Aquaculture 428–429 (2014) 1–6

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Selection for enhanced growth performance of Nile tilapia(Oreochromis niloticus) in brackish water (15–20 ppt) in Vietnam

Nguyen Huu Ninh a,⁎, Ngo Phu Thoa a,b,1, Wayne Knibb b, Nguyen Hong Nguyen b

a Research Institute for Aquaculture No. 1, Dinh Bang, Tu Son, Bac Ninh, Viet Namb Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Maroochydore QLD 4558, Australia

⁎ Corresponding author. Tel.: +84 4 38780938; fax: +E-mail address: nhninh@ria1.org (N.H. Ninh).

1 A joint first author.

http://dx.doi.org/10.1016/j.aquaculture.2014.02.0240044-8486/© 2014 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 30 October 2013Received in revised form 19 February 2014Accepted 20 February 2014Available online 28 February 2014

Keywords:Genetic parametersSelection responseGrowthBrackish water

The main aim of this paper was to report genetic parameters and selection response from a synthetic populationof Nile tilapia selected for improved growth performance in brackish water systems in Vietnam. The syntheticbase population was formed in 2007 from the best performing individuals for growth produced from a completediallel cross involving three strains of Nile tilapia, namely GIFT (Genetically Improved Farmed Tilapia), Taiwanand NOVIT4 (GIFT-derived) strains. Selection was practised for increased harvest weight in brackish water(15–20 ppt) over four generations from2008 to 2011. A total of 12,006 individuals had performance data records.They were offspring of 341 sires and 450 dams (averaging 3000 offspring and 70 sires and 90 dams in each gen-eration). Mixed models fitted to the data included the fixed effects of generation, sex, their two way interactionand a linear covariate of age within sex and generation. The random terms in the model were sire within gener-ation anddamwithin sire and generation. The estimates of heritability for body traits and survivalweremoderateto high (0.27 to 0.53). Genetic correlations between harvest weight and body length were high and positive(0.97), whereas those betweenbody traits and survivalwere low and not significantly different from zero. Genet-ic gain per generationwasmeasured as estimated breeding values and expressed in actual units (original scale ofmeasurement) and genetic standard deviation unit (σG). The improvement achieved for harvest weight rangedfrom 1.1 to 1.6 σG after four generations of selection (one year per generation). Selection for increased harvestweight was however accompanied by a non-significant decrease in survival by −0.24%-units or −0.16σG. Thelarge genetic variation in both harvest weight and survival, however, suggests that there is a scope for simulta-neous improvement of both traits in this population of Nile tilapia. It is concluded that our selective breeding pro-gramme has succeeded in developing a productive strain of Nile tilapia under brackish water systems, but thefuture work should include survival rate in the recording system, selection index and breeding objective.

© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Tilapia is one of the important culture species in Vietnam andworld-wide (FAO, 2012). Vietnamese production in 2010was 120,000 tonnes,making up 5% of total aquaculture production in the country(Vietnamese Directorate of Fisheries, MARD, 2011). Production of tila-pia in Vietnam has been mainly practised in freshwater systems, rang-ing from small scale backyard farming, rice-fish integrated systems tolarge scale semi-extensive and intensive culture in ponds or in cagesinstalled in rivers and reservoirs.

Vietnam is characterised by a long coastal areawhere a large body ofbrackish water is available for aquaculture. The presently availablebreeds of Nile tilapia generally have limited capacity to reproduce, sur-vive and grow in brackish water systems. Only a few other species of

84 4 38273070.

tilapia of commercial importance are known to tolerate salinity over15 ppt (Hopkins et al., 1988; Legendre et al., 1989). The Florida red tila-pia hybrid, considered to be one of the high performing tilapia breedscultured under high salinity (15–30 ppt) in tropical conditions, was de-rived from crossbreeding a mutant red Oreochromis mossambicus withOreochromis aureus, Oreochromis niloticus and Oreochromis urolepishornorum. However, this breed suffers from lack of cold tolerance(Watanabe et al., 2006) and red tilapia strains generally show slowergrowth than Nile tilapia (Santos et al., 2014).

Salinity tolerance differences were reported among tilapia speciesand between species of Oreochromis genus. In the Oreochromis genus,O. spilurus, O. mossambicuss and O. aureus show greater degree of salin-ity tolerance than Nile tilapia (O. niloticus) (Stickney, 1986; Suresh andLin, 1992). Significant differences in the growth of five strains of Asianred tilapia were found (Romana-Eguia and Eguia, 1999) when grownin fresh, brackish and salt water. The overall growth of the five strainswas more rapid in brackish water (17 ppt) than in either freshwateror salt water (34 ppt). Basiao et al. (2005) also reported a significant

2 N.H. Ninh et al. / Aquaculture 428–429 (2014) 1–6

difference in growth between three strains of O. niloticus in both freshand saline water (32 ppt).

