Genetic effects and genotype × environment interactions for growth-related traits in common carp, Cyprinus carpio L.

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Aquaculture 272 (2007) 267 – 272 www.elsevier.com/locate/aqua-online

Genetic effects and genotype × environment interactions for growth-related traits in common carp, Cyprinus carpio L. Cheng-hui Wang, Si-fa Li ⁎ Key Laboratory of Aquatic Genetic Resources and Aquacultural Ecosystem, Ministry of Agriculture, Shanghai Fisheries University, 200090, China Received 9 July 2006; received in revised form 3 July 2007; accepted 9 July 2007

Abstract A diallel cross was conducted with three variants of red common carp, Cyprinus carpio var. singuonensis, C. carpio var. wuyuanensis and C. carpio var. color, raised in two separate experimental stations. Additive effects, dominance effects, additive × environment (A × E) and dominance × environment (D × E) interactions of growth-related traits of 8-month-old fish were estimated by using a mixed genetic model. It was found that the traits of body weight (BW), standard length (SL) and pre-dorsal height (PDH) were mainly controlled by dominance effects, whereas they were very weakly controlled by the additive, genotype × environment (A × E and D × E) interaction effects. For the trait of pre-dorsal width (PDW), additive effects were the predominant effects, while dominance and genotype × environment interaction effects were less important. Also, significant D × E interaction effects in BW, and significant A × E interaction effects in PDH and PDW were detected. In all the studied traits, the prediction of genetic merit (breeding values) for the three variants indicated that C. carpio var. color was the best one for genetic improvement through direct selection in different environmental conditions, and the cross combination of C. carpio var. color and C. carpio var. singuonensis was the best for heterosis utilization by hybridization, while C. carpio var. wuyuanensis was the best for improving the body height in red common carp. © 2007 Published by Elsevier B.V. Keywords: Common carp; Diallel cross; Growth-related traits; Genetic effects; G × E interactions

1. Introduction It is recognized that the range of phenotypic expression of quantitative traits results from both genetic and environmental sources of variation, and the interaction between the two (Fishback et al., 2002). In aquatic animals, estimates of general genetic parameters (e.g. heritability and correlations) for growth-related ⁎ Corresponding author. Tel.: +86 21 6571 0333; fax: +86 21 6568 4153. E-mail addresses: [email protected], [email protected] (S. Li). 0044-8486/$ - see front matter © 2007 Published by Elsevier B.V. doi:10.1016/j.aquaculture.2007.07.011

traits have been extensively conducted (Gjerde and Schaeffer, 1989; Winkelman and Peterson, 1994; Pante et al., 2002), and studies of genotype by environment (G × E) interactions on quantitative traits have also been widely reported (McKay et al., 1984; Iwamoto et al., 1986; Elvingson and Johansson, 1993; Winkelman and Peterson, 1994; Taniguchi et al., 1996, Su et al., 1999; Fishback et al., 2002; Gall and Neira, 2004; Saillant et al., 2006). Although the expression display of G × E interactions differed in different quantitative traits and in different environmental conditions, it is clear that G × E interactions occur and may be important contributors to phenotypic variation in some genetic improvement

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programs for aquatic animals. Also, different genetic components, such as additive, dominance and epitasis (these were all included as genotype components), will interact with environmental factors. Few studies, however, cover the division of genotype by environment (G × E) interactions into additive by environment (A × E) interactions and dominance by environment (D × E) interactions in aquatic animals. Common carp (Cyprinus carpio L.) is the longest cultured and the most domesticated fish species in the world; it has been cultured for approximately 4000 years (Wohlfarth, 1993; Balon, 1995). During this time, the common carp has developed numerous varieties through a combination of forces including geographic isolation, adaptation, accumulation of mutations, and natural as well as human selection pressures (Hulata, 1995). So the common carp is a dominant species in quantitative genetics analysis and genetic improvement practices (Moav and Wohlfarth, 1976; Wohlfarth et al., 1983; Wohlfarth, 1993; Hulata, 1995; Vandeputte, 2003; Vandeputte et al., 2004). However, many estimates of the genetic parameters, especially estimates of G × E interactions, for growth-related traits in the common carp still remain to be studied. In China, numerous varieties of common carp have developed in regional distributions and cultivation zones over thousands of years. Of these, Xingguo red common carp (C. carpio var. singuonensis) and Purse red common carp (C. carpio var. wuyuanensis) are the most famous variants of common carp produced by mass selection during the 1960s–1970s. Since the 1970s, more than 10 hybrids have been produced from these varieties, together with other carp strains, and these hybrids have become widely distributed and cultured in China (Li, 1996; Lou, 1999; Wu, 2000; Li and Wang, 2001). However, our knowledge of the quantitative genetics of the two common carp variants is still unclear. Moreover, the Oujiang color common carp (C. carpio var. color), a colorful variant of common carp found in the Oujiang River basin of Zhejiang province, has suffered a decline in growth because there is no selective breeding program and practice. It is necessary to understand the genetic effects and merits to assess the potential breeding values of these common carp strains. In this study, a diallel cross was conducted with the three variants of common carp in China (C. carpio var. singuonensis, C. carpio var. wuyuanensis and C. carpio var. color), and the progenies were reared in two separate environments (two stations). The aim of the study was to obtain information about the genetic improvement and utility (e.g. heterosis and selection within the variants) of these variants, and to perform a

