Aquaculture 451 (2016) 213–222

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Aquaculture

journal homepage: www.elsevier.com/locate/aqua-online

Evaluation of the growth and carcass quality of diallel crosses of four

strains of Nile tilapia (Oerochromis niloticus)
Roberto Neira a,b,⁎, Ximena García a, Jean Paul Lhorente b, Michael Filp b,
José Manuel Yáñez b,c, Ana María Cascante d
a
Facultad de Ciencias Agronómicas, Universidad de Chile, Casilla 1004, Santiago, Chile
b
Aquainnovo S.A. Talca 60, Puerto Montt, Chile
c
Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile
d
Aquacorporación Internacional (ACI) Cañas, Guanacaste, Costa Rica

a r t i c l e i n f o a b s t r a c t

Article history: This study examined four commercial lines of Nile tilapia (Oerochromis niloticus) ultimately to implement a
Received 18 November 2014 breeding program to produce clean fillets from an all-male fish population that is grown to 1 kg. Contemporary
Received in revised form 20 August 2015 progenies were produced to perform a complete 4 × 4 diallel cross. Two experimental populations were studied:
Accepted 27 August 2015
(1) a set of hormonal sex-reversed (SR) progeny populations that were processed at 1 kg to obtain carcass quality
Available online 3 September 2015
data and (2) a set of populations that did not receive hormone treatment (no hormone, NH) that were used to
Keywords:
assess growth between 100 g to 400 g. The growth traits of 3997 NH fish from 124 families were recorded at
Nile tilapia 400 g, and the processing plant traits were obtained from 2721 SR fish from 99 families. In general, all sources
Oerochromis niloticus of variation were highly significant for most traits with the effect of linebreeding explaining the largest (from
Diallel cross 35 to 50%) fraction of the explained variance (FEV) for all traits, except for the dressing percentage, for which
Growth the effect of the general combining ability (gca) was the most important source of variation (51%). The gca
Carcass quality exerted the second most important effect on the body weight, fillet weight, and abdominal fat percentage, and
Profit heterosis reciprocal effects constituted the second most important influence on the head, dressing and fillet percentages,
with an FEV of 20% to 35% being observed. The maternal effect was relatively important only for the specific
growth rate (SGR), explaining 26% of the total variance. The effect of heterosis was highly significant for all traits
but corresponded to only 5% or less of the explained variance for almost all traits, except for the fillet percentage
and for days to 1000 g with FEVs of 16% and 9%, respectively. In the NH population, the heterosis for all traits in-
dicates a favorable effect of crossbreeding, particularly the heterosis for body weight (6.7%) and average daily
gain (6.8%). In the SR population, the levels of heterosis demonstrated the favorable moderate effects of cross-
breeding on the body wt. at 400 g (4.0%), days to 1 kg (− 6.3%), average abdominal fat % (− 7.4%), and fillet
yield (1.6%). These results suggest that crossbreeding does not further improve the exploitation of genetic vari-
ation for single traits in this particular farmed tilapia population; however, the observed composite trait fillet pro-
ductivity, i.e., the total biomass of fillet produced per number of farmed fish,yielded promising levels of heterosis
with levels that reached 38% and 43% in specific crosses. Furthermore, four of six cases exhibited a cross that was
better than the best pure line, demonstrating that profit heterosis is a relevant parameter to consider for
assessing breeding strategies.
Statement of relevance: Total biomass of fillet produced, yielded promising levels of heterosis.
© 2015 Elsevier B.V. All rights reserved.

1. Introduction
Since the mid-1980s, the primary worldwide production method of
tilapia has shifted from wild-caught sources to aquaculture production
(FAO, 2010), with farmed tilapia production growing at an average rate
of 11% over the last 10 years. Tilapia production in the Americas
⁎ Corresponding author at: Facultad de Ciencias Agronómicas, Universidad de Chile,
Casilla 1004, Santiago, Chile.
E-mail address: rneira@uchile.cl (R. Neira).
contributed over 315 thousand tons (9%) to the world tilapia production
in 2010 (FAO, 2012; Fitzsimmons et al., 2012). Most of this increase was
destined for export. Tilapias were introduced to more than ten coun-
tries of the Americas, primarily in the 1950s and 1960s (Fitzsimmons,
2000). The main cultured species is Oreochromis niloticus; however,
Oreochromis mossambicus, Oreochromis aureus and Oreochromis spp.
are also farmed, and approximately 90% of tilapias are produced by
Brazil, Honduras, Colombia, Ecuador and Costa Rica (FAO, 2010).
Genetic improvement has been part of the development of farmed
fish production. Specifically, repeated artificial selection is generally

