would require permanent and visible markings. As to growth, heterosis seems not to be very important in trout; nearly all F-values were insignificant. Possibly the strains are insufficiently differentiated yet. This agrees with the investigations of Gall (1969) and Savostydnova (1972). However, mating between distant strains - e.g., early and late maturing - was made possible only recently by development of sperm conservation (Stein, 1975). Genetic relationships between fish populations can be inferred from gene marker frequencies (Keese, 1972; Utter and Hodgins, 1972) and they should allow distant strains to be selected for crossing. Of particular interest would be species hybrids (Adumua-Bossman, 1970; Suzuki and Fukuda, 1971). If sterile, their growth would suffer no break due to spawning. Similar possibilities should arise when polyploidization succeeds (Lieder, 1964; Lincoln et al., 1974). Nevertheless, most differences between strains and crosses are highly significant and differences between strains become greater with increasing age. This is particularly evident in Expt. 1. Genetic variance (G) between strains with an average inbreeding coefficient f equals 2 fG while the variance between crosses of such strains should equal fG. Therefore strains are more differentiated than crosses, and a higher F-value should be expected. In the factorial analysis the paternal variance should be caused primarily by differences in breeding value while the maternal variance should, in addition to this, also reflect the maternal effects. Gall’s results (1974) from trout support this assumption. The ratios given in Table VIII differ from heritabilities to the extent that maternal effects cause differences between families. Such effects should be important at younger ages, which is also suggested by the dam MS being relatively much larger at younger ages than the size MS. Maternal effects may also explain the apparent contradiction between the strain analysis of Expt. 1 where strains appear to become more distinct with advancing age, and the larger size of heritability ratios at younger ages from Expt. 2 as given in Table VIII. Aulstad et al. (1972), albeit also with limited material, report variances due to sire effects to increase with age. Nevertheless, the size of heritability ratios found here, in particular of those found from later ages, indicates important genetic variability within trout strains which should lead to a reasonable response to mass selection. Response to selection was reported also by a number of workers, e.g. Donaldson and Olson (1957), Dollar and Katz (1964), Savostyanova (1972) and Gjedrem (1975), and it seems quite easily explainable in view of our results.

133 REFERENCES Adumua-Bossman, J., 1970. Vergleichende Untersuchungen iiber Wachstum und morphologische Eigenschaften von reinrassigen Karpfen (Cyptinus carpio L) and Goldgiebeln (Carassius auratus gibelio (Bloch)) sowie ihrer aus reziproken Kreuzungen hervorgegangenen Bastarde. Dissertation, Technische Universitiit, Miinchen-Weihenstephan, 127 pp. Aulstad, D., Gjedrem, I. and Skjervold, H., 1972. Genetic and environmental sources of variation in length and weight of rainbow trout (S. gairdneri). J. Fish. Res. Board Can., 29: 337-341. Brown, M., 1946. The growth of brown trout (S. trutta). 1. Factors influencing the growth of trout fry. J. Exp. Biol., 22: 118-129. Cordone, A. and Nicola, St., 1970. Harvest of four strains of rainbow trout (S. goirdneri) from Beardsley Reservoir California. Calif. Fish Game, 56: 271-287. Dickerson, G.E., 1963. Techniques for research in quantitative animal genetics. In: Techniques and Procedures in Animal Production Research. Am. Sot. Anim. Sci., Bethesda, Md., pp. 57-96. Dollar, A. and Katz, M., 1964. Rainbow trout brood stocks and strains in American hatcheries as factors in the occurrence of hepatoma. Prog. Fish Cult., 26: 167-174. Donaldson, L.R. and