first trial to assess additive by environment (A × E) interactions and dominance by environment (D × E) interactions in common carp. 2. Materials and methods 2.1. Mating design In April 2001, a complete 3 × 3 diallel cross was conducted on the three variants of common carp, Xingguo red common carp (XG), Purse red common carp (PR) and Oujiang color common carp (OJ). The Xingguo red common carp came from the National Farm of Xingguo Red Common Carp in Jiangxi Province; the Purse red common carp came from the National Farm of Purse Red Common Carp in Jiangxi Province; and the Oujiang color common carp came from the Provincial Farm of Oujiang Color Common Carp in Zhejiang Province. The cross mating experiments with the three variants were conducted in nine concrete tanks with five females and five males in each tank at the Nanhui Fish Breeding Experimental Station (NFBES) of Shanghai Fisheries University (Table 1). Mass spawning was employed without hormone injection, and all females finished spawning in 15 h. At the swim-up stage, 1000 fish per tank were transferred to the Longquan Station in Zhejiang Province (LSZP) and 1000 fish were kept in each hatchery tank at NFBES in Shanghai, while the other fish were removed. 2.2. Rearing When the fry averaged 4–5 cm in length at two stations, the same size samples from each tank at the two stations were finclipped (beginning on May 30 at LSZP and June 2 at NFBES, in 2001). Communal stocking by using the fin clipping as group tagging was adopted with two parents and their reciprocal hybrids in the same tank; for example, the parents XG, PR and their reciprocal hybrids XG(♀) × PR(♂), PR (♀) × XG(♂) were each combined in a single tank. The stocking densities differed at the two stations due to the different tank volumes. At LSZP, a total of 160 fish, with 40 individuals from each mating combination, were stocked in the same 50-m3 tank. At NFBES, a total of 120 fish, with 30 individuals from each mating combination, were stocked in the same 15-m3 tank. There were three replicates of each cross at

Table 1 A diallel cross mating for three variants of common carp Strains

XG(♂)

PR(♂)

OJ(♂)

XG(♀)

Purebred (5♀: 5♂) Crossbred (5♀: 5♂) Crossbred (5♀: 5♂)

Crossbred (5♀: 5♂)

Crossbred (5♀: 5♂)

Purebred (5♀: 5♂)

Crossbred (5♀: 5♂)

Crossbred (5♀: 5♂)

Purebred (5♀: 5♂)

PR(♀) OJ(♀)

XG: C. carpio var. singuonensis; PR: C. carpio var. wuyuanensis; OJ: C. carpio var. color.

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LSZP with a total of nine tanks, each containing two parents and their reciprocal hybrids, and two replicates at Shanghai station with a total of six tanks.

Unbiased Prediction (AUP) method (Zhu, 1993; Zhu and Weir, 1994, 1996a,b). The t-test was then used to test the significance level of each estimate from zero.

2.3. Traits measurement

3. Results

When the fish were 8 months of age, all individuals in each tank at the two stations were collected for weighing and measuring, including body weight (BW, g), standard length (SL, cm, the distance from the most anterior tip of the mouth to the posterior end of the backbone), pre-dorsal height (PDH, cm, the vertical body height anterior to the dorsal fin) and predorsal width (PDW, cm, the horizontal body width anterior to the dorsal fin).

