Contents lists available atScienceDirect
Aquaculture
journal homepage:www.elsevier.com/locate/aquaculture
Evaluation of genetic parameters for reproductive traits and growth rate in the Paci fi c white shrimp Litopenaeus vannamei reared in brackish water
Jian Tan
a,b, Sheng Luan
a,b, Baoxiang Cao
a,b, Kun Luo
a,b, Xianhong Meng
a,b, Jie Kong
a,b,⁎aYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 106 Nanjing Road, Qingdao 266071, China
bLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, 1 Wenhai Road, Qingdao 266237, China
A R T I C L E I N F O
Keywords:
Litopenaeus vannamei Brackish water Reproduction traits Growth rate Heritability Genetic correlation
A B S T R A C T
It is very common to culture L.vannameiin brackish water or under low salinity conditions, but brackish water or low salinity genetic breeding for broodstock shrimp have not yet been studied. This study provides a pre- liminary evaluation of feasibility of broodstock shrimp genetic selection in brackish water. Shrimps were initially reared at brackish water (10 ppt) eight months, and female and male shrimps were selected from each family for reproductive traits test at the salinity of 30 ppt. The heritability and genetic correlations among growth rate and reproductive traits can have important implications to the design of breeding programmes to enhance the growth rate and reproductive efficiency. However, there are no reports on the relationship between growth rate and fecundity in shrimps reared eight months in brackish water. The principal objective of the present study was to estimate the genetic parameters concerning the growth rate and reproductive traits using a restricted maximum likelihood (REML) approach based on a univariate or multivariate animal model. The goal was to confirm the genetic relationship between growth rate and fecundity inLitopenaeus vannameiunder the brackish water se- lection about eight months. In this study, the growth and reproduction traits of 115L. vannameifamilies were tested when they were cultured until 11 months. The traits of the body weight at 2 months (M2BW), body weight at 4 months (M4BW), body weight at 8 months (M8BW), growth rate before 4 months (G1R), growth rate be- tween 8 and 11 months (G2R),first spawning age (FSA), egg-laying frequency (ELF), average spawning interval (ASI), and body weight after testing (11 months, M11BW) were collected. The heritability levels of the G2R, ELF, and ASI were 0.03 ± 0.03, 0.074 ± 0.02, and 0.10 ± 0.03, respectively, which are low heritability levels. The heritability levels of the G1R, FSA, M8BW, and M11BW were 0.53 ± 0.06, 0.92 ± 0.08, 0.58 ± 0.08, and 0.52 ± 0.08, respectively, which are high heritability levels. The genetic correlations between M8BW and M11BW, between G2R and ASI, between M8BW and FSA, and between M11BW and FSA were 0.99 ± 0.01, 0.93 ± 0.10, 0.64 ± 0.10, and 0.67 ± 0.10, respectively, which are medium-high correlations; the genetic correlations between M11BW and ASI, between M8BW and ASI, and between G1R and ASI were−0.04 ± 0.21,
−0.20 ± 0.19, and−0.30 ± 0.18, respectively, which are negative correlations. The genetic relationship between the growth rate and reproductive traits was different according to the growth stage. In the early growth stage of L.vannamei, early growth rate and reproductive were not trade-offs, but there is a clear trade-off between growth rate and reproductive at breeding season. The estimates of the genetic parameters indicate that these traits can be subjected to selection in the brackish water to improve reproductive efficiency in females. The genetic breeding programme according to the growth rate from 0 to 4 months is not associated with a negative selection for reproductive traits.
1. Introduction
Pacific white shrimp (Litopenaeus vannamei, also known asPenaeus vannamei) is one of the most important cultured shrimp species worldwide.L. vannameiis distributed in the Eastern Pacific Ocean from
Northern Peru through the Equator to Mexico (Rendon et al., 2007).
The highest output is observed for penaeid shrimp, which comprise approximately 80% of the total shrimp output in the world (Thanasak and Soottawat, 2019).L. vannameiwasfirst introduced to China in 1988 (Ruan et al., 2013); and now, after 30 years of cultivation, it has
https://doi.org/10.1016/j.aquaculture.2019.734244
Received 25 March 2019; Received in revised form 21 June 2019; Accepted 22 June 2019
⁎Corresponding author at: Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 106 Nanjing Road, Qingdao 266071, China.
E-mail addresses:[email protected](S. Luan),[email protected](K. Luo),[email protected](X. Meng),[email protected](J. Kong).
Available online 26 June 2019
0044-8486/ © 2019 Elsevier B.V. All rights reserved.
T
become the dominant species in China. L. vannameiuses 70% of the total area and provides 80% of the yield of farmed shrimp; the pro- duction of L.vannameiwas 1,672,287 t in 2017, and 35% of the pro- duction was cultured in low-salinity water in China (China fishery statistical yearbook, 2018). The L.vannameigenetic selective breeding programme started in the Oceanic Institute, Oahu, Hawaii in 1984.
Selected L. vannameican adapt better to artificial environments, and some of their economic traits, such as their growth rate and disease resistance, were improved (Gjedrem and Fimlano, 1995). Over the past 30 years, the L.vannameiselective breeding programme in China has made great progress, and a system adapted to Chinese agricultural conditions has been developed. In 2011, the Yellow Sea Fisheries Re- search Institute, Shandong, China was launched a selective breeding programme to improve the harvested pond survival and body weight of reared L.vannamei(Sui et al., 2016).
Genetic breeding programmes for shrimp and broodstock shrimp rearing are usually carried out at high salinity, such as oceanic water, but not in freshwater or low salinity (such as brackish water). However, L. vannameiis a widespread saltwater species that has adapted to live under different salinities (from 1 to 50‰) (Menz and Blake, 1980 Ponce-Palafox et al., 1997). Recently, the diseases of shrimps have in- creased as a result of the expansion of the farming scale in coastal areas.
