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Estimates for the heritability of size in juvenile Penaeus monodon prawns from half-sib matings
ELSJWIER
Aquaculture 152 (1997) 49-53
Estimates for the heritability of size in juvenile Penaeus monodon prawns from half-sib matings J.A.H. Benzie
*,
’
M. Kenway, L. Trott
Australian Institute of Marine Science, P.M.B. 3, Townsuille, Qld. 4810, Australia
Accepted 15 November
1996
Abstract Eighteen half-sib groups of the giant tiger prawn, Penaeus monodon, were obtained using artificial insemination of two females by each male. The total length (mm) and wet weight (mg) of the young were measured at 6 and 10 weeks after hatching. Sire component estimates were approximately 0.10 for both total length and wet weight at each age. Dam components were greater suggesting large non-additive genetic effects and/or common environment effects that could not be differentiated on the available data. A reduction in the dam component for both total length and wet weight from approximately 0.5-0.6 at 6 weeks to 0.3-0.4 at 10 weeks suggested significant maternal effects were present. The results emphasised the strong environmental controls on prawn growth, particularly potential maternal effects that are likely to play a role earlier in development. These influences resulted in highly variable data, emphasising the need for higher degrees of replication of sire and dam groups in order to detect significant sire effects in P. monodon. 0 1997 Elsevier Science B.V. Keywords: Genetics; Environmental
effects; Breeding;
Penaeus monodan; Hatchery
production;
Larval quality
1. Introduction Although techniques to farm the giant tiger prawn, Penaeus monodon, were developed more than 20 years ago the species is still in the earliest stages of domestication (AQUACOP, 1977, 1983; McVey, 1993). Data from hatcheries using different stocks that differ in performance have been used to support the view that genetic differences are important in determining size and growth in penaeid prawns (Chow and Sandifer,
* Corresponding author. Tel.: 61 77 534211; Fax.: 61 77 725852. ’ This is contribution number 847 from the Australian Institute of Marine Science. 00448486/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SOO44-8486(96)01528-l
50
J.A.H. Benzie et al./Aquaculture
152 (1997) 49-53
1991). However, sound estimates of the degree of genetic control (the heritability) of growth in penaeids is lacking. Previous analyses of the heritability of growth in penaeids used full-sib families where the results were confounded by large environmental effects. Heritability estimates for several characteristics of larvae and postlarvae of Penaeus uannamei and P. stylirostris had large errors which encompassed the whole range of heritability (O-1) and attested to the strong influences of environmental factors on prawn larval growth (Lester, 1988; Lester and Lawson, 1990). Comparisons of half-sib groups are less likely to be affected by environmental influences (Gjedrem, 1992) but the utility of this approach has yet to be tested in penaeids. The present paper reports an analysis of the heritability for total length and wet weight of 6- and lo-week-old postlarvae of P. monodon estimated from matings of 18 males each with two females.
2. Materials
and methods
Penaeus monodon to be used as broodstock were trawled near Cairns, North Queensland and freighted by air and road to the maturation unit. Animals were acclimatised for 3 days in 4-m X l-m circular fibreglass 10-t tanks before they were individually eye-tagged. Females were also tagged by glueing 2-mm X 2-mm squares of waterproof paper on the carapace allowing easy detection of females that had moulted. Male and female broodstock were held in separate tanks at 28°C under a 14:lO 1ight:dark cycle, with up to 50 females or 60 males stocked per tank. Broodstock were fed a mixture of squid, mussels, pippies, ox liver and a maturation pate produced in house, the total feed being lo-15% of prawn biomass. Two days after they moulted, each of two females was artificially inseminated with one of the pair of spermatophores freshly extracted from a male. Females were ablated before being returned to the tank after insemination. The gonadal index of each female was monitored daily until Stage IV of development (ripe ovaries). Stage IV females were placed in separate 70-l spawning tubs with 28°C recirculated water. One day after hatching 4000 nauplii were taken at random from each batch and stocked into 50-l larval rearing tubs (80 larvae 1-l >. Samples from each batch were assessed microscopically immediately prior to stocking to determine their general health and three 500-ml subsamples were taken immediately and counted to confirm stocking density. Larvae were reared on a mixed diet of resuspended Chaetoceros muerilli paste, egg yolk, dried Spirulina, Frippak microencapsulated feeds, Artemia and Frippak postlarval pellets. Water temperature was maintained at 28°C throughout the experiment. Daily water exchanges of 25% total volume were commenced at zoeal three stage (23) and increased to 50% during the older postlarval stages. On reaching PL15 stage the entire batch was harvested and 200 individuals were taken at random from each family and families stocked separately in 80-cm X 30-cm X 30-cm plankton mesh cages. The cages were suspended in a 4.5-m-diameter fibreglass tank filled to l-m depth, with a maximum of 14 cages per tank. Larvae were fed ad libitum on a formulated pellet diet supplemented with a daily ration of minced squid. Water quality was maintained using a reverse sand filtration system, with a daily exchange of lo-15% filtered seawater. At 3
J.A.H. Ben& et al./Aquaculture
152 (1997) 49-53
51
Table 1 Results of analyses of variance, variance components and percent of variance associated analyses for total length (mm) and wet weight (mg) of juvenile P. monodon d.f.