A large body of the literature generally indicates that highly euryha-line tilapia species exhibit lowgrowth performance. Attempts have beenmade to increase the salinity tolerance of Nile tilapia (O. niloticus) bycrossing it with high euryhaline species to produce hybrids for aquacul-ture. Significant variation in growth and survival was observed among27 tilapia crosses (5 purebred and 22 crossbred), involving euryhalinespecies (O. spilurus, O. aureus, O. mossambicus) and O. niloticus namelyGenetically Improved Farmed Tilapia (GIFT) strain (6th generation),Freshwater Selected Tilapia (FaST) and super male (YY male) tested in10 different varying salt culture environments (Tayamen et al., 2002).Progenies ofO. aureus× O. spilurus showed the highest growth,whereassurvival rate was greatest for O. mossambicus × O. spilurus. Lutz et al.(2010) also reported that six lines of tilapia of various origins and theircross combinations exhibited highly significant genetic andmaternal ef-fects on salinity tolerance. A synthesised result from the literature showsthat while between species differences are highly suggestive of geneticcomponent to salinity tolerance, there is actually no published data toshow if salinity tolerance could be increased by selection.

There is also a paucity of scientific knowledge regarding genetic var-iation in salinity tolerancewithin Nile tilapia strains. Initial experimentswere conducted at the Research Institute for Aquaculture No. 1 (RIA1),Northern Vietnam, to evaluate the growth and survival of the GIFTand Vietnamese strains of Nile tilapia in fresh and brackish water earth-en ponds. The heritability estimates for harvest weight were moderatein both brackish (0.19) and fresh water (0.22). The genetic correlationsof harvest body weight and survival were relatively low (0.45 and 0.42,respectively) between the two test environments. These results suggesta substantial additive genetic variance for the traits that can be furtherexploited through a selective breeding programme. However, in viewof the strong genotype by environment interaction for harvest weightand survival traits observed, separate breeding programmes should beconsidered for Nile tilapia in fresh and brackish water farming (Luanet al., 2008).

Therefore, we, at RIA1, conducted a selective breeding programmeto develop a saline tolerant strain of Nile tilapia for brackish water envi-ronment. In the present paper, we report genetic parameters and selec-tion response for body weight, standard length and survival recorded inthe synthetic population of Nile tilapia (O. niloticus) which has under-gone four generations of selection for high growth in 15–20ppt brackishwater from 2007 to 2011.

2. Materials and methods

2.1. Origin and establishment of the base population

The base population was formed from three strains of Nile tilapia(O. niloticus), namely GIFT (Genetically Improved Farmed Tilapia),Taiwanese andNOVIT4 strains. TheGIFT strain originated from106 fam-ilies selected for high growth rate over six generations in the Philippines(Bentsen et al., 2012; Eknath et al., 2007). The fish were imported toRIA1 in 1997 from the GIFT International Foundation Inc., Philippines.The Taiwanese strain of Nile tilapia was introduced from Taiwan tothe southern part of Vietnam in 1973 and was then transferred for cul-ture in theNorth. The Taiwanese stock has been kept in theNational LifeGene Bank since 1978. TheNOVIT4 strain is the GIFT-derivative selectedover seven generations for high growth under freshwater environmentat RIA1 from 1998 to 2006 (Luan et al., 2008).

In 2007, a complete diallel cross involving three strains (GIFT,Taiwanese and NOVIT4 strains) was carried out using parental broodersrandomly sampled from each strain. Single pair mating conducted infreshwater hapas resulted in a total of 87 full-sib families, nine to tenfamilies per cross. The progenies were nursed in a freshwater environ-ment until fingerling size about 5 to 18 g/fish. They were tagged usingPIT (Passive Integrated Transponders) tag. Fingerlings were then

acclimatized and gradually transferred from freshwater to brackishwater, initially at 9–10 ppt and increased to 14–15 ppt and 20–22 pptin five days. Fish were closely monitored in hapas during the firstthree weeks in brackish water pond. The survival was generally moder-ate (47.4%) to high (96.8%) during this period. Growth testing was con-ducted in brackish water ponds varying between 15 and 22 ppt over aperiod of 8 months. At harvest, body traits data were recorded and ge-netic evaluation was then performed to estimate breeding values forall individuals in the pedigree. The model included the fixed effects ofsex, cross combinations and their two way interaction, and the randomeffect of the additive genetics of individual fish. The best performing(highest EBV) individuals were selected to form the base population(G0) regardless of their genetic make-up.

2.2. Family production of subsequent generations (G1 to G4)

In subsequent generations, single pair mating was conducted in sepa-rate hapa (2×1×1.5m) toproduce paternal full- andhalf-sibs (onemalemated to two females). Before mating, the female and male breederswere conditioned in separate hapas of 200m2 (5 × 20 × 2m) suspendedin brackish water ponds of 8 to 10 ppt. The female was transferred to thebreeding hapa before the male was introduced. A total number of 50breeding hapas were installed in a brackish water pond. Fertilized eggor larvae were collected weekly and immediately transferred to hatchingtrays (40 × 20 × 10 cm) for artificial incubation in brackishwater of 14 to15 ppt. The water temperature during incubation varied between 22 °Cand 30 °C. The collection date of eggs or larvae was recorded for eachmating pair. Once the pairmatingwas successful, a given spawned femalewas removed to allow the given male to mate with a second female sothat production of any given twopaternal familieswas completed usuallywithin two weeks.

