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Purebred Hatching Eggs

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Kelly Klober Saturday Poultry Seminar 2012

Heterosis and combining abilities in growth and survival in sea scallops along the Atlantic coast of Canada.

ABSTRACT Selective breeding and crossbreeding are seen widely in
genetic improvement of crops as well as molluscs. In this study, we
constructed complete 4 x 4 diallel crosses using broodstock from 4
geographical subpopulations of sea scallops along the Atlantic coast of
Canada, and heterosis and combining abilities in growth and survival
rates at larval and adult grow-out stages were analyzed. The results
indicated that variable heterosis in growth and survival exist in larval
and adult stages. In many cases, the fitness traits increased with
general combining abilities, especially at the larval stage, but in some
cases, groups with high growth or survival rate but low general
combining abilities were also observed. Reciprocal effects and maternal
reciprocal effects were observed in growth and survival at the larval
stage and also in adult growth. Two hybrid strains with superior growth
and survival traits over purebred and other hybrid groups were selected
that can be used in future culture practice.

KEY WORDS: Placopecten magellanicus, crossbreeding, combining
ability, heterosis, growth, survival

INTRODUCTION

Culture of sea scallops Placopecten magellanicus along the Atlantic
coasts of Canada started during the early 1970s (Dadswell 2000) and is
now becoming one of the major aquaculture practices in the Maritime
provinces and Quebec. Domestication of the species has been the longtime
pursue of the industry for profitability and sustainability of the
business. One of the major goals of domestication is to obtain strains
with superior traits, especially in terms of growth rate and survival
rate.

Intraspecific hybridization has been used widely in agriculture to
produce strains with superior production traits in crops and livestock
(Tsaftaris 1990, Madalena 1993, Virmani 1996, Crow 1998, Cheng et al.
2007, Freyer et al. 2008, Sorensen et al. 2008). The major advantage of
this approach is the utilization of heterosis, or hybrid vigor, as well
as additive genetic effects in the hybrids. Intraspecific hybridization
has also been used to improve the genetic stock in molluscs such as
oysters (Mallet & Haley 1983, Newkirk 1986, Hedgecock et al. 1995,
Hedgecock et al. 1996), the hard clam Mercenaria mercenaria (Manzi et
al. 1991), and scallops (Cruz & Ibarra 1997, Chang & Xiang 2002,
Liu et al. 2003, Zheng et al. 2004, Zheng et al 2006, Liu et al. 2005,
Chang et al. 2006, Zhang et al. 2007, Wang & Li 2010).

Pec-Nord, Inc., started sea scallop farming and domestication in
northern Quebec during the late 1980s. During the late 1990s, Pec-Nord,
Inc., established 4 stocks of sea scallops from broodstock collected
from 4 different sites along the Atlantic coast of Canada from
Lunenburg, Nova Scotia, to Lower North Shore, Quebec, and their
performance was monitored during the following years. The results showed
that although there was no significant difference in growth among stock,
some stock outperformed others in terms of survival. To improve the
production traits in both growth and survival, we crossbred the 4 stocks
and evaluated their performance in the hatchery and adult grow-out
stages.

MATERIALS AND METHODS

Broodstock

Broodstock for this project was the inbreeding progenies produced
in the hatchery of Pec-Nord, Inc., in 1997 using sea scallops from 4
different sites along the Atlantic coast of Canada from Lunenburg, Nova
Scotia, to Lower North Shore, Quebec. For the interests of business,
these 4 cohorts are denoted anonymously as A, B, C, and D. The scallops
were taken into the hatchery in early March 2001 and conditioned at
increasing temperature ranging from 1-10[degrees]C for 40 days before
spawning.

Spawning

When the scallops became fully mature, the females were induced to
spawn in 1,000-L tanks and males in 20-L buckets by exposing them to air
for 30 rain followed by a temperature shock of 3-4[degrees]C. When
enough eggs were obtained, the eggs from each of 4 groups were divided
into 4 tanks by siphoning the water into neighboring tanks; the groups
were fertilized with sperm from each of 4 groups immediately. Thus, a
complete set of diallel crosses including 4 inbreeding lines and 12
crossbred cohorts were produced. The derived cohorts were named in the
format of female x male; for example, the hybrid produced with eggs from
group A and sperm from group B is denoted as A x B. After hatching, 3
replicate tanks with a density of 10 larvae/mL were set up for each
cohort.