6 weeks Sires Dams/sires Progeny
with each level in the
Wet weight
Total length
F
m.s.
Var. comn.
% var.
m.s.
F
Var. camp.
% var.
17 18 684
121.7 101.5 22.5
1.20 NS 4.52 ’ * *
0.5 4.0 22.5
1.9 14.7 83.5
9468 7050 1612
1.24 NS 4.37 * * *
60 272 1612
3.1 14.0 82.9
16 17 646
342.0 226.5 85.7
1.51’s 2.64 * * *
2.9 7.0 85.7
3.0 7.4 89.6
384875 283726 87455
1.36 NS 3.24 - - *
2529 9814 87455
2.5 9.8 87.6
10 weeks Sires Dams/sires Progeny
NS, not significant:
* * * P < 0.001; d.f., degrees of freedom; ms, mean square.
and 6 weeks after placement in the cages, a random sample of 20 individuals from each cage was harvested and the total length and wet weight of each individual was measured. Statistical analyses were performed using a nested analysis of variance program in SAS (SAS Institute Inc., 1985). Sire and dam effects were considered random for calculating expected mean squares. Standard errors of he&abilities were calculated after equations in Becker (1992). 3. Results Analyses of variance demonstrated highly significant differences in length and weight of juveniles from different females mated with the same male, at both 6 and 10 weeks (Table 1). In contrast, no significant differences in length and weight of juveniles were detected between males using the mean square from the dams as the denominator in the F test. Only 1.9 to 3.1% of the variation was associated with differences in length and weight, respectively, of juveniles sired by different males. Heritability estimates for length based on sire components were not significantly different from zero, but the mean for both was approximately 0.10 (Table 2). Heritability
Table 2 Heritabilites
and phenotypic
parameters
for lengths and weights of juvenile
P. nwnodon
Mean
CV
hi
s.e.
h:,
s.e.
Number of families
21.8 57.3
0.24 0.77
0.08 0.12
0.10 0.02
0.59 0.56
0.30 0.03
18s: 36D 18s: 36D
40.8 448.7
0.24 0.70
0.12 0.10
0.07 0.002
0.30 0.39
0.11 0.004
17s: 34D 17s: 34D
6 weeks Total length (mm) Wet weight (mg) 10 weeks Total length (mm) Wet weight (ma) CV, coefficient
of variation.
52
J.A.H. Benzie et al. /Aquaculture
152 (1997) 49-53
estimates for weight based on the sire were significantly different from zero, and the mean for both was approximately 0.10. Heritability estimates based on the dam were far larger than those based on the sire components and, except for the estimate for length at 6 weeks, they were all significantly different from zero. Heritability estimates based on the dam for both length and weight decreased from 0.5-0.6 at 6 weeks to 0.3-0.4 at 10 weeks. Coefficients of variation were high indicating considerable variation for length and weight of the prawns measured (Table 1).
4. Discussion No significant difference in length and weight of P. monodon juveniles between male groups was detected. However, heritability estimates for wet weight calculated from the sire were significantly different from zero, suggesting potential for genetic improvement of growth rate in P. monodon. Heritability for body weight of Atlantic salmon and rainbow trout increases with age (Gjedrem, 1985; Gjerde, 19861, and the juvenile P. monodon data may provide similarly minimum estimates of heritability. The much larger he&abilities calculated from the dam component emphasised the strength of common environmental effects, maternal effects and/or non-additive genetic variance. The source of the additional variation between females cannot be determined with the available data, but the fact that the dam he&abilities decreased from 6 to 10 weeks invites speculation that maternal effects, derived from environmental influences on the female during egg development, might be important. The reduced errors for the heritability estimates derived from the half-sib analyses relative to the errors in the full-sib data published previously for other species (Lester, 1988) suggests that the half-sib method has promise for the analysis of quantitative traits in prawns. The data also demonstrate the requirement for greater replication of sire groups and female treatment to detect genetic variation given the large environmental effects on P. monodon. Although showing a dominant effect of environment, probably largely a function of egg quality, the preliminary data from this study do show a significant influence of additive genetic factors on weight.