When yolk-sac was absorbed, the full-sib larvae were transferred tonurse separately in hapas (3 × 1.2 × 1.5 m) installed in the same brack-ish water (14–15 ppt) earthen pond. The same stocking density of 20fish per m2 was applied to all families. During the first 3 to 4 weeks ofrearing in hapas, the fry were fed five times daily by a commercial pow-der feed with a dietary protein level of 30%, at the rate of 10% of theirbody weight. The next nursing period until physically tagging (averagebodyweight of 5 to 18 g/fish)was applied by feeding 30% of protein pel-let feed twice daily at 7 am and 4 pm at the rate of 5% of total bodyweight. When fingerlings reached about 5–18 g, a random sample of30–60 fingerlings per family was tagged using PIT tags. Tag identity,standard length and live body weight were recorded for each fish.Data on time of mating, spawning, egg or larvae collection, family nurs-ing, survival rate, number of tagged fish were also recorded. After tag-ging, the fingerlings from different families were pooled together andconditioned 2–3 days in hapas of 200 m2 suspended in earthen ponds.During this period, fingerlings that lost their tags or died were replacedby other individuals from the same family. The difference in survivalrate among family after tagging resulted in a large variation in the num-ber of individuals tagged per family.

2.3. Performance testing

Communal grow-out of all families was conducted in a brackishwater pond (3000m2). The salinity level in brackish water pond fluctu-ated between 15 and 20 ppt due to the variation in ambient tempera-ture during the grow-out period. In each generation, one grow-outpond was prepared according to standard procedures before stocking.Stocking density of fish in the pond was from one to two fish per m2

of surface water. The fish were fed twice daily a commercial pellet con-taining 28% protein content at a rate of 5% bodyweight. Water parame-ters such as dissolved oxygen, pH, temperature, and saline level in thepond were monitored every day. After harvesting, male and femalebrooders were evaluated as candidates for selection and then condi-tioned separately for maturation in hapa of 200 m2.

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2.4. Harvest and measurements

Following a grow-out period of about 150 to210 days,fishwere har-vested initially using three drags of a seine net, then to complete theharvest, the ponds were drained out the following day, early in themorning. The harvest fish were immediately transferred to largehapas of 200 m2 (5 × 20 × 2 m) for one to two days of conditioningwithout feeding before the individual tag number, body measurementsand sexwere recorded. Theywereweighed using a digital scale (nearestto 0.1 g). Standard length was also measured with a ruler. The sex ratiowas close to 1:1 (50.8% male and 49.2% female). Over the growth testperiod, the percentage of fish that lost their tags was 1.2 to 2.6% acrossgenerations. There were no observed differences in body weight be-tween the animals that lost or retained their tags. Survival was recordedas a binary trait and coded as 1 if the fish were still alive or 0 if the fishwere absent at harvest. When this trait was expressed as percentage,survival rate was high and averaged from 75.3 to 91.9% across the selec-tion generations. Somemortality occurred due to coldweather or due toextreme draught weather in some years during the course of the selec-tion programme.

2.5. Selection and mating

The harvest data was entered into a database and genetic evaluationwas then conducted to determine estimated breeding values (EBVs) forall individuals in the pedigree. The animals with the highest EBV forbody weight were selected to become parents to produce the next gen-eration. The model used to estimate breeding values included the fixedeffects of generation, sex, their two-way interaction and a linear covar-iate of age by generation and sex subclass. A combined between andwithin family selection was applied in the selection programme. A re-stricted number of individuals (6–8 females and 2–4 males) were se-lected per family to constrain inbreeding. The number of selectedfemales and males were two or three times greater than the actualneeds to prevent breeding failure from mortalities during breeding. In-breeding was restricted by avoiding mating of full-sibs, half-sibs orcousins. Across generations, the average proportions of females andmales selected were 4.43 and 3.48% respectively which correspondedto the selection intensities of 2.38 and 2.33, respectively. This selectionprocedure and experimental size were adhered to, as much as possible,in all generations (G0–G4 corresponding to years 2008 to 2011) fromwhich the data used for this study were collected. The pedigree struc-ture (number of sires and dams, number of family and progeny ineach generation) is presented in Table 1.

2.6. Quantitative genetic analysis

2.6.1. Genetic parametersEstimation of genetic parameters for performance data and survival

were carried out on a total of 12,006 individual fish produced from 341sires and 450 dams over four generations of selection from 2008 to2011. A preliminary analysis using a general linear model (GLM) wasfirstly performed to determine significance of fixed effects, using theGLM procedure in SAS (SAS Institute Inc., 2005) and also verified byWald statistics in ASReml (Gilmour et al., 2009). The GLM model

Table 1Number of sires, dams and progeny with performance records at harvest by generationand line.

Generation Population Sire Dam Progeny

2007 Base 87 87 13722008 Selection 47 66 30322009 Selection 74 108 38452010 Selection 74 104 24772011 Selection 59 85 1280Total 341 450 12,006

included the effects of generation, sex and their two way interactions.Age from birth to harvest within generation and sex was fitted as a lin-ear covariate for body traits.