Although some water treatment methods can kill pathogens in water, air is another way that disease spreads. It is difficult to avoid this path of pathogen transmission, which is a challenge for shrimp breeding of specific pathogen-free (SPF) shrimp. Reduced-salinity culture systems for marine broodstock shrimp, which are used brackish water exchange, can be set up on farms far removed from potentially contaminated oceanic water (Parnes et al., 2004). Therefore, one proposed solution to broodstock L.vannameiproduction problems is the use of water with salinity lower than oceanic water (Araneda et al., 2008). Although brackish water or low salinity genetic breeding for broodstock shrimp have not yet been studied, it is very common to culture L.vannameiin brackish water or under low salinity conditions. Low salinity water aquaculture production of L.vannameihas accounted for 35% of the total production of shrimps farming in China (Chinafishery statistical yearbook, 2018)). Currently, the production of desalination seed usually uses shrimps grown in high salt water as broodstock; nauplii also grow in high salt water, which is also used to reared postlarvae.
Shrimps are then desalinated to shorten the incubation cycle, usually using the rapid salt reduction method, and salinity can be reduced by 5–8‰per day. Using this process, inevitable problems, such as a low survival rate, poor shrimp quality and genotype and environment in- teraction, arise.L. vannameipostlarvae are not tolerant to large salinity fluctuations when they are very young (Saoud et al., 2003). For ex- ample, BothMcGraw et al. (2002)andSaoud et al. (2003)reported that increased survival rate as the organisms reached 15 days old at salinity greater than 4 ppt when they were evaluated of postlarvae survival.
Van-Wyk et al. (1999)reported that using water with 0.5 ppt salinity, the growth rates and survival below those with seawater. Therefore, the genotype and environment interaction problems may occur because broodstock shrimps are not domesticated under desalination condi- tions. We use desalination cultured shrimps as broodstock shrimps so that its offspring will carry the gene that regulates desalination adapt- ability. Therefore, it is necessary to carry out shrimp selective breeding for growth rate and reproductive traits under low salinity conditions.
Current reliance on oceanic water broodstock is risky and it is necessary to selection brackish water broodstock through selective breeding (Andriantahina et al., 2013). In this study, it may be advantageous to breed of new variety in low-salinity water and improve the quality of Germplasm. To achieve this goal, it is necessary to determine the ge- netic parameters of growth rate and reproductive traits of desalination breeding shrimps.
The growth rate is one of the main economic traits of shrimp pro- duction. Ordinarily, body weight shows a highly phenotypic variation in many aquaculture species (Gjedrem, 1983); due to the individuals'
high reproductive potential, it is possible to produce high selection intensity. Therefore, even under low heritability, the potential for the genetic improvement in the growth rate through selective breeding for additive gene effects is promising. In L.vannamei, Tan et al. (2016) found that the heritability levels for body weight are 0.43 and 0.44 at low and high density, respectively, which indicates a moderate level.
Sui et al. (2016) reported that that the heritability levels for body weight are 0.28 ± 0.136 and 0.423 ± 0.065 respectively. Castillo- Juárez et al. (2007)estimated that the bodyweight heritability levels are ranged from 0.24 to 0.45 for different models. The growth rate is regarded as a trait of main economic importance for many aquaculture species. Rapid growth accelerates the turnover of re-production, and usually, larger animals attain a higher price per unit weight compared with smaller ones. The growth rate is also easy to measure through measurement of the body length or body weight (Gjerde, 1986).
Reproductive efficiency is another economically important trait in commercial larvae production, especially for shrimp breeders who produce fertilized eggs. Most studies of reproductive traits and their relationship to the body weight are derived from data recorded on natural populations or from individuals reared in different environ- ments. Thus, the environmental and genetic variance components are often confused, and body weight is often confused with the age of the individual under consideration. Due to this reason, available study on genetic variation in reproductive traits and their relationship to the growth rate is very seldom (Gjerde, 1986). Consequently, the herit- ability and genetic correlations between growth rate and reproductive traits can have important implications in the design of breeding pro- grammes to enhance the growth rate and reproductive efficiency. The results of several species have shown that strains with high growth rates had lower fecundity and that strains with high fecundity had lower growth rates. However, no report has described the relationship be- tween the growth rate and reproductive traits in L.vannamei.
It should be emphasized that in planning a genetic breeding pro- gramme including only one trait, it is sufficient to know whether the heritability is low, medium or high, as long as the estimation is reliable.
However, for the sake of optimizing a genetic breeding programme, including multi-traits, more accurate estimates of the heritability levels and genetic correlations between the traits included in the programme are needed (Gjerde, 1986). L. vannamei is generally cultured for 4–5 months, usually harvesting at around 15 g in China, which is the main reason for our genetic evaluation of growth rate from 0 to 4 months old. L.vannameiis an introduced species, and the shrimp is up to 300 RMB per pair.L. vannameican spawning eggs several times, so the number of spawning, the average spawning interval and the age of first spawning are very important for the nursery. If the female can spawn eggs several times, and the ovulation cycle is short, the age of spawning is early, and the spawning period is long, such a shrimp can obtain the greatest economic benefit for the nursery. So, the re- productive traits are important commercially, it should be selected. In this study, estimates of the additive genetic variation for the growth rate and reproduction traits for shrimp reared in brackish water are summarized, and the relationship between the growth and reproduction is also reviewed.
Selection for high-performance spawners using traits associated with fast growth could be an important strategy to improve nauplii and shrimp production assuming that these traits are heritable and the ge- netic correlations of traits are positive (Wyban and Sweeney, 1991 Ibarra et al., 1997 Racotta et al., 2003). Therefore, this experiment tested the growth rate and reproductive traits in brackish water to verify the genetic relationship between the growth rate and re- productive traits. Reliable estimates of the genetic correlations between the growth and reproductive traits in brackish water are a prerequisite for planning breeding programmes. This study is of great significance to determine the genetic breeding strategy for reproductive traits and growth traits in brackish water. It may be feasible to breed of new variety in low-salinity water and improve the quality of Germplasm.