Olson, P.R., 1957. Development of rainbow trout brood stock by selective breeding. Trans. Am. Fish. Sot., 85: 93-101. Dzwillo, M., 1962. Domestikation bei Fischen. Z. Tierz. Ziichtungsbiol., 77: 172-185. Fenderson, 0. and Carpenter, M.R., 1971. Effects of crowding on the behaviour of juvenile hatchery and wild landlocked Atlantic salmon (S. salar L.). Anim. Behav., 19: 439-447. Gall, G.A., 1969. Quantitative inheritance and environmental response of rainbow trout. In: O.W. Newhaus and I.E. Halver (Editors), Fish in Research. Academic Press, New York, N.Y., pp. 117-184. Gall, G.A., 1974. Influence of size of eggs and age of females on hatchability and growth in rainbow trout. Calif. Fish Game, 60: 26-35. Gall, G.A., 1975. Genetics of reproduction in domesticated rainbow trout. J. Anim. Sci., 40: 19-28. Gjedrem, T., 1975. Possibilities for genetic gain in salmonids. Aquaculture, 6: 23-29. Hayford, C. and Embody, C., 1930. Further progress in the selective breeding of brook trout at the New Jersey State Hatchery. Trans. Am. Fish. Sot., 60: 109-113. Heland, M., 1971. Influence de la densite du peuplement initial sur l’acquisition des territoires chez la truite commune (S. trutta L.) en ruisseau artificiel. Ann. Hydrobiol., 2: 25-32. Keenleyside, M. and Yamamoto, F., 1962. Territorial behaviour of juvenile Atlantic salmon. Behaviour, 19: 139-169. Keese, A., 1972. Elektrophoretische Studien zur Populationsanalyse bei der Regenbogenforelle. Dissertation, Universitiit Giittingen, 110 pp. Klupp, R., 1976. Ziichterische Probleme in der Fischerei. Fischwirt, 26: 19-23. Lewis, R.C., 1944. Selective breeding of rainbow trout at Hot Creek Hatchery. Calif. Fish Game, 30: 95-97. Lieder, U., 1964. Polyploidisierungsversuche bei Fischen mittels Temperaturschock und Colchizinbehandlung. Z. Fischerei, NF, 12: 247-257. Lincoln, R.F., Aulstad, D. and Grammeltvedt, A., 1974. Attempted triploid induction in Atlantic salmon (S. salar) using cold shocks. Aquaculture, 4: 287-297. Moav, R., Hulata, G. and Wohlfarth, G., 1975. Genetic differences between the Chinese and the European races of common carp. 1. Analysis of genotype-environment interactions for growth rate. Heredity, 34: 323-340. Newman, M., 1956. Social behaviour and interspecific competition in two trout species. Physiol. Zool., 29: 64-81. Probst, E., 1949. Vererbungsuntersuchungen beim Karpfen. Allg. Fisch. Ztg., 74: l-8. Reichle, G., 1974. Kann man die Regenbogenforelle ziichterisch noch verbessern. Fischer Teichwirt, 25: 75-76.

134 Riggs, C.D. and Sneed, K.E., 1959. The effect of controlled spawning and genetic selection on the fish culture of the future. Trans Am. Fish. Sot., 88: 53-57. Savostyanova, G., 1972. Comparative fishery characteristics of different groups of rainbow trout. In: B. Cherias (Editor), Genetics, Selection and Hybridisation of Fish. Israel Programme for Scientific Translations, Jerusalem, pp. 221-227. Stein, H., 1975. Spezielle Untersuchungen am Fischsperma unter besonderer Beriicksichtigung der Spermakonservierung. Dissertation, Technische Universitlit, MiinchenWeihenstephan, 147 pp. Suzuki, R. and Fukuda, Y., 1971. Survival potential of Fl hybrids among salmonid fishes. Bull. Freshwater Fish. Res. Lab., Tokyo, 21: 69-83. Tack, E., 1958. Erstmalige echte Leistungspriifungen in der Forellenzucht. Allg. Fisch. Ztg., 83: 196-199. Tack, E., 1973. Ziichtungsfragen in der Forellenzucht. Gsterr. Fischerei, 26: 77-84. Utter, F. and Hodgins, H., 1972. Biochemical genetic variation at six loci in four stocks of rainbow trout. Trans. Am. Fish. Sot., 101: 494-502. Vincent, R., 1960. Some influences of domestication upon three stocks of brook trout (Suloelinus fontindia Mitchill). Trans. Am. Fish. Sot., 89: 35-52. Von Limbach, B., 1969. Progress in sport fishery research, 1969. Fish Genetics Laboratory, Beulah, Wyoming. Zarnecki, S., 1964. Das Problem der Vorwiichse in den Karpfenteichen. Z. Fischerei, NF, 12: 685-706.