A mixed model was fitted to analyse the whole data set to estimatethe fixed effects and variance components. The mixed model was writ-ten as follows:

yiknpq ¼ μ þ Gi þ Sk þ G � Sð Þ þ AGE G; Sð Þ þ Sn þ Dp þ eiknpq ð1Þ

where, yiknpq is an observation for body weight, length and survival ofthe individual q; μ is the overall mean; Gi is the fixed effect of generation(i=1, 2, 3, 4); Sk is the fixed effects of sex (k=1, 2); AGE is a linear co-variate; Sn is the randomeffect of the nth sire; Dp is the randomeffects ofmaternal and common environment to full-sibs; and eiknpq is the ran-dom residual effect associated with individual iknpq.

A complete pedigree of the experimental fish from G0 onwards(2007–2011) was available to account for genetic relationships amongindividuals and was used in the analysis to avoid possible bias in the es-timation of phenotypic and genetic parameters and to improve their ac-curacy (Kennedy, 1990). All computations were carried out using theASREML software package (Gilmour et al., 2009). Variance and covari-ance components were estimated using residual maximum likelihood.Convergence for log-likelihood of variance component estimation wasconsidered satisfactorywhen two successive rounds of iteration changedby less than 0.1%. All known pedigree information was included in theanalyses through a relationship matrix. Sire and dam (the non-geneticcomponent including maternal and common environmental effects)were fitted as random effects. This model used pedigree information topartition the observed phenotypic variance of a trait into various geneticand environmental components hence it enabled the estimation of var-iance components with minimum bias.

Heritabilities for body traits and survival were estimated from aunivariate model (Eq. (1)). Survival was recorded and analysed onthe observed (0, 1) scale, using linear mixed model. Thresholdmodels with both logit and probit link functions to analyse survivalwere not converged. The genetic variance (σA

2) was calculated as4× σS

2 where σS2 is sire variance. The dam variance component

(σD2), in this case, was a combination of the maternal, dominant

and common environmental effects, also named as common full-sib effects (σD

2 = σC2). The “and(dam)” option used in ASReml as-

sumed equal sire and dam variances (σS2 = σD

2). The phenotypic var-iance (σP

2) was calculated as the sum of the additive genetic sirevariance (σS

2), the dam variance (σD2), the common full-sib (σC

2) andthe residual variance (σe

2), as σP2 = σS

2 + σD2 + σC

2 + σe2 or σP

2 = 2σS2 +

σC2 + σe

2. Then the heritability was calculated as h2 ¼ σ2A

σ2P. The common

environmental effect was calculated as c2 ¼ σ2C

σ2P. Genetic and phenotypic

correlations were estimated from a two-trait sire and dam model withthe same fixed effects as described above (Eq. (1)). The correlationswere calculated as the covariance divided by the product of the stan-dard deviations of traits: r ¼ σ12

ffiffiffiffiffi

σ21

p ffiffiffiffiffi

σ22

p where σ12was the estimated addi-

tive genetic or phenotypic covariance between the two traits, and σ12

and σ22 are the additive genetic or phenotypic variances of traits 1 and

2, respectively. Standard errors of all the estimates were obtained di-rectly from ASReml (page 218, release 3.0). As square root transforma-tion of body trait data did not improve genetic parameter estimates,only the results on original scale of measurements are presented.

2.6.2. Selection responseGenetic gains in body traits and survival were measured as changes

in estimated breeding values (EBV) using the model that included bothanimal and fullsib family as the randomeffects (Eq. (2)). The animal anddam model was used to obtain EBV for all individuals in the pedigree,and expected to result in minimum bias in breeding value estimates.The EBVs calculated for body weight in both original scale of

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measurements and square root transformation as well as in standard-ized scale by generation and sex were in good agreement. Hence, theEBV estimates on the observed scale were used and were expressed inboth actual unit (original scale of measurement) and in genetic stan-dard deviation unit. The mathematical notation of the model is writtenas follows:

yiknpq ¼ μ þ Gi þ Sk þ G � Sð Þ þ AGE G; Sð Þ þ In þ Fp þ eiknpq ð2Þ

where Gi, Sk and AGE are the same fixed effects as described in Eq. (1),whereas In is the additive genetic effect of individual fish and Fp is thecommon full-sib effect of dam.

3. Results

3.1. Descriptive statistics

Basic statistics for body traits and survival by generations (spawningyears) are given in Table 3. Survival rate recorded over an average grow-out period of 271 days from stocking to harvest variedwith generations,being lower in 2010 and 2011 than in 2008 and 2009. The coefficient ofvariation (CV, %) was greater for body weight than for total length(Tables 2 and 3).

3.2. Significance of fixed effects

Wald F statistics which resulted from mixed model in ASRemlshowed that the main effects of generation, sex and their interactionwere all statistically significant (P b 0.001). A linear covariate of agewithin sex and generation fitted in themodel also had significant effectson body traits and survival. As observed in several tilapia populations,males had significantly larger body weight at harvest than that of fe-males (293 ± 8.1 vs. 248 ± 7.8 g). The difference in body weight be-tween the two sexes was 4.8, 16.0, 8.8 and 23.4% in generations 1, 2, 3and 4, respectively.