3.1. Phenotypic variation

2.4. Statistics Additive, dominance and G × E interaction variances were evaluated using the following mixed linear genetic model (Zhu and Weir, 1994, 1996a,b; Zhu, 2000): Yhijk ¼ u þ Eh þ Aij þ Dij þ AEijh þ DEijh þ Tk ðhÞ þ ehijk

where, Yhijk is the average phenotypic value of individuals from maternal line i × paternal line j within the kth tank (block) within the hth environment; u is the population mean; Eh is the fixed environment effect; Aij is the additive effect from maternal line i and paternal line j, Aij ∼ (0, σ2A); Dij is the dominance effect from maternal line i × paternal line j, Dij ∼ (0, σ2D); EAijh is the additive × environment interaction (A × E) effect, EAijh ∼ (0, σ2EA); EDijh is the dominance × environment interaction (D × E) effect, EDijh ∼ (0, σ2ED); Tk(h) is the tank (block) effects within h environment, Tk(h) ∼ (0, σ2k); ehijk is the random residual, ehijk ∼ (0, σ2e ). The variance components of additive (VA), dominance (VD), additive × environment interactions (VAE) and dominance × environment interactions (VDE) and residual (Ve) were estimated using the MINQUE(1) method by setting 1 for all prior values (Rao, 1970, 1971; Zhu, 1992; Zhu and Weir, 1996a,b). The phenotypic variances (VP) for growth-related traits were partitioned as follows: VP ¼ VA þ VD þ VAE þ VDE þ Ve : The predictions of the genetic merits or breeding values (EV) for the three variants were estimated by the Adjusted

The means, standard deviations, and coefficients of variation for body weight in each mating combination at the two stations are listed in Table 2. The lowest means and coefficients of variation for body weight were found in the purebred cross of XG(♀) × XG(♂) at both stations. Also, the lowest mean weight of all six cross combinations at both stations was observed in the crossbreeding of PR(♀) × OJ(♂). Due to obvious environmental differences (e.g. stocking density) between both stations, the body weight of all progeny from mating combinations at the Zhejiang station (LSZP) was about three times that at the Shanghai station (NFBES). However, the coefficients of variation of body weight at both stations were high, almost similar or only slightly different. So, the values of the measured growth-related traits were logtransformed to reduce the scale difference between both locations. 3.2. Variance components The evaluations of each genetic variance ratio to phenotypic variance for the growth-related traits are shown in Table 3. Significantly high dominance variances were detected for the traits of BW (0.31), SL (0.37) and PDW (0.31), but relatively low additive variance, additive × environment (A × E) and dominance × environment (D × E) interaction variances were found for these traits. This indicated that dominance effects were the main genetic effects, whereas additive, A × E and D × E interaction effects were less important for the three traits. For the PDH trait, the additive variance (0.40) was significant and the highest in all variance components. This showed that the additive effect predominates in the PDH trait. Of course, the significant additive variance in BW, SL and PDW, the significant D × E variance in BW, and the significant A × E variances in PDH and PDW demonstrated that these effects also played a role in the traits.

Table 2 Means (M), standard deviations (SD) and coefficients of variation (CV) for body weight of three common carp variants and their reciprocal hybrids at two experimental stations Stations

LSZP

M ± SD CV (%) NFBES M ± SD CV (%)

Purebred

Crossbred

XG

PR

OJ

XG(♀) × PR (♂)

PR(♀) × XG (♂)

XG(♀) × OJ (♂)

OJ(♀) × XG (♂)

PR(♀) × OJ (♂)

OJ(♀) × PR (♂)

142.8 ± 47.4 33.2 51.1 ± 16.2 31.7

176.3 ± 63.7 36.1 61.9 ± 24.0 38.7

177.3 ± 87.9 49.6 60.8 ± 26.6 43.7

183.6 ± 73.8 40.2 66.2 ± 26.2 39.6

194.0 ± 69.6 35.9 60.7 ± 27.0 44.5

184.9 ± 68.0 36.8 78.4 ± 37.2 47.5

189.5 ± 67.9 35.8 65.1 ± 23.6 36.2

167.8 ± 60.3 35.9 57.6 ± 25.3 43.8

182.0 ± 62.9 34.5 61.7 ± 21.7 35.2

XG: C. carpio var. singuonensis; PR: C. carpio var. wuyuanensis; OJ: C. carpio var. color.

