Trop Anim Health Prod DOI 10.1007/s11250-015-0758-y

REGULAR ARTICLES

Inbreeding effects on reproductive traits in Iranian Guilan sheep Bahareh Eteqadi & Navid Ghavi Hossein-Zadeh & Abdol Ahad Shadparvar

Received: 22 July 2014 / Accepted: 6 January 2015 # Springer Science+Business Media Dordrecht 2015

Abstract The objective of the present study was to evaluate the effects of inbreeding on reproductive traits in Guilan sheep. Traits included were litter size at birth (LSB), litter size at weaning (LSW), litter mean weight per lamb born (LMWLB), litter mean weight per lamb weaned (LMWLW), total litter weight at birth (TLWB), and total litter weight at weaning (TLWW). Data and pedigree information used in this study were collected during 1994 to 2011 by the Agriculture Organization of Guilan Province in the north of Iran. Data were comprised of 14,534 records of lambs from 136 sires and 2021 dams. All the animals were grouped into three classes according to the inbreeding coefficients (F) obtained by their pedigree: the first class included non-inbred animals (F= 0 %), and the second and third classes included inbred animals (05 %, respectively). The regression coefficients of LSB, LSW, LMWLB, LMWLW, TLWB, and TLWW on lamb inbreeding for a change of 1 % in inbreeding were estimated to be 0.035±0.0038 (P<0.001), −0.029± 0.0077 (P<0.05), −0.333±0.009 (P<0.001), −2.21±0.071 (P < 0.001), −0.254 ± 0.013 (P < 0.001), and −1.95 ± 0.093 (P<0.001), respectively. Effect of inbreeding on reproductive traits in Guilan sheep was very pronounced in the flock. The utilization of a program for planned mating system, in the present flock, suggested keeping the level of inbreeding under control and avoiding appearance of its detrimental effects.

Keywords Fat-tailed sheep . Reproductive traits . Inbreeding depression . Mating system B. Eteqadi : N. Ghavi Hossein-Zadeh (*) : A. A. Shadparvar Department of Animal Science, Faculty of Agricultural Sciences, University of Guilan, P. O. Box: 41635-1314, Rasht, Iran e-mail: [email protected] N. Ghavi Hossein-Zadeh e-mail: [email protected]

Introduction The Guilan sheep is a fat-tailed breed of domestic sheep in Iran, numbering some 400,000 animals in the north of the country, and distributed in the northern and western parts of Guilan province. Mean adult live weight in this breed is 35 kg (77 lbs) for rams and 31 kg (67 lbs) for ewes. The coat color for this breed is yellowish white to pure white, but brown patches are found on the head, face, and at the bottom of the legs (Eteqadi et al. 2014). Genetic improvement programs applied in livestock have been based on two main approaches: selection and crossbreeding. By contrast to crossbreeding, intensive selection within a single population reduces genetic diversity and increases the inbreeding rate. One definition for inbreeding is given by the mating of individuals whose relatedness is greater than the average degree of relationship existing in the population and capable of changing the genotypic frequencies of a population without modifying the gene frequencies (Ghavi Hossein-Zadeh 2013). The inbreeding level is considerably influenced by the ratio of males to females, reproduction ability, mating system, and population size (Norberg and Sorenson 2007; Barczak et al. 2009). Intensive use of a few breeding animals, where the selection intensity is high, could result in greater rates of inbreeding in the population. Thus, a small number of seed stock, 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; Ghavi Hossein-Zadeh 2012). Heterozygosity and allelic diversities can be lost from small, closed, selected populations in 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

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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 (Dario and Bufano 2003; Khan et al. 2007; Van Wyk et al. 2009; Ghavi Hossein-Zadeh 2012). 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; Ghavi HosseinZadeh 2012). In sheep production, reproductive traits as fertility, litter size, and lamb survival are the most important traits in all systems of sheep production and in all environments (Vatankhah 2005; Matika et al. 2003; Gallivan 1996). Improvement in number or total weight of lamb weaned per ewe is a key target in sheep breeding and could partly be attained by increasing the number of lambs weaned and weight of lambs weaned per ewe within a specific year (Duguma et al. 2002). Litter size at birth is directly related to ovulation rate, which is influenced by only a few hormones and the responsible genes, but selection for only this trait would not be effective for increasing lamb production, since it does not include the survival rate and weight of the individual lambs at weaning (Rosati et al. 2002). Litter size at weaning includes survival of lambs at weaning but not the weight. On the other hand, litter weight of lambs weaned per ewe lambing combines ewe’s fertility, litter size at birth, survival rate, growth performance of lambs from birth to weaning, and dam’s level of milk production. Therefore, this trait is considered as the most important factor in determining an ewe’s reproduction and the economic efficiency of a lamb enterprise (Mohammadi et al. 2013). There is no published research on effects of inbreeding on reproductive traits in Guilan sheep. Thus, the objective of this study was to evaluate the effects of inbreeding on reproductive traits in Iranian Guilan sheep over an 18-year period from 1994 to 2011.

Materials and methods Data and pedigree information Pedigree information and data on reproductive performance of Guilan sheep were collected from 1994 to 2011 at the

Agriculture Organization of Guilan province of Iran. Young ewes were randomly exposed to the rams for the first time at approximately 1.5 years of age. Ewes were kept in the flock up to 7 years old. Ewes were supplemented, depending upon the ewes’ requirements, for a few days after lambing. Rams were kept until a male offspring was available for replacement. There was a controlled mating system so that the identification of sire and dam of each lamb was known. During the breeding season (from September to November), single-sire pens were used allocating 20–25 ewes per ram. Lambs remained with their dam until weaning. Lambs were eartagged and weighted immediately after lambing. During the suckling period, lambs suckled their mothers while being allowed dry alfalfa after 3 weeks of age. Lambs were weaned at approximately 90 days of age. Animals were kept on natural pasture during spring, summer, and autumn seasons. Since environmental conditions were adverse during the winter, therefore the animals were kept indoors during the winter months. The flock was mainly kept on range and fed cereal pasture, but supplemental feed, including alfalfa and wheat straw, was provided especially around mating season (Eteqadi et al. 2014). Studied traits The traits analyzed were assigned as basic and composite traits. Basic traits were litter size at birth (LSB=number of lambs born alive per ewe lambing), litter size at weaning (LSW=number of lambs weaned per ewe lambing), litter mean weight per lamb born (LMWLB), and litter mean weight per lamb weaned (LMWLW). LMWLB and LMWLW were the average weights of lambs from the same parity at birth and weaning, respectively. Based on the observations from basic traits, composite traits were derived. Composite traits were total litter weight at birth per ewe lambing (TLWB) and total litter weight at