317

ARTICLE
Genetic correlations for reproductive and growth traits
in rabbits
Rym Ezzeroug, Rafik Belabbas, Maria José Argente, Ali Berbar, Samir Diss, Zoulikha Boudjella,
Djamal Talaziza, Nassima Boudahdir, and Maria de la Luz García

Abstract: The objective of this study was to obtain heritability estimates for reproductive (litter size at birth,
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number born alive, litter size at weaning) and growth traits (individual weaning weight, individual weight at the
end of the fattening period), then determine the genetic correlation between them in a synthetic rabbit line.
A total of 805 females, 3242 parities, and 18 472 growth records were measured from 2006 to 2017. A pentavariate
animal model was used with reproductive and growth traits. Heritability ranged from 0.025 to 0.126 for reproduc-
tive traits and from 0.033 to 0.059 for growth traits. These traits showed a large coefficient of variation (from 32% to
56% for reproductive traits and from 21% to 28% for growth traits). The repeatability of reproductive traits was low
and the common litter effect for growth traits was the most important component of total variance. The genetic
and phenotypic correlations between reproductive and growth traits were high and negative, especially with
weight at weaning (−0.848, −0.922, and −0.854 for litter size at birth, number born alive, and litter size at weaning,
respectively). In conclusion, because of the high negative correlation between reproductive and growth traits,
both reproductive and growth traits should be selected in independent lines and the response to selection should
For personal use only.

be due mainly to the high coefficient of variation of the traits.

Key words: genetic correlation, heritability, litter size, weaning weight, rabbits.
Résumé : Le but de cette étude est d’estimer l’héritabilité des caractères de reproduction (la taille de la portée à la
naissance, le nombre des nés vivants, la taille de la portée au sevrage) et de ceux de croissance (le poids individuel
au sevrage et à la fin de la période d’engraissement). Les données concernant 805 femelles, 3242 parités et 18 472
individus en croissance ont été enregistrées de 2006 à 2017. Un modèle avec 5 effets fixes a été utilisé pour l’analyse
de l’ensemble des paramètres de reproduction et de croissance. L’héritabilité a varié de 0,025 à 0,126 pour les
caractères de reproduction et de 0,033 à 0,059 pour les caractères de croissance. Ces caractères présentaient un
coefficient de variation élevé (de 32 % à 56 % pour les caractères de reproduction et de 21 % à 28 % pour les
caractères de croissance). La répétabilité des paramètres de reproduction était faible et l’effet commun de la
portée était la plus importante composante de la variance totale. Les corrélations génétiques et phénotypiques
entre les paramètres de reproduction et ceux de croissance sont fortes et négatives, en particulier avec le poids
au sevrage (−0,848, 0,922 et 0,854 pour la taille de la portée, le nombre des nés vivants et la taille de la portée au
sevrage, respectivement). En conclusion, en raison de la forte corrélation négative entre les caractères de reproduc-
tion et de croissance, les caractères de reproduction et de croissance doivent être sélectionnés dans des lignées
différentes et la réponse à la sélection doit être due principalement aux coefficients de variation élevés de ces
caractères.
Mots-clés : corrélations génétiques, héritabilité, lapin, poids au sevrage, prolificité.

Received 3 March 2019. Accepted 14 November 2019.

R. Ezzeroug, R. Belabbas, and A. Berbar. Laboratoire des Biotechnologies liées à la Reproduction Animale, Institut des Sciences
Vétérinaires, Université BLIDA1, B.P 270, Route de Soumaa, 09000, Blida, Algerie.
M.J. Argente and M.L. García. Departamento de Tecnología Agroalimentaria, Universidad Miguel Hernández de Elche, Ctra. Beniel km
3.2, 03312 Alicante, Spain.
S. Diss, Z. Boudjella, D. Talaziza, and N. Boudahdir. Technical institute for Animal Production (ITELV), B.P 03, Birtouta, Algiers,
Algeria.
Corresponding author: Rym Ezzeroug (email: arymvet@hotmail.com).
Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.