3.3. Heritability estimates

Estimated heritabilities for traits studied were moderate to high(Table 4). The fraction of variance due to maternal and common envi-ronmental effects was from 3 to 8%. The heritability for survival usingsire and dam linear mixed model was high.

3.4. Genetic and phenotypic correlations

Genetic and phenotypic correlations between bodyweight and stan-dard length were positive and high, close to unity (Table 5). The geneticcorrelation of body weight and length with survival was not differentfrom zero. The sign of the phenotypic correlations was consistent withthat of the genetic correlation estimates (Table 5).

Table 2Reproduction and management timeline (day-month-year).

Generation Activities

Mating Stocking

2007 20–29 April 2007 09 July 20072008 25 May–06 September 2008 02 September

20 September12 November

2009 26 April–16 June 2009 25 August 2002010 22 April–10 June 2010 27 August 2012011 22–29 March 2011 08 August 201

3.5. Selection responses

Genetic gain was measured as estimated breeding values (EBVs) forbody traits (weight and length) and survival from bivariate and uni-variate animalmodels including also a fullsib family effect, respectively.The EBVs were expressed in actual units of measurements and geneticstandard deviation units. The predicted yearly genetic trend for bodyweight increased steadily from5.7 g in 2008 to 31 g in 2011 correspond-ing to 0.30 to 1.61 genetic standard deviation units, respectively(Table 6). In contrast to bodyweight, survival rate had a tendency to de-cline during the course of the selection programme, although magni-tude of the reduction was small (only −0.24%-units or −0.16 geneticstandard deviation units after four generations of selection) (Table 6).

4. Discussion

Our study demonstrated that genetic selection effectively im-proved performance of Nile tilapia in brackish water of moderate sa-linity (15–20 ppt). The improved strain of Nile tilapia developed inthe present project for aquaculture in brackish water systems is ofpractical significance in the context of Vietnam with long coastalline where a large area in Deltas is projected to be affected by salinityintrusion due to sea water rise and changing climate (Allison et al.,2009). Survival of the animal from stocking to harvest was relativelyhigh (75.3–91.9%). The gain achieved for harvest weight in thepresent population is comparable to those reported in the same spe-cies (Nile tilapia) from selection programmes conducted underfavourable freshwater pond environments. The currently selectedpopulation still shows large genetic variation in characters studied,with the estimates of heritability for body traits ranging from 27 to53%. The heritabilities obtained in our study were generally higherthan those reported for Nile tilapia of GIFT origin in the literature(Bentsen et al., 2012; Eknath et al., 2007; Nguyen et al., 2007, 2010;Ponzoni et al., 2011; Trọng et al., 2013). The estimates reported forNile tilapia in the literature ranged from 0.10 to 0.65 (Nguyen, un-published review). Survival is also an economically important traitfor Nile tilapia especially under brackish water systems because itaffects the number of fish harvested and marketed, and henceproduction yield per unit of culture and farmers' income. The highheritability for survival in our study also suggests possibilities for im-provement of this trait in future breeding programmes for this pop-ulation. The estimate of heritability for survival reported previouslyby Luan et al. (2008) was 0.20 for Nile tilapia also reared in brackishwater (8–20 ppt). A number of studies also report high heritabilityfor field survival in Atlantic salmon (Lillehammer et al., 2013;Ødegård et al., 2006). However, the heritability for this trait reportedin other species is low, being around 10% (Gjerde et al., 2004; Ryeet al., 1990).

Consistent with other reports in fish, genetic correlations betweenbody weight and standard length in the present population are highand positive which suggests that body trait measurements were closelygenetically correlated and are likely to be controlled by similar sets ofgenes. Hence, any one of these traits tested could be used upon which

Grow-out Harvest

July 2007–Feb 2008 10 February 2008200820082008

Sept 2007–Feb 2009 04 February 2009

9 August 2009–Jan 2010 15 January 20100 August 2010–March 2011 20 March 20111 August 2011–Feb 2012 15 February 2012

Table 3Number of observations (N), simple mean, minimum and maximum, standard deviation and coefficient of variation (%).

Trait Generation N Mean Minimum Maximum Standard deviation Coefficient variation (%)

Weight at harvest (g) 2008 3032 217.6 50.0 499.0 78.7 36.22009 3845 232.1 69.8 504.3 64.8 27.92010 2477 323.7 55.7 676.9 114.5 35.42011 1280 366.3 107.2 732.5 109.2 29.8

Length (cm) 20082009 3845 18.8 5.2 24.5 1.7 9.320102011 1280 21.9 2.1 30.9 2.3 10.5

Survival (%)a 2008 3302 91.8 20.0 100.0 40.8 51.92009 4191 91.7 62.5 100.0 27.5 30.42010 3328 74.5 36.7 93.4 43.6 58.72011 1484 86.3 50.0 100.0 34.4 39.5

Measurements of standard length were not available in generations 1 (2008) and 3 (2010).a Survival was recorded as a binary trait (0 and 1) and expressed as percentage in Table 3. For survival, minimum value = the lowest survival family and maximum value = highest

survival family.