2. Materials and methods
2.1. Historical background and establishment of full-sib/half-sib families The breeding programme was carried out at the Yellow Sea Fisheries Research Institute, Marine Genetic Breeding Centre of the Ministry of Agriculture, China. In June and July 2012, broodstock shrimp was introduced from America and Singapore (G0). Broodstock was assessed for the presence of different virus (WSSV, TSV, IHHNV, YHV) strains using RT-PCR, and only virus-free broodstocks were used.
Each broodstocks shrimp was individually tagged by placing numbered rings on one ocular peduncle after isolation and conservation. After one month of temporary rearing, broodstock with a mature gonad and healthy appearance were chosen. The G1 to G6 generations were pro- duced using a half-sib/full-sib mating design.
2.2. Cultivation of juvenile shrimp
The trial was carried out at Xinhai Aqua Biotechnology Co. Ltd., Huanghua, Hebei, China (N38°37′, E117°33′). After hatching, about 10,000 nauplii were randomly selected from each half-sib/full-sib fa- mily for separate training with uniform management. Chlorella was used as weaning food, followed byArtemiaandRotifera. In total, 1500 shrimp (PL5) from each family were cultured under the condition of decreased salinity of ten parts per thousand. A total of 600 juvenile shrimp were selected randomly from every family when they had grown to the PL20 stage and were isolated for cultivation in a 40 × 40 × 100 cm net cage in a 100 m2tank. Each shrimp was injected with a visiblefluorescent elastomer implant (VIE) to identify families until shrimp reached approximately 2 months. This tagging identifica- tion allowed families to be mixed in tanks for the performance eva- luation. Artificial feed was supplied during the growth period, and the feeding regimen in all tanks consisted of commercial pellets containing 33% protein. The water temperature ranged from 26 to 28 °C, and the salinity was 10 ± 0.5 ppt. One hundred andfifteen families (involving 111 dam and 97 sire) from G6 generations were selected as experi- mental shrimp.
2.3. Growth traits test of L. vannamei
A total of 50 shrimps per family were tagged and weighed. We obtain the average weight of each family after 2 months (M2BW). The tagging identification allowed families to be mixed in a tank for the performance evaluation. At 60 days of growth in brackish water (aged 4 months), each member of the family (3264 individuals) was measured to determine the body weight (M4BW). The growth rate was calculated from the birthdate until M4BW measurement (G1R). G1R (g/d)
=days of growthM4BW
2.4. Reproductive test of L. vannamei
The mixed culture in brackish water was continued when the growth trait test was completed. When the shrimp grew to the age of 8 months, the females were subjected to unilateral eyestalk ablation, and a number-coded ring was placed on the remaining eyestalk. At the same time, the individual body weight at 8 months (M8BW) was re- corded. Male and female shrimps were selected from each family for growth at an enhanced salinity of 30 ppt. After an acclimation period, reproductive trait testing was initiated. The diet comprised 40% squid and 60% nereis, was divided into four equal daily rations that ac- counted for a total daily supply of 20% of wet weight biomass, and was adjusted daily. The test was carried out in several 25 m2tanks with a density of 12 shrimp/m2. Female shrimp of sexual maturity were placed into the male shrimp tank for natural mating at 8:00 am every day (recording the female shrimp number-coded ring). The female shrimp
were collected at 18:00, the mating female shrimp were placed in the spawning tank (recording number-coded ring), and the unmated fe- males were returned to the original tank. The main record egg-laying frequency of female during the test (ELF), average spawning interval (ASI),first spawning age (FSA), female body weight at the end of the reproductive test (aged 11 months, M11BW). The growth rate was calculated from the beginning of reproductive test until M11BW mea- surement (G2R). G2R (g/d) =days of reproductive testedM11BW−M8BW .
2.5. Statistical analyses
The variance of the components of the growth traits according to different growth stage and reproductive traits were estimated using the average information REML method in ASReml 4.1 (Gilmour et al., 2009). In this research, the complete pedigree information used in the animal models from 2012 to 2017 was used to provide the A matrix (additive genetic relationship matrix).
The ELF trait was analysed using a generalized linear mixed (GLMM) model with a multinomial distribution and a logit link func- tion. GLMM model is an extension of generalized linear model that was developed by McCullagh and Nelder (1989). In GLMM model, the combined effect offixed and random effects on the underlying scale is expressed as the linear predictor (η). The relationship between the linear predictor and vector of observations in a GLMM is described asy|
u~ (h(η),R), which specifies that the conditional distribution ofygiven uhas a meanh(η) and varianceR. The relationship between the linear predictor (η) and the conditional mean (μ) of the trait is modelled through a link (inverse) function (μ=hη). The selection of inverse link functions is typically based on the error distribution (Kachman, 2008).
Heritability was estimated for ELF by considering it a categorical phe- notype (e.g., 1–15 spawning).
= + + +
yijl μ BWj al eijl (Model 1)
whereyijlis the linear predictor on the logit scale,μis the overall mean, andBWj is the fixed effect of the jth body weight;alis the additive genetic effect of thelthshrimp andeijlis the random residual error of the ithindividual, which isfixed atπ2/3≈3.28987 under the logit scale according to the ASReml 4.1 User Manual (Gilmour et al., 2009). The common environment effect was excluded from this model.
Heritability was calculated as:
= +
h σ
σ σ
a
a e
2 2
2 2
whereh2is the heritability estimate of the families,σ2ais the additive genetic variance between individuals of the families, andσ2eis the re- sidual variance between individuals of the families.