Can. J. Anim. Sci. 100: 317–322 (2020) dx.doi.org/10.1139/cjas-2019-0049 Published at www.nrcresearchpress.com/cjas on 5 December 2019.
 318
Introduction
Traditionally, intensive rabbit production for meat is
based on the three-way crossbreeding scheme. The hybrid
doe comes from the cross of two maternal lines so as to
exploit heterosis and the complementarity of the mater-
nal traits (Baselga 2004). Maternal lines are selected for lit-
ter size at birth or at weaning (Piles et al. 2006; Ragab and
Baselga 2011), while the terminal sire line is selected for
improvement of feed efficiency through either selection
for growth rate post weaning or for body weight
approaching market age (Piles and Blasco 2003; Larzul
et al. 2005). Although this scheme involves the mainte-
nance of three lines of rabbits, one of the primary
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challenges in animal production is sufficient and
cost-effective meat production. Thus, other selection
schemes could be proposed to develop a more efficient
production scheme. In this sense, new selection strategies
for countries with hot climates have been proposed and
new synthetic lines have been developed by crossbreed-
ing between exotic maternal lines and local breeds with
the aim of providing farmers with more productive ani-
mals adapted to heat stress (Iraqi et al. 2010; Khalil 2010)
and to exploit the effect of heterosis (Reddy et al. 2003).
To provide solid support for rabbit genetic evaluation
For personal use only.
programmes, it is crucial to estimate variance compo-
nents for reproductive and growth traits. However, the
estimates of genetic correlation between reproductive
and growth traits are scarce and contradictory (Gomez
et al. 1998; García and Baselga 2002b). Thus, the aim of
this study was to estimate the heritability and the
genetic correlation for reproductive and growth traits
in a synthetic rabbit line.
Materials and Methods
This study was approved by the scientific council of
the Biotechnology Laboratory of Animal Reproduction,
part of the Institute of Veterinary Sciences at the
University of Saad Dahleb Blida (Blida, Algeria).
Animals
The animals came from the ITELV2006 synthetic line.
This line was created as a part of co-operative rabbit
project between the Institute of Animal Breeding (ITELV,
Algeria) and INRA (France). The F1 was created by insemi-
nating does from a local Algerian rabbit population
(see more characteristics of this population in Zerrouki
et al. 2005) with the semen of bucks from INRA2666,
which itself is a synthetic strain (Brun and Baselga 2004).
The breeding programme was previously described by
Gacem and Bolet (2005). The F1 offspring were distributed
among nine families consisting of nine females and two
to four males each. The F2, F3, and F4 were produced
using a system of rotation between families without
selection in order to minimise inbreeding. Selection
for live litter size at birth and body weight at 75 d
was then applied for three generations (Bolet et al.
2012). Subsequently, the line has been maintained in
Can. J. Anim. Sci. Vol. 100, 2020
discrete generations without selection and by avoiding
inbreeding.
Housing and feeding
Animals were housed in buildings equipped with
wired flat-deck cages ventilated with a cooling system.
They were kept under a consistent photoperiod of
16L:8D (light:dark hours). Females were mated first at
20 wk of age and at day 10 after parturition. Kits were
weaned between 25 and 48 d of age. All animals were
weighed, sexed, and identified, then placed in collective
cages housing eight rabbits in each cage. Rabbits were
again weighed individually at the end of the fattening
period at 75 d of age (ranged from 58 to 88 d). Rabbits
were fed a standard commercial pelleted diet ad libitum
(16% crude protein, 15% crude fibre, and 2.6% ether
extract) and had free access to water.
Traits recorded and statistical analyses
A total of 3242 parities from 805 females and 18 472
growth records (Table 1) from 2006 to 2017 were analysed.
The pedigree file included 18 695 individuals. The traits
studied were litter size at birth, number born alive, litter
size at weaning, individual weaning weight (WW), and
individual weight at the end of the fattening period (WS).
Variance and covariance components were estimated
using the derivative-free, multiple-trait maximum
likelihood procedure in VCE software, version 6.0.2
(Neumaier and Groeneveld 1998). A pentavariate animal
model was used with reproductive and growth traits.
The mixed model used for reproductive traits was as
follows:
yijk = μ + YSi + RSj + ak + pk + eijk
where yijk is the reproductive trait of animal k; μ is the
general mean; YSi is the fixed effect of year-season of par-
ity (3 mo per each year-season: 38 levels); RSj is the fixed
effect of reproductive status at mating (seven levels:
nulliparous animals, lactating and non-lactating
primiparous animals, lactating and non-lactating at
third effective mating of the animals, lactating and
non-lactating at fourth or more effective mating of the
animals); ak is the additive genetic value of the animal
k; pk is the permanent environmental and non-additive
genetic effect of the animal k over all its parities
(805 levels); and eijk is the residual effect.
Growth traits were analysed with the following mixed
linear model:
yijkl = μ + b × Aijk + YSW i + POj + mk + cijk + aijkl + eijkl
where yijkl is the growth trait of animal l; μ is the general
mean; Aijk is the covariate age at weaning for WW or age
at slaughter for WS, and b is the regression coefficient on
this covariate; YSWi is the fixed effect of year-season in
which the animal was weaned (3 mo per each year-
season: 34 levels); POj is the fixed effect of parity order
Published by NRC Research Press
 Ezzeroug et al. 319

