Very little is known about the genetic aspects of sexual
dimorphism of body weight in domestic sheep, and therefore this study was
conducted to quantify the genetic basis of sexual dimorphism for
early-growth-related traits in Afshari lambs. Traits evaluated included birth
weight (BW), weaning weight (WW), and growth rate (GR) in male and female
lambs. Male lambs were 6.6 % heavier at birth, had 14.4 % higher
preweaning growth rates and were 16.0 % heavier at weaning compared to
female lambs. Levels of sexual-size dimorphism (SSD), expressed as the ratio
of male to female means, for BW, WW and GR were 1.07, 1.14 and 1.15,
respectively, which indicated low levels of SSD in the traits studied. Fixed
effects of year of birth and type of birth interacted with sex effects, with
greater variability in birth and weaning weights among years and birth types
in male lambs, suggesting greater environmental sensitivity in the males.
Bivariate animal models and restricted maximum likelihood (REML) procedures were used to estimate phenotypic
variances and their genetic and non-genetic components in male and female
lambs. Estimates of the direct heritability (
Sexual-size dimorphism (SSD), i.e., size differences between conspecific males and females, is common in the animal kingdom and particularly marked in the mammalian species, both in wild and domestic populations (Milner et al., 2000; Poissant et al., 2008; Polak and Frynta, 2009, 2010; Gudex et al., 2009). The SSD is the outcome of combined effects of several factors such as specific selection pressure, sex-biased phenotypic and genetic variation, and it may also reflect an imperfect genetic correlation between sexes for body size (Badyaev, 2002). In a group of related species, SSD is often larger in larger species and decreases as the size of species decreases. This phenomenon is termed Rensch's rule (Rensch, 1950). In addition, in related species, SSD is normally more pronounced in wild, compared to domestic, species because of the reduced role of male combat in captive herds; the effect of reduced sexual segregation in captivity, where males usually graze together with females in mixed herds; and relaxed intrasexual selection as a result of the female-biased operational sex ratio (Polak and Frynta, 2009).
Pedigree structure of the Afshari sheep.
Characteristics of the data structure.
BW: birth weight; WW: weaning weight; GR: growth rate; SD: standard deviation; CV: phenotypic coefficient of variation.
The Afshari sheep breed is one of the heaviest and largest mutton breeds in Iran and is widely distributed in mountainous areas in the west of the country. Today, a large percentage of the Afshari sheep population is raised in Zanjan province. The Afshari is a fat-tailed, carpet-wool sheep with brown color and is primarily used for meat production (Eskandarinasab et al., 2010). In Afshari sheep, there are distinct differences in growth pattern between sexes: male lambs are heavier at birth, grow faster in all growth phases, and tend to be leaner than females. On average, mature Afshari rams are over 25 % heavier than mature ewes (66 vs. 53 kg).
Although SSD is apparent in domestic animals such as sheep (Gudex et al., 2009), goat (Polak and Frynta, 2009), pig (Dunshea, 2001), cattle (Polak and Frynta, 2010), rabbit (Eason et al., 2000) and chicken (Maniatis et al., 2013), little effort has been made to investigate its genetic basis and explore its potential use in sheep breeding programs. Accurate estimation of breeding values and the definition and realization of optimal multiple-trait selection response for each sex are challenges when SSD is present in sheep production, especially if heritabilities for measures taken on males and females are unequal and (or) genetic correlations between the sexes are less than unity (Gudex et al., 2009). For this reason, the present study was designed to investigate phenotypic and genetic differences in body weights between male and female Afshari lambs and estimate the genetic correlation between sexes.
The flock was established in 1998 and maintained as a closed flock. Animals
were maintained by the Department of Animal Science of the University of
Zanjan, Zanjan, Iran. The farm is located 1663 m above mean sea level and at
35
Data used for this study included body weight at birth (BW) and weaning weight (WW). Weaning weights were adjusted to 120 days of age by adding 120 times the preweaning average daily gain to birth weight. The total weight gain from birth to weaning was calculated and subsequently used to calculate the growth rate (GR) as total gain divided by the age at weaning. Tables 1 and 2, respectively, show the characteristics of the pedigree and data used in the analyses. As shown, the quality of pedigree was high. All dams were recorded, and only five animals had unknown sires.
The SSD was expressed using the Lovich and Gibbons ratio (Lovich and
Gibbons, 1992) of M
To identify fixed effects, least-squares analyses were conducted using the General Linear Model (GLM) procedure (SAS, 2004) with a model that included fixed effects of year of birth; age of dam at lambing; type of birth; and sex–year-of-birth, sex–type-of-birth and sex–age-of-dam-at-lambing interactions. In bivariate analyses the effect of sex of lambs together with the corresponding interactions were dropped from the model. Multiplicative adjustment factors to correct traits measured in twins and triplets to a single-lamb basis were calculated by dividing least-squares means of traits measured in single lambs to similar traits measured in twins and triplets. (Co)variance components and genetic parameters were estimated using the DFREML program of Meyer (2000). Recorded traits were related to early growth, and maternal effects were therefore expected to be important. Maternal effects can arise from additive genetic differences expressed in related dams, permanent environmental maternal effects associated with repeated lambings, and litter effects associated with full-sib littermate lambs. However, separation of these different sorts of maternal effects is difficult, requiring deep and well-structured pedigrees with relatively large groups of half-sib dams, reasonably large numbers of lambings by individual dams, and substantial numbers of twin and triplet litters. In particular, estimation of separate genetic parameters for lambs of each sex in our study halved the average numbers of progeny per dam and per litter, which would further complicate partitioning of maternal effects. Albuquerque and Meyer (2001) reported that fitting only an additive genetic or permanent environmental maternal effect generally accounted for the total maternal variation arising from both sources. The component that should be fitted would be the “one which is less sensitive to data structure” and would normally be the maternal permanent environmental effect. Also, for our data, litter effects could only be estimated from litters containing two or more lambs of the same sex. These restrictions led us to conclude that a model that only included additive direct and maternal permanent environmental effects was most appropriate for these data.