The animal models used for the genetic parameter estimation of other traits are as follows:
= + + +
yijl μ Sj al eijl (Model 2)
whereyijlis the phenotypic value of the traits (M4BW, M8BW, M11BW, G1R, G2R, ASI, and FSA) of theithshrimp,μis the overall mean,Sjis the fixed effect of thejthindividual,alis the additive genetic effect of thelth shrimp, andeijlis the random residual error of theithindividual. The common environment effect was excluded from this model because the separate culture is very short (shrimp was cultured in a same water environment when PL20).
Heritability was calculated as:
= +
h σ
σ σ
a
a e
2 2
2 2
whereh2is the heritability estimate of the families,σ2ais the additive genetic variance between individuals of the families, andσ2eis the re- sidual variance between individuals of the families.
Genetic correlations were calculated as:
=
raij σaij/(σaii·σajj).
whereraijis the genetic correlation estimate of the families,σaijis the genetic covariance of the families, andσaii·σajjis the additive genetic variance between individuals of the families.
3. Results
3.1. Phenotypic statistical analysis of the growth rate and reproductive traits of L. vannamei
Statistical analysis of the sample size, mean, maximum, minimum, standard deviation, and coefficient variation for the growth rate and reproductive traits are presented inTable 1. The average growth rate during early period of L. vannamei was 0.10 g/d, and the average growth rate during the reproductive period was 0.29 g/d because the reproductive season mainly used fresh feed, which has a high nutri- tional value. Thefirst spawning age ranged from 226 to 303 days, with a mean of 258.39 days. The egg-laying frequency was between 1 and 15 times, and the coefficient of variation reached 49.83%, which indicates significant differences between different families and individuals. The average spawning interval was between 2.5 and 60 days, which reflects the reproductive performance of different females after spawning. The coefficient of variation was as high as 75.59%. The above data reflect the extreme differentiation of reproductive traits in different families or individuals and that are necessary for the genetic breeding and re- productive performance.
.
3.2. Variance component and heritability of the growth rate and reproductive traits of L. vannamei
The variance components and heritability estimate for each growth and reproductive trait are shown inTable 2. The heritability levels of M4BW, M8BW, and M11BW were 0.32 ± 0.05, 0.58 ± 0.08, and 0.52 ± 0.08, respectively, both of which showed medium-high herit- ability, which indicates that growth traits are more affected by her- edity. The heritability levels of reproductive traits such as ELF and ASI were 0.07 ± 0.02 and 0.10 ± 0.03, respectively, which indicates low heritability. Thus, reproductive traits were relatively less affected by heredity. The heritability levels of the FSA and G1R were 0.92 ± 0.08 and 0.53 ± 0.06, respectively, which were medium-high heritability levels, which indicates that thefirst spawning time and early growth rate were mainly affected by genetic factors. The G2R was at a low heritability level, only 0.03 ± 0.03, which indicates that the growth rate during reproductive period is greatly affected by other factors, and the genetic effect is minimal.
3.3. Genetic correlation of the growth rate and reproductive traits of L.
vannamei
The genetic correlation and heritability estimate for the growth and reproductive trait are shown inTable 3. The genetic correlations among body weight traits in different periods show high correlation, ranging from 0.63 ± 0.10 to 0.99 ± 0.01, and the correlation of the body weight traits was higher during each period. The genetic correlation between thefirst spawning age (FSA) and body weight in each period ranged from 0.34 ± 0.11 to 0.67 ± 0.10. The genetic correlation be- tween the average spawning interval (ASI) and body weight in each period ranged from −0.21 ± 0.20 to −0.04 ± 0.21 The genetic correlation between the G1R and average spawning time interval (ASI) was−0.30 ± 0.18, which indicates that the early growth rate of the female shrimp was faster and re-spawning time interval of the female shrimp was shorter. Thus, the female's spawning frequency is higher during the reproductive period, reflecting the higher fertility. However, the genetic correlation between the G2R and average spawning time interval (ASI) was 0.93 ± 0.10, which indicates that the female's growth rate during the reproductive period was faster and the re- spawning time interval of the female shrimp was longer. Thus, the fe- male's spawning frequency was lower during reproductive period, which reflects the reduced fertility. The genetic relationship between the growth rate and reproductive traits was different according to growth stage. In the early growth stage of L.vannamei, the early growth rate and reproductive traits were not trade-offs. There is a clear trade- offbetween the growth rate and reproductive traits during breeding season. The estimates of the genetic parameters indicate that these traits can be selected to improve the reproductive efficiency of females.
4. Discussion
This study was carried out the test of growth and reproduction traits of L. vannamei which reared eight months in brackish water, and evaluated the heritability and genetic correlation of L.vannamei. The heritability and genetic correlations among growth rate and re- productive traits can have important implications to the design of breeding programmes to enhance the growth rate and reproductive efficiency in brackish water. In this study, the common environment effect was excluded from this model because the separate culture is very short (shrimp was communal rearing in a same water environment when PL20, just 20 days), for which common environmental effects are difficult to disentangle. Indeed, the shrimps were cultured in one pond environmental early in PL20 so that the common environmental effects were very small. Sonesson et al. (2013) attempted to analyze the common environmental effects and genetic parameter estimations of the body weight. However, they found it difficult to separate common environmental effects in the model. These authorsfinally excluded the common environmental effects from the model.Luan et al., 2015found Table 1
Descriptive statistics for the growth rate and reproductive traits of L.vannamei.
