two-way selection in common carp (cyprznus carpi0 · 2003. 7. 26. · two-way selection for growth...

TWO-WAY SELECTION FOR GROWTH RATE IN THE COMMON CARP (CYPRZNUS CARPI0 L.)I,

R. MOAV

Department of Genetics, The Hebrew University, Jerusalem, Israel

AND

G. WOHLFARTH

Agricultural Research Organization, Fish and Aquaculture Station, Dor, Israel

Manuscript received May 28, 1975 Revised copy received August 18, 1975

ABSTRACT

The domesticated European carp was subjected t o a two-way selection for growth rate. Five generatioils of mass selection for faster growth rate did not yield any response, but subsequent selection between groups (families) resulted in considerable progress while maintaining a large genetic variance. Selection for slow growth rate yielded relatively strong response for the first three generations. Random-bred control lines suffered from strong inbreeding depression and when two lines were crossed, the F, showed a high degree of heterosis. Selection was performed on pond-raised fish, but growth rate was also tested in cages. A strong pond-cage genetic interaction was found. A theoretical explanation was suggested involving overdominance for fast growth rate and amplification through competition of intra-group but not inter-group variation.

HE common carp has been cultivated for food in China for over 2500 years T ( D ~ ~ ~ ~ 1971), and in Europe since at least the Middle Ages (MANN 1961; HICKLING 1968; BARDACH, RYTHER and MCLARNEY 1972). In spite of the increasing importance of fish farming as a source of animal protein, only little is known about the genetics of their economically important characters. Extensive selection and hybridization of carp has been practiced in the USSR, particularly in the adaptation of new strains to harsh environments (KIRPICHNIKOV 1971 and 1972; KIRPICHNIKOV et al. 1972). Heterosis for fast growth rate in carp has been well documented ( MOAV and WOHLFARTH 1973; MOAV, HULATA and WOHLFARTH 1975). Between 1960 and 1964 we conducted, in ponds, several small-scale, single-step selection experiments for high and low growth rate in carp. Selection response was asymmetrical, being zero or even slightly negative in the high direction and appreciable in the low direction ( MOAV and WOHLFARTH 1966 and 1973). These studies, as well as others, indicated that the selected breeds of the European carp has reached a selection plateau for fast growth rate, while maintaining a large genetic variance (MOAV, WOHLFARTH and LAHMAN 1964; WOHLFARTH et al. 1965; WOHLFARTH, MOAV and HULATA 1975).

This research was supported in part by the “United States-Israel Binational Science Foundation” grant no. 83.

Genetics 82: 83-101 January, 1976.

84 R. MOAV AND G . WOHLFARTH

This paper describes the results of a large-scale selection experiment for growth rate initiated in 1965. It covered five generations of two-way selection plus subsequent testing of a single fast-growing line that originated from selection in the high direction.

MATERIALS A N D METHODS

The experiments were conducted with the local strain of the domesticated European carp (TAL and SHELUVSKY 1952). The base population serving for the first cycle of selection was composed of mixed offspring of a single multiple spawn, involving 110 females and 21 males. The females belonged to five different familial lines and the males of two additional lines, each collected at a different fish farm. This multiple spawn was arranged at the Gan-Shmuel fish farm on April 24, 1965, and approximately 30,000 fry were transferred to Dor on May 20. Soon afterwards, a random sample of fry was chosen for a random-bred control and the highest and smallest 2% were selected to form High and Low lines (Figure 1). In subsequent years, selection was performed only after termination of the growth tests in ponds. The selected fish were raised to spawners and in the following spring (April, 1966) each group (High, Random and Low) was divided into three suh-groups of parents.

The sub-groups (replicated spawns) were spawned in separate ponds. Some were located at Dor and others at several collaborating carp-breeding farms, each contributing the spawning, nursing and tcsting ponds required for our experiments (WOHLFARTH et al. 1965). Into each spawning pond a number of males and females were introduced, but not all of them participated in the mass spawning and the gametic contribution of those that did participate varied widely. Therefore, the effective number of parents was smaller than that introduced into the pond. Ten to thirty days after hatching, roughly counted samples of fry were transferred from the spawning ponds into nursing ponds where they were reared to a size (20-50g) enabling their brandmarking (MOAV, WOHLFARTH and LAHMAN 1960). Counted and weighed samples of marked fish were stocked into the experimental ponds and cages, usually during July. The tests were terminated during November and December.

Technical difficulties caused the failure of two of the three attempted spawns of the random-bred control, leaving only one offspring group which was discarded after testing (Figure 1). In 1966 the fish were tested only in ponds. When the tests were completed (Novem- ber, 1966), the largest individuals within each one of the three High replications, and the smallest individuals within each one of the three Low replications were selected for spawning in the following year. The discarded random-bred control group was replaced by two new random- bred controls, henceforth designated High-R and Low-R. The two were derived, respectively, from the High and Low lines by choosing random samples from all the replications and mating females of one replication with males of a second replication. These two control groups were supplemented by a third control group (henceforth designated crossbred control), made up of specific F, crossbreds whose growth rates were similar to that of the base population. One crossbred was used repeatedly every year by repeat spawning of parents of the same generation (carp can be bred for many years) from 1966 to 1970. Five replicated spawns of this cross were tested in 1969 (Table 1).

In order to minimize the rate of inbreeding in the four lines (High, Low, High-R and Low-R) males of each replicate spawn were always mated to females of other replications within the same line. Thus, replicate spawns were not separate selection lines. Rather, the genetic reshuffling every generation kept variation between them t o single-generation genetic drift, ‘common environment’ and residual ‘error’ variance components.