We first fitted a univariate animal model including lambs of both sexes, and
with sex effects included in the model, to provide baseline estimates of
variance components and genetic parameters under the assumption that sex
effects do not influence these parameters. Following this, a bivariate model
was fitted including observations on males and female lambs as different
traits. The bivariate model was
Least-squares means
BW: birth weight; WW: weaning weight; GR: growth rate; means within a
factor and column that do not have a common superscript are significantly different
(
Least-squares means (
Type of birth had significant effects on body weight in both sexes (
Least-squares means
BW: birth weight; WW: weaning weight; GR: growth rate; means within a
factor and column that do not have a common superscript are significantly different
(
The age of the dam at lambing affected (
As shown in Table 2, male lambs were 6.6 % heavier at birth, had 14.4 %
higher growth rates, and consequently were 16.0 % heavier at weaning
compared to female lambs. The M
Estimates of variance components and genetic parameters from a univariate analyses with both sexes included and with fitting of a fixed effect of lamb sex.
Log L: the logarithm of the converged likelihood function;
Estimates of variance components and genetic parameters in male and female lambs.
Differences between male and female lambs reflect difference in the endocrine environment, and associated differences in nutrient requirements, between the sexes. Regulatory mechanisms controlling growth hormone (GH) secretion are sexually dimorphic (Gatford et al., 1996; Jaffe et al., 1998). Gatford et al. (1996) reported that sex significantly affected patterns of changes in circulating growth hormone, IGF-I (insulin-like growth factor), and IGFPB-3 (insulin-like growth factor binding protein) concentrations in growing prepubertal lambs. Mean plasma GH concentrations, GH pulse amplitude, and integrated plasma GH concentrations were greater in rams than in ewes at a variety of different ages. They concluded that differences in circulating patterns and concentrations of GH, IGF-I, and IGFBP-3 may arise from the action of steroids during sexual differentiation and before puberty. Steroids such as testosterone and estrogen affect the growth of males and females differentially. In males, testosterone is produced in large quantities, whereas in females estrogen and progesterone predominate. Testosterone stimulates muscle growth by affecting the rate of protein synthesis, protein breakdown, and the net gain or loss of muscle protein (Mateescu and Thonney, 2002). In addition, exposure to high estrogen levels limits growth of long bones and consequently affects body size in females.
Results of univariate animal models including data from lambs of both sexes
are shown in Table 5. Heritability estimates for BW, WW, and GR were 0.32,
0.17, and 0.12, respectively. Maternal permanent environmental effects
(
Estimates of variance components and genetic parameters from the bivariate
analysis are presented in Table 6. In most cases, estimates of additive
genetic variances were higher in females, while estimates of maternal
permanent environmental and residual variances were higher in males. As
expected, results from the univariate model in Table 5 were generally
intermediate to, but not simple averages of, the sex-specific estimates in
Table 6, indicating that differences between the sexes are reflecting
variation in overall (co)variance structures. Our results regarding additive
genetic variance were in agreement with Gudex et al. (2009) – who estimated
greater additive genetic variance in females than males for weaning and
post-weaning body weights in Australian Coopworth, Poll Dorset and White
Suffolk sheep breeds – but contradicted Milner et al. (2000), who found higher
additive genetic variance in male lambs for body weight, hind leg length and
incisor breadth in a free-living population of Soay sheep. High values for
Estimates of
Genetic (
Correlations between random effects estimated in different sexes.
If the traits of interest were controlled by genes that are differently
expressed in lambs of the two sexes, the
Departure of
In conclusion, male lambs were heavier at birth, grew more rapidly to weaning, and were therefore heavier at weaning compared to female lambs. Effects of lamb sex on weaning weight and preweaning rate of gain interacted with effects of birth year and birth type. These interactions, and the generally greater residual and maternal variances observed for male lambs, suggest greater environmental sensitivity of male, compared to female, lambs. Additive genetic variances for preweaning gains and weaning weights were somewhat larger in female lambs. However, additive genetic correlations for body weight traits between male and female lambs were large, suggesting that these traits were controlled by similar genes. Opportunities for sex-specific selection to create or modify sexual-size dimorphism in sheep therefore appear limited and cannot be used to diverge phenotypes for body weights between the sexes.
We thank M. P. Eskandarinasab, the head of the Department of Animal Science of the Zanjan University and H. S. Mohammadi, the manager of the Afshari sheep experimental flock, who provided us the data used in this study. Also, we wish to thank two anonymous referees for their comments and suggestions. Edited by: A.-E. Freifrau von Tiele-Winckler Reviewed by: two anonymous referees