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to select, on its own or simultaneously. The genetic correlations be-tween body traits and survival were low and not significant in this pop-ulation. Several studies report low but positive genetic correlationsbetween body weight and survival rate (i.e. favourable) (Gitterle et al.,2005; Rezk et al., 2009). There are also exceptions of high and positivegenetic correlations between growth and survival as reported by Luanet al. (2008) and Nielsen et al. (2010). Survival may be effectively im-proved through improved husbandry, management and feeding prac-tices. Santos et al. (2014) show that high protein diet remarkedlyimproved survival rate from stocking to harvest in both Nile and redtilapia.

Our breeding programme forNile tilapia in salinitywater (15–20 ppt)yielded a good response to selection for increased harvest body weight.The yearly improvement from 0.30 to 1.62 genetic standard deviationunits (σG) is comparable with other selection programmes for the GIFTstrain tested in freshwater pond environments that are more conduciveto tilapia culture (Hamzah et al., in press; Nguyen et al., 2010; Ponzoniet al., 2005). The gain obtained in our study was also somewhat higherthan that reported for the Egyptian Nile tilapia of 0.48σG by Rezk et al.(2009). When the genetic gain was expressed in percentage of the basepopulation mean in 2007, it was in the range from 3 to 7.5% across gen-eration. The percentage of genetic gain in Nile tilapia ranges from 10 to13.3% in pedigreed population estimated by fitting animal models(Bolivar and Newkirk, 2002; Gall and Bakar, 2002; Hamzah et al., inpress; Ponzoni et al., 2005). The genetic gain per generation achievedin our current breeding programme under brackish water was in linewith those reported in aquatic animals generally ranging from 5 to 20%(Gjedrem, 2000).

Despite the significant improvement inharvest bodyweight achieved,survival during grow-out had a tendency to decline. However,magnitudeof the reduction was small (only−0.29% in actual unit or−0.16 geneticstandard deviation units) and not significant based on the prediction er-rors. A reduction in survival by−0.07% or −0.41 genetic standard devi-ation units was also associated with a selection programme for highgrowth after three generations in Egyptian Nile tilapia (Rezk et al.,2009). The long term selection for increased harvest weight in the GIFTstrain also resulted in a decline in survival rate by −0.02 to −0.12σG

after 10 generations in Malaysia (Hamzah et al., unpublished). These re-sults suggest that there is a need to conduct a routine data recording to

Table 4Heritability (±standard errors) and common environmental effects (±s.e.) for body traitsand survival.

Traits h2 c2

Weight 0.53 ± 0.12 0.07 ± 0.02Length 0.27 ± 0.19 0.08 ± 0.02Survival 0.53 ± 0.07 0.03 ± 0.005

incorporate this trait in selection indices and breeding objectives in thefuture breeding programme for populations of Nile tilapia, undergoingthorough selection for high performance. Because determination of eco-nomic values for traits of economic importance especially for fitnessand functional traits such as survival is difficult, a desired selectionindex approach can be used to restrict undesired changes in survivalrate during grow-out for this species.

Our results reported here demonstrate that selection to improve ti-lapia performance in brackish water environments is effective. Al-though the genotype by environment (G × E) effect was not examinedin the present study, the earlier results reported by Luan et al. (2008)showed that the magnitude of this effect was large, with a low geneticcorrelation for homologous body traits between freshwater and brack-ish water (rG = 0.45). In practical terms, only 45% gain can be capturedin production when the animals are selected in one or another environ-ment. Culture of this improved strain of Nile tilapia under freshwater isnot the sole objective of our present study. It is, however, likely that thesaline-tolerant strain of Nile tilapia developed from our programme canalso performwell in freshwater systems. In a review of 24 studies acrossspecies, Falconer (1990) argued that antagonistic selection (i.e. selec-tion under less favourable environments) may produce genotypes thatcan perform well across testing environments, whereas synergistic se-lection (i.e. selection under ‘ideal’ environments)may result in sensitivegenotype. This hypothesis deserves further studies across farmed aqua-culture species when resources permit. The selection line originatedfrom this study also constitute a valuable source of genetic materialsfor subsequent studies to have a better understanding of physiologyand genomic aspects of this improved strain as well as mechanisms ofosmoregulatory adaptation in Nile tilapia.

5. Conclusion

The genetic gain estimated from the present population of Niletilapia indicates that significant and sustained genetic progress in thedesired direction has been achieved in harvest body weight after fourgenerations of selection under brackish water. The high heritabilityobtained for body weight also suggests that the population will contin-ue responding to future selection. Due to the antagonistic genetic

Table 5Phenotypic (above) and genetic (below the diagonal) correlations among traits estimatedusing bivariate animal model.

Weight Length Survival

Weight 0.89 ± 0.003 0.24 ± 0.02Length 0.97 ± 0.005 0.07 ± 0.02Survival 0.30 ± 0.16ns 0.06 ± 0.04 ns

ns = non-significant different from zero.

Table 6Response to selection measured as estimated breeding value in actual unit (±s.e.) and genetic standard deviation (σA) unit.