Trait N Mean Min Max SD CV (%)
M2BW (g) 115 6.08 3.05 9.54 1.31 21.55
M4BW (g) 3264 17.10 2.90 31.00 4.09 23.89
G1R (g/d) 3264 0.10 0.02 0.20 0.03 26.18
M8BW (g) 1428 31.23 17 49.0 5.74 18.38
M11BW (g) 911 58.90 48.60 77.2 5.40 9.17
G2R (g/d) 911 0.29 0.15 0.45 0.03 9.55
FSA (d) 1428 258.39 226 303 14.10 5.46
ELF (times) 1428 5.98 1.00 15.00 2.98 49.83
ASI (d) 1387 11.39 2.5 60 8.61 75.59
M2BW: family body weight at 2 months; M4BW: body weight at 4 months; G1R:
growth rate before 4 months; M8BW: body weight at 8 months; M11BW: body weight at 11 months; G2R: growth rate between 8 months and 11 months; FSA:
first spawning age; ELF: egg-laying frequency; ASI: average spawning interval;
N: sample size; Max, Min, Mean, SD, and CV represent the maximum, minimum, mean, standard deviation, and coefficient variation.
Table 2
Variance components and heritability of growth rate and reproductive traits of L.vannamei.
σa2 σe2 σp2 h2
M4BW 4.43 9.56 13.99 0.32 ± 0.05
M8BW 18.11 13.17 31.28 0.58 ± 0.08
M11BW 14.55 13.49 28.04 0.52 ± 0.08
G1R 0.30E-3 0.26E-3 0.56E-3 0.53 ± 0.06
G2R 0.21E-4 0.71E-3 0.73E-3 0.03 ± 0.03
FSA 153.83 12.90 166.73 0.92 ± 0.08
ELF 0.26 3.29 3.55 0.07 ± 0.02
ASI 7.08 67.35 74.43 0.10 ± 0.03
M4BW: body weight at 4 months; M8BW: body weight at 8 months; M11BW:
body weight at 11 months; G1R: growth rate before 4 months; G2R: growth rate between 8 months and 11 months; FSA: first spawning age; ELF: egg-laying frequency; ASI: average spawning interval.
that the common environmental effect of our L.vannameipopulation is only 0.07 ± 0.06 when the shrimp 7 g (about 90 days).Kong, 2018 found that the common environmental effect is minimal in the com- munal rearing at early stage mode (communal rearing begins at PL20) for our L.vannamei population, close to zero (0.0016). The common environmental effect is 0.073 ± 0.112 in the separate rearing at early stage mode (communal rearing begins at PL100) for ourL. vannamei population. In addition, body weight at tagging rather than age was fitted as thefixed effect to reduce the impact of common environmental effect inModel 1.
Heritability is a crucial parameter to estimating the response to the selection for a potential trait in a breeding population (Falconer and Mackay, 1996 Lynch and Walsh, 1998 Kruuk, 2004). Estimation of the heritability of potential traits in a breeding population is a necessary methodology to assess the sustainability of breeding and achieve ge- netic progress. Evaluation of genetic parameters for growth traits has been widely reported. In seawater, most of the heritability levels re- ported in some studies of L.vannameiwere between 0.17 ± 0.04 and 0.44 ± 0.05 (Pérez-Rostro and Ibarra, 2003a, 2003b;Gitterle et al., 2005a, 2005b Tan et al., 2016). In brackish water,Kong et al. (2017) reported the heritability of body weight of L.vannameiwas 0.3 ± 0.07.
The results of our study showed that the heritability levels of the har- vested body weight of L.vannameiwere moderate to high at different growth stages, and the variation range of the heritability levels was not large at different growth stages (0.32 ± 0.05, 0.58 ± 0.08, 0.52 ± 0.08). However, the heritability of body weight shows a de- creasing trend during the reproductive period. The results of our study are slightly higher than other research results. This may be because our results cannot disentangle common environmental effects in the model, which leads to certain confusion between additive genetic variance and common environmental variance in the data (Thodesen et al., 2011 Bentsen et al., 2012) and to a larger estimate of the heritability than the actual value. Indeed, the shrimp were cultured in one pond early in 2 months so that the common environmental effects were very small.
Therefore, different estimation methods or population may lead to differences in heritability estimates. Additionally, environmental in- terventions involving some unpredictable genetic effects may affect the estimation of heritability. In our study, the coefficient of variation of the body weight and estimated heritability indicate that the genetic variation of L.vannameiis larger and has a large potential for genetic selection.
Knowledge of the genetic parameters for reproductive traits would assist in the decision of whether to include these traits in breeding programmes targeting growth, disease resistance, or survival, which the potential negative effects on reproduction that might be caused by genetic breeding selection for growth. Only a few reports have de- scribed estimates of the genetic parameters of reproductive and body weight traits. In previous studies, the heritability levels of the egg- laying frequency and egg number were 0.06 ± 0.06 and 0.12 ± 0.08, respectively, both of which were lower heritability levels (Tan et al., 2017).Caballero-Zamora et al. (2015)andArcos et al. (2004)reported
that the heritability levels of the egg number of L. vannamei were 0.17 ± 0.24 and 0.13 ± 0.04, respectively. InOreochromis niloticus, Trong et al. (2013)reported that the heritability estimates for spawning success were 0.14 to 0.18 for the logit model and 0.20 to 0.22 for the linear model.Arcos et al. (2004)demonstrated a significant genetic and phenotypic correlation between the body weight and egg number of female L. vannamei, with values of −0.13 and 0.34, respectively.
Caballero-Zamora et al. (2015)obtained a negative genetic correlation between the body weight and egg number of femaleL. vannamei, with a value of−0.21 ± 0.19. In other aquaculture species, genetic correla- tions between the body weight and reproductive traits have been esti- mated and range from 0.33 to 0.69 (Gall, 1975 Gall and Neira, 2004 Su et al., 1997), showing a favourable association. However, it was no reported in broodstock genetic breeding under brackish water. The heritability of the egg-laying frequency and average spawning interval obtained in this study was 0.07 ± 0.02 and 0.10 ± 0.03, respectively.