Larval Rearing

The newly hatched D-formed larvae were cultured at 14 [+ or -]
1[degrees]C in 1,000-L tanks. They were fed with microalgae, a Tahitian
strain of Isochrysis sp. (TISO) at concentrations of 10,000-100,000
cells/mL during the first 14 days and then with a 1:1 mixture of TISO
and PAV (Pavlova sp.) until metamorphosis. The density of larvae in the
tank was maintained at 10 larvae/ mL by adjusting the water volume. When
eye-spots became apparent on around day 26 after fertilization, plastic
netrons were put into the tanks for eyed larvae to set on.

At the beginning and the end of the larval stage, four 50-mL
seawater samples were taken randomly from each tank--after the tank was
stirred thoroughly--and were pooled together in a plastic jar. From the
mixed samples, three 1-mL samples were taken after the jar was mixed
thoroughly by bubbling it with air. The numbers of live larvae were
counted to estimate the density in the jar. The total number of live
larvae in each tank was estimated based on the average density of live
larvae and the actual volume of water in the tank. The survival rate
during the larval stage was determined by dividing the total number of
live eyed larvae before metamorphosis by that of the D-formed larvae
after hatching. The average shell height of the larvae was examined by
measuring 10 randomly selected larvae from each replicate tank. The
average growth rate (GR) in height during the larval stage was
calculated for each tank by the equation

GR = [Hd - He]/[Td - Te]

where Hd and He are the average shell height of newly hatched
D-formed and eyed larvae, respectively, and Td and Te are days after
fertilization of newly hatched D-formed and eyed larvae, respectively.

Grow-out Stage

About 10 days after the netrons were set in the tanks, the netrons
with spat were transferred to the field and stayed there until they were
sorted in July 2002. After sorting, all animals from each line were
pooled together and 2,000 animals from each line were selected randomly
and deployed into 3-ram pearl nets at a density of 100 animals per net
for grow-out in Johnson's Island and Isaac Cove in Shekatika Bay of
Lower North Shore, Quebec, in the first year. With the growth of the
scallops, the density was reduced to 50 animals per 6-mm pearl net in
July 2003 and to 30 animals per 9-ram pearl net in July 2004. Dead
shells were not removed during sorting to estimate mortality. The shell
heights of the scallops were determined by measuring 10 randomly
selected individuals from 5 nets for each line. The numbers of live and
dead scallops from all nets for each line were counted to calculate the
survival rate during the grow-out stage.

Statistical Analyses and Estimates

The estimates of heterosis (/4) were made using the formula
modified from that used by Cruz and Ibarra (1997):

H = [[[X.sub.F1] ([X.sub.P1] + [X.sub.P2]/2]/[([X.sub.P1] +
[X.sub.P2]/2]] x 100%,

where [X.sub.F1] is the mean size (or survival rate) of the
interpopulation cross [F.sub.1], and [X.sub.P1] and [X.sub.P2] are the
mean size (or survival rate) of the corresponding inbreeding parental
lines involved in the crossbreeding.

We used Griffing's (1956) Method 1 to estimate the general
combining ability (GCA), special combining ability (SCA), and reciprocal
hybrid effects using a random model (Model II). The linear model is

[X.sub.ijk] = u + [g.sub.i] + [g.sub.j] + [s.sub.ij] + [r.sub.ij] +
[e.sub.ijk]

where u is the population mean, [g.sub.i] and [g.sub.j] are the
GCA, [s.sub.gi] is the SCA, [r.sub.ij] is the reciprocal effect
involving the reciprocal crosses between the ith sire and jth dam line,
and [e.sub.ijk] is the random observation error among replicates.

We first tested whether there existed a significant difference
among the genotypes by 2-way ANOVA using SPSS v19.0 software (SPSS,
Inc.) (Zar 1996). If a significant difference was found among genotypes,
we then examined the significance of the difference between the GCAs and
SCAs using ANOVA before estimating these effects. All analyses were
carried out using the Data Processing System program (http://www.
chinadps.net; Tang & Fens 1997)

RESULTS

Larval Survival

The average survival rates of the diallel crosses including all the
parental and reciprocal cross lines are given in Table 1. One-way ANOVAs
of the data indicated a significant difference among varieties (P <
0.001). The highest survival rate was observed in the B x A group
whereas the lowest was seen in the C x D group. Two-way ANOVA of the
survival rate data showed that the origins of females and males, as well
as their interaction, have significant effects on the survival rate of
the progenies (ANOVA, P < 0.0001; Table 2). ANOVA of the combining
abilities and reciprocal effects indicated that GCA, SCA, and reciprocal
effect all affect the larval survival rate significantly (P < 0.001;
Table 3). It is noteworthy that the sum of the square of the GCA is
larger than that of the SCA. The GCAs and SCAs, as well as the
reciprocal effects in larval survival, are given in Table 4. The order
of GCA is A > B > C > D. It can also be seen that the highest
SCA appears in the A x C group whereas the group that exhibited the
highest reciprocal effect is D x A.