Table 1. Summary descriptive statistics of the traits in hot climates (9.0 kits vs. 6.9 kits and 7.1 kits; Sid et al.
analysed in rabbits. 2018; Belabbas et al. 2016) and slightly lower than in
European maternal lines (9.0 kits vs. 11.1 kits and 10.7 kits;
LSB NBA NW WW (g) WS (g)
Ragab and Baselga 2011; Theau-Clément et al. 2012). The
No. 3242 3242 3238 18 472 14 781 synthetic line showed similar litter size at weaning as
Minimum 1 0 0 145 600 local populations (Sid et al. 2018) but was lower than
Maximum 19 17 13 1280 3055
European maternal lines (Ragab and Baselga 2011; Theau-
Mean 9.0 8.1 5.5 554 1665
SD 3.0 3.3 3.1 156 349 Clément et al. 2012). Coefficient of variation of litter size
CV (%) 32 41 56 28 21 increased from birth to weaning (32%–56%), in accordance
with Ragab and Baselga (2011). Weight at weaning was 12%
Note: No., number of data; SD, standard deviation; higher than in other maternal lines (García and Baselga
CV, coefficient of variation; LSB, total litter size at birth;
2002a). Zorrouki et al. (2014) reported high lactating per-
NBA, number of rabbits born alive; NW, number of rabbits
weaned; WW, weight of rabbits at weaning; WS, weight at
formances in this synthetic line. However, the adverse
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the end of the fattening period.
in which the animal was born (seven levels: 1st–7th
parity); mk is the environmental maternal random effect
of the overall parities (animal k is the dam of the individ-
ual l: 760 levels); cijk is the random effect of the common
litter in which the animal l was born (2460 levels); aijkl is
the random additive genetic value of the animal l; and
eijkl is the residual effect.
Heritability (h2) was defined as the ratio between the
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effect of heat stress on growth rates during the fattening
period is well known (Pla et al. 1994), which would explain
a lower weight at the end of fattening in our synthetic
line than in European maternal lines (−9%) (García and
Baselga 2002b) despite the fact that the fattening period
concludes at 63 d in these lines.
Genetic parameters
Heritability for litter size was low and decreased from
birth to weaning (Table 2). The estimates were 0.126 for
total litter size at birth, 0.054 for number born alive,