In the following three years (1967, 1968 and 1969) the same reproduction and selection procedures described for 1966 were followed. The spawning and nursing ponds were again distributed between Dor and the collaborating farms. In an attempt to slow down inbreeding and possible genetic drift, larger numbers of individuals were selected at the expense of lower selection intensities (Table 1). and to ensure a sufficient number of replications, six separate

SELECTION FOR GROWTH RATE IN CARP 85

1965

1966

a b c 482 496 501

Randombred control

(discarded)

a b c 537 541 541

l g 6 7 ~ Low-R

a b c d a b c d e f 450 457 470 504 508 539 545 546 546 553

a b c d a b 601 616 617 628 700 754

a b a b c 583 629 561 572 573 -

A a b c 761 812 846

a b c d 731 733 788 790

a b c d 562 562 571 515

a b c d e 580 609 613 614 630

a b a b c a b a b c a b

FIGURE 1 .-Lineage and mean corrected weight gains of the replicate spawns of the High and Low selection lines and the two random-bred controls High-R and Low-R when tested in ponds. a, b, . . . designate replicate spawns of each line arranged in an increasing order. Mean weight gains (in g) over ponds were corrected for differences in initial weights but not standardized, hence direct comparisons can be made only within years. See Table 2B for supplementary results of Crossbred control lines, and text for further explanations.

501 501 606 617 639 580 583 491 537 555 570 655

spawns were attempted in each selection and random-bred control lines. The high proportion of failures was due primarily to young (one year old) and relatively small-sized spawners, and lack of sufficient technical control over the spawning and nursing operations that were carried out in collaborating fish farms.

Beginning in 1967, some replicates of the selection and control lines were also tested in small (0.53 = 0.125 m3) cages placed in separate ponds at Dor. The fish tested in cages were randomly-


TABLE 3

Selection intensities and corrected weight gains of the crossbred conlrol when tested in ponds A. Selection intensities in the High and Low selection lines

Year 1966 1967 1968 1969

No. of selected High 43 269 305 115 parents Low 97 147 375 198

Percent of selected High 19 21 37 43 parents Low 15 27 37 45

B. Corrected weight gains of the crossbred control in ponds (T, V, X, Y and Z were five different, commercially approved F, crossbreds all having similar

growth rate.)

Year 1966 1967 1968 1969 1970

g g g g g T 543 835 V a 51 7 640 851 647 703

b 671 C 687 d 618 e 623

X 576 Y 654 Z 634

Mean 530a13 608+-14 843+18 6 4 9 k 9 664-+11

drawn samples from exactly the same progeny populations and the same nursery ponds from which similar random samples were drawn for stocking the test ponds. Thus, except for small sampling ‘errors’, the samples tested in ponds and in cages were genetically identical. We should emphasize that although the fish of the same progeny populations were tested simultane- ously in ponds and in cages, selection was performed only on pond-grown fish. Thus, response in cages may be considered a correlated, rather than direct, response to selection. In 1967 and 1968 random samples of 6 fish of each replicated spawn were stocked respectively in 10 and 14 separate cages. In subsequent years mixed cages were added, i.e., cages costocked with fish of several groups (Tables 3 and 4).

Data analysis

All the experimental ponds in which the nursed fish were grown were mixed ponds; i.e., all the replicates of all the lines were costocked together into the same ponds. In common statistical terminology each mixed pond was a ‘block‘, located at a different fish farm (DAN, NIR DAVID, etc., Table 2). Differences in pond fertility and fry density introduced variation in mean weights of the nursed groups of fish. Since growth rate in the tests was causally correlated with initial weight, an appropriate correction had to be made and this was done as follows (WOHLFARTH and MOAV 1972): y=y’ - b ( z -z.), where y= corrected weight gain (uncorrelated with initial weight) and taken as a measure of growth capacity; b= coefficient of linear regression of weight gain ( y ’ ) on initial weight (z), and z.= mean initial weight of all the groups partici- pating in a given test. The correction factor b varies between experimental conditions; therefore different b values had to be fitted to different ponds and cages. Estimation of the b values was made by application of the “multiple-nursing” technique as described by WOHLFAXTH and MOAV (1972) and by MOAV and WOHLFARTH (1973).

87 SELECTION FOR GROWTH RATE I N CARP

TABLE 2

Mean corrected weight gains in ponds

Mean Number Corrected weight gains in grams initial Number of ___--

Group weight of replicate Nir- Gan- Beit- Year (line) (g) fish spawns Dan+ David Shmuel Yehiam Zera Mean

High 32 1055 3 792 624 444 254 585 540210 1966 Random 42 629 1 693 522 389 221 474 460218

Low 31 1594 3 705 576 410 241 532 493 t lO Cross-C.* 39 920 2 763 632 449 266 540 530213

Correction factor b 4 3 3 2 3 ~

High 38 2154 3 693 491 805 - 284 5 6 8 k l l High-R 33 824 2 761 511 853 - 299 606214

Low 39 1319 4 547 415 688 - 231 470210 Cross-C. 38 560 2 777 499 881 275 608214

1967 Low-R 32 3170 6 658 457 767 - 276 539+8

Correction factor

~

b 4 3 4 - 2

High 40 1314 4 884 464 935 - - 761k12 High-R 35 928 3 931 482 1006 - - 8062 14

1968 Low-R 50 540 2 811 440 930 - - 727 t18 Low 32 1441 6 669 400 727 - - 6152 12 Cross-C. 35 630 2 987 479 1067 - - 843218

Correction factor b 4 3 4 - - High 28 2348 5 814 557 496 568 - 609k9 High-R 23 2661 4 796 507 442 525 - 568k10

1969 Low-R 28 1872 4 762 481 443 485 - 542k10 Low 33 3522 5 752 492 445 506 - 549 Cross-C. 30 2440 5 907 553 559 581 - 649 k 9

Correction factor b 4 3 3 3 -

High 26 11581 2 592 523 1111 223 - 612k 14 High-R 24 1466 3 536 400 1011 171 - 530211

1970 Low 16 1018 2 477 411 941 176 - 501 f 14 Cross-C. 33 1203 3 633 593 1206 221 - 664f11 H69XLR69 22 1064 2 573 484 1080 189 - 582+14 HR69XLR69 33 1562 3 589 536 1142 216 621 2 11

Correction factor b 3 3 5 2

The weight gains in this table are averages over the replicate spawns of Figure 1 and Table 1B. * Crossbred control. +Dan, Nir-David, etc. are names of fish farms. One test pond was located in each farm.