http://dx.doi.org/10.1016/j.aquaculture.2015.08.033
0044-8486/© 2015 Elsevier B.V. All rights reserved.
214 R. Neira et al. / Aquaculture 451 (2016) 213–222
utilized to improve the additive genetic performance of farmed pop-
ulations (Gjedrem et al., 2012). This strategy has been applied to dif-
ferent species, such as Atlantic salmon, Salmo salar (Gjerde, 1986;
Quinton et al., 2005), coho salmon, Oncorhynchus kisutch (Hershberger
et al., 1990; Neira et al., 2006), rainbow trout, Oncorhynchus mykiss
(Gjedrem, 2000; Quinton et al. 2004), channel catfish, Ictalurus punctatus
(Dunham and Brummett, 1999), rohu carp, Labeo rohita (Mahapatra
et al., 2006) and Nile tilapia, O. niloticus (Bentsen et al., 1998; Ponzoni
et al., 2005; Eknath et al., 2007; Thodesen et al., 2011). Diallel cross ex-
periments have been used as a tool to evaluate strains or lines, establish
composite base populations and estimate genetic parameters (Gjerde,
1988; Gjerde and Refstie, 1984; Bentsen et al., 1998, 2007; Gjerde et al.,
2002; Quinton el at, 2004). Alternative approaches to exploit potential
heterosis via intraspecific crossbreeding, which is a standard practice in
other animal breeding programs, e.g., poultry (Bell, 1982; Wei et al.,
1991), have been scarcely used in fish aquaculture. The preferential use
of a cumulative response from selection instead of crossbreeding pro-
grams is primarily due to the low level of expressed heterosis, possible
effects of the genotype on non-additive genetic performance via envi-
ronmental interactions and the dependence on a specialized hatchery
for producing hybrid fingerlings in each cycle (Gjerde and Refstie,
1984; Bentsen et al., 1998). In contrast, hybrid crosses have been demon-
strated to perform better than pure lines in some instances, e.g., the com-
mon carp, Cyprinus carpio (Bakos and Gorda, 1995; Hulata, 1995), and
hybrid crossing was shown to be successful in breeding programs in
carp (Wohlfarth et al., 1980; Kirpichnikov, 1981; Wohlfarth, 1993) and
tilapia (Circa et al., 1994).
The selection of a breeding strategy depends on the stage of develop-
ment of individual aquaculture industries and the breeding objectives
for specific cultured species. In intensive cultured tilapia production,
exploiting both additive and dominance genetic variation together
with complementation among commercial strains may be an alterna-
tive to traditional breeding programs that warrants examination. Signif-
icant dominance effects have been identified for growth, which may be
utilized in Atlantic salmon (Rye and Mao, 1998), rainbow trout (Pante
et al., 2002) and Coho salmon (Gallardo et al., 2010). The present
study was performed at Aqua Corporación Internacional (ACI), which
is a private tilapia farm in Costa Rica whose main product is frozen
fish that sold in a first-class market. This study examined the growth
and carcass quality traits of a complete diallel cross in four available ti-
lapia strains. The resultant information was used as the basis for
selecting a breeding strategy for the implementation of an efficient ge-
netic improvement program.
2. Materials and methods
2.1. General design
Four commercial lines of Nile tilapia (Oerochromis niloticus) were
used to perform this study to implement a breeding program at Aqua
Corporación Internacional (ACI), which is a tilapia-producing company
in Cañas, Costa Rica. ACI’s main product is clean tilapia fillets that are ob-
tained from an all-male fish population grown to 0.9 to 1 kilogram.
These four stocks, called ACI-A, ACI-G, ACI-T and ACI-R (henceforth sim-
ply named lines A, G, T and R), do not represent specific geographical
lines; instead, these lines are mixed populations that have been sepa-
rately maintained by the company for several years. The ACI-A stock
was based on two key lines imported by ACI from Auburn in 1986 and
1992. The Auburn stocks derived from several O. niloticus samples intro-
duced to Auburn University in the late 1970s and early 1980s. Of these
samples, the one collected in 1982 from the Ismailia Canal, a branch of
the Nile 75 km Northeast of Cairo, constituted the basis of the lines
imported by ACI in 1986 and 1992. These two populations of Egyptian
fish were later crossed, and the F2 progeny were combined with Fishgen
fish. At the time of the experiment, approximately 50%, 25% and 25% of
the ACI-A stock were thought to consist of the 1986 Auburn sample, the
1992 sample and the Fishgen population, respectively. In 2006, the ACI-
A stock was genetically characterized in detail. This characterization did
not identify substantial genetic bottlenecks due to the management of
the stocks prior to their introduction to ACI. An analysis of allozymes re-
vealed no evidence of introgression by O. mossambicus into the ACI
stocks, whereas a small degree of introgression by O. aureus was detect-
ed. Genetic characterization of ACI stocks and variable or inbred refer-
ence stocks using 5 microsatellite DNA loci revealed that the ACI
stocks are likely to have retained much of the genetic variability of
their founder populations.
Little information was available on the genetic background of the
other three lines. Specifically, they were imported to ACI in 2005. The
ACI-G stock is a composite strain developed by the Bureau of Fisheries
and Aquatic Resources of the Philippines. The ACI-T stock originated
from Carmen Aquafarm in the Philippines, and the ACI-R line was
imported from Modercorp in Ecuador (Red Niloticus + Red Hibryd
Ecuador). In each case, several thousand fingerlings were imported
from an unknown number of families. The management of the fish by
ACI was the same for all stocks and is unlikely have substantially nega-
tively or positively impacted the current culture performance and ge-
netic diversity of the stocks at the time this study was initiated based
on the aforementioned genetic study.
Contemporary progenies of the four lines were produced to obtain
breeding individuals to be used in the planned crosses; however, in-
stead of random samples of the existing lines, test progeny were select-
ed from the best 50% of females and from the best 25% of males (body
weight at 28 weeks of age) from each of the 4 lines.
These progeny fish were grown for use in the crosses, and 250 fe-
males and 100 males were randomly selected as breeding individuals
within each line. A complete 4 × 4 diallel cross was designed, with 12
females in each of the 16 subclasses, i.e., 48 females and 24 males
from each tilapia line; one male was mated with two females in a nested
mating design to produce paternal half-sib families. Two sets of experi-
mental populations were obtained. First, a hormonally sex-reversed
(SR) population (all males) was used to produce fish to be processed
at approximately 1 kg and from which carcass quality data were obtain-
ed. Additionally, a second population not treated with hormones (no
hormone, NH) was used to measure growth traits between 100 g to
400 g and served as possible breeders for the next generation. This pro-
cess was designed to measure carcass quality traits in the type of fish
that is commercially produced, i.e., males that are obtained by hormonal
sex reversion.
Potential breeding males and females were transferred to condi-
tioning hapas one month before stocking in breeding hapas. Matings
were performed in 2 m2 hapas, and the mouths of males were
clipped to reduce female mortality. Larvae from each family were
collected and transferred to a 2 × 1 × 1 m hapa for alevin growth at
an average of 21 days after reproduction. The number of alevins
was reduced to 600 individuals at 30 days of age in each family.
PIT-tags were used to mark a random sample of 40 130-158-day-
old individuals per family at an average body weight of 15.2 and
25.9 g at for the SR and NH populations, respectively. These individ-
uals were then randomly allocated to four 16 m2 hapas at ten indi-
viduals per hapa for a communal growing period.
The data structure is shown in Table 1. During the first set of crosses,
the progeny of the sex-reversed (SR) population were produced from
99 obtained effective families. A family was considered effective when
more than 600 larvae were collected and successfully transferred to a
family hapa for growth. One hundred and twenty-four effective families
produced the NH population, and 4200 and 5040 alevins were marked
in the SR and NH populations, respectively.
2.2. Recorded traits
The following traits were recorded. In the SR populations, the indi-
vidual body weight of alevins (BWA) was recorded at tagging, and the
 R. Neira et al. / Aquaculture 451 (2016) 213–222 215

Table 1 2.3. Statistical analyses

Number of effective families (Fam) and number of alevins marked (Ale) per type of cross
between 4 commercial lines of tilapia (A, G, T and R) in the sex-reversed (SR) population
and in the non-hormone (NH) population.
The body weight, length, growth and carcass traits were analyzed
with two models of fixed effects; the first model was used to estimate
Dam line ► A G T R Total the adjusting factors, and the second model was used to perform the ge-
Sire line Fam Ale Fam Ale Fam Alev Fam Alev Fam Alev netic analysis.
▼

Sex-reversed population Model 1

A 10 400 7 280 12 480 4 208 20 896
The information was analyzed using the GLM program of the Statis-
G 8 320 7 280 5 200 7 280 33 1368
T 6 240 4 208 6 240 4 208 20 1080 tical Analysis System (SAS, 1996). The NH population was analyzed
R 4 208 5 200 6 240 4 208 19 856 using the following model:
Total 28 1168 23 968 29 1160 19 904 99 4200