Larval Growth

The average growth rates of different crossbred combinations are
shown in Table 1. One-way ANOVAs of the growth data showed a significant
difference among varieties (P < 0.001). The highest growth rate was
observed in the B x C and B x D groups whereas the lowest was found in
the C x D group. Two-way ANOVA of the growth rate data demonstrated that
the origins of females and males, as well as their interaction, exerted
significant effects on the growth rate of their offspring (ANOVA, P <
0.0001; Table 2). As shown in Table 4, ANOVAs of the combining abilities
and reciprocal effects indicated that GCA, SCA, and reciprocal effect
all have a significant effect on larval growth rate (P < 0.001). The
sum of the square of GCA and the reciprocal effect is also larger than
that of the SCA. The GCAs and SCAs, as well as the reciprocal effects of
the larval growth rate, are shown in Table 4. The order of GCA for
larval growth rate is A > B > C > D. The highest SCA for larval
growth was seen in the A x C group whereas the group with the highest
reciprocal effect was the C x B group.

Adult Survival

The average survival rates of different crossbred combinations at
adult grow-out stage are shown in Table 5. One-way ANOVAs of the data
showed a significant difference among varieties (P < 0.001). The
highest survival rate was observed in the C x B group whereas the lowest
was found in the D x C group. Two-way ANOVA of the survival rate during
the grow-out stage demonstrated that the origins of females and males,
as well as their interaction, had significant effects on the survival
rate of the resulting offspring during the grow-out stage (ANOVA, P <
0.0001; Table 2). As shown in Table 3, ANOVAs of the combining abilities
and reciprocal effects indicated that GCA, SCA, and reciprocal effect
all have a significant effect on adult survival rate (P < 0.001). The
GCAs and SCAs, as well as the reciprocal affects on adult survival rate,
are given in Table 4. The order of GCA for larval growth rate is B >
A > C > D. The highest SCA for adult survival rate was seen in the
A x D group whereas the group with the highest reciprocal effect was the
D x C group.

Adult Growth

The average shell heights of different crossbred combinations at
the adult grow-out stage are shown in Table 5. One-way ANOVAs of the
size data showed a significant difference among varieties (P <
0.001). The largest size was observed in the A x A group whereas the
lowest was found in the B x A group. Two-way ANOVA of the growth data
demonstrated that the origins of females and males, as well as their
interaction, exerted significant effects on the growth of the resulting
offspring during the adult grow-out stage (ANOVA, P < 0.0001; Table
2). As shown in Table 3, ANOVA of the combining abilities and reciprocal
effects indicated that GCA, SCA, and reciprocal effect all have a
significant effect on adult growth (P < 0.001). The GCAs and SCAs, as
well as the reciprocal effects on adult growth arc shown in Table 4. The
order of GCA for adult growth is D > A > B > C. The highest SCA
for adult growth was seen in the B x D group whereas the group with the
highest reciprocal effect was the B x A group.

DISCUSSION

Improvement of production traits such as growth rate and survival
rate has been the major pursuit for genetic breeding of aquatic animals
(Mallet & Haley 1983, Cruz & Ibarra 1997, Hedgecock et al. 1995,
Hedgecock & Davis 2007, Wang & Li 2010). In the current study,
we constructed complete 4 x 4 diallel crosses including 4 parental and
12 crossbred groups, and compared their growth and survival rates. If
survival and growth are of equal importance to the breeder, the best
groups are BA at larval stage and CB and BC at the adult stage. Because
the yield at harvest is of greater interest to the scallop industry, CB
and BC are obviously the choice for culture. However, for a sustainable,
long-term breeding program, it is important for us to partition the
variance of these traits into causal components to determine the future
direction of selection and crossbreeding.

Combining Abilities and Reciprocal Effects

Besides the direct and indirect effects of environments, the traits
of fitness are mainly affected by genetic factors, which are composed of
both additive and nonadditive actions. To estimate the additive and
nonadditive genetic effects, Sprague and Tatum (1942) introduced the
concepts of GCA and SCA. In this study, we evaluated the combining
abilities as well as the reciprocal effects with the models and methods
developed by Griffing (1956).