88 R. MOAV A N D G . W O H L F A R T H

TABLE 3

Supplementary details of the tests in cages

Year 1967 1968 1969 1970 Stocking Separate Separate Separate Mixed Separate Mixed

No. cages/replicate 14 10 6 20 3 28

Mean initial weight (g) 41 43 35 33 28 29 No. of fish/cage 6 6 10 14 20 10;20;30

Dates 23.7-13.12 20.9-29.11 25.7-4.12 24.9-5.12 5.8-16.11 5.8-27.11 SErep (€9 6.2 3.1 6.7 5.5 3.4 3.5 % i n , (g) 6.2 3.3 6.4 2.2 4.2 3.1

Correction factor (b) 1.84 1.40 2.00 1 .oo 1.64 2.50

TABLE 4

Mean corrected weight gains (in grams) of the tests in cages

Year 1967 1968 1969 1970 Stocking Separate Separate Separate Mixed (S+ M ) * Separate Mixed (S M)

Wt. wt. W!. WJ. Wt. wy. Wy. wy. Replic. gain Replic. gain Replic. gain gain gam Replic. gain gain gain

a 235 b 117 High c 253 c 123

d 133 Mean 244 124

a 205 a 97 High-R b 211 b 97

c 106 Mean 208 100

b 214 a 114 Low-R c 222 b 113

Mean 218 114

b 175 a 93 Low c 189 c 105

d 102 Mean 182 100

Crossbred Va 127

Mean 127

Overall mean 213 111

control

b 207 d 181 e 187

192

a 172 b 178 d 166

172

b 187 c 197 d 173

186

b 159 d 194 e 192

159t

Va 161 Y 195

178

179

137 203 a 133 129 185 b 128 127 187 131 192 131

104 169 b 105 107 173 e 114 105 166 105 169 103

a b 111

111

119 171 Va 131 195 Y 119

119 183 125

118 180 122

127 129

128

114 108

111

85 105

95

120 123 121

115

133 132

133

113 115

114

92 i l l

101

129 125 127

119

(Two types of stocking fish in cages were used; separate ( S ) and mixed (M). Replicate spawns are the same as those tested in ponds (Figure 1 and Table 1B) .)

* (S+M) =separate plus mixed cages. In pooling together the results of the separate and mixed cages, the differences between their overall means were added to the mixed cages means, i.e. if Y , = mean in separate cage and Y , = mean in mixed cage, then the shifted pooled mean is (Y , - Y,, + (Y , + Y,).

2 + Mean does not include replications d and e.


Mean weight gains varied widely between years, and even between ponds and cages of the same experiment. This variation was due to fluctuations of environmental factors, such as stocking densities, pond fertility, management practices, etc. Since the standard deviation of weight in carp is approximately proportional to mean weight, selection differentials and selection gains were standardized to the crossbred-control mean by multiplication of the annual means of the selected and random-bred lines by 600g and divided by the mean of crossbred control. In cages the same procedure was applied, except that 2OOg replaced 600g in the adjustment factor. The lower value in cages was a reflection of the poorer growth rate of the carp stocked in cages.

The “observation’’ (Yiik) of our ponds tests was the mean corrected weight gain of the ith replicate spawn of the ith line (High, High-R, etc.) in the kth pond. For partitioning into variance components it can be expressed as follows,

y . . * J k - - P + Pk + Li + R i j + ( P L ) ,k + Wijk

when, p = mean of all the ponds (in one year) ; = deviation of the kth pond; = deviation of the i th line; = deviation of the j th replication from the mean of the i t h line;

= the “error” deviation including pond x replication interaction.

P, Li Ri j (PL) ik = deviation of the pond x line interaction; Wi j k

An estimate of the “error” variance component is the mean square of

( Y i j k - y . . k ) - ( y i f . - Y..J=(PL,,- PL.,- PL,. +P..)-(wijk-Wij.-W..k+W...).

( Y i j . - Y,..) = ( R i j - Ri.) + (Wij. - W,.J

vi.. - Y. . , ) = (Li--L.) + (Ri . --R.,) + ( P L , . - P L . . ) + Wi.. - W ... 1.

An estimate of the “between replicates within lines” variance component is the mean square of

and an estimate of the ‘between lines’ variance component is the mean square of

These three equations show that in this experiment the computable estimate of the ‘error’ variance includes a pond x line component which is not present in the two other variance components of interest. Since the assumption that this interaction is zero is unjustified (MOAV, HULATA and WOHLFARTH 1975), therefore the ‘error’ variance is unuseful and had not been presented.