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Table 3 Proportions of additive, dominance, additive ×environment, dominance × environment interaction variances to phenotype variance for growthrelated traits of common carp Traits

VA/VP

VD/VP

VAE/VP

VDE/VP

Ve/VP

BW SL PDH PDW

0.13⁎⁎ 0.18⁎⁎ 0.40⁎⁎ 0.22⁎⁎

0.31⁎⁎ 0.37⁎⁎ 0.09⁎ 0.31⁎⁎

0.01 0.00 0.06⁎ 0.05⁎

0.15⁎⁎ 0.06 0.00 0.04

0.40⁎⁎ 0.39⁎⁎ 0.45⁎⁎ 0.38⁎⁎

BW, body weight; SL, standard length; PDH, pre-dorsal height; PDW, pre-dorsal width. ⁎⁎P b 0.01; ⁎P b 0.05.

3.3. Prediction of genetic merits (breeding values) The predicted additive effects (A) and A × E interactions of the three variants as brooders for breeding are shown in Table 4. The different genetic effects were observed in different variants and at both stations. For the BW trait, the prediction value of additive effects (A) for the XG brooder was significantly negative, and for the OJ brooder it was significantly positive. On the other hand, the prediction values of A × E interactions for three variants were not significant. The prediction values of the additive effects of SL were negative for the XG and PR brooders, but significantly positive for the OJ brooder. The values of A and A × E of PDH for the XG brooder were significantly negative, while the values of A and A × E for the PR brooder were significantly positive. For the PDW trait, significant negative values of A and A × E were observed in the XG brooder, and positive values of these effects were detected in the OJ brooder.

Table 4 Predicted genetic effects of additive (A) and additive × environment interactions (A × E) for growth-related traits in the three variants of common carp Traits

Brooders

A

A × E1

A × E2

BW

XG PR OJ XG PR OJ XG PR OJ XG PR OJ

− 0.45⁎ 0.08 0.37⁎ − 0.10 − 0.14⁎ 0.24⁎⁎ − 0.13⁎⁎ 0.16⁎⁎ − 0.03 − 0.06⁎ 0.03 0.03⁎

− 0.06 0.01 0.05 0.00 0.00 0.00 − 0.06⁎ 0.11⁎ − 0.05 − 0.03 0.03 0.00

− 0.10 0.02 0.08 0.00 0.00 0.00 − 0.02⁎ 0.00 0.02 − 0.01⁎ − 0.01 0.02⁎

SL

PDH

PDW

BW, body weight; SL, standard length; PDH, pre-dorsal height; PDW, pre-dorsal width. E1, Environment 1 (Shanghai station); E2, Environment 2 (Zhejiang station). ⁎⁎P b 0.01; ⁎P b 0.05. These figures were obtained with log-transformed data.

Table 5 Dominance effects for growth-related traits in three combinations of three variants of common carp

XG × PR XG × OJ PR × OJ

BW

SL

PDH

PDW

0.77⁎ 0.79⁎ − 0.73⁎

0.25⁎ 0.54⁎ − 0.37⁎

0.02 0.02 − 0.02

0.04 0.22⁎ − 0.13⁎

BW, body weight; SL, standard length; PDH, pre-dorsal height; PDW, pre-dorsal width. XG: C. carpio var. singuonensis; PR: C. carpio var. wuyuanensis; OJ: C. carpio var. color. These figures were obtained with log-transformed data.

The predictions of heterosis between cross combinations of the three variants are presented in Table 5. This clearly shows that the largest prediction values of heterosis for all the traits BW, SL, PDH and PDW existed in the cross combination of XG and OJ.

4. Discussion In this study, the four traits studied in the three common carp variants were found to be predominately controlled by genetic main effects (additive and dominance effects), and very weakly controlled by genotype × environment (A × E and D × E together) interaction effects. However, the significantly positive D × E interaction variances (VDE) in the BW trait and A × E interaction variances (VAE) in the PDW and PEW traits indicated that the genotype × environment interaction effects would play important roles in different traits. This gives the breeder the useful information that obvious heterosis should be obtained for the weight traits by using hybridization among these three variants. At the same time, it is important to consider the influence of genotype × environment interactions on different traits in genetic improvement programs for common carp. In fish breeding programs, breeders need to know not only the heritability and inheritance magnitude of the target traits, but also the genetic merits of improved stocks. In this study, the genetic merits (breeding values or potential) of the studied traits in the three variants of common carp, reared in two environments, were evaluated. For body weight, the prediction values of additive effects indicated that the XG brooder would significantly decrease the weight of progeny and the OJ brooder would significantly increase the weight of progeny in selection or hybridization programs. Also, the predictions of negative values of A × E (A × E1 and A × E2) interactions from the XG brooder and positive values of A × E interactions from the PR and OJ