Non-hormone population
A 7 280 10 400 6 240 4 200 27 1120
Y ijkl ¼ μ þ Gi þ H j þ Sk þ ðG  SÞjk þ βðA−AÞ þ eijkl
G 12 480 10 400 11 440 7 280 40 1600
T 8 320 7 280 10 400 7 280 32 1280
R 9 360 4 200 6 240 6 240 25 1040 where Yijkl is the value of the trait under analysis in individual l; μ is the
Total 36 1440 31 1280 33 1320 24 1000 124 5040
overall mean; Gi is the fixed effect of the ith genetic line combination
(i = , 2, …,16); Hj is the fixed effect of the jth hapa (j = 1, 2, 3 or 4);
Sk is the fixed effect of sex (k = 1, 2); G*S is the interaction of genetic
body weight was recorded at the processing plant (BW) to the line combination by sex; and β represents the regression coefficient of
nearest 0.1 g. In addition, the body length (BL), body width (BWd) Y on age A. The model for the SR population, which conformed only to
and body height (BH) were also measured at processing to the the males, did not include sex or interaction G*S terms. The data,
nearest 0.1 cm, as illustrated in Fig. 1. The carcass weight (CW), which are expressed as percentages, were transformed using an arcsin
head weight (HW), clean fillet weight (FW), abdominal fat weight (e.g., corrected D% = arcsin(sqrt(D%))). In the SR population, the
(AFW) and viscera weight (VW) were also recorded at processing adult body weight (BW), the fillet weight (FW), the days to 1000 g
to the nearest 0.1 g. Only highly trained personnel that normally pro- (D1000), the SGR, the head percentage (H%), the dressing percentage
cess tilapia manipulated the fish at the processing plant. A clean fillet (D%), the fillet percentage (F%) and the abdominal fat percentage
is defined as a fillet without skin, bones and fat that is ready to go to (AF%) were corrected using a linear regression to an average age of
market. The following variables were also derived: the dressing per- 390 days. In the NH population, BW100 and BL100 were linearly
centage, D% = CW × 100 / BW; the abdominal fat percentage, AF% = corrected to a mean age of 220 d and BW400 and BL400 were linearly
AFW × 100 / BW; the fillet percentage F% = FW × 100 / BW; the head corrected to a mean age 304 d within recording. Because G*S interac-
percentage H% = HW × 100 / BW; the viscera percentage V% = tions were invariably significant, all variables were expressed for the
VW × 100 / BW; and the specific growth rate SGR = 100*(lnBW − male sex within line using an additive correction factor. All variables
lnBWA) / d, where d is the number of days from tagging to process- were also adjusted with an additive correction factor to an average
ing. The average number of days from larvae to 1000 g body weight cage within both the SR and NH populations.
(D1000) was calculated based on a linear regression. A composite
trait, i.e., fillet productivity or total yield, was calculated for each Model 2
cross by dividing the final fillet biomass produced by the number of The adjusted data were analyzed using the following model (Harvey,
initial alevins marked and allowed to grow. 1975; Kidwell et al., 1960):
In the NH populations, the body weight of alevins was recorded to
the nearest 0.1 g at tagging (BWA), 100 g (BW100) and 400 g
(BW400), and the body length was recorded at 100 g (BL100) and Y hijk ¼ μ þ ah þ p1ii þ g 2i þ g 2 j þ m2 j þ c2ij þ r 2ij þ eijk
400 g (BL400) to the nearest 0.1 cm. The derived variables from 100 to
400 g were the specific growth rate SGR100 − 400 = 100*(lnBW400 –
lnBW100) / d and the average daily gain ADG100 − 400 = BW400 − where Yhijk is the kth observation on the individual fish from the ith ge-
BW100) / d, where d is the number of days between the recording netic line of sire and the jth genetic line of dam in the hth type of breed-
dates at 100 g and 400 g. ing (linebred or crossbred); μ is the overall mean; ah is the effect
common to all progeny of the hth type of breeding (linebred or cross-
bred); p1ii is the effect common to all progeny of a mating between
the ith breed of sire and the ith breed of dam; g2i is the effect of general
combining ability (gca) of the ith breed of sire; g2j is the effect of general
combining ability of the jth breed of dam; m2j is the effect of maternal
ability of the jth breed of dam; c2ij is the effect of specific combining abil-
ity (sca) of the ijth or jith cross (i ≠ j); r2ij is the sex-linked or reciprocal
effect of the ijth cross (i ≠ j) and eijk is the random error effect. Subscript
1 denotes that the effects were measured only among the progeny of
linebred mating, and subscript 2 denotes the effects that were measured
only among the progeny of the crossbred mating.
The relative importance of the general combining ability over the
total combining ability was calculated as the ratio of the sum of squares
SSgca / (SSgca + SSsca), which was modified from Baker (1978). Indi-
vidual cross heterosis was also calculated using the least squares
means (LSM) estimations from Model 2, in which the difference of the
LSM of a particular cross to the average LSM of the parental lines was
Fig. 1. Measures of body length (BL), body width (BWd) and body height (BH). expressed as the percentage of the mid-parent performance.
216 R. Neira et al. / Aquaculture 451 (2016) 213–222

Table 2 3.3. Main genetic effects

Means and standard deviations for measured traits in the sex-reversed (SR) population
and in the non-hormone (NH) population.
The results of the diallel cross analysis in the SR population are pre-
Trait N Mean SD CV sented in Table 3, where the relative impact of heterosis, linebreeding,
Population SR general and specific combining abilities, maternal and reciprocal effects
Tagging weights (g) 4200 15.2 9.4 60.1 on body weight and carcass quality traits are shown. Model 2 explained
Body weight BW (g) 2721 904.2 267.0 29.5 approximately 9 to 15% of the total variance for most analyzed traits, ex-
Body length BL (cm) 2721 34.4 3.1 9.0
cept for SGR and head percentage, for which the R2 value were 57% and
Fillet weight FW (g) 2700 355.0 110.0 30.9
Fillet percentage F% 2700 39.1 2.3 5.9 6%, respectively. In general, all sources of variation were significant
Head weight H (g) 2720 202.7 56.0 27.4 (p b 0.05) for most traits, with the exceptions of the effects of the specif-
Head percentage H% 2720 22.4 2.1 9.1 ic combining ability on the fillet weight, dressing percentage and fillet
Specific growth rate SGR (g) 2721 1.1 0.3 28.5 percentage as well as the reciprocal effects on the abdominal fat per-
Carcass weight CW (g) 2718 603.6 187.0 30.9
Dressing percentage D% 2718 66.7 2.4 3.7
centage. The linebred effect explained the largest fraction of variance,
Abdominal fat weight AFW (g) 2694 23.1 11.9 51.8 except for dressing percentage, for which the effect of the general com-
Abdominal fat percentage AF% 2694 2.5 1.0 43.1 bining ability was the most important source of variation. The general
Viscera weight VW (g) 2694 41.8 13.6 32.5 combining ability was the second most important source of variation
Viscera percentage V% 2694 4.6 1.0 21.5
for the body weight, fillet weight and abdominal fat percentage, and re-
Population NH ciprocal effects were the second most important influence on the head,
Tagging weights (g) 5040 25.9 18.2 70.2 dressing and fillet percentages. The maternal effect was relatively im-
Body weight at 100 g BW100(g) 3997 141.7 56.5 47.3
portant only for the SGR. The effect of heterosis was highly significant
Body weight at 400 g BW400(g) 3997 420.8 128.2 33.1
Body length at 100 g BL100(cm) 3997 19.2 2.8 14.6
for all traits (p b 0.01) but corresponded only to 5% or less of the ex-
Body length at 400 g BL400(cm) 3997 25.9 2.8 10.8 plained variance for almost all traits, except for the fillet percentage
Average daily gain ADG100–400 3997 3.3 1.0 32.1 and for days to 1000 g, for which it explained 16% and 9% of the total
Specific growth rate SGR100–400 3997 1.3 0.3 22.4 variance, respectively. The general combining ability was always more
important than the specific combining ability for all traits that were
measured at the processing plant, with the exception of the SGR. Differ-
3. Results ences between reciprocal crosses were the second most important
source of variation for days to 1000 g, head percentage, dressing per-
3.1. Outcomes from crossing centage and fillet percentage.
The results of the analysis of the diallel cross in the NH population
The average number of days from the stocking of males and females are presented in Table 4. Again, all sources of variation were significant
to larvae and the average number of larvae collected were 23 days (d) (p b 0.01) for all traits, with the exception of the effect of the specific
and 941 larvae (l), respectively, in the SR population (18 d, 987 l; 26 d, combining ability on the body weight at 400 g and abdominal fat per-
962 l; 22 d, 1044 l and 24 d, 200 l for A, G, T and R line breeds, respective- centage. In these cases, the models explained approximately 5% to 11%
ly). The average number of days to larvae and the average number of of the total variance. Again, the linebred and general combining ability
larvae collected were 19 days and 977 larvae, respectively, in the NH effects were responsible for most of the explained variance. The line-
population (19 d, 1053 l; 19 d, 1003 l; 20 d, 1092 l and 18 d, 679 l for bred effect was the most important source of variation for the body
A, G, T and R line breeds, respectively). weight, length at 400 g and average daily gain. The general combining
ability was the most important source of variation for the body weight,
3.2. Phenotypic means and variation length at 100 g and SGR 100–400. Maternal effects were the second im-
portant source of variation for body weight and length at 100 g. The ef-
The means and standard deviations for the recorded traits from both fect of heterosis was highly significant for all traits (p b 0.01) and usually
the SR and NH populations are presented in Table 2. The data corre- constituted approximately 10% of the explained variance for body
spond to averages and standard deviations across all 16 types of crosses weights and average daily gain, whereas it comprised no more than
and pure breeds at an average of 390.6 days. The NH individuals corre- 6% of the variance in body length and SGR100–400. The general combin-
spond to males and females that were measured at an average of 220.3 ing ability was also more important than the specific combining ability
and 304.2 days. for all traits that were measured in the NH population. The reciprocal

Table 3
Analysis of variance of body weight and carcass traits in the sex-reversed (SR) population. FEV is the fraction of the explained variance attributed to each source of variation as the per-
centage of the appropriate sum of squares over the total sum of squares, and SSgca/(SSgca + SSsca) is the ratio of the sum of squares of the general combining ability to the total combining
ability sum of squares.