The ‘between replications within lines’ (S2,,,) variance in a given year was computed as follows,

lines rep

3 4 (yij.-Yi..)’ ’Z,,, =

lines (rep - 1 )

Dividing S2,,, by the number of replicates and taking the square root gave us Standard Errors for the line means (right-hand column, Table 2). Similarly, the estimate of the variance between lines was computed by the following equation,

__ (lines - 1) ‘‘lines =

RESULTS

Tests in ponds The performance in ponds of all the genetic groups, averaged over replicate

spawns and corrected for differences in initial weights, are summarized in Table 2. The standardized generation means are illustrated graphically in


Figure 2, and the non-standardized replications means (averaged over ponds) in Figure 1 and in Table 1B. The single spawn of the random-bred control of 1966 had an unexpectedly low weight gain (460 g, Table 2). This was contradictory to earlier as well as subsequent results, and had no reasonable explanation. Hence, this line was omitted from further considerations. The means of the two crossbred controls of 1966 (T and V, Table 1) was 530 g; that is only 10 g below the High selection line, but 38 g above the Low selection line. This asymmetry was consistent with our earlier findings (MOAV and WOHLFARTH 1966). The results of the following generation (1967) may be summarized by the following points: (i) The High line had a poorer performance than the High-R control (568 g uersus 606 g) , showing a negative response to selection in the high direction. (ii) The High-R was practically identical to the crossbred control. (iii) The mean of the Low line (470 g) was 69 g lower than that of Low-R (539 g) indicating a continuous response to selection in the Low direction. (iv) The apparent downtrend of the two random lines is probably indicative of inbreeding depression. Note that this downtrend is not due to environmental fluctuation between years -the use of the repeat crossbred control has eliminated this factor. The 1968 results were very similar to those o€ the previous year. The High line was below the High-R control despite another generation of selection. The Low line continued to respond, but at a lower rate, and all the four lines (High, High-R, Low and Low-R) continued the downward trend relative to the crossbred control, indicating further inbreeding depression. The 1969 results were remarkably different from those of the earlier generations. Most striking was the reversal in ranking between the High line and the High-R control. The High line stopped its downward slippage relative to the crossbred control, when the High-R (on all its four replicates) had plunged down to a low level not much higher than the Low-R. Its deterioration in growth rate was accompanied, in two of the four replicates (b and c ) , with a high proportion of deformations, i.e., over 60% of the individuals had reduced dorsal fin, ranging from only a small reduction to complete absence. These deformations are typical manifestations of inbreeding depression in carp.

A most unlikely result was the fast growth rate of the two Low line replicates d and e (Figure 1 ) . A thorough check did not uncover any reason for suspecting their legitimacy. The two were reciprocal crosses between two replicate spawns of the Low line of 1968, and each of the remaining three (a, b and c) Low line replications had one parent in common with them. The great similarity between these two deviant groups is strongly founded on large samples of fish tested in four ponds (Table 2) and many cages (Table 3-to be discussed later). Thus, it appears that random genetic drift, sampling ‘errors’ and partial contamination of parents can be ruled out. The only possible, but unlikely. mistake is a substitu- tion, without knowing, of a whole group of parents. The mean of all the five LOW replicates was 549 g. Removal of d and e lowered it to 503 g and only this last value (after standardization) was used in Figure 2.

In the Fall of 1969 a rather weak selection intensity was applied in only three replicates (b, c and d) of the High line and in three replicates (a, b, and c) of the

SELECTION FOR GROWTH RATE I N CARP 91

650

600

h

v M

E d

550 U

d CM g 2

T

a 500

U a

450

, ̂^

\ LOW-R ‘A High-R

3 Low 4uu 1965 1966 1967 1968 1969 1970

Year

FIGURE &.--Standardized mean weight gains in ponds of the four selection lines, crossbred controls and two inter-line crossbreds (in 1970) , averaged over replicate spawns.

n OI, v

+50 - g

r) f -100 -

LOW

3 -150 - Q \ U

4

200 300 400 500 600 7 00

I -*0° - 100

4 0

Acumulated s e l e c t i o n d i s t a n c e ( 9 )

FIGURE 3.-The regressions of the cummulative standardized selection response on the cummulative standardized selection distance in the High and Low selection lines (1965-1970).


Low line. While the two High replicates a and e were left out due to technical complications, the two Low replicates d and e were selected against because of their fast growth rates. Low-R was excluded from further testing. Instead, the following two crosses were made (in April, 1970) and tested: High x Low-R and High-R x Low-R. The first cross was intermediate to its parents (Figure 2), but the second exhibited a marked degree of heterosis.

Figure 3 shows the accumulated selection differentials and responses over five generations. The complete lack of response in the High direction is contrasted with an appreciable response in the Low direction during the first two or three generations. The realized heritability of the latter, before it stopped responding, was around 0.3.

Tests in cages Details of the growth tests in cages are given in Table 3. The results are

summarized in Table 4 and the standardized weight gains are presented in

250

240

230

h M

e rl

4 M

- 220

* 210 5 $ 8 200

: 190

rl

E Tt

5

Tt Q -

180

170

160

150

140 1965 1966 1967 1968

gains in cages

1969 1970

of the four selection

1971 Year

and crossbred FIGURE 4.-Standardized mean weight control. (Symbols as in Figure 2).

lines


Figure 4. We might remention at this point that the fish tested in ponds and cages were random samples of nursed off springs of pond-grown parents. A comparison of the 1967 and 1968 weight gains in cages and ponds shows a drastic change in ranking between the High and High-R lines and the 1969 and 1970 results tended to agree with. and thus strengthen, the earlier results. The large changes in relative growth rates in cages and ponds proved the existence of a strong interaction between genotypes and method of stocking. The most spectacular interaction involved the High-R line in 1967 and 1968. While in ponds High-R was the best of the four experimental lines (Figure 2), its performance in cages was almost as poor as that of the Low line. Its decline in ponds in 1969 and 1970 had no reflection in cages. Both lines High and Low-R performed better (relative to the crossbred control and High-R) in cages than in ponds. The correlation between weight gains in ‘separate’ and ‘mixed’ cages was high (around 0.8) both in 1969 and in 1970. Therefore, the results were pooled in Figure 4.

