Inbreeding effects on body weight traits of Iranian Moghani sheep

The objective of the present study was to evaluate the effects of inbreeding on body weight at different ages in Moghani sheep. Traits included were birth weight (BW), 3-month weight (3MW), 6-month weight (6MW), 9-month weight (9MW), and yearling weight (YW). Data and pedigree information used in this study were collected at the Breeding Station of Moghani sheep, Iran during 1987-2005. All the animals were grouped into three classes according to the inbreeding coefficients obtained by their pedigree: the first class included non-inbred animals (F=0 %); and the second and third classes included inbred animals (0<F≤0.10 and F>0.10, respectively). Average inbreeding rate was 2.93 % in the pedigree of Moghani sheep. The BW of animals within second class of inbreeding was significantly higher than those of lambs belonging to the third class (P<0.05). The 3MW of animals within third class of inbreeding was significantly (P<0.05) higher than those of lambs belonging to the first and second classes. The 6MW of animals within third class of inbreeding was significantly (P<0.05) lower than those of lambs belonging to the first and second classes. Animals within third class of inbreeding had greater mean of 9MW than two other groups (P<0.05). Also, the YW of animals within second class of inbreeding was significantly (P<0.05) lower than those of lambs belonging to the first and third classes. The utilization of designed mating system could be a suitable approach to maintain the level of inbreeding under control.


Introduction
One definition for inbreeding is given by the mating of individuals whose relatedness between them is greater than the average degree of relationship existing in the population (Lush 1945), and capable of changing the genotypic frequencies of a population without modifying the gene frequencies.Most inbreeding results from the intensive use of a few breeding animals, where the selection intensity is high.Thus, a small number of seedstock, with a strong family relationship, is responsible for the maintenance of almost the whole genetic pool in the population.This is an aspect of great influence in the genealogical analysis of a population structure, because of its effect on the probability of genes lost between generations and the consequent reduction in genetic variability (Pedrosa et al. 2010).
Heterozygosity and allelic diversities can be lost from small, closed, selected populations at a rapid rate.The loss of diversity and resulting increase in homozygosity may result in decreased productions and/or fitness of inbred animals.Furthermore, inbreeding depression in domestic animals can lead to a decrease in selection response and in potential genetic gains in economic traits.Measurement of the effect of inbreeding on these traits is important in order to estimate the magnitude of change associated with increases in inbreeding.The inbreeding depression has been well documented in many populations for a variety of traits (Lamberson & Thomas 1984, Ercanbrack & Knight 1991, Analla et al. 1998, Dario & Bufano 2003, Khan et al. 2007, Van Wyk et al. 2009).Inbreeding impairs growth, productions, health, reproduction traits (such as fertility) and survival.The emergence of disorders due to recessive gene action may also occur.It is apparent that different breeds and populations, as well as different traits vary in their response to inbreeding.Some populations may show a very pronounced effect of increased inbreeding for a trait, whereas others may not demonstrate much of an effect (Negussie et al. 2002, Barczak et al. 2009).
The rate of inbreeding needs to be limited to maintain diversity at an acceptable level so that genetic variation will ensure that future animals can respond to changes in the environment and to selection.Without genetic variation, animals cannot adapt to these changes (Van Wyk et al. 2009).The objective of this study was to evaluate the effects of inbreeding on different weights of Iranian Moghani sheep over a 19-year period from 1987 to 2005.

Data and pedigree information
Moghani breed, numbering about 5.5 million, is one of the most important meat breeds among Iranian sheep.They are well-known for their large size, tolerance to climatic changes and capability to produce heavy lambs (Shodja 2006).The breed is fat-tailed, its coat colour is predominantly white and its face, legs and feets are brown.In this breed, both sexes are polled.A breeding station of Moghani breed was established in 1952 in Ardebil province of Iran in order to genetically improve the performance of Moghani sheep, through identifying the best rams and distributing them to the commercial flocks.Body weights at birth, weaning and at higher ages were sometimes considered as criteria in selection of replacements.Data and pedigree information used in this study were collected at the breeding station of Moghani sheep from 1987 to 2005.The included traits were: birth weight (BW), 3-month weight (3MW), 6-month weight (6MW), 9-month weight (9MW), and yearling weight (YW).The CFC program (Sargolzaei et al. 2006) was used to calculate pedigree statistics and regular inbreeding coefficients for individuals in the pedigree.The number of animals (in total), inbred animals, sires, dams, founders and non founders in the pedigree of Moghani sheep were 8 494, 1 060, 625, 2 828, 1 835 and 6 659, respectively.Also, there were totally 1 210 full-sib groups with average family size of 2.12 in the pedigree of Moghani sheep.On the basis of individual inbreeding coefficient, all the animals were grouped in three classes: first class including non-inbred animals (F=0); second and third classes including inbred animals (0<F≤0.10 and F>0.10, respectively).The incidences of triplets and quadruplets were so low (<0.8 %) that records from lambs born in triplet and quadruplet litters were discarded.