BW FW D1000 SGR H% D% F% AF%

Source of variation df1
F FEV F FEV F FEV F FEV F FEV F FEV F FEV F FEV

Heterosis 1 8.7⁎⁎ 3% 13.8⁎⁎ 5% 20.0⁎⁎ 9% 10.6⁎⁎ 1% 7.7⁎⁎ 5% 25.7⁎⁎ 7% 24.4⁎⁎ 16% 12.0⁎⁎ 4%
Linebred 3 48.3⁎⁎ 53% 38.8⁎⁎ 44% 35.9⁎⁎ 50% 118.4⁎⁎ 43% 18.4⁎⁎ 36% 16.9⁎⁎ 14% 18.1⁎⁎ 35% 46.1⁎⁎ 45%
General combining ability 3 18.4⁎⁎ 20% 24.0⁎⁎ 27% 8.0⁎⁎ 11% 36.0⁎⁎⁎ 13% 11.4⁎⁎ 22% 62.5⁎⁎ 51% 5.4⁎⁎ 10% 37.7⁎⁎ 36%
Maternal effects 3 6.7⁎⁎ 7% 6.6⁎⁎ 8% 7.5⁎⁎ 10% 71.5⁎⁎ 26% 1.2 2% 4.6⁎⁎ 4% 2.8 ⁎ 5% 9.2⁎⁎ 9%
Specific combining ability 2 7.4⁎⁎ 5% 2.2 2% 4.2 ⁎ 4% 40.1⁎⁎ 10% 6.5⁎⁎ 8% 2.8 2% 0.7 1% 7.2⁎⁎ 5%
Reciprocal effects 3 10.6⁎⁎ 12% 12.1⁎⁎ 14% 10.5⁎⁎ 15% 21.8⁎⁎ 8% 13.3⁎⁎ 26% 28.6⁎⁎ 23% 16.9⁎⁎ 33% 1.8 2%
R2 13% 12% 9% 57% 6% 15% 11% 11%
SSgca / (SSgca + SSsca) 79% 94% 74% 57% 72% 97% 92% 89%

The following traits are indicated: body weight (BW), filet weight (FW), days to 1000 g (D1000), specific growth rate (SGR), head percentage (H%), dressing percentage (D%), filet per-
centage (F%) and abdominal fat percentage (AF%).
⁎⁎ Significant at p b 0.01.
⁎ Significant at p b 0.05.
1
Error df = 2703
 R. Neira et al. / Aquaculture 451 (2016) 213–222 217

Table 4
Analysis of variance of body weight and growth traits in the non-hormone (NH) population. FEV is the fraction of the explained variance attributed to each source of variation as the per-
centage of the appropriate sum of squares over the total sum of squares, and SSgca / (SSgca + SSsca) is the ratio of the sum of squares of the general combining ability to the total com-
bining ability sum of squares.

BW100 BL100 BW400 BL400 SGR 100–400 ADG

1
df F FEV F FEV F FEV F FEV F FEV F FEV

Heterosis 1 31.1⁎⁎ 10% 11.2⁎⁎ 5% 49.9⁎⁎ 12% 13.7⁎⁎ 6% 7.0⁎⁎ 2% 45.1⁎⁎ 9%

Linebred 3 16.9⁎⁎ 16% 13.5⁎⁎ 17% 50.5⁎⁎ 37% 38.4⁎⁎ 48% 42.0⁎⁎ 32% 76.6⁎⁎ 46%
General combining ability 3 42.0⁎⁎ 40% 24.4⁎⁎ 32% 37.0⁎⁎ 27% 17.6⁎⁎ 22% 59.7⁎⁎ 45% 48.7⁎⁎ 29%
Maternal effects 3 23.1⁎⁎ 22% 14.2⁎⁎ 18% 12.4⁎⁎ 9% 6.0⁎⁎ 7% 11.7⁎⁎ 9% 6.4⁎⁎ 4%
Specific combining ability 2 6.0⁎⁎ 4% 14.2⁎⁎ 12% 1.2 1% 5.4⁎⁎ 4% 16.4⁎⁎ 8% 0.6 0%
Reciprocal effects 3 9.4⁎⁎ 9% 11.8⁎⁎ 15% 17.3⁎⁎ 13% 10.5⁎⁎ 13% 5.5⁎⁎ 4% 19.8⁎⁎ 12%
R2 7% 5% 9% 6% 9% 11%
SSgca / (SSgca + SSsca) 91% 72% 98% 83% 85% 99%

The following traits are indicated: body weight at 100 g (BW100), body length at 100 g (BL100), body weight at 400 g (BW400), body length at 400 g (BL400), specific growth rate from
100 to 400 g (SGR 100–400) and average daily gain (ADG).
⁎⁎ Significant at p b 0.01.
1
Error df = 3981.

effects were less important in the NH population, which were the third
most important source of variation.
3.4. Linebred and crossbred effects
For the heterosis and linebred lines at the processing plant, Table 5
shows the least-squares means for body weight and carcass traits of
the sex-reversed population (SR), and Table 6 shows the least-squares
means of growth traits in the non-hormone population (NH). Highly
significant (P b 0.01) differences between linebred and crossbred lines
were found for all traits in both the SR and NH populations. The general
heterosis was invariably positive in terms of production and moderate
levels. Highly significant differences (P b 0.01) in the performance traits
between the different lines were found for all traits in both the SR and
NH populations, except for the body weight at 100 g – the lines could
not be differentiated at this early age. One of the lines, (T), was consis-
tently the best or second best in most traits for early and late measure-
ments. The second highest performance was that of line G, and except
for the weight at 100 g, line R ranked the lowest.
3.5. Combining abilities, maternal and reciprocal effects
NH populations. Line G exhibited the second highest performance in
the general combining ability for the average daily gain from 100 to
400 g and for the adult body weight, fillet weight, days to 1000 g and ab-
dominal fat percentage. Moreover, the specific combining abilities sig-
nificantly differed for most traits in both the SR and NH populations;
however, because these differences accounted for a small fraction of
the explained variance (Tables 3 and 4), reduced exposure is merited.
Reciprocal cross effects were significant in most cases. The main ex-
ception was the reciprocal cross AT-TA in the NH population, which
showed no significant differences between reciprocals, except for head
percentage. Other exceptions were observed in the SR population,
where the cross GR-RG showed no significant reciprocal effects for
body weight, fillet weight, days to 1000 g and head percentage; the
body and fillet weights of the cross GT–TG did not significantly differ,
nor did the dressing and fillet percentages of the cross AT-TA.
Maternal effects significantly impacted the early body weights, and
crosses in which lines A and T were used as females produced better
body weights and lengths at 100 g. Crosses from females of line R
yielded higher body and fillet weights, dressing percentages, fillet per-
centages and abdominal fat percentages, which is interesting because
this line performed the worst for these traits.

Tables 7 and 8 show the least-squares means of body and carcass
traits that were measured in the SR population and body weight and
growth traits that were measured in the NH population for the general
and specific combining abilities, maternal and reciprocal effects. The
general combining ability of line T was better than those of the other
three lines in most of the traits that were measured in both the SR and
3.6. Heterosis for single and composite traits
Individual cross heterosis estimations for traits that were measured
at the processing plant, such as the body weight, days to 1000 g, specific
growth rate from tagging to the processing plant, clean fillet percentage
and abdominal fat percentage (AF%) in the SR population, are presented

Table 5
Least-squares means for body and carcass traits in the SR population for linebred, crossbred and percent heterosis.