The results showed that stock A and stock B exhibited the highest
GCA in survival rate during the larval and adult stages, respectively.
In terms of growth, stock A and stock D had the highest GCA at the
larval and adult stages, respectively. Because GCA is considered to be
the measure for the additive genetic actions, the large variance of GCA
thus suggests that selection on these traits is feasible for a selective
breeding program. However, because stocks with high GCA at the larval
stage may not have a high GCA at the adult stage, it is risky to exclude
stocks with a low GCA at early stages. The major goal of aquaculture is
to obtain high biomass, which is affected more by adult survival than
any other traits. It is thus suggested that selection in the sea scallop
should be focused more on adult survival rate.

Our results also show that both additive and nonadditive actions
are important for the performance of animals at larval and adult stages.
Many traits increased with GCA, especially at the larval stage, but in
some cases, groups with high growth or survival rate, high SCA but low
GCA, were also observed. These results imply that it is necessary to
combine selection of superior lines and crossbreeding to use both
inheritable genetic gains and heterosis in a sea scallop breeding
project.

Heterosis in the Crossbred Groups

Variable heterosis was observed in the production traits at
different stages. The results showed that positive heterosis in survival
rates was obtained in some groups at larval stage and in most groups at
adult stages. Heterosis in survival rate of as high as 30 or more was
seen in AC, AD, and DC at the larval stage, and in AD, CA, CB, and DA at
the adult stage. In contrast, positive but small heterosis in growth was
found in some groups at the larval stage, but at the adult stage, most
groups exhibited negative heterosis in growth. Crossbreeding did improve
survival rates greatly at all stages, but had little or no effect on
growth performance. Similar results have also been reported in other
intraspecific crossbreeding studies (Zhang et al. 2007, Wang and Li
2010). In a similar crossbreeding study involving 4 populations of the
hermaphroditic bay scallop, we also found much higher heterosis in
survival rate than in growth rate (Wang & Li 2010).The larger
variations in survival rate than in growth rate among parental
populations may have provided the basis for the larger heterosis in
survival rates. Crossbreeding may have masked some deleterious or even
lethal genes in the progenies and thus improved their survival as a
result of epistasis. In another study in which we hybridized the
Peruvian scallop Argopecten purpuratus introduced from Peru and the
local bay scallop from Qingdao, China, we did obtain considerable
heterosis in growth, especially in total body weight (Wang et al. 2011).
Thus, it seems that the genetic distances among the subpopulations in
these intraspecific crossbreeds may not be large enough to bring about
significant heterosis in growth. Therefore, realistically, intraspecific
crossbreeding should focus more on improvement of progeny survival.

Reciprocal and Maternal Effects

Significant reciprocal effects were detected in both growth and
survival rates at all stages. Similar results have also been reported in
other studies (Hedgecock & Davis 2007, Deng et al. 2010). The
reciprocal effects (extranuclear effects) can be partitioned further
into maternal and nonmaternal effects (Hedgecock & Davis 2007). The
maternal effects may be caused by the expression of maternal
mitochondria genes in the progenies or the difference in the energy
reserves in the eggs, or both.

In this study, by comparing the sum of squares caused by origin of
females with that caused by males, maternal effects are obvious in the
survival and growth traits at the larval stage and in growth at the
adult stage, but not in survival rate at the adult stage. Similar trends
were also observed for the reciprocal effects. This coincidence may
suggest that maternal effects were the major components for the total
reciprocal effects.

In conclusion, the results from this study suggest that we are able
to improve the production traits through combination of selective
breeding of superior lines and interline crossbreeding. Because of the
existence of considerable reciprocal effects, the direction of interline
crossbreeding has to be selected to use maximum heterosis.

ACKNOWLEDGMENT

We thank Drs. Paul-Aime Joncas and Sebastien Joncas, Anne St-Jean,
Marcel Driscol, Maria Driscol, and many other staff members at Pec-Nord,
Inc., for their assistance in this project.

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CHUNDE WANG (1,2) * AND JEAN COTE (2)

(1) Qingdao Agricultural University, Marine Science and Engineering
College, 700 Changcheng Road, Qingdao, China 266109; (2) Pec-Nord, Inc.,
2800 Avenue Saint-Jean-Baptiste, Suite 230, Quebec City, Quebec, Canada
G2E 6J5

* Corresponding author. E-mail: pacificshells@yahoo.ca

DOI: 10.2983/035.031.0425

TABLE 1.
Survival rates and heterosis of lines during the larval and
adult stages.