Variation between replicate spawns of the same line The high degree of uniformity of the replicated spawns within all the lines

(with the few notable exceptions) was a reflection of the large samples of fish in each replicated spawn, and of the fact that at least three mixed ponds (blocks) were used for testing each year. I t also indicates that the ‘effective’ number of parents in each spawn was sufficiently large to minimize divergence due to random drift. Note again, in this respect, that the replications within each line were genetically reshuffled each generation by mating females of one replication with males of others. The variances of the corrected weight gains of the replicate spawns within each line, averaged over the three-to-five mixed test ponds and standardized to 600 g crossbred control (see MATERIALS AND METHODS) were computed separately each year. (Variation within the crossbred control and the exceptional replications d and e of Low 1969 were excluded). A comparison of these variances with the equivalent ‘between line means’ variances (Table 5 ) demonstrates the wide genetic divergence between the lines.

Between-groups selection-I971 to 1974 After completion of the 1970 tests, we concluded that the hypothesis set up for

TABLE 5

“Beiween-replicate spawns within lines” and “between lines” variinces of standardized corrected mean weight gains of the iests in ponds

Year 1966 19F7 1968 1969 1970

.Prep = Variance between replicate spawns

S*, i n e = Variance between line

Unweighted mean (in g) of all ponds

of the same line (in g’) 65 368 492 298 589

means (in gz) 1831 3942 5066 2121 3810

including all the tested groups of carp, even those not related to the present experiments (used for standardization of line means) 513 545 738 586 589


testing in 1965 had been verified. Namely, our local breed of carp had reached a selection plateau for fast growth rate while maintaining a large genetic variance. Although many of the results remained without explanation, we decided to devote our limited facilities to a crossbreeding program. Replicate a of High- 1970 had been chosen as a parental line and was labeled Dor-70 by MOAV, HUI~ATA and WOHLFARTH (1975). In 1971 a selected group of the largest individuals (around 50%) of this line was mass-spawned and their offspring (High-71) were tested on a large scale, both in ponds and in cages (Figure 4 and 5 ) . The tests showed an improvement that lifted High-71 to a position above the crossbred control. In 1972 a repeated spawn of the Dor-70 line (the two-year-old, selected parents of replicate a of High-70) was retested in ponds on a larger scale. The tests fully confirmed the 1971 findings (Figure 5 ) . Thus, for the first time. we possessed a closed line of carp whose growth rate did not appear to suffer inbreeding depression. Furthermore, its own performance, as well as that of some

+ 200

+ 150 h

v M

c 4 nJ M

u ."M +loo I

2

4

c

W 2 *50 3

W -z .cI

(600) 0

-50

-100 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974

Year

FIGURE 5.--Standardized mean weight gains in ponds of the replicate spawns of the High selection line-deviations from the crossbred control.

SELECTION FOR GROWTH RATE IN C A R P 95

of its crossbreds excelled over our earlier best F, crossbred (MOAV, HULATA and WOHLFARTH 1975 and unpublished results). These results suggested that between family selection might be effective. Consequently, in 1973 three progenies of parents selected (around 50%) from High-72 were tested. Only a small number of parents (2 to 7 individuals of each sex) were placed into each spawning pond. For control we used, again, a repeat-spawning of High-70 (three-year-old parents, respawned in 1973), and a crossbred control. The large differences between the three replicates (Figure 5) revealed that High-72 was segregating. We should note that the progeny (replicate) with the poorest growth rate had a high proportion of individuals with skeletal deformities, an indication of inbreeding. Around 50% of the largest individuals of the best 1973 progeny group were selected and in 1974 three full-sib progenies of single-pair spawns, plus one progeny of a mass spawn of several parents were tested (Figure 5 ) . The 1974 tests were not as extensive as those of the previous years (only two mixed ponds) ; yet, when they are considered jointly with the 1973 results, little doubt is left that the High line was segregating and that most of its replicates had faster growth rates than earlier generations.

DISCUSSION

The evolution of the genetic control of growth rate in the domesticated European carp

Our investigations suggest strongly that the domesticated European carp has reached a selection plateau for fast growth rate, while maintaining a large genetic variance. That many generations of persistent unidirection selection result in a selection plateau has been amply demonstrated in many investigations with laboratory animals (i.e., THODAY and BOAM 1961; ROBERTS 1966; JONES, FRANK- HAM and BARKER 1968; OSMAN and ROBERTSON 1969; FALCONER 1971; LATTER 1973; EISEN 1972 and others). In farm animals, non-response to selection has been a problem with reproductive traits such as egg production and litter size, (LERNER 1958; DICKERSON 1965; CLAYTON 1972a, b; NORDSKOG, FESTING and VERGHESE 1967; FESTING and NORDSKOG 1967). On the other hand, selection for faster growth rate at an early age-the trait under the present consideration- has been very successful in all farm livestock and common laboratory animals (CLAYTON 1972a). Thus, growth rate of carp behaves in a manner expected of reproductive traits and this similarity, we believe, is a major key to the understanding of the evolution of its genetic control.