D
EFFECTS BW FW SGR H% D% F% AF% N
1000

Heterosis(μ ̂ + âi)
Linebred 885.2b 343.1b 490.8a 1.06a 22.9a 66.1b 38.6b 2.7a 747
Crossbred 920.4a 361.5a 459.7b 1.08b 22.6b 66.6a 39.2a 2.5b 3052

100[(μ ̂ + â2) − (μ ̂ + â1)] / (μ ̂ + â1)

% heterosis 4.0 5.4 −6.3 1.9 −1.3 0.8 1.6 −7.4

Linebred (μ ̂ + â1 + p̂ 2ii)
AA 811.1c 322.3c 516.5c 1.09c 22.3c 66.7a 39.7a 2.7b 256
GG 909.8b 351.2b 469.7b 1.07b 22.8b 66.4a 38.5b 2.5c 214
TT 1074.7a 415.0a 397.5a 1.16a 23.0a 66.6a 38.5b 2.1d 186
RR 745.2d 284.0d 579.4d 0.92d 23.5d 64.6a 37.9c 3.7a 91

The following traits are indicated: body weight (BW), filet weight (FW), days to 1000 g (D 1000), specific growth rate (SGR), head percentage (H%), dressing percentage (D%), filet per-
centage (F%) and abdominal fat percentage (AF%).
a–d
Values with different superscripts in the same column are significantly different at p b 0.01.
218 R. Neira et al. / Aquaculture 451 (2016) 213–222

Table 6 lines, and cross TG was superior to all lines and crosses. The abdominal
Least-squares means of body weight and growth traits in the NH population for linebred, fat percentage exhibited extremely good levels of heterosis, as observed
crossbred and percent heterosis. Traits are indicated in Table 4.
for both reciprocal crosses TR and RT; however, the pure line T per-
EFFECTS BW100 BL100 BW400 BL400
SGR
ADG N
formed better than these crosses.
100–400 Because the ultimate goal was to sell fillets, we constructed a simple
Heterosis (μ ̂ + âi) composite trait to assess the different lines and crosses. We called this
Linebred 137.2b 19.0b 407.1b 25.7b 1.33b 3.22b 1104 composite trait the fillet productivity (FP), which was defined as the
Crossbred 146.2a 19.3a 434.5a 26.0a 1.35a 3.44a 2893 total biomass of the clean fillet weight that was produced by a particular
100 [(μ ̂ + â2) − (μ ̂ + â1)] / (μ ̂ + â1) line or cross per marked fish allowed to grow. Fig. 3 presents the results
% heterosis 6.6 1.4 6.7 1.0 2.0 6.8 of this analysis. Specifically, the average FP exceeded 20% and reached
̂ ̂
approximately 40% in some cases.
Linebred (μ + â1 + p 2ii)
AA 121.6b 18.4b 367.3c 25.5c 1.36b 2.93c 331
GG 140.0a 19.3a 436.0b 26.8a 1.37b 3.53b 332
TT 142.9a 19.3a 457.2a 26.5b 1.42a 3.74a 244 4. Discussion
RR 144.3a 19.2a 367.9c 24.1d 1.15c 2.67d 197
a–d
Values with different superscripts in the same column are significantly different at 4.1. Breeding strategy
p b 0.01.
In this study, we estimated the effects of genetics on the productive
traits in Nile tilapia for four different commercial lines and their combi-
in Fig. 2. The least-squares means for each of the reciprocal crosses and nations using a 4 × 4 diallel cross analysis. Moreover, we investigated
the participating parental lines, which are connected by dashed lines to the influence of hormone-induced sex reversion on the genetic effects
identify the mid-parent values, are also presented. The degree of indi- of growth-related and carcass quality traits in an all-male population,
vidual heterosis for the different crosses varied according to the lines which reflects the actual type of production of this particular farm.
that were involved. For instance, the degree of individual heterosis var- Selective breeding is the most used approach for genetic improve-
ied from a negative heterosis of the cross TA to a large positive heterosis ment in aquaculture species. This strategy has been demonstrated to be
for body weight, as observed in the cross AR. Individual cross heterosis extremely effective in the improvement of most important species of
values for days to 1000 g were generally negative, which is favorable farmed fish, such as carp, tilapia and salmon (Gjedrem 2012; Ponzoni
for this trait; again, the cross AR showed the highest degree of heterosis. et al. 2011). The non-additive variation between lines (i.e., heterosis)
Individual cross heterosis for the SGR and clean fillet percentage were may be exploited by a crossbreeding strategy. Nevertheless, to our
low; however, crosses GT–TG and TR-RT were superior to both parental knowledge, improvement programs that utilize crossing between lines

Table 7
Least-squares means of body and carcass traits in the SR population for the general combining ability, maternal effects, specific combining ability and reciprocal crosses. Traits are indicated
in Table 5

EFFECTS BW FW D 1000 SGR H% D% F% AF% N

̂ ̂
General combining ability (μ + â2 + g 2i)
A 916.6c 361.4c 458.0b 1.05d 22.2c 67.0b 39.4b 2.7a 1961
G 946.1b 371.6b 446.0c 1.06c 22.6b 66.8c 39.1c 2.3b 1890
T 972.9a 386.9a 445.3c 1.11a 22.7b 67.4a 39.7a 2.1c 1225
R 846.1d 326.0d 489.6a 1.07b 23.0a 65.3d 38.4d 2.8a 1028

Maternal effect (μ ̂ + â2 + mj)

A 884.2b 346.9c 483.2a 1.09b 22.8 66.6b 39.0j 2.4c 783
G 892.8b 350.0c 473.8a 1.09b 22.6 66.4b 39.2j 2.7a 1509
T 944.1a 368.8b 437.4b 1.11a 22.5 66.5b 39.0j 2.6b 891
R 960.7a 380.3a 444.6b 1.01c 22.7 67.1a 39.5i 2.3c 616

Specific combining ability (μ ̂ + â2 + ĝ 2i + ĝ 2j + ĉ 2ij + ((m̂ 2j + m̂ 2j’)/2)

AG 910.9c 359.1 459.0k 1.08c 22.4b 67.1 39.3 2.6b 1172
AT 947.1b 376.8 457.4k 1.12a 22.4b 67.5 39.7 2.2c 513
AR 859.5d 334.0 482.8j 1.00d 22.4b 66.0 38.7 3.0a 276
GT 1011.7a 400.8 418.2l 1.10b 22.4b 67.5 39.6 2.2c 339
GR 862.4d 316.6 507.9i 1.08c 23.1a 65.2 38.2 2.5b 379
TR 931.0bc 365.1 452.5k 1.12a 23.2a 66.2 39.1 2.3c 373

Reciprocal effects (μ ̂ + â2 + ĝ 2i + ĝ 2j + ĉ 2ij + r̂ 2ij + m̂ 2j)

AG1 872.3d 340.3cd 478.9ab 1.10 cd 22.7c 66.7c 39.0d 2.8 256
GA 949.5c 377.8b 439.2c 1.05f 22.2d 67.5b 39.7b 2.3 139
AT 1016.4a 405.9a 415.9de 1.13b 22.1d 67.4b 39.9b 2.4 230
TA 877.7d 347.7cd 498.8 a 1.11c 22.7bc 67.5b 39.5bc 2.1 156
AR 901.2d 352.7c 457.4bc 0.94h 22.2d 66.7c 39.1cd 2.9 350
RA 817.7e 315.2e 508.1a 1.05f 22.7bc 65.4e 38.4ef 3.1 183
GT 1025.6a 400.0a 400.8e 1.14ab 22.8bc 66.9c 39.0d 2.2 227
TG 997.9ab 401.6a 435.6 cd 1.07e 22.0d 68.2a 40.3a 2.2 212
GR 865.3de 338.4cd 497.7a 1.00g 23.0bc 66.1d 38.8de 2.4 214
RG 859.4de 328.1de 479.4ab 1.08de 23.1b 64.8f 38.1f 2.7 186
TR 966.8bc 378.7b 438.4cd 1.09de 23.5a 65.8de 39.0d 2.3 163
RT 895.2d 351.4c 466.6b 1.15a 22.8bc 66.7c 39.2cd 2.4 174
a–d
Values with different superscripts in the same column are significantly different at p b 0.01.
i–l
Values with different superscripts in the same column are significantly different at p N 0.05.
 R. Neira et al. / Aquaculture 451 (2016) 213–222 219

Table 8
Least-squares means of the body weight and growth traits in the NH population for the general combining ability, maternal effects, specific combining ability and reciprocal crosses. Traits
are indicated in Table 4.