Acknowledgements We would like to thank E. Seymour, M. van Nouhys, D. Hocking, Marsden for their technical assistance on this experiment.
L. Linton and T.
References AQUACOP, 1977. Reproduction in captivity and growth of Penaeus monodon Fabricius in Polynesia. In: J. Avault Jr. (Editor), Proc. 8th Annu. Workshop World Maricult. Sot., 9-13 January 1977, San Jose, Costa Rica. Louisiana State University Press, Baton Rouge, USA, pp. 927-948. AQUACOP, 1983. Constitution of broodstock, maturation, spawning and hatching system for penaeid shrimps
J.A.H. Benzie et al./Aquaculture
152 (1997) 49-53
53
in the Centre Oceanologique du Pacifique. In: J.P. McVey (Editor), CRC Handbook of Mariculture. Vol. 1. Crustacean Aquaculture. CRC Press, Miami, FL, USA. Becker, W.A., 1992. Manual of Quantitative Genetics. Academic Enterprises, Pullman, WA, USA. Chow, S. and Sandifer, P.A., 1991. Differences in growth, morphometric traits and male sexual maturity among Pacific white shrimp, Penaeus uannamei, from different commercial hatcheries. Aquaculture, 92: 165-178. Gjedrem, T., 1985. Improvement of productivity through breeding schemes. GeoJoumal, 10: 233-241. Gjedrem, T., 1992. Breeding plans for rainbow trout. Aquaculture, 100: 73-83. Gjerde, B., 1986. Growth and reproduction in fish and shellfish. Aquaculture, 57: 37-55. Lester, L.J., 1988. Difference in larval growth among families of Penaeus srylirostris Stimpson and P. uannamei Boone. Aquacult. Fish. Manage., 19: 243-251. Lester, L.J. and Lawson, K.S., 1990. Inheritance of size as estimated by principal component analysis at two temperatures in Penaeus uannamei. Aquaculture, 85: 323 (abstract). McVey, J.P. (Editor), 1993. CRC Handbook of Mariculture. Vol I. Crustacean Aquaculture. CRC Press, Boca-Raton, FL, USA. SAS Institute Inc., 1985. SAS Users Guide: Statistics, Version 5 Edition. SAS Institute Inc., Cary, NC.
Aquaculture 152 (1997) 49-53
Estimates for the heritability of size in juvenile Penaeus monodon prawns from half-sib matings J.A.H. Benzie
*,
’
M. Kenway, L. Trott
Australian Institute of Marine Science, P.M.B. 3, Townsuille, Qld. 4810, Australia
Accepted 15 November
1996
Abstract Eighteen half-sib groups of the giant tiger prawn, Penaeus monodon, were obtained using artificial insemination of two females by each male. The total length (mm) and wet weight (mg) of the young were measured at 6 and 10 weeks after hatching. Sire component estimates were approximately 0.10 for both total length and wet weight at each age. Dam components were greater suggesting large non-additive genetic effects and/or common environment effects that could not be differentiated on the available data. A reduction in the dam component for both total length and wet weight from approximately 0.5-0.6 at 6 weeks to 0.3-0.4 at 10 weeks suggested significant maternal effects were present. The results emphasised the strong environmental controls on prawn growth, particularly potential maternal effects that are likely to play a role earlier in development. These influences resulted in highly variable data, emphasising the need for higher degrees of replication of sire and dam groups in order to detect significant sire effects in P. monodon. 0 1997 Elsevier Science B.V. Keywords: Genetics; Environmental
effects; Breeding;
Penaeus monodan; Hatchery
production;
Larval quality
1. Introduction Although techniques to farm the giant tiger prawn, Penaeus monodon, were developed more than 20 years ago the species is still in the earliest stages of domestication (AQUACOP, 1977, 1983; McVey, 1993). Data from hatcheries using different stocks that differ in performance have been used to support the view that genetic differences are important in determining size and growth in penaeid prawns (Chow and Sandifer,
* Corresponding author. Tel.: 61 77 534211; Fax.: 61 77 725852. ’ This is contribution number 847 from the Australian Institute of Marine Science. 00448486/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SOO44-8486(96)01528-l
50
J.A.H. Benzie et al./Aquaculture
152 (1997) 49-53
1991). However, sound estimates of the degree of genetic control (the heritability) of growth in penaeids is lacking. Previous analyses of the heritability of growth in penaeids used full-sib families where the results were confounded by large environmental effects. Heritability estimates for several characteristics of larvae and postlarvae of Penaeus uannamei and P. stylirostris had large errors which encompassed the whole range of heritability (O-1) and attested to the strong influences of environmental factors on prawn larval growth (Lester, 1988; Lester and Lawson, 1990). Comparisons of half-sib groups are less likely to be affected by environmental influences (Gjedrem, 1992) but the utility of this approach has yet to be tested in penaeids. The present paper reports an analysis of the heritability for total length and wet weight of 6- and lo-week-old postlarvae of P. monodon estimated from matings of 18 males each with two females.