Gonad size, hence fecundity of carp as well as most other fish, is highly correlated with body weight (BAGENAL 1967; MCCRIMMON 1968; HULATA, MOAV and WOHLFARTH 1974) and this strong correlation makes selection for body weight an indirect, but strong selection for fecundity-a major component of reproductive fitness. This view gains support from results of selection experiments in the guppyfish (Lebistes reticulatus) that led the author (RYMAN 1972 and 1973) to conclude that despite the low estimates of realized heritability, a relatively large non-additive genetic variation was present. Also, the overwhelming


majority of fish fry die within a short period after hatching, and only the fastest- growing individuals escape this lethal period. (WOHLFARTH and MOAV 1970; MOAV and WOHLFARTH 1974). Thus, early fast growth rate as well as large adult body weight are probably major components of reproductive fitness and both could have reached plateau through natural selection. For many generations, European carp breeders have been selecting for fast growth rate, i.e., in the same direction as natural selection (MANN 1961 ; WOHLFARTH, MOAV and HULATA 1975). The very high fecundity of carp and the great ease of selecting the largest carp enabled considerably stronger selection intensities than those practiced with farm livestocks.

Comparative studies of growth rate of non-selected (wild European and cultivated Chinese) with selected carp revealed that artificial selection was effective in increasing growth rate only after the onset of sexual maturation (STEFFENS 1974; MOAV, HULATA and WOHLFARTH 1974). This evidence, probably, means that early and late growth rate in carp are partially controlled by different genes and that negative genetic correlation between the two could, if present, contribute to the maintenance of genetic variability at the plateau for fast growth rate.

Interpretation of the present results The 1966 to 1970 results led to the conclusion that our base population had

already been at a selection plateau for fast growth rate while maintaining a large genetic variance. What mechanisms maintain this balanced polymorphism? We have already mentioned the possible contribution of negative genetic correlations between early and late growth rates. Phenotypic assessments of growth rate in our tests were made when the fish were 7 months old. At this age in our climate the gonads are already developed and represent a sizable proportion of the total fish weight (HULATA, MOAV and WOHLFARTH 1974). A similar situation was described by COLLINS, ABPLANALP and HILL (1970) in the quail. A second, highly likely agent is interaction of genotypes with age, season, pond fertility and management ( WOHLFARTH, LAHMAN and MOAV 1964; MOAV, HULATA and WOHLFARTH 1974 and 1975).

Completely recessive genes at a low frequency had been suggested for the genetic variance in mice at a selection plateau for large body weight (AL- MURRANI and ROBERTS 1974). However, the immediate and large response of the Low line, the fast deterioration of the High-R control line and the very strong pond-cage genetic interactions require higher frequencies of negative alleles than are permissible by the ‘rare recessives’ hypothesis. Furthermore, the latter cannot account for the negative response observed in the present High selection line and an earlier one reported by MOAV and WOHLFARTH (1 973).

The most likely explanation is heterozygous advantage with unequal effects of the homozygotes. Assuming that the relative frequency of the negative allele is below 0.5 but not very low, say around 0.2, in a population with overdominance for fast growth rate, then selection for large size would increase the frequency of the negative allele toward 0.5. In the following generation, the expected

SELECTION FOR GROWTH RATE IN CARP

TABLE 6

A single gene model showing how Overdominance may cause negative response to selection

97

~ ~~~

Genotype aa AA Aa - Mean of Genetic values -3 0 +1 offspring

Frequencies in a random sample of parents when p ( a ) = 0.2 (equilibrium value) 0.04 0.64 0.32 0.20

Frequencies in selected sample when p ( a ) = 0.4 0.16 0.36 0.48 0.00 Frequencies in selected sample when p ( a ) = 0.6 0.36 0.16 0.48 -0.60

performance of the High line will be lower than that of a repeat-spawning or a random-bred control. To clari€y this relationship, Table 6 shows an hypothetical example with a single locus. Similar theoretical situations were studied by HILL and ROBERTSON (1968). The rapid deterioration of High-R (beginning in 1969) may be explained by a fixation of negative alleles with strong effects. Increased frequencies (toward 0.5) of negative alleles may also account for the drift-like augmentation of the between-replicates variance in the later generations of the High line (Figure 5 ) . Higher heterozygosity of the High line as contrasted with increased fixation in the random-bred controls fit very well the finding of strong heterosis in the High-R X Low-R cross, as well as its absence from the High X Low-R cross.

Although we lack sufficient strong evidence, we believe that the apparent plateau in the Low line was maintained, at least partially, by opposing force of natural selection. This situation is similar to the plateau described by ROBERTS (1966) in small mice. We may add, in this connection, that the high dependence of viability on early growth rate makes genes for slow early growth rate de facto semi-lethals. How, then, can carp survive the heavy genetic load introduced by the postulated polymorphism of these genes? VERGHESE (1974) provided an obvious answer by showing that when we consider a fixed amount of resources that can support a fixed number of individuals, we are really dealing with relative, and not absolute fitness values, and under these circumstances, it is possible to have overdominance at many loci.

The abrupt response of the Low line, the quick deterioration of the High-R line, and the wide divergence between the High line replicates of 1973 and 1974 indicate that a small number of segregating loci determine a high proportion of the genetic variance. This conclusion is in agreement with many selection experiments that demonstrated major roles played by single genes ( WEHRHAHN and ALLARD 1965; SPICKETT and THODAY 1966; LAW 1967; JONES, FRANKHAM and BARKER 1968; OSMAN and ROBERTSON 1968; LATTER 1973).

A marked improvement started in the High line in 1971, after we switched from a procedure of crossing between phenotypically selected individuals of different replicates to selection between replicates. We shall now outline a hypothetical explanation built around the assumption that the genetic control of relative growth rate within groups differs from that determining differences


between group means. Such a situation may be created by strong intra-group competition (GRIFFINS 1967; MOAV and WOHLFARTH 1974).