EFFECTS BW100 BL100 BW400 BL400 SGR 100–400 ADG N

̂ ̂
General combining ability (μ + â2 + g 2i)
A 134.2d 18.9c 416.9c 26.3b 1.43a a
3.37b 1466
c b c c c b
G 138.5 19.0 419.4 25.8 1.34 3.35 1449
b a a a b a
T 154.8 19.7 475.5 26.9 1.40 3.82 1622
a a b d d c
R 157.3 19.6 426.4 25.1 1.24 3.21 1249
Maternal effect (μ ̂ + â2 + mj)
a a a c c a
A 158.5 19.8 456.5 25.5 1.29 3.56 655
c b c b b c
G 143.5 19.3 421.4 26.0 1.36 3.31 730
b b b a b a
T 150.4 19.4 444.1 26.3 1.35 3.50 946
d c c ab a b
R 132.4 18.8 416.1 26.2 1.41 3.38 562
̂ ̂ ̂ ̂ ̂ ̂
Specific combining ability (μ + â2 + g 2i + g 2j + c 2ij + ((m 2j + m 2j’)/2)
AG1 128.8 d
18.6 e
405.5 25.9 d
1.41 a
3.30 529
b a a a
AT 155.0 19.9 477.8 27.1 1.40 3.85 644
c d e b
AR 143.2 19.0 407.1 25.0 1.34 3.15 293
c c b a
GT 146.5 19.3 455.0 26.6 1.41 3.68 471
c c e c
GR 145.3 19.3 399.5 25.0 1.22 3.03 449
a b c b
TR 158.5 19.7 462.3 26.4 1.33 3.62 507
Reciprocal effects (μ ̂ + â2 + ĝ 2i + ĝ 2j + ĉ 2ij + r̂ 2ij + m2j)
d h e d a e
AG 118.7 18.2 387.3 26.3 1.46 3.20 346
c de d f de d
GA 138.8 19.1 423.7 25.5 1.36 3.40 183
b abc ab a cd bc
AT 154.8 20.0 475.7 27.6 1.39 3.83 326
b bc ab c bc ab
TA 155.1 19.8 479.9 26.6 1.42 3.87 318
d gh e fg b fg
AR 128.8 18.4 383.4 25.1 1.42 3.03 139
ab c d g g e
RA 157.6 19.7 430.8 24.8 1.26 3.26 154
ab c a b bc a
GT 157.5 19.7 487.9 27.2 1.40 3.94 300
c ef d de b d
TG 135.5 18.8 422.2 26.1 1.42 3.42 171
d fg e g g g
GR 129.7 18.5 374.8 24.9 1.27 2.92 236
a a d f h ef
RG 161.0 20.1 424.3 25.2 1.17 3.13 213
a ab b c f c
TR 161.0 20.1 473.9 26.8 1.31 3.73 187
b d c e ef d
RT 156.1 19.3 450.7 26.0 1.34 3.52 320
a–h
Values with different superscripts in the same column are significantly different at p b 0.01.
1
(sire × dam)

as a breeding strategy to exploit such variation are not currently
employed in aquaculture (Rye et al. 2010, Neira, 2010). This lack of use
may be due to the absence or low to moderate levels of heterosis found
in previous studies for various traits in different fish species, such as
growth and survival. These levels may be considered insufficient to justify
the implementation of a crossbreeding program and the practical compli-
cations that this implementation may involve (Gjerde & Refstie 1984;
Bentsen et al. 1998; Gjerde 1988; Gjerde et al. 2002, Pongthana et al.
2010). However, the magnitude of heterosis when crossing domesticated
strains, which have been developed over several generations of selection,
has not been studied (Gjedrem, 2012). Based on the results obtained
here, we discussed the implementation of a crossbreeding strategy to in-
crease the productive performance of a farmed tilapia population.
4.2. Linebred and crossbred effects
Linebred and heterosis effects were significant for all analyzed traits
in both the SR and NH populations. Moreover, the linebred effect consis-
tently explained a higher proportion of the total variance than the het-
erosis effect. We also found significant differences between lines for all
the analyzed traits in both the SR and NH populations. Generally, for
most measured traits in both populations, line T outperformed other
strains and line R showed the poorest performance; lines G and A exhib-
ited intermediate performances. These differences were less marked for
the body weight (BW100 and BW400) in the NH population, most likely
due to the early measurement of the trait and the low differentiation of
the strains at these stages. The reasons for the superior performance of
some strains are not easily inferred because the lines were of different
origins and have been maintained in the company for many genera-
tions. However, differences in the growth performance between many
tilapia strains of different origins and captivity histories have been
widely reported (Maluwa and Gjerde 2006; Moreira et al. 2005;
Bentsen et al. 1998; Eknath et al. 1993). In this study, the determination
of differences in the productive performance of the strains is important
to establish a breeding management strategy for this population.
Our findings demonstrated a favorable (either positive or negative)
effect of crossbreeding on the productive traits that were studied in
both populations (SR and NH). The overall level of heterosis depended
on both the two-line combination and the trait that was analyzed. In
the NH population, the percentage of heterosis for all traits was consis-
tently positive, which indicates a favorable effect of crossbreeding, par-
ticularly on the body weight and the average daily gain (heterosis N 6%).
In the SR population, the overall percentages of heterosis for the body
weight were lower than those in the NH population; however, overall
heterosis was significant for the fillet weight, days to 1 kg and abdomi-
nal fat content. Specifically, for single crosses in the SR population, the
maximum heterosis was 10% for the body weight for one specific cross-
bred, whereas all other levels of heterosis were below 7%. These levels
are consistent with the results of a previous study in tilapia, in which
only a few line combinations from 64 crosses (8 strains) in 7 different
environments showed more than 10% heterosis for the body weight,
with a maximum of 14% (Bentsen et al. 1998). Compared with other
fish species, the levels of heterosis for the body weight reported herein
may be considered low. For example, the maximum levels of heterosis
of 24%, 29% and 36% have been reported for body weights of silver
perch (Bidyanus bidyanus), common carp (C. carpio) and rainbow
trout, respectively.
Despite the relatively high levels of heterosis for some traits for spe-
cific combinations in the SR population (i.e., 10% for the body weight
and −11% for days to 1000 g in AR hybrids and −19% for the abdominal
fat percentage in TR hybrids), these magnitudes were not superior to
the performance of the better strain in most cases (Figure 2). Cross-
breeding does not improve the exploitation of genetic variation for sin-
gle traits in this particular farmed tilapia population. This situation has
also been observed in other studies of tilapias and other economically
important fish species, such as Atlantic salmon, rohu carp and rainbow
220 R. Neira et al. / Aquaculture 451 (2016) 213–222

Fig. 2. Heterosis for single crosses observed in the sex-reversed (SR) population of hybrids from crossing 4 strains of O. niloticus. Dashed lines are used to identify the mid-parent values.