               Larval Survival
Groups            Rate (%)             Heterosis

AA       72.47 [+ or -] 1.88 (g)
BB       85.67 [+ or -] 4.03 (g)
CC       49.07 [+ or -] 1.84 (b,c)
DD       46.03 [+ or -] 2.06 (b)
AB       86.10 [+ or -] 2.72 (h)          8.90
AC       85.37 [+ or -] 3.10 (h)         40.48
AD       83.40 [+ or -] 2.46 (h)         40.76
BA       86.53 [+ or -] 3.17 (h)          9.44
BC       61.07 [+ or -] 1.87 (d)         -9.35
BD       66.13 [+ or -] 2.66 (e,f)        0.43
CA       67.47 [+ or -] 2.46 (f)         11.03
CB       61.67 [+ or -] 1.80 (d,e)       -8.46
CD       21.13 [+ or -] 2.94 (a)        -55.56
DA       51.93 [+ or -] 2.11 (c)        -12.35
DB       48.07 [+ or -] 1.70 (b,c)      -27.01
DC       62.97 [+ or -] 2.80 (d,e)       32.42

                Larval Growth
Groups       Rate ([micro]m/day)       Heterosis

AA       5.14 [+ or -] 0.11 (e,f,g)
BB       5.23 [+ or -] 0.06 (g)
CC       4.80 [+ or -] 0.12 (b,c,d)
DD       4.80 [+ or -] 0.11 (b,c,d)
AB       4.64 [+ or -] 0.06  (a,b)      -10.58
AC       5.03 [+ or -] 0.09 (e,f)         1.34
AD       4.65 [+ or -] 0.08  (a,b,c)     -6.47
BA       5.18 [+ or -] 0.09 (f,g)        -0.10
BC       5.25 [+ or -] 0.10 (g)           4.75
BD       5.25 [+ or -] 0.11 (g)           4.58
CA       5.07 [+ or -] 0.11 (e,f,g)       2.01
CB       4.55 [+ or -] 0.11 (a)          -9.21
CD       4.62 [+ or -] 0.10 (a,b)        -3.72
DA       4.63 [+ or -] 0.13 (a,b)        -6.89
DB       4.83 [+ or -] 0.11 (c,d)        -3.72
DC       4.97 [+ or -] 0.13 (d,e)         3.65

Note: Different superscript letters in the same column indicate a
significant difference (P < 0.05).

TABLE 2.
Two-way analyses of variance of the survival rates during
larval and adult stages.

      Source          df       SS          MS          F       P Value

Larval survival
  Female               3    9,271.123   3,090.374    467.236    0.0001
  Male                 3    2,003.975     667.992    100.994    0.0001
  Female x male        9    4,256.045     472.894     71.497    0.0001
  Errors              32      211.653       6.614
Larval growth
  Female               3        1.640       0.547     51.824    0.0001
  Male                 3        0.424       0.141     13.398    0.0001
  Female x male        9        0.847       0.094      8.922    0.0001
  Errors              32        0.338       0.011
Adult survival
  Female               3        0.250       0.083     92.069    0.0001
  Male                 3        0.271       0.090     99.668    0.0001
  Female x male        9        0.491       0.055     60.323    0.0001
  Errors              80        0.072       0.001
Adult shell height
  Female               3      151.941      50.647     12.426    0.0001
  Male                 3       57.283      19.094      4.685    0.0001
  Female x male        9      291.980      32.442      7.959    0.0001
  Errors             144      586.941       4.076

df, degree of freedom; MS, mean square; SS, sum of square.

TABLE 3.
Analyses of variance of the combining abilities in survival and
growth at larval and adult stages.

      Source         df        SS          MS          F       P Value

Larval survival
  GCA                  3   2,974.5008    991.5003   683.4332    0.0001
  SCA                  6     508.7764     84.7961    58.4493    0.0001
  Reciprocal           6   1,693.7706    282.2951   194.5838    0.0001
  Errors              32      69.6367      1.4508
Larval growth
  GCA                  3       0.1740      0.0580    32.7001    0.0001
  SCA                  6       0.2539      0.0423    23.8575    0.0001
  Reciprocal           6       0.5426      0.0904    50.9872    0.0001
  Errors              32       0.0851      0.0018
Adult survival
  GCA                  3       0.0637      0.0210   795.5131    0.0001
  SCA                  6       0.0796      0.0132   499.0312    0.0001
  Reciprocal           6       0.0237      0.0039   148.7099    0.0001
  Errors              62       0.0017      0.0000
Adult shell height
  GCA                  3      17.2959      5.7761    16.1362    0.0001
  SCA                  6      18.6647      3.1253     8.6814    0.0001
  Reciprocal           6      14.2596      2.3617     6.6365    0.0001
  Errors             125      44.8611      0.3507

GCA, general combining abilities; SCA, specific combining abilities; df,
degree of freedom; MS, mean square; SS, sum of square.