These results are like otherfindings, which indicates that reproductive traits were relatively less affected by heredity and reproductive traits may be more affected by the environment, female nutrition and ma- turation, male shrimp, and other factors. Therefore, for the selection of reproductive traits, multiple generations need to be selected to obtain enough genetic progress.
However, studies investigating the heritability and genetic correla- tion between reproductive and growth rate-related traits remain scarce in L. vannamei which reared in brackish water. The relationship be- tween the growth rate and reproduction is core to animal life history theory. In general, artificial selection may lead to trade-offs (Wootton, 1977 Reznick, 1983 Morgan and Metcalfe, 2001 Robinson and Wardrop, 2002) because natural populations are subjected to growth variation and individual feeding, which may mask the representation of a trade-off(Roff, 1992). Some species results showed that the strains with a high growth rate had lower fecundity, and those with high fe- cundity had a lower growth rate. Thus, the relationship between the growth rate and fertility is very worthy of concern. Tsikliras et al.
(2007)reported that theSardinella auritaindividual specific growth rate at the spawning period was negatively related to its fecundity. How- ever, contrary to the trade-offtheory,Schultz and Warner (1991)re- ported a positive relationship between the reproduction and growth rate traits. The relationship between growth and reproduction has not been discussed for L.vannamei. In this study, we studied the relation- ship between the growth rate and reproduction at two different stages.
The results have important implications to the design of breeding programmes to enhance the growth rate and reproductive efficiency.
In the present study, the population that was used was based on genetically selected families of growth traits. Therefore, the preliminary study conclusions can be drawn from the genetic relationship between the growth rate and reproductive performance under artificial selection pressure. The genetic correlation between the G1R and average spawning time interval (ASI) was−0.30 ± 0.18, which indicates that the early growth rate of the female shrimp was faster and the re- spawning time interval of the female shrimp was shorter. Thus, the Table 3
Heritability and genetic correlation between growth rate and reproductive traits of L.vannamei.
M4BW M8BW M11BW G1R G2R FSA ELF ASI
M4BW 0.32 ± 0.05
M8BW 0.65 ± 0.09 0.58 ± 0.08
M11BW 0.62 ± 0.10 0.99 ± 0.01 0.52 ± 0.08
G1R – 0.77 ± 0.06 0.72 ± 0.08 0.53 ± 0.06
G2R −0.84 ± 0.29 – – −0.99 ± 0.75 0.036 ± 0.03
FSA 0.34 ± 0.11 0.64 ± 0.09 0.67 ± 0.09 0.45 ± 0.10 −0.50 ± 0.28 0.92 ± 0.08
ELF – – – – – – 0.07 ± 0.02
ASI −0.21 ± 0.20 −0.20 ± 0.19 −0.04 ± 0.21 −0.3 ± 0.189 0.93 ± 0.10 −0.14 ± 0.17 – 0.10 ± 0.03 M4BW: body weight at 4 months; M8BW: body weight at 8 months; M11BW: body weight at 11 months; G1R: growth rate before 4 months; G2R: growth rate between 8 months and 11 months; FSA:first spawning age; ELF: egg-laying frequency; ASI: average spawning interval.
spawning frequency of the females was higher during the reproductive period, which reflects higher fertility. In the early growth stage of L.
vannamei, the early growth rate and reproductive traits were not trade- offs. However, the genetic correlation between the G2R and average spawning time interval (ASI) was 0.93 ± 0.10, which indicates that the growth rate of the female shrimp was faster and the re-spawning time interval of the female shrimp was longer. Thus, the spawning frequency of the females was lower during reproductive period, which reflects lower fertility. There is a clear trade-offbetween the growth rate and reproductive traits during breeding season, which is likely because energy is mainly used for reproductive regulation during the breeding season, and the trade-off of energy distribution leads to a negative correlation between the growth rate and reproduction. The genetic relationship between the growth rate and fecundity was found to be different according to the growth stage. Therefore, in the practice of breeding programmes, we can choose shrimps with a fast growth rate of 0–4 months to achieve the purpose of indirect breeding of re- productive traits (average spawning interval), to obtain females with more spawning times. This breeding programmes is a win-win result for both farmers and nurseries.
5. Conclusion
In summary, although L.vannameihas been grown in brackish water for 8 months, the heritability levels estimate for the body weight and reproductive traits are similar to those reported by others in seawater.
Therefore, broodstock shrimp culture can be carried out in the brackish water. The genetic relationship between reproductive traits and the growth rate during the breeding season of L.vannameiunder artificial selection pressure is a trade-off, and a faster growth rate of L.vannamei has a negative impact on reproductive performance. However, an early growth rate and reproductive traits is not trade-off. Thus, the genetic breeding programme based on the growth rate from 0 to 4 months does not cause a negative selection for reproductive traits.
Acknowledgements
This research was supported by the National Natural Science Foundation of China (31702338), the Shandong Proovince Postdoctoral Innovative Foundation (201703047), the Qingdao Postdoctoral Science Foundation Funded Project (2017270), the Taishan Scholar Program for Seed Industry, the Projects of China Agriculture Research System (CARS-48), the Projects of International Exchange and Cooperation in Agriculture, Ministry of Agriculture and Rural Affairs of China Science, Technology and Innovation Cooperation in Aquaculture with Tropical Countries, the Projects of Shandong Province Agricultural Seed Improvement Project (2017LZN011). We thank Shengyu Xu and Jutao Guo for providing technical support and collecting the data during this study.
References
Andriantahina, F., Liu, X., Feng, T., Xiang, J.H., 2013. Current status of genetics and genomics of reared Penaeid shrimp: information relevant to access and benefit sharing. Mar. Biotechnol. 15 (4), 399–412.