Let gl and el designate, respectively, the genetic and environmental components of individual growth rate operating during the nursing stage when there is large phenotypic variance with strong positive skewness ( NAKAMURA and KASA- HARA 1955; MOAV and WOHLFARTH 1973). Competition strongly magnifies these effects so that their combined contribution to final weight-the character undergoing selection-may be presented as

( 1 +a> (gl+e, )

when a is the ‘magnification through competition’ factor (MOAV and WOHL- FARTH 1974). Even if we adopt the extreme view that the genes controlling gl stop their direct contribution to growth rate with termination of the nursing stage, a may still be sufficiently large to make the joint component (l-ka) (g,+el) a major determinant of the phenotypic variance of final weight and therefore, the major underlying variable under selection. If a second genetic component, g2 , begins to play its role when the fish are 2-3 months old, then, even if g , has a considerably stronger direct effect than g,, the contribution of gl to final weight ranking may be larger because i t had been exposed for a longer period to amplification by competition { ( l+al)gl > (l+&,)g,}. Neglecting, for emphasis, the smaller magnification of g2 (a2g2=0), the selected phenotype (final weight) of an individual fish i of group i may be presented as,

Pif = p + G,i + Gli + ( g z i j + e2,j) + (l+a) (gltj+elii) when p = grand mean of all the groups,

G,, = mean deviation of g2 of group i, G,, = mean deviation of gl of group i, gzij = individual deviation of gz from the group’s mean, gl,i = individual deviation of gl from the group’s mean,

and elzj and e2ii are, respectively, the pre- and post-nursing environmental effects o n the individual fish.

The within- (U: ) and between-group ( U ; ) variances (disregarding co-vari- an‘ces) are, respectively,

and u2w = UZg2 + UZg1 + U Z e 2 + u2e1 + ( 2 a + d ) ( U Z g 1 + UZ,,)

U26 = U2G2 + u201 . The amplification factor (a) can create situations where ups2 contribution to

the within-variance is negligibly small, while at the same time, uZG1 is the major determinant of u 2 b . Even slight negative co-variation between g, and gl or e, would contribute markedly to the above contrast.

Thus, it appears that further progress in our understanding of the genetics of growth rate in carp requires detailed genetic studies of component traits. Similar situations where complex interactions between component traits created apparent inexplicable selection responses were encountered in other experiments ( EISEN 1972; COLLINS, ABPLANALP and HILL 1970). When LATTER (1970) was exposed


to similar circumstances in Drosophila he concluded that when the separate components OI a given metric trait are subject to different systems of regulation, then observations of a single phenotype may be inadequate to suggest an appropriate model at the limits to selection.

The above model may even be extended to provide a tentative explanation to the strong ponds-cages interactions. This requires the assumption that cages stimulate prolonged direct activity of gl well into the test period, while rendering g2 less effective. A somewhat similar genotype-environment interaction was described in maize by ARBOLEDA-RIVERA and COMPTON ( 1974).

We are grateful t o MR. GIDEON HULATA for his continuous help throughout the preparation of the manuscript. PROF. MOSHE SOLLER and DR. THOMAS BRODY criticized the manuscript most helpfully.

LITERATURE CITED

AL-MURRANI, W. K. and R. C. ROBERTS, 1974 Genetic variation in a line of mice selceted to its limit for high body weight. Anim. Prod. 19: 273-289.

in diverse selection environments. Theoret. Appl. Genet. 44: 77-81. ARBOLEDA-RIVERA, F. and W. A. COMPTON, 1974 Differential response of maize to mass selection

A short review of fish fecundity. Pp. 89-111. In: The Biological Basis of

BARDhCH, 5. E., J. H. RYTHER and W. 0. MCLARNN, 1972 Aquaculture. The farming and

Selection plateaux in poultry. Ann. Gknkt. Sdl. Anim. 4: 561-568. Effects of selection on reproduction in avian species. J. Reprod. Fert. (Suppl.)

Mass selection for body weight in quail.

Experimental evolution of selection theory in poultry. Proc. 11th

Raising fish for food in Southeast Asia. Pp. 121-142. In: Fish as Food,

Long-term selection response for 12-day litter weight in mice. Genetics 72:

Improvement of litter size in a strain of mice at a selection limit. Genet.

Response to selection for body weight and egg

Selection in reference to biological groups. I. Individual and group selection

BAGENAL, T. B., 1967 Freshwater Fish Production. Edited by S. D. GERKIN. Blackwell, Oxford.

husbandry of fresh water and marine organisms. J. Wiley, New York. 868 pp.

CLAYTON, G. A., 1972a -, 15: 1-21.

1972b

COLLINS, W. M., H. ABPLANALP and W. G. HILL, 1970 Poultry Sci. XLIX: 926-933.

DICKERSON, G. E., 1965 Intern. Congr. Genet. 3: 747-759.

DREW, R. A., 1961 Vol. I, Edited by BORGSTROM. Academic Press, New York.

EISEN, E. J., 1972 129-1 42.

FALCONER, D. S., 1971 Res. 17: 215-235.

FESTING, M. F. and A. W. NORDSKOG, 1967 weight in chicken. Genetics 55: 219-231.

GRIFFINS, B., 1967

HICIILING, C. F., 1962

HILL, W. G. and A. ROBERTSON, 1968

applied to populations of unordered groups. Australian J. Biol. Sci. 20: 127-139.

Fish Culture. Faber and Faber, London. 295 pp.

The effects of inbreeding at loci with heterozygote advantage. Genetics 60: 615-628.

HULATA, G., R. MOAV and G. WOHLFARTH, 1974 The relationship of gonad and egg size to weight and age in the European and Chinese races of the common carp (Cyprinus carpio L.)- J. Fish Biol. 6: 745-758.