trout (Gjerde & Refstie 1984; Bentsen et al. 1998; Gjerde 1988; Gjerde
et al. 2002).
4.3. Combining abilities, maternal and reciprocal effects
As previously stated, diallel cross experiments are useful for compar-
ing the performance of not only different commercial stocks or lines
with each other but also in hybrid combinations. Specifically, diallel
crosses can be used to compare the average performance of a line
with hybrids in which the line participates (general combining ability:
gca) or that of a specific combination with a particular line (specific
combining ability: sca). Maternal effects, which assess the average per-
formance of the different lines participating as female lines, and the re-
ciprocal effect of the crossed lines can also be estimated in diallel
crosses.
The significance and the relatively high proportion of the variance
explained by the general combining ability for all traits in both popula-
tions indicate the relevance of additive genetic effects. This finding
suggests that these traits can be improved by selection because im-
provement has been shown by other studies in which significant genet-
ic parameters have been estimated for body weight and carcass traits in
this species (Ponzoni et al. 2005; Rutten et al. 2005). We also found
 R. Neira et al. / Aquaculture 451 (2016) 213–222
Fig. 3. Heterosis of filet productivity (total biomass of filet produced per marked fish) in the sex-reversed (SR) population. This characteristic is a composite trait defined as the total filet
weight produced by a particular line or cross per marked fish allowed to grow. The horizontal lines over the bars indicate the mid-parent values.
significant differences in the general combining ability component be-
tween the four strains, indicating the opportunity that superior parental
contribution from a given strain for a particular trait can be distin-
guished when producing hybrids.
The specific combining ability was not significant for the FW, D% and
F% in the SR population or for the BW400 and ADG in the NH population.
Moreover, the specific combining ability only explained up to 10% of the
total variance of the remaining traits in both populations. These results
suggest that specific combinations among the two parental lines are
minimally significant for a given trait and reflect the low relevance of
non-additive effects (dominance and epistasis) for these traits. Howev-
er, line T yielded the three best specific crosses for any one trait, and the
cross GT is the best cross for processing plants. The reported SSgca /
(SSgca + SSsca) ratio for the traits that were analyzed, which consis-
tently exceeded 70% except for the SGR in the SR population (57%), con-
firmed the relative importance of additive genetic effects compared
with non-additive genetic effects. These generally low levels of non-
additive genetic effects are attributed to the assumption that this com-
ponent is higher for crosses among genetically divergent populations
or among highly homozygous strains, and such strains most likely
were not involved in the present study.
As expected, maternal effects were more evident for early mea-
surements (BW100 and BL100) in the NH population. Strikingly,
the maternal component for the SGR was also high in the SR popula-
tion; however, this effect was not observed for the SGR between 100
to 400 g in the NH population. Our results also showed that maternal
abilities of the lines may differ for some traits because of the signifi-
cant differences in maternal effects between the lines. However, the
pattern of maternal performance was unclear across all traits for the
different strains, indicating that the better maternal line was not eas-
ily determined for any of the traits. Moreover, further research is re-
quired to elucidate the correlation of good maternal progeny growth
and fillet traits with reproductive traits to determine a dam line. The
presence of significant reciprocal effects for almost all of the traits
suggests that specific male and female strains should be used when
implementing a crossbreeding scheme.
4.4. Profit heterosis
As observed many domestic animals and in tilapias in this exper-
iment, heterosis for individual traits that are related to growth is
generally not significant. However, the heterosis calculated for a
measurement of overall performance, such as a composite trait, is
high and has been referred to as profit heterosis by Moav (1966,
1973). As discussed in Section 4.2, the heterosis levels for single
traits are similar to the values that have been previously reported
for body weight in tilapias and somewhat below the levels that
have been shown in other fish species. In addition, the magnitude
of heterosis for other growth-related and fillet traits that are report-
ed here is not substantial. However, for the composite trait of fillet
221
productivity, which is the total biomass of fillet produced per fish
allowed to grow, heterosis was encouraging between specific crosses
that may be exploited in this particular production system (Fig. 3).
As expected, not only were the levels of heterosis much higher for
this type of trait, which demonstrated the effect of complementation
between lines, but in 4 of the 6 hybrid crosses, a cross that was better
than the best pure line was observed. Noticeably, the crosses be-
tween the two best lines (T & G) were equal or better than the best
line, suggesting an advantage of using hybrids for commercial pro-
duction in this particular case, despite the fact the average level of
heterosis was 15%.
5. Conclusions
This study confirmed that moderate levels of heterosis for single
traits reported to date are associated with growth in farmed tilapia. Fur-
thermore, this study also determined that these levels of crossbreeding-
induced heterosis exert a favorable effect (either positive or negative)
on the studied productive traits in both sex-reversed and normal popu-
lations. Linebreeding and the general combining ability explained most
of the variance, of which the latter comprised more than 80% of the total
combining ability. These results ratify the importance of additive genet-
ic effects for these traits, and the preference of selective breeding is the
most common approach for genetic improvement in tilapia production.
Maternal effects and reciprocal effects were also relevant. To improve
the efficiency of fillet production, which is measured based on a com-
posite trait that includes survival, growth and fillet yield, profit heterosis
can serve as a relevant parameter to assess breeding strategies. Addi-
tionally, specialized sire and dam lines may be tested if the differences
betwen reciprocal crosses are important.
Acknowledgments
The authors wish to acknowledge Aquacorporación Internacional
(ACI) for financing this work and for allowing us to publish these data.
In particular, the authors wish to acknowledge the support given by
Yaacob Berman and Carl Baum to this study. This work was made possi-
ble by the dedicated work of Carlos Alvarado, who managed the fish and
data collection, and by the personnel of the processing plant of ACI, who
accurately processed the fish and recorded the carcass quality. This
work was funded by Aquainnovo S.A. and ACI.
References
Baker, R.J., 1978. Issues of diallel analysis. Crop. Sci. 18, 533–536.
Bakos, J., Gorda, S., 1995. Genetic improvement of common carp strains using Intraspecific
hybridization. Aquaculture 129, 183–186.
Bell, A.E., 1982. Selection for Heterosis — Results With Laboratory and Domestic Animals.
Proceedings of the 2nd World Congress on Genetics Applied to Livestock Production,
Madrid. vol. VI, pp. 206–227.
Bentsen, H.B., Eknath, A.E., Palada-de Vera, M.S., Danting, J.C., Bolivar, H.L., Reyes, R.A.,
Dionisio, E.E., Longalong, F.M., Circa, A.V., Tayamen, M.M., Gjerde, B., 1998. Genetic
222 R. Neira et al. / Aquaculture 451 (2016) 213–222
improvement of farmed tilapias: growth performance in a complete diallel cross ex-
periment with eight strains of Oreochromis niloticus. Aquaculture 160, 145–173.