Araneda, M., Eduardo, P.P., Gasca-Leyva, E., 2008. White shrimpPenaeus vannameicul- ture in freshwater at three densities: condition state based on length and weight.
Aquaculture 283 (1–4), 13–18.
Arcos, F.G., Racotta, I.S., Ibarra, A.M., 2004. Genetic parameter estimates for re- productive traits and egg composition in Pacific white shrimpPenaeus(Litopenaeus) vannamei. Aquaculture 236 (1–4), 151–165.
Bentsen, H.B., Gjerde, B., Nguyen, N.H., Rye, M., Ponzoni, R.W., Vera, M.S.P., 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:
genetic parameters for body weight at harvest inOreochromis niloticusduringfive generations of testing in multiple environments. Aquaculture 338–341, 56–65.
Caballero-Zamora, A., Cienfuegos-Rivas, E.G., Montaldo, H.H., Campos-Montes, G.R., Martínez-Ortega, A., Castillo-Juárez, H., 2015. Genetic parameters for spawning and growth traits in the Pacific white shrimp (Penaeus(Litopenaeus)vannamei). Aquac.
Res. 46, 833–839.
Castillo-Juárez, H., Casares, J.C.Q., Campos-Montes, G., Villela, C.C., Ortega, A.M., Montaldo, H.H., 2007. Heritability for body weight at harvest size in the Pacific white shrimp, Penaeus (Litopenaeus) vannamei, from a multi-environment experiment using univariate and multivariate animal models. Aquaculture 273 (1), 42–49.
Chinafishery statistical yearbook, 2018. Chinafishery statistical yearbook. China Agriculture Press, Beijing, pp. 2018.
Falconer, D., Mackay, T., 1996. Introduction to quantitative genetic. Longman House, Hessex, UK.
Gall, G.A., 1975. Genetics of reproduction in domesticated rainbow trout. J. Anim. Sci. 40 (1), 19–28.
Gall, G.A., Neira, R., 2004. Genetic analysis of female reproduction traits of farmed coho salmon (Oncorhyncus kisutch). Aquaculture 234 (1), 143–154.
Gilmour, A.R., Gogel, B.J., Cullis, B.R., Thompson, R., 2009. ASReml User Guide Release 3.0. VSN, Hemel Hempstead, UK.
Gitterle, T., Salte, R., Gjerde, B., Rye, M., Salte, R., 2005a. Genetic (co)variation in re- sistance to white spot syndrome virus (WSSV) and harvest weight inPenaeus (Litopenaeus)vannamei. Aquaculture 246, 139–149.
Gitterle, T., Rye, M., Salte, R., Cock, J., Johansen, H., Lozano, C., Suárez, J.A., 2005b.
Gjerde B. genetic (co)variation in harvest body weight and survival inPenaeus (Litopenaeus)vannameiunder standard commercial conditions. Aquaculture 243, 83–92.
Gjedrem, T., 1983. Genetic variation in quantitative traits and selective breeding infish and shellfish. Aquaculture 33, 51–72.
Gjedrem, T., Fimlano, I.E., 1995. Potential benefits from high health and genetically improved shrimp stocks. In: Browdy, C.L., Hopkins, J.S. (Eds.), Swimming Through Troubled Water. Proceedings of the Special Session on Shrimp Farming World Aquaculture Society, Baton Rouge, LA, USA, pp. 60–65.
Gjerde, B., 1986. Growth and reproduction infish and shellfish. Aquaculture 57 (1–4), 37–55.
Ibarra, A.M., Ramirez, J.L., Garcia, G.A., 1997. Stocking density effects on larval growth and survival oftwo catarina scallop,Argopecten ventricosus (circularis)(Sowerby II, 1842), populations. Aquac. Res. 28, 443–451.
Kachman, S.D., 2008. An introduction to generalized linear mixed models. Statistics 24, 59–73.
Kong, Z.W., 2018. Research and Application of Molecular Markers in Selection and Breeding of the Pacific White Shrimp,Litopenaeus vannamei. Ocean University of China.
Kong, J., Luan, S., Luo, K., Li, X.P., Meng, X.H., Cao, B.X., Liu, N., 2017. Genetic eva- luation for body weight and survival of Pacific white shrimp (Litopenaeus vannamei) at different salinity. J. Fish. China 41 (4), 573–579.
Kruuk, L.E.B., 2004. Estimating genetic parameters in natural populations using the 'animal model'. Philos. Trans. R. Soc. B 359, 873–890.
Luan, S., Luo, K., Chai, Z., Cao, B.X., Meng, X.H., Lu, X., Liu, N., Xu, S.Y., Kong, J., 2015.
An analysis of indirect genetic effects on adult body weight of the Pacific white shrimpLitopenaeus vannameiat low rearing density. Genet. Sel. Evol. 47 (1), 02–95.
Lynch, M., Walsh, B., 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
McCullagh, P., Nelder, J.A., 1989. Generalized Linear Models, 2nd ed. Chapman and Hall, London.
McGraw, W.J., Davis, D.A., Teichert-Coddington, D., Rouse, D.B., 2002. Acclimation of Litopenaeus vannameipostlarvae to low salinity: influence of age, salinity endpoint, and rate of salinity reduction. J. World Aquacult. Soc. 33, 78–84.
Menz, A., Blake, B.F., 1980. Experiments on the growth ofPenaeus vannameiBoone. J.
Exp. Mar. Biol. Ecol. 48 (2), 99–111.
Morgan, I.J., Metcalfe, N.B., 2001. Deferred costs of catch-up growth after autumnal food shortage in juvenile salmon. Proc. R. Soc. B Biol. Sci. 268, 295–301.
Parnes, S., Mills, E., Segall, C., Raviv, S., Davis, C., Sagi, A., 2004. Reproductive readiness of the shrimpLitopenaeus vannameigrown in a brackish water system. Aquaculture 236 (1–4), 593–606.