TABLE 4.
Analyses of the effects of combining abilities and reciprocal
effects on survival and growth during larval and adult stage.

                                    Dams

     Sires               A         B         C          D

Larval survival
  A                  11.0250    2.6792     8.1667     3.4292
  B                  -0.2167    7.9208    -3.7792    -4.0333
  C                   8.9500   -0.3000    -7.4667    -3.6958
  D                  15.7500   -9.0333   -20.9167   -11.4792
Larval growth
  A                   0.1062   -0.1308     0.1450    -0.1996
  B                  -0.2717    0.0183    -0.0896     0.1142
  C                  -0.0167      0.35    -0.0279     0.0067
  D                     0.01    0.2083    -0.1767    -0.0967
Adult survival
  A                   0.0059   -0.0160     0.0166     0.1126
  B                  -0.0412    0.0715     0.1031    -0.0105
  C                  -0.0773   -0.0042    -0.0319    -0.0591
  D                  -0.0308    0.0044     0.0588    -0.0451
Adult shell height
  A                   0.5016   -1.4966    -0.6435    -0.8732
  B                   1.7631   -0.1076     0.1121     0.3055
  C                  -0.2598    0.6127    -1.1283    -0.0953
  D                  -0.9116    0.6494    -1.5161     0.7672

The general combining abilities are shown in the diagonal, the
specific combining abilities are shown at the upper right
triangle, and the reciprocal effects are shown at the lower left
triangle.

TABLE 5.
Survival rates and shell height at adult grow-out stage.

Groups        Survival Rate (%)        Heterosis

AA       51.55 [+ or -] 0.50 (b,c)
BB       68.22 [+ or -] 1.14 (e)
CC       49.42 [+ or -] 6.23 (b)
DD       48.52 [+ or -] 2.79 (b)
AB       63.72 [+ or -] 0.91 (d)          6.40
AC       53.18 [+ or -] 2.08 (c)          5.35
AD       66.07 [+ or -] 1.37 (d,e)       32.05
BA       71.95 [+ or -] 1.02 (f,g)       20.15
BC       75.70 [+ or -] 1.04 (h)         28.71
BD       63.72 [+ or -] 5.21 (c)          9.17
CA       68.52 [+ or -] 2.21 (e,f)       35.72
CB       76.52 [+ or -] 3.58 (h)         30.09
CD       53.88 [+ or -] 0.58 (c)         10.04
DA       72.20 [+ or -] 3.22 (g)         44.30
DB       62.85 [+ or -] 4.61 (d)          7.68
DC       42.30 [+ or -] 3.26 (a)        -13.61

Groups        Shell Height (mm)        Heterosis

AA       62.39 [+ or -] 2.58 (f)
BB       57.11 [+ or -] 1.81 (b,c)
CC       58.74 [+ or -] 2.97 (c,d,e)
DD       60.52 [+ or -] 1.37 (c)
AB       57.88 [+ or -] 1.84 (b,c,d)     -3.12
AC       57.80 [+ or -] 2.19 (b,c,d)     -4.56
AD       57.80 [+ or -] 2.28 (b,c,d)     -5.96
BA       54.39 [+ or -] 0.74 (f)         -8.97
BC       57.78 [+ or -] 0.46 (b,c,d)     -0.25
BD       58.88 [+ or -] 1.13 (c,d,e)      0.11
CA       58.31 [+ or -] 2.28 b,c,d       -3.72
CB       56.55 [+ or -] 1.18 (b)         -2.37
CD       57.40 [+ or -] 2.66 (b,c)       -3.75
DA       59.60 [+ or -] 1.73 (d,e)       -3.02
DB       57.57 [+ or -] 1.92 (b,c,d)     -2.11
DC       60.36 [+ or -] 2.98 (c)          1.22

Note: Different superscript letters in the same column indicate a
significant difference (P < 0.05).

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