Year Direct response Correlated responses

Weight Length Survival

Actual unit σA unit Actual unit σA unit Actual unit σA unit

2008 5.74 ± 0.08 0.299 0.02 ± 0.0011 0.012 0.00013 ± 0.5 × 10−4 0.00862009 12.63 ± 0.07 0.658 0.10 ± 0.0010 0.048 −0.00012 ± 0.6 × 10−4 −0.00792010 18.84 ± 0.12 0.982 0.18 ± 0.0013 0.088 −0.0120 ± 0.1 × 10−3 −0.79132011 30.9 ± 0.15 1.611 0.28 ± 0.0023 0.140 −0.0024 ± 0.5 × 10−4 −0.1583

σA unit = actual unit/σA where σA is the genetic standard deviation (the square root of the additive genetic variance for corresponding traits given in Table 4).

6 N.H. Ninh et al. / Aquaculture 428–429 (2014) 1–6

correlation between weight and survival, a desired gain selection indexshould be applied to avoid unfavourable changes in survival in the fu-ture breeding programme for this species.

Acknowledgements

This project was funded by Vietnamese Ministry of Agriculture andRural Development, Grant No. 1462/QĐ-BNN-KHCN. We would like tothank Dr Pham Anh Tuan, Deputy Director of the Vietnamese Director-ate of Fisheries for his support and technical advice during the course ofthe selection programme. We also thank Dr Bjarne Gjerde and twoanonymous referees for constructive comments that helped improvethe manuscript.

References

Allison, E.H., Perry, A.L., Badjeck, M.C., Neil Adger, W., Brown, K., Conway, D., Halls, A.S.,Pilling, G.M., Reynolds, J.D., Andrew, N.L., 2009. Vulnerability of national economiesto the impacts of climate change on fisheries. Fish Fish. 10, 173–196.

Basiao, Z.U., Eguia, R.V., Doyle, R.W., 2005. Growth response of Nile tilapia fry to salinitystress in the presence of an ‘internal reference’ fish. Aquac. Res. 36, 712–720.

Bentsen, H.B., Gjerde, B., Nguyen, N.H., Rye,M., Ponzoni, R.W., Palada deVera,M.S., Bolivar,H.L., Velasco, R.R., Danting, J.C., Dionisio, E.E., Longalong, F.M., Reyes, R.A., Abella, T.A.,Tayamen, M.M., Eknath, A.E., 2012. Genetic improvement of farmed tilapias: geneticparameters for body weight at harvest in Nile tilapia (Oreochromis niloticus) duringfive generations of testing in multiple environments. Aquaculture 338–341, 56–65.

Bolivar, R.B., Newkirk, G.F., 2002. Response to within family selection for body weight inNile tilapia (Oreochromis niloticus) using a single-trait animal model. Aquaculture204, 371–381.

Eknath, A.E., Bentsen, H.B., Ponzoni, R.W., Rye, M., Nguyen, N.H., Thodesen, J., Gjerde, B.,2007. Genetic improvement of farmed tilapias: composition and genetic parametersof a synthetic base population of Oreochromis niloticus for selective breeding. Aqua-culture 273, 1–14.

Falconer, D., 1990. Selection in different environments: effects on environmental sensitiv-ity (reaction norm) and on mean performance. Genet. Res. 56, 57–70.

FAO, 2012. Fisheries Statistics. http://www.fao.org/fishery/statistics/en.Gall, G.A., Bakar, Y., 2002. Application of mixed-model techniques to fish breed improve-

ment: analysis of breeding-value selection to increase 98-day body weight in tilapia.Aquaculture 212, 93–113.

Gilmour, A.R., Gogel, B., Cullis, B., Thompson, R., Butler, D., 2009. ASReml User Guide Re-lease 3.0. VSN International Ltd., Hemel Hempstead, UK.

Gitterle, T., Rye,M., Salte, R., Cock, J., Johansen, H., Lozano, C., Arturo Suárez, J., Gjerde, B., 2005.Genetic (co)variation in harvest body weight and survival in Penaeus (Litopenaeus)vannamei under standard commercial conditions. Aquaculture 243, 83–92.

Gjedrem, T., 2000. Genetic improvement of cold-water fish species. Aquac. Res. 31, 25–33.Gjerde, B., Terjesen, B., Barr, Y., Lein, I., Thorland, I., 2004. Genetic variation for juvenile

growth and survival in Atlantic cod (Gadus morhua). Aquaculture 236, 167–177.Hamzah, A., Ponzoni, R.W., Nguyen, N.H., Khaw, H.L., Yee, H.Y., Nor, S.A.M., 2014. Genetic

evaluation of the Genetically Improved Farmed Tilapia (GIFT) strain over ten gener-ations of selection in Malaysia. J Trop. Agric. Sci. (in press).

Hopkins, K., Hopkins, M., Pauly, D., 1988. A multivariate model of tilapia growth, appliedto seawater tilapia culture in Kuwait. The Second International Symposium on Tilapiain Aquaculture. ICLARM Conference Proceedings, pp. 29–39.

Kennedy, B., 1990. Use ofmixedmodel methodology in analysis of designed experiments.Advances in StatisticalMethods for Genetic Improvement of LivestockSpringer 77–97.