Pérez-Rostro, C.I., Ibarra, A.M., 2003a. Heritabilities and genetic correlations of size traits at harvest size in sexually dimorphic Pacific white shrimp (Litopenaeus vannamei) grown in two environments. Aquac. Res. 34 (12), 1079–1085.
Pérez-Rostro, C.I., Ibarra, A.M., 2003b. Quantitative genetic parameter estimates for size and growth rate traits in Pacific white shrimp,Penaeus vannamei(Boone 1931) when reared indoors. Aquac. Res. 34 (7), 543–553.
Ponce-Palafox, J., Martinez-palacios, C.A., Ross, L.G., 1997. The effects of salinity and temperature on the growth and survival rates of juvenile white shrimp,Penaeus vannamei, Boone, 1931. Aquaculture 157 (1), 107–115.
Racotta, I.S., Ramirez, J.L., Ibarra, A.M., Rodríguez-Jaramillo, M.C., Carreño, D., Palacios, E., 2003. Growth and gametogenesis in the lion's paw scallopNodipecten(Lyropecten) subnodosus. Aquaculture 217, 334–349.
Rendon, R.S., Macias, R.E., Calderon, P.J.A., Nunez, P.A., Solis, I.R., 2007. Comparison of some reproductive characteristics of farmed and wild white shrimp malesLitopenaeus vannamei(Decapoda:Penaeidae). Revista de Biologia Tropical 55, 199–206.
Reznick, D.N., 1983. The structure of guppy life histories: the trade-offbetween growth and reproduction. Ecology 64, 862–873.
Robinson, B.W., Wardrop, S.L., 2002. Experimentally manipulated growth rate in three- spine sticklebacks: assessing trade offs with developmental stability. Environ. Biol.
Fish 63, 67–78.
Roff, D.A., 1992. The Evolution of Life Histories. Theory and Analysis. Chapman and Hall, New York.
Ruan, X.H., Luo, K., Luan, S., Kong, J., Xu, S.Y., Chen, R.J., Chen, G.L., 2013. Evaluation of growth performance inLitopenaeus vannameipopulations introduced from other nations. J. Fish. China 1, 37–42.
Saoud, I.P., Davis, D.A., Rouse, D.B., 2003. Suitability studies of inland well waters for Litopenaeus vannameiculture. Aquaculture 217, 373–383.
Schultz, E.T., Warner, R.R., 1991. Phenotypic plasticity in life history traits of female Thalassoma bifasciatum(Pisces: Labridae): 2. Correlation of fecundity and growth rate in comparative studies. Environ. Biol. Fish 30, 333–344.
Sonesson, A.K., Ødegård, J., Rönnegård, L., 2013. Genetic heterogeneity of within-family variance of body weight in Atlantic salmon (Salmo salar). Genet. Sel. Evol. 45, 41–48.
Su, G.S., Liljedahl, L.E., Gall, G.A., 1997. Genetic and environmental variation of female reproductive traits in rainbow trout (Oncorhynchus mykiss). Aquaculture 154 (2), 115–124.
Sui, J., Luan, S., Luo, K., Meng, X.H., Lu, X., Cao, B.X., Li, W.J., Chai, Z., Liu, N., Xu, S.Y., Kong, J., 2016. Genetic parameters and response to selection for harvest body weight of pacific white shrimp,Litopenaeus vannamei. Aquac. Res. 452, 134–141.
Tan, J., Luan, S., Luo, K., Guan, J.T., Li, W.J., Sui, J., Guo, Z.J., Xu, S.Y., Kong, J., 2016.
Heritability and genotype by environment interactions for growth and survival in Litopenaeus vannameiat low and high densities. Aquac. Res. 48 (4), 1430–1438.
Tan, J., Kong, J., Luo, K., Cao, B.X., Liu, N., Meng, X.H., Guo, Z.J., Xu, S.Y., Luan, S., 2017. Genetic parameter estimation of reproductive traits ofLitopenaeus vannamei. J.
Ocean Univ. China 16 (1), 161–167.
Thanasak, S.L., Soottawat, B., 2019. Prevention of quality loss and melanosis of Pacific white shrimp by cashew leaf extracts. Food Control 95, 257–266.
Thodesen, J., Rye, M., Wang, Y.X., Yang, S.K., Bentsen, H.B., Gjedrem, T., 2011. Genetic improvement of tilapias in China: genetic parameters and selection responses in growth of Nile tilapia (Oreochromis niloticus) after six generations of multi-trait se- lection for growth andfillet yield. Aquaculture 322–323, 51–64.
Trong, T.Q., Van-Arendonk, J.A.M., Komen, H., 2013. Genetic parameters for re- productive traits in female Nile tilapia (Oreochromis niloticus): II. Fecundity and fer- tility. Aquaculture 416, 72–77.
Tsikliras, A.C., Antonopoulou, E., Stergiou, K.I., 2007. A phenotypic trade-offbetween previous growth and present fecundity in round sardinellaSardinella aurita. Popul.
Ecol. 49 (3), 221–227.
Van-Wyk, P., Davis-Hodgkins, M., Laramore, C.R., Main, K.L., Mountain, J., Scarpa, J., 1999. Farming Marine Shrimp in Recirculating Freshwater Systems. FDACS contract M520. Florida Department of Agriculture and Consumer Services, Tallahassee, Florida, USA.
Wootton, R.J., 1977. Effect of food ration during the breeding season on the size, body components and egg production of female sticklebacks (Gasterosteus aculeatus L.). J.
Anim. Ecol. 46, 823–834.
Wyban, J.A., Sweeney, J.N., 1991. The Oceanic Institute Shrimp Manual: Intensive Shrimp Production Technology. The Oceanic Institute, Makapu'u Point, HI.