100 R. MOAV A N D G . WOHLFARTH

JONES, L. P., R. FRANKHAM and J. S. BARKER, 1968 The effects of population size and selection intensity in selection for a quantitative character in Drosophila. 11. Long-term response to selection. Genet. Res. 12 : 249-266.

Genetics of the common carp and other edible fish. Seminar/Study Tour in the USSR on genetic selection and hybridization of cultivated fishes. Rep. FAO/ UNDP (TA) (2926), 186-201. __ , 1972 Methods and effectiveness of breeding the Ropshian carp. Communication I. Purposes of breeding, initial farms and systems of crosses. Genetika 8 : 65-72.

KIRPICHNIKOV, V. S., K. V. PONOMARENKO, N. V. TOLMACHEVA and R. M. TSOI, 1972 Idem. 11. Methods of selection. Genetika 8 : 42-53.

LATTER, B. D. H., 1970 Selection for a threshold character in Drosophila. 111. Genetic control of variability in plateaued populations. Genet. Res. 15: 285-300. - , 1973 Selection for a threshold character in Drosophila. IV. Chromosomal analysis of plateaued populations. Genetics 73: 497412.

The location of genetic factors controlling a number of quantitative characters in wheat. Genetics 56: 445-461.

KIRPICHNIKOV, V. S., 1971

LAW, C. N., 1967

LERNER, I. M., 1958 MANN, H., 1961

MCCRIMMON, H. R., 1968 MOAV, R. and G. WOHLFARTH, 1966

The Genetic Basis of Selection. J. Wiley, New York. Fish cultivation in Europe. Pp. 77-102. In: Fish as Food, Vol. I. Edited by

BORGSTROM. Academic Press, New York. Carp in Canada. Bull. Fish. Res. Board Can. 165: 1-93.

Genetic improvement of yield in carp. FAO Fish. Rept. 4.2: 12-29. -, 1973 Carp breeding in Israel. In: Agricultural Genetics-Selected Topics. Edited by R. MOAV. J. Wiley, New York. - , 1974 Magnification through competition of genetic differences in yield capacity in carp. Heredity 33: 181-202.

The breeding potential of growth curve differences between the European and Chinese races of the common carp. Proc. 1 s t World Cong. Genet. Appl. to Livestock Production 3: 573-578. --, 1975 Genetic differences between the Chinese and European races of the common carp. I. Analysis of genotype- environment interactions for growth rate. Heredity 34: 323-340.

MOAV, R., G. WOHLFARTH and M. LAHMAN, 1960 An electric instrument for brandmarking fish. Bamidgeh 12: 92-95. --, 1964 Genetic improvement of carp. VI. Growth rate of carp imported from Holland relative to Israeli carp and some crossbred progeny. Bami- dgeh 16: 142-149.

A study of the phenomenon of the tobi koi or shoot carp. I. On the earliest stage at which the shoot carp appears. Bull. Jap. Soc. Sci. Fish. 21: 73-76. (In Japanese with English summary.)

Selection for egg production and correlated responses in the fowl. Genetics 55: 179-191.

The introduction of genetic material from inferior into superior strains. Genet. Res. 12: 221-236.

The limits to artificial selection for body weight in the mouse. 11. The genetic nature of the limits. Genet. Res. 8: 361-375.

An attempt to estimate the magnitude of additive genetic variation of body size in the guppy-fish, Lebistes reticulatus. Hereditas 71 : 237-244. - , 1973 Two-way selection for body weight in the guppy-fish, Lebistes reticulatus. Hereditas 74: 239-246.

Regular responses to selection. I. Interactions between located polygenes. Genet. Res. 7: 96121.

Results of crossing between wild and domesticated carp Cyprinus carpi0 L. Biol. Zbl. 93: 129-139.

MOAV, R., G. HULATA and G. WOHLFARTH, 1974

NAKAMURA, N. and S. KASAHARA, 1955

NORDSKOG, A. W., M. FESTING and M. W. VERGHESE, 1967

OSMAN, H. S. and A. ROBERTSON, 1968

ROBERTS, R. C., 1966

RYMAN, N., 1972

SPICKETT, S. G. and J. M. THODAY, 1966

STEFFENS, W., 1974


TAL, S. and A. SHELUVSHY, 1952 A review of the fish farming industry in Israel. Trans. Am. Fish. Soc. 81: 218-223.

THODAY, J. M. and T. B. BOAM, 1961 Regular responses to selection. I. Description and responses. Genet. Res. 2: 161-176.

VERGHESE, M. W., 1974 Interaction between natural selection for heterozygotes and direc- tional selection. Genetics 76: 163-168.

WEHRHAHN, C. and R. W. ALLARD, 1965 The detection and measurement of the effects of individual genes involved in the inheritance of a quantitative character in wheat. Genetics 51: 109-119.

The effects of variation in spawning time on subsequent relative growth rate and viability in carp. Bamidgeh 22: 42-47. - , 1972 Theregres- sion of weight gain on initial weight in carp. I. Methods and results. Aquaculture 1: 7-28.

Genetic improvement of carp. V. Comparison of fall and winter growth of several carp progenies. Bamidgeh 16: 71-76.

Genetic differences between the Chinese and European races of the common carp. 11. Multi-character variation-a response to the diverse methods of fish cultivation in Europe and China. Heredity 34: 341-350.

Activities of the Carp Breeders Union in 1964. Bamidgeh 17: 9-15.

Corresponding editor: R. W. ALLARD

WOHLFARTH, G. and R. MOAV, 1970

WOHLFARTH, G., M. LAHMAN and R. MOAV, 1964

WOHLFARTH, G., R. MOAV and G. HULATA, 1975

WOHLFARTH, G., M. LAHMAN, R. Moav and Y. ANKORION, 1965

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