Statistical analysis
The effects of inbreeding rate on body weight traits were analysed using the linear mixed model (Proc Mixed) with the best fitted covariance structure of SAS 9.1 (SAS Institute Inc., Cary, NC, USA).The least-squares means were estimated by restricted maximum likelihood (REML) method.Level of significance for the inclusion of effects into the model of analysis was declared at P<0.05.The final model included the fixed class effects of year-season (76 levels), inbreeding class, sex of lamb, parity of dam, litter size (single and twin), age of dam (from 2 through 7 years old) and random effect of animal.All the interactions of first order were included in the preliminary models, but only sex by parity, litter size by inbreeding class, sex by inbreeding class and litter size by parity interaction effects were kept in the final models.Trend of inbreeding was estimated using the linear regression of individual inbreeding on birth year.Also, inbreeding depression was estimated as the regression of body weight traits on the individual inbreeding coefficients.

Results
The analysis of pedigree revealed that inbreeding rate ranged from 0 to 28.13 % with an average of 2.93 %. Figure 1 shows the average of inbreeding coefficients over years.The trend of inbreeding was significantly positive over the years (P<0.05) and its estimate was 0.027±0.011.Table 1 shows the summary statistics for body weight traits in different inbreeding classes of animals.The BW of animals within second class of inbreeding was higher than those of lambs belonging to the first and third classes, but only differences were Distribution of inbreeding rate, % over the years significant only between second and third classes (P<0.05).The 3MW of animals within third class of inbreeding was significantly (P<0.05)higher than those of lambs belonging to the first and second classes but there was no significant differences between the first and second classes of inbreeding.On the other hand, the 6MW of animals within third class of inbreeding was significantly (P<0.05)lower than those of lambs belonging to the first and second classes.There were significant differences between three classes of inbreeding on 9MW and animals within third class of inbreeding had greater mean of the trait than two other groups (P<0.05).Also, the YW of animals within second class of inbreeding was significantly (P<0.05)lower than those of lambs belonging to the first and third classes.Single-or twin-born lambs showed no significant differences in their BW and YW irrespective of the inbreeding rate (Table 2).In addition, single-born lambs showed no significant differences in their 3MW.But twin-born lambs in the third class of inbreeding had greater 3MW than those of twin-born lambs belonging to the first and second classes (P<0.05).
Although twin-born lambs showed no significant differences in their 6MW and 9MW, singleborn lambs in the third class of inbreeding showed significant differences on 6MW and 9MW with lambs belonging to the second class (Table 2).Male lambs showed no significant differences in their BW, 9MW and YW irrespective of the inbreeding rate (Table 3).The 3MW and 6MW of male lambs within third class of inbreeding was significantly higher than those of male lambs belonging to the first and second classes (P<0.05).Female lambs showed no significant differences in their 3MW irrespective of the inbreeding rate.The BW and 9MW of female lambs in third class of inbreeding were significantly different with those of two other groups (P<0.05).The 6MW of female lambs within first class of inbreeding was significantly (P<0.05)greater than that of female lambs belonging to the second class.On the other hand, the YW of female lambs within third class of inbreeding was significantly (P<0.05)greater than that of female lambs belonging to the second class.Table 4 shows the regression coefficients of body weights on inbreeding of lambs for a change of 1 % in inbreeding.There were trends for significance for the regression coefficients of BW and YW on inbreeding of all lambs.The regression coefficients of birth and yearling weights on lamb inbreeding were estimated to be −0.009±0.005and −0.159±0.095(P<0.08),respectively, then birth and yearling weights decreased respectively by 0.009 kg and 0.159 kg due to 1 % increase in inbreeding.The regression coefficient of 3MW on inbreeding of lambs for change of 1 % in inbreeding was positive and non significant, but the coefficients of 6MW and 9MW were negative and non significant.Considering the birth type, the regression coefficient of 3MW on inbreeding of twin-born lambs was significantly positive (0.129±0.057,P<0.01).Therefore, 3MW of twins increased 0.129 kg due to 1 % increase in inbreeding.There were trends for significance for the regression coefficients of YW in single-born lambs and BW in twin-born lambs and their corresponding values were −0.183±0.105and −0.012±0.006,respectively (P<0.10).Also, considering the sex of lambs, the 3MW and YW of male lambs increased and decreased respectively by 0.126 kg (P<0.01) and 0.357 kg (P<0.05)due to 1 % increase in inbreeding.On the other hand, the BW and 6MW of female lambs decreased respectively by 0.025 kg (P<0.01) and 0.234 kg (P<0.01)due to 1 % increase in inbreeding.