2. Materials
and methods
Penaeus monodon to be used as broodstock were trawled near Cairns, North Queensland and freighted by air and road to the maturation unit. Animals were acclimatised for 3 days in 4-m X l-m circular fibreglass 10-t tanks before they were individually eye-tagged. Females were also tagged by glueing 2-mm X 2-mm squares of waterproof paper on the carapace allowing easy detection of females that had moulted. Male and female broodstock were held in separate tanks at 28°C under a 14:lO 1ight:dark cycle, with up to 50 females or 60 males stocked per tank. Broodstock were fed a mixture of squid, mussels, pippies, ox liver and a maturation pate produced in house, the total feed being lo-15% of prawn biomass. Two days after they moulted, each of two females was artificially inseminated with one of the pair of spermatophores freshly extracted from a male. Females were ablated before being returned to the tank after insemination. The gonadal index of each female was monitored daily until Stage IV of development (ripe ovaries). Stage IV females were placed in separate 70-l spawning tubs with 28°C recirculated water. One day after hatching 4000 nauplii were taken at random from each batch and stocked into 50-l larval rearing tubs (80 larvae 1-l >. Samples from each batch were assessed microscopically immediately prior to stocking to determine their general health and three 500-ml subsamples were taken immediately and counted to confirm stocking density. Larvae were reared on a mixed diet of resuspended Chaetoceros muerilli paste, egg yolk, dried Spirulina, Frippak microencapsulated feeds, Artemia and Frippak postlarval pellets. Water temperature was maintained at 28°C throughout the experiment. Daily water exchanges of 25% total volume were commenced at zoeal three stage (23) and increased to 50% during the older postlarval stages. On reaching PL15 stage the entire batch was harvested and 200 individuals were taken at random from each family and families stocked separately in 80-cm X 30-cm X 30-cm plankton mesh cages. The cages were suspended in a 4.5-m-diameter fibreglass tank filled to l-m depth, with a maximum of 14 cages per tank. Larvae were fed ad libitum on a formulated pellet diet supplemented with a daily ration of minced squid. Water quality was maintained using a reverse sand filtration system, with a daily exchange of lo-15% filtered seawater. At 3
J.A.H. Ben& et al./Aquaculture
152 (1997) 49-53
51
Table 1 Results of analyses of variance, variance components and percent of variance associated analyses for total length (mm) and wet weight (mg) of juvenile P. monodon d.f.
6 weeks Sires Dams/sires Progeny
with each level in the
Wet weight
Total length
F
m.s.
Var. comn.
% var.
m.s.
F
Var. camp.
% var.
17 18 684
121.7 101.5 22.5
1.20 NS 4.52 ’ * *
0.5 4.0 22.5
1.9 14.7 83.5
9468 7050 1612
1.24 NS 4.37 * * *
60 272 1612
3.1 14.0 82.9
16 17 646
342.0 226.5 85.7
1.51’s 2.64 * * *
2.9 7.0 85.7
3.0 7.4 89.6
384875 283726 87455
1.36 NS 3.24 - - *
2529 9814 87455
2.5 9.8 87.6
10 weeks Sires Dams/sires Progeny
NS, not significant:
* * * P < 0.001; d.f., degrees of freedom; ms, mean square.
and 6 weeks after placement in the cages, a random sample of 20 individuals from each cage was harvested and the total length and wet weight of each individual was measured. Statistical analyses were performed using a nested analysis of variance program in SAS (SAS Institute Inc., 1985). Sire and dam effects were considered random for calculating expected mean squares. Standard errors of he&abilities were calculated after equations in Becker (1992). 3. Results Analyses of variance demonstrated highly significant differences in length and weight of juveniles from different females mated with the same male, at both 6 and 10 weeks (Table 1). In contrast, no significant differences in length and weight of juveniles were detected between males using the mean square from the dams as the denominator in the F test. Only 1.9 to 3.1% of the variation was associated with differences in length and weight, respectively, of juveniles sired by different males. Heritability estimates for length based on sire components were not significantly different from zero, but the mean for both was approximately 0.10 (Table 2). Heritability
Table 2 Heritabilites
and phenotypic
parameters
for lengths and weights of juvenile
P. nwnodon
Mean
CV
hi
s.e.
h:,
s.e.