Circa, A.V., Eknath, A.E., Taduan, A.G., 1994. Genetic improvement of farmed tilapias: the
growth performance of the GIFT strain of Nile tilapia in rice-fish environments. Fifth
International Symposium on Genetics in Aquaculture. Halifax, Canada.
Dunham, R.A., Brummett, R.E., 1999. Response of two generations of selection to in-
creased body weight in channel catfish, Ictalurus punctatus, compared to hybridiza-
tion with blue catfish, I. furcatus, males. Journal of Applied Aquaculture 9, 37–45.
Eknath, A.E., Tayamen, M.M., Palada-de Vera, M.S., Danting, J.C., Reyes, R.A., Dionisio, E.E.,
Capili, J.B., Boliver, H.L., Abella, T.A., Circa, A.V., Bentsen, H.B., Gjerde, B., Gjedrem, T.,
Pullin, R.S.V., 1993. Genetic improvement of farmed tilapias: the growth performance
of eight strains of Oreochromis niloticus tested in different farm environments. Aqua-
culture 111, 171–188.
Eknath, A.E., Bentsen, H.B., Ponzoni, R.W., Rye, M., Nguyen, N.H., Thodesen, J., Gjerde, B.,
2007. Genetic improvement of farmed tilapias: composition and genetic parameters
of a synthetic base population of Oreochromis niloticus for selective breeding. Aqua-
culture 273, 1–14.
FAO, 2010. Fisheries Department, Fishery Information, Data and Statistics Unit. Fishstat
Plus: Universal Software for Fishery Statistical Time Series. Version 2.3 Available:
http://www.fao.org/fishery/statistics/software/fishstat/en (Accessed: Jan 4, 2012).
FAO, 2012. The State of World Fisheries and Aquaculture 20012. FAO Fisheries and Aqua-
culture Department. Food and Agriculture Organization of the United Nations, Rome
(209 pp.).
Fitzsimmons, K., 2000. Future Trends of Tilapia Aquaculture in the Americas. In: Costa-
Pierce, B.A., Rakocy, J.E. (Eds.), Tilapia Aquaculture in the Americas vol. 2. The
World Aquaculture Society, Baton Rouge, Louisiana, United States, pp. 252–264.
Fitzsimmons, K., Martinez, R., Ramotar, P., Tran, L., 2012. Global Production and Market
Situation in 2012 — Tilapia Continues to Climb the Charts. AQUA 2012. Meeting Ab-
stract 1261. World Aquaculture Society, Prague, Czech Republic.
Gallardo, J., Lhorente, J.P., Neira, R., 2010. The consequences of including non-additive ef-
fects on the genetic evaluation of harvest body weight in Coho salmon. Genet. Sel.
Evol. 42 (1), 19–27.
Gjedrem, T., 2000. Genetic improvement of cold water fish species. Aquaculture Research
31, 25–33.
Gjedrem, T., 2012. Genetic improvement for the development of efficient global aquacul-
ture: a personal opinion review. Aquaculture 344-349 (2012), 12–22.
Gjedrem, T., Robinson, N., Rye, M., 2012. The importance of selective breeding in aquaculture
to meet future demands for animal protein: a review. Aquaculture 350–353, 117–129.
Gjerde, B., Refstie, T., 1984. Complete diallel cross between five strains of Atlantic salmon.
Livestock Production Science 11 (2), 207–226.
Gjerde, B., 1986. Growth and reproduction in fish and shellfish. Aquaculture 57, 37–55.
Gjerde, B., 1988. Complete diallel cross between six inbred groups of rainbow trout, Salmo
gairdneri. Aquaculture 75, 71–87.
Gjerde, B., et al., 2002. Growth and survival in two complete diallele crosses with five
stocks of Rohu carp (Labeo rohita). Aquaculture 209 (1-4), 103–115.
Harvey, W.R., 1975. Least-squares Analyses of Data With Unequal Subclass Numbers. ARS
H-4.USDA
Hershberger, W.K., Myers, J.M., McAuley, W.C., Saxton, A.M., 1990. Genetic changes in the
growth of coho salmon (Oncorhynchus kisutch) in marine net-pens, produced by ten
years of selection. Aquaculture 85, 187–197.
Hulata, G., 1995. A review of genetic improvement of the common carp (Cyprinus
carpio L.) and other hybrids by crossbreeding, hybridization and selection. Aqua-
culture 129, 143–155.
Kidwell, J.F., Weeth, H.J., Harvey, W.R., Haverland, L.H., Shelby, E.E., Clark, R.T., 1960.
Hetrosis in crosses of inbred lines of rats. Genetics 45, 225–231.
Kirpichnikov, V.S., 1981. Genetic basis of fish selection. Springer Verlag, Berlin 410 p.
Mahapatra, K., Jana, R.K., Saha, J.N., Gjerde, B., Sarangi, N., 2006. In: Ponzoni, R.W., Acosta,
B.O., Ponniah, A.G. (Eds.), Development of Aquatic Animal Genetic Improvement and
Dissemination Programs: Current Status and Action Plans. 73. WorldFish Center con-
ferences proceedings, pp. 34–40
Maluwa, A.O., Gjerde, B., 2006. Genetic evaluation of four strains of Oreochromis shiranus
for growth in a diallel cross. Aquaculture 259, 28–37.
Moav, R. (1973) In "Agricultural Genetics, Selected Topics", p. 319-352, Editor R. Moav,
Moav, R., 1966. Specialized sire and dam lines I. Economic evaluation of crossbreeds.
Anim. Prod. 8, 193–202.
Moreira, A.A., Moreira, H.L.M., Hilsdorf, A.W.S., 2005. Comparative growth performance of
two Nile tilapia (Chitralada and Red-Stirling), their crosses and the Israeli tetra hybrid
ND-56. Aquaculture Research 36 (11), 1049–1055.
Neira, R., Diaz, N.F., Gall, G.A.E., Gallardo, J.A., Lhorente, J.P., Manterola, R., 2006. Genetic
improvement in Coho salmon (Oncorhynchus kisutch). I: Selection response and in-
breeding depression on harvest weight. Aquaculture 257, 9–17.
Neira, R., 2010. Breeding in Aquaculture Species: Genetic Improvement Programs in De-
veloping Countries. 9th World Congress on Genetics Applied to Livestock Production,
Leipzig, Germany, p. 8 (August 1–6).
Pante, M.J., Gjerde, B., McMillan, I., Misztal, I., 2002. Estimation of additive and dominance
genetic variances for body weight at harvest in rainbow trout Oncorhynchus mykiss.
Aquaculture 204, 383–392.
Pongthana, N., Nguyen, N.H., Ponzoni, R.W., 2010. Comparative performance of four red
tilapia strains and their crosses in fresh- and saline water environments. Aquaculture
308, S109–S114.
Ponzoni, R.W., Hamzah, A., Tan, S., Kamaruzzaman, N., 2005. Genetic parameters and re-
sponse to selection for live weight in the GIFT strain of Nile Tilapia (Oreochromis
niloticus). Aquaculture 247 (1-4), 203–210.
Ponzoni, R.W., Nguyen, N.H., Khaw, H.L., Hamzah, A., Abu Bakar, K.R., Yip Yee, H., 2011.
Genetic improvement of Nile tilapia (Oreochromis niloticus) with special reference
to the work conducted by the WorldFish Center with the GIFT strain. Reviews in
Aquaculture 3 (1), 27–41.
Quinton, C.D., McKay, L.R., McMillan, I., 2004. Strain and maturation effects on female
spawning tima in diallel crosses fo three strains of rainbow trout (Oncorhynchus
mykiss). Aquaculture 234, 99–110.
Quinton, C.D., McMillan, T.I., Glebe, B.D., 2005. Development of an Atlantic salmon (Salmo
salar) genetic improvement program: genetic parameters of harvest body weight and
carcass quality traits estimated with animal models. Aquaculture 247, 211–217.
Rutten, M.J.M., Bovenhuis, H., Komen, H., 2005. Genetic parameters for fillet traits
and body measurements in Nile tilapia (Oreochromis niloticus L.). Aquaculture
246 (1-4), 125–132.
Rye, M., Mao, I.L., 1998. Non additive genetic effects and inbreeding depression for
body weight in Atlantic salmon (Salmo salar L.). Livestock Production Science
57, 15–22.
Rye, M., Gjerde, B., Gjedrem, T., 2010. Genetic Development Programs for Aquaculture
Species in Developed Countries. 9th World Congress on Genetics Applied to Livestock
production, Leipzig, Germany, p. 8 August 1–6.
SAS, 1996. SAS’ Procedure Guide. “Version 6.12 Ed.”. SAS Institute Inc., Cary, NC, USA.
Thodesen (Da-Yong Ma), T., Rye, M., Wang, Y.X., Yang, X.S., Bentsen, H.B., Gjedrem,
T., 2011. Genetic improvement of tilapias in China: genetic parameters and se-
lection responses in growth of Nile tilapia (Oreochromis niloticus) after six gener-
ations of multi-trait selection for growth and fillet yield. Aquaculture 322–323,
51–64.
Wei, M., van der Werf, J.H.J. and Brascamp, E.W. 1991. Relationship between purebred
and crossbred parameters. II. Genetic correlation between purebred and crossbred
performance under the model with two loci. J. Anim. Breed. Genet. 108, 262–269.
Wohlfarth, G., Lahman, M., Hulata, G., Moav, B., 1980. The story of “Dor-70”, a selected
strain of the Israeli common carp. Isr. J. Aquacult. Bamidgeh 32, 3–5.
Wohlfarth, G., 1993. Heterosis for growth rate in common carp. Aquaculture 113, 31–46.