Discussion
The inbreeding level estimates are strongly determined by the two main factors: depth and completeness of pedigree and selection intensity.Selection intensity is often increased by the reproductive technologies being focused on a few superior animals (especially sires) and the application of advanced methods of genetic evaluation.A high inbreeding level is observed for populations rebuilt from small number of founders, but on the other hand in this case the accuracy is strongly determined by the incompleteness of pedigrees (Barczak et al. 2009).Consistent with the result of this study, Pedrosa et al. (2010)  The rapid increase in the rate of inbreeding in 1994 and 1998 could be resulted from the decrease in the number of sires.Also, some animals of the studied population had presented high levels of inbreeding, reflecting the intensive use of few sires.Similar to the current results, Barczak et al. (2009) reported positive trend for inbreeding over the years.
There are several methodological and biological factors which determine the estimated inbreeding impact on performance traits.It is well known that both negative effects and positive ones exist.Hence, in a given population, »bad« and »good« inbreeding effects are mixed (Barczak et al. 2009).Similar to the current results, Van Wyk et al. (1993) who observed a reduction of 0.008 kg in BW for a 1 % increase of inbreeding in Dormer sheep, Ercanbrack and Knight (1991) who found a mean value of −0.010 kg, Khan et al. (1995) and Mirza et al. (1999) who reported a regression coefficient of −0.008 and −0.007 respectively.Also, similar to the present study, Barczak et al. (2009) reported for sheep of eight lines and breeds an average estimate of −0.0095 kg.MacKinnon (2003) obtained inbreeding depression results of −0.012 kg for crossed sheep and Van Wyk et al. (2009), −0.006 kg for the Elsenburg Dormer sheep breed.Causes of variation in inbreeding effects could be due to differences among breeds in alleles segregating, amount of genetic variation in the base population, location, management, and diversity of the founders in the flocks tested (MacKinnon 2003).
Similar to the current results, Lamberson & Thomas (1984) reported no significant reduction of 3MW due to inbreeding in different breeds of sheep.The 3MW of twins and or male lambs was increased due to 1 % increase in lamb inbreeding rate and inconsistent with the current result, Van Wyk et al. (2009) and Selvaggi et al. (2010) reported significant reduction in 3MW of lambs due to 1 % increase in inbreeding.Lamb sex was a significant effect in the current analysis of inbreeding, but it should be noted that negligible differences between males and females was observed in the study of Barczak et al. (2007).Barczak et al. (2009) reported positive inbreeding effects on fourth week weight in a multi-breed sheep population.Also, the 6MW of female lambs was reduced 0.234 kg per 1 % increase in inbreeding and similar to this result Pedrosa et al. (2010) reported a decrease of 0.204 kg in weight at 180 days due to 1 % increase in inbreeding.To my knowledge, there was no published report regarding to the effect of inbreeding on YW, but the results of this study indicated a significant reduction in YW of male lambs (0.357 kg) and a trend for significance for the effect of inbreeding on the YW of all lambs.The explanation for the strong inbreeding depression observed for YW in this study was the lower heritability of this trait compared to other weight traits of Moghani sheep (Ghavi Hossein-Zadeh & Ardalan 2010), since traits of low heritability tend to show less additive genetic variation and more dominance deviation than more heritable traits (Lamberson & Thomas 1984).
In conclusion, average inbreeding rate was 2.93 % in Iranian Moghani sheep and an increasing trend for inbreeding was observed over the years.Both positive and negative inbreeding effects were found in the current study.From the results of this study it can be seen that there was a trend for the negative effects of inbreeding on the BW and YW of all lambs but the regression coefficients of other body weight traits on inbreeding of all lambs for a change of 1 % in inbreeding were not significant.The results of this study indicated a significant reduction in YW of male lambs, but the 3MW of twins and or male lambs was increased due to 1 % increase in lamb inbreeding rate.Although inbreeding depression was not generally a possible cause of the reduction in the growth performance of Iranian Moghani sheep until now, but the utilization of designed mating system, at the current flock, could be a suitable approach to maintain the level of inbreeding under control.

Table 1
Distribution of records for body weight traits in different inbreeding classes of animals born between 1987 and 2005 Distribution of records for body weight traits in different inbreeding classes of animals grouped by the type of birth and born between 1987 and 2005 a,b,c Means within a column that do not have a common superscript are significantly different (P<0.05).BW: birth weight, 3MW: 3-month weight, 6MW: 6-month weight, 9MW: 9-month weight, YW: yearling weightTable 2

Table 3
Distribution of records for body weight traits in different inbreeding classes of animals grouped by the sex of lamb and born between 1987 and 2005 a,b Means within a column and for each lamb sex that do not have a common superscript are significantly different (P<0.05).BW: birth weight, 3MW: 3-month weight, 6MW: 6-month weight, 9MW: 9-month weight, YW: yearling weight Table4Regression coefficients (±SE) of body weight traits on inbreeding of lambs for a change of 1 % in inbreeding *significant at P<0.05, **significant at P<0.01, ***trend for significance (0.05<P<0.10).BW: birth weight, 3MW: 3-month weight, 6MW: 6-month weight, 9MW: 9-month weight, YW: yearling weight reported the average inbreeding was 2.33 % in Santa Inês sheep in Brazil.But, Van Wyk et al. (2009) and Selvaggi et al. (2010) reported higher inbreeding rates in Elsenburg Dormer sheep (16 %) and Leccese sheep (8.1 %), respectively.