Number of families
21.8 57.3
0.24 0.77
0.08 0.12
0.10 0.02
0.59 0.56
0.30 0.03
18s: 36D 18s: 36D
40.8 448.7
0.24 0.70
0.12 0.10
0.07 0.002
0.30 0.39
0.11 0.004
17s: 34D 17s: 34D
6 weeks Total length (mm) Wet weight (mg) 10 weeks Total length (mm) Wet weight (ma) CV, coefficient
of variation.
52
J.A.H. Benzie et al. /Aquaculture
152 (1997) 49-53
estimates for weight based on the sire were significantly different from zero, and the mean for both was approximately 0.10. Heritability estimates based on the dam were far larger than those based on the sire components and, except for the estimate for length at 6 weeks, they were all significantly different from zero. Heritability estimates based on the dam for both length and weight decreased from 0.5-0.6 at 6 weeks to 0.3-0.4 at 10 weeks. Coefficients of variation were high indicating considerable variation for length and weight of the prawns measured (Table 1).
4. Discussion No significant difference in length and weight of P. monodon juveniles between male groups was detected. However, heritability estimates for wet weight calculated from the sire were significantly different from zero, suggesting potential for genetic improvement of growth rate in P. monodon. Heritability for body weight of Atlantic salmon and rainbow trout increases with age (Gjedrem, 1985; Gjerde, 19861, and the juvenile P. monodon data may provide similarly minimum estimates of heritability. The much larger he&abilities calculated from the dam component emphasised the strength of common environmental effects, maternal effects and/or non-additive genetic variance. The source of the additional variation between females cannot be determined with the available data, but the fact that the dam he&abilities decreased from 6 to 10 weeks invites speculation that maternal effects, derived from environmental influences on the female during egg development, might be important. The reduced errors for the heritability estimates derived from the half-sib analyses relative to the errors in the full-sib data published previously for other species (Lester, 1988) suggests that the half-sib method has promise for the analysis of quantitative traits in prawns. The data also demonstrate the requirement for greater replication of sire groups and female treatment to detect genetic variation given the large environmental effects on P. monodon. Although showing a dominant effect of environment, probably largely a function of egg quality, the preliminary data from this study do show a significant influence of additive genetic factors on weight.
Acknowledgements We would like to thank E. Seymour, M. van Nouhys, D. Hocking, Marsden for their technical assistance on this experiment.
L. Linton and T.
References AQUACOP, 1977. Reproduction in captivity and growth of Penaeus monodon Fabricius in Polynesia. In: J. Avault Jr. (Editor), Proc. 8th Annu. Workshop World Maricult. Sot., 9-13 January 1977, San Jose, Costa Rica. Louisiana State University Press, Baton Rouge, USA, pp. 927-948. AQUACOP, 1983. Constitution of broodstock, maturation, spawning and hatching system for penaeid shrimps
J.A.H. Benzie et al./Aquaculture
152 (1997) 49-53
53
in the Centre Oceanologique du Pacifique. In: J.P. McVey (Editor), CRC Handbook of Mariculture. Vol. 1. Crustacean Aquaculture. CRC Press, Miami, FL, USA. Becker, W.A., 1992. Manual of Quantitative Genetics. Academic Enterprises, Pullman, WA, USA. Chow, S. and Sandifer, P.A., 1991. Differences in growth, morphometric traits and male sexual maturity among Pacific white shrimp, Penaeus uannamei, from different commercial hatcheries. Aquaculture, 92: 165-178. Gjedrem, T., 1985. Improvement of productivity through breeding schemes. GeoJoumal, 10: 233-241. Gjedrem, T., 1992. Breeding plans for rainbow trout. Aquaculture, 100: 73-83. Gjerde, B., 1986. Growth and reproduction in fish and shellfish. Aquaculture, 57: 37-55. Lester, L.J., 1988. Difference in larval growth among families of Penaeus srylirostris Stimpson and P. uannamei Boone. Aquacult. Fish. Manage., 19: 243-251. Lester, L.J. and Lawson, K.S., 1990. Inheritance of size as estimated by principal component analysis at two temperatures in Penaeus uannamei. Aquaculture, 85: 323 (abstract). McVey, J.P. (Editor), 1993. CRC Handbook of Mariculture. Vol I. Crustacean Aquaculture. CRC Press, Boca-Raton, FL, USA. SAS Institute Inc., 1985. SAS Users Guide: Statistics, Version 5 Edition. SAS Institute Inc., Cary, NC.