Legendre, M., Hem, S., Cisse, A., 1989. Suitability of brackish water tilapia species from theIvory Coast for lagoon aquaculture. II—growth and rearing methods. Aquat. LivingResour. 2, 81–89.

Lillehammer, M., Ødegård, J., Madsen, P., Gjerde, B., Refstie, T., Rye, M., 2013. Survival,growth and sexual maturation in Atlantic salmon exposed to infectious pancreaticnecrosis: a multi-variate mixture model approach. Genet. Sel. Evol. 45, 8.

Luan, T.D., Olesen, I., Ødegård, J., Kolstad, K., Dan, N.C., 2008. Genotype by environment in-teraction for harvest body weight and survival of Nile tilapia (Oreochromis niloticus)in brackish and fresh water ponds. The Proceedings of the 8th International Sympo-sium on Tilapia in Aquaculture, pp. 231–238 (Egypt).

Lutz, C.G., Armas‐Rosales, A.M., Saxton, A.M., 2010. Genetic effects influencing salinity tol-erance in six varieties of tilapia (Oreochromis) and their reciprocal crosses. Aquac.Res. 41, e770–e780.

MARD, 2011. Fisheries Statistics. Vietnamese Directorate of Fisheries.Nguyen, N.H., Khaw, H.L., Ponzoni, R.W., Hamzah, A., Kamaruzzaman, N., 2007. Can sexual

dimorphism and body shape be altered in Nile tilapia (Oreochromis niloticus) by ge-netic means? Aquaculture 272, S38–S46.

Nguyen, N.H., Ponzoni, R.W., Abu-Bakar, K.R., Hamzah, A., Khaw, H.L., Yee, H.Y., 2010. Cor-related response in fillet weight and yield to selection for increased harvest weight ingenetically improved farmed tilapia (GIFT strain), Oreochromis niloticus. Aquaculture305, 1–5.

Nielsen, H.M., Ødegård, J., Olesen, I., Gjerde, B., Ardo, L., Jeney, G., Jeney, Z., 2010. Geneticanalysis of common carp (Cyprinus carpio) strains: I: genetic parameters and hetero-sis for growth traits and survival. Aquaculture 304, 14–21.

Ødegård, J., Olesen, I., Gjerde, B., Klemetsdal, G., 2006. Evaluation of statistical models forgenetic analysis of challenge test data on furunculosis resistance in Atlantic salmon(Salmo salar): prediction of field survival. Aquaculture 259, 116–123.

Ponzoni, R.W., Hamzah, A., Tan, S., Kamaruzzaman, N., 2005. Genetic parameters and re-sponse to selection for live weight in the GIFT strain of Nile tilapia (Oreochromisniloticus). Aquaculture 247, 203–210.

Ponzoni, R.W., Nguyen, N.H., Khaw, H.L., Hamzah, A., Bakar, K.R.A., Yee, H.Y., 2011. Geneticimprovement of Nile tilapia (Oreochromis niloticus) with special reference to thework conducted by the WorldFish Center with the GIFT strain. Rev. Aquac. 3, 27–41.

Rezk, M.A., Ponzoni, R.W., Khaw, H.L., Kamel, E., Dawood, T., John, G., 2009. Selectivebreeding for increased body weight in a synthetic breed of Egyptian Nile tilapia,Oreochromis niloticus: response to selection and genetic parameters. Aquaculture293, 187–194.

Romana-Eguia, M.R.R., Eguia, R.V., 1999. Growth of five Asian red tilapia strains in salineenvironments. Aquaculture 173, 161–170.

Rye, M., Lillevik, K.M., Gjerde, B., 1990. Survival in early life of Atlantic salmon and rain-bow trout: estimates of heritabilities and genetic correlations. Aquaculture 89,209–216.

Santos, A.I., Nguyen, N.H., Ponzoni, R.W., Yee, H.Y., Hamzah, A., Ribeiro, R.P., 2014. Growthand survival rate of three genetic groups fed 28% and 34% protein diets. Aquac. Res45, 353–361.

SAS InstituteInc., 2005. SAS/STAT User's Guide, Version 9.1.3. SAS Institute Inc., Cary, NC,USA.

Stickney, R.R., 1986. Tilapia tolerance of saline waters: a review. Progress. Fish Cult. 48,161–167.

Suresh, A.V., Lin, C.K., 1992. Tilapia culture in saline waters: a review. Aquaculture 106,201–226.

Tayamen, M., Reyes, R., Danting, M.J., Mendoza, A., Marquez, E., Salguet, A., Gonzales, R.,Abella, T., Vera-Cruz, E., 2002. Tilapia broodstock development for saline waters inthe Philippines. Naga ICLARM Q. 25, 32–36.

Trọng, T.Q., Mulder, H.A., van Arendonk, J.A.M., Komen, H., 2013. Heritability and geno-type by environment interaction estimates for harvest weight, growth rate, andshape of Nile tilapia (Oreochromis niloticus) grown in river cage and VAC inVietnam. Aquaculture 384–387, 119–127.

Watanabe, W.O., Fitzsimmons, K., Yang, Y., Lim, C., Webster, C., 2006. Farming tilapia insaline waters. Tilapia: Biology, Culture, and Nutrition 347–447.