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brooders at both stations indicated that the XG brooder could decrease the body weight of progeny, whereas the PR and OJ brooders could increase the weight gains of progeny in two different conditions. Of the three parents, the largest genetic gains for body weight were in the OJ variant through selection. The prediction values of additive (A) and additive × environment (A × E) effects were all negative for the traits of SL, PDH and PHW in the XG brooder, which indicated that all these effects from XG should decrease the body shape (length, height and width) of progeny. In particular, the PR brooder, which showed the highest values of the PDH trait, should make the largest contribution to promoting a gain in the PDH trait of progeny. The results showing that the prediction values of A × E interactions from PR and OJ brooders were different at two stations suggests that the additive effects would increase or decrease the traits of SL, PDH and PDW, depending on the environmental conditions. On the other hand, the predictions of heterosis for all the traits of BW, SL, PDH and PDW indicated that the largest heterosis would have occurred if the XG and OJ brooders had been chosen to conduct the hybridization. By evaluating the predicted breeding values of additive effects, dominance effects, and G × E interaction effects in different environments for different brooders, our study has clarified for breeders how to select the best brooder stocks for improving the target traits in different selection environments. In this study, the predictions of genetic merit suggested that C. carpio var. color (OJ) was the best, and C. carpio var. singuonensis (XG) was the worst, of the three variants of red common carp for direct selection in different environmental conditions. However, it is interesting that the cross combination of C. carpio var. color (OJ) and C. carpio var. singuonensis (XG) was the best for using heterosis. The results also suggested that C. carpio var. wuyuanensis (PR) was the best parent to improve the height trait of body shape. The environmental variance was not separately evaluated in this study. However, the influences of environmental factors on genetic variation were evaluated by evaluating the G × E (A × E and D × E) interactions. The additive and A × E interaction variances show the inheritable magnitude and selection potential of improved traits in different environmental conditions, while dominance and D × E interaction variances indicate the magnitude of heterosis of improved traits in different environmental conditions. These methods have been widely used in crops (Shi et al., 1996, 2000, 2002; Chen and Zhu, 1999), and this study suggests that they can also be effectively used for evaluating genetic parameters and

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predicting the breeding values of common carp reared in different environments. In this study, 5 males and 5 females were used in each mating combination, and a total of 15 males and 15 females were used for each carp variant; numbers that would not be adequate for evaluating brood stocks. Also, due to the natural mass spawning method used in the study, it was difficult to discriminate the exact number of effective males for spawning, and to identify them with individual tagging. Thus these results would be subject to a sampling variance and high error variance. Furthermore, the large difference between the environments of the two stations would promote the dominance variance. However, it was still useful to perform this trial to assess additive by environment (A × E) interactions and dominance by environment (D × E) interactions in common carp in genetic improvement programs. Acknowledgements The authors are very grateful to the anonymous reviewers for their insightful comments and suggestions on the manuscript. The authors would like to thank Prof. Jun Zhu at Zhejiang University, China and Prof. John Liu at Auburn University, USA for their suggestions and guidance on the manuscript. This work was supported by the Shanghai Leading Academic Discipline Project (grant no. Y1101), and the Shanghai Education Committee Project (grant no. 07ZZ136). References Balon, E.K., 1995. Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129, 3–48. Chen, J.G., Zhu, J., 1999. Genetic effects and genotype × environment interactions for cooking quality traits in indica–japonica crosses of rice (Oryza sativa L.). Euphytica 109, 9–15. Elvingson, P., Johansson, K., 1993. Genetic and environmental components of variation in body traits of rainbow trout (Oncorhynchus mykiss) in relation to age. Aquaculture 118, 191–204. Fishback, A.G., Danzmann, R.G., Ferguson, M.M., Gibson, J.P., 2002. Estimates of genetic parameters and genotype by environment interactions for growth traits of rainbow trout (Oncorhynchus mykiss) as inferred using molecular pedigrees. Aquaculture 206, 137–150. Gall, G.A.E., Neira, R., 2004. Genetic analysis of female reproduction traits of farmed coho salmon (Oncorhyncus kisutch). Aquaculture 234, 143–154. Gjerde, B., Schaeffer, L.R., 1989. Body traits in rainbow trout II. Estimates of heritabilities and of phenotypic and genetic correlations. Aquaculture 80, 25–44. Hulata, G., 1995. A review of genetic improvement of the common carp (Cyprinus carpio L.) and other cyprinids by crossbreeding, hybridization and selection. Aquaculture 129, 143–155.

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