additive effect variance and the phenotypic variance,
calculated as the sum of variances of the random effects
and the error. Permanent effect (p2) was defined as the
ratio between permanent environmental and non-
additive genetic effect variance and the phenotypic vari-
ance. Common litter effect (c2) was defined as the ratio
between the common litter effect variance and the
phenotypic variance. Maternal effect (m2) was defined as
the ratio between the environmental maternal effect
variance and the phenotypic variance.
The distribution for additive genetic effects was
N (0, A⊗Ga), where A was the additive genetic relation-
ship matrix and Ga was the genetic (co)variance matrix
between the traits. Environmental maternal effects
(m k ) of growth traits and permanent environmental
effect of the doe (p k ) on reproductive traits are
correlated. The distribution for the pk and the mk was N
(0, I⊗G p ), where G p was the (co)variance matrix
between these effects. There is a correlation between
the residual term of the reproductive traits and the
common litter effect (c ijk) of the growth traits (García
and Baselga 2002b; Mínguez et al. 2016), so an environ-
mental covariance structure between growth traits
and reproductive traits was established. The residual
distributions were N (0, Iσ2e). The order of the identity
matrix I was equal to the number of records measured
in each case.
Results and Discussion
Descriptive analysis
Table 1 shows raw means and standard deviations for
reproductive and growth traits. Litter size at birth in our
synthetic line was higher than in local populations reared
and 0.025 for number of weaned. Heritability estimates
for litter size traits vary considerably in the literature,
from low to moderate values. Our estimates were similar
to those reported by Gomez et al. (1998), Rastogi et al.
(2000), and Nguyen et al. (2017), higher than those of
García and Baselga (2002a) and Piles et al. (2006), and
lower than those of García and Baselga (2002c),
Mantovani et al. (2008), and Lenoir and Garreau (2009).
The estimates of the ratio between the variance of non-
additive genetic effects plus permanent environmental
effects and the phenotypic variance (p 2) for litter size
were low but different from zero, with values ranging
from 0.052 to 0.087. Repeatability estimates were 0.178
for total litter size at birth, 0.141 for number born alive,
and 0.087 for number weaned. Note that when repeat-
ability is low, several litter sizes of the female should be
recorded to increase the accuracy in the genetic evalu-
ation under a repeatability model. A selection index for
litter size at different parities considered as different
traits could be considered, taking into account that
genetic correlations are less than 0.8 between litter size
at first, second, and subsequent order parities in differ-
ent maternal lines (Piles et al. 2006). However, Piles
et al. (2006) concluded that the response to selection
would probably be the same if selecting for litter size
under a repeatability model, or using a selection index
for litter size at different parities considered as different
traits, because the accuracies of predicted breeding value
under the two models are almost equal.
Heritability estimates for growth traits were low
(Table 2); 0.033 for WW and 0.059 for WS. Rochambeau
(1998) reported heritabilities for WW equal to 0.08 and
0.09 for two lines selected over 18 generations for
Published by NRC Research Press
 320 Can. J. Anim. Sci. Vol. 100, 2020

Table 2. Estimates of h2, p2, m2, and c2 with their standard errors in rabbits.
LSB NBA NW WW WS
h2
0.126 ± 0.026 0.054 ± 0.017 0.025 ± 0.011 0.033 ± 0.013 0.059 ± 0.020
p2 0.052 ± 0.022 0.087 ± 0.019 0.062 ± 0.016 — —
m2 — — — 0.072 ± 0.014 0.081 ± 0.013
c2 — — — 0.636 ± 0.039 0.381 ± 0.018
Note: h2, heritability; p2, ratio between the variance of non-additive plus permanent
environmental effects and the phenotypic variance; m2, ratio between the
environmental maternal effect variance and the phenotypic variance; c2, ratio between
the common litter effect variance and the phenotypic variance; LSB, total litter size at
birth; NBA, number of rabbits born alive; NW, number of rabbits weaned; WW, weight
of rabbits at weaning; WS, weight at the end of the fattening period.
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Table 3. Estimates of genetic correlations above the diagonal and phenotypic

correlations below the diagonal for the studied traits in rabbits.
LSB NBA NW WW WS
LSB — 0.896 ± 0.069 0.280 ± 0.195 −0.848 ± 0.161 −0.432 ± 0.164
NBA 0.820 — 0.677 ± 0.166 −0.922 ± 0.047 −0.765 ± 0.141
NW 0.404 0.599 — −0.854 ± 0.179 −0.991 ± 0.031
WW −0.057 −0.051 −0.025 — 0.611 ± 0.123
WS −0.011 −0.021 −0.023 0.631 —
Note: LSB, total litter size at birth; NBA, number of rabbits born alive; NW, number
For personal use only.

of rabbits weaned; WW, weight of rabbits at weaning; WS, weight at the end of the
fattening period.

litter size at birth and at weaning, respectively. García
and Baselga (2002b) obtained higher heritability in
another maternal line (0.224 for weight at weaning and
0.302 for weight at 63 d). The environmental maternal
effect (m 2 ) had higher estimates than heritabilities
(0.072 for WW and 0.081 for WS). The common environ-
mental effect of litter (c 2 ) explained a greater part of
phenotypic variance and was 0.636 for WW and 0.381
for WS. These estimates were higher than their additive
and m 2 variance and this tendency agrees with the
results reported by Su et al. (1999) and García and
Baselga (2002b). Moreover, there is evidence that
common litter effect decreases over time, so the
estimates are higher for growth at weaning than at the
end of the fattening period (Su et al. 1999; García and
Baselga 2002b).
Response to selection is directly proportional to the
intensity of selection, to the heritability, and to the stan-
dard deviation of the traits (Falconer and Mackay 1996).
Therefore, due to the low heritability estimates for both
reproductive and growth traits, it is expected that the
response to selection should be mainly due to the high
coefficient of variation.
Correlations
The genetic and phenotypic correlations were similar
in sign and magnitude in both reproductive and growth
traits (Table 3). The genetic correlations for litter size at
birth and the number born alive were positive and
high with the number of weaned rabbits. Similar results
were observed by Ragab and Basalga (2011). Moreover,
weight at weaning was positive and highly correlated
with weight at slaughter, a finding in agreement with
Hanaa et al. (2014).
Litter size at birth, number born alive, and the number
of weaned rabbits were negative and highly correlated
with growth traits, especially with WW (−0.848, −0.922,
and −0.854 for litter size at birth, number born alive,
and litter size at weaning, respectively). The results are
in agreement with Gomez et al. (1998) for traits measured
at first parity in a maternal line. García and Baselga
(2002b) reported a correlation between litter size at wean-
ing and growth traits close to zero, whereas Camacho
and Baselga (1990) showed positive correlations
measured in lines selected for daily gain. Indeed, it was
reported that increases in litter size related to the
selection on prolificacy resulted in a decrease of individ-
ual weight at weaning (Rochambeau et al. 1994; Bolet
1998; Poigner et al. 2000).
Moura et al. (2001) indicated that in countries where
the rabbit industry has not yet reached a high level of
organisation, it may not be possible to implement the
three-way crossbreeding scheme. They proposed that an
alternative approach could be the development of a
multi-purpose line, achieved through simultaneous
selection for litter size and growth traits. In our case, this
methodology is not recommended due to the high
negative genetic correlation between these traits.
Published by NRC Research Press
 Ezzeroug et al.
We concluded that genetic correlation between repro-
ductive and growth traits is negative; it is recommend-
able to select them in independent lines; and the
expected response to selection should be mainly due to
the high coefficient of variation of the traits.
Acknowledgements
We are very grateful to the ITELV and especially to
Ghania Zitouni, Director of the Monogastric
Department, for her valuable contribution to this study.
Declaration of interest
The authors declare that they have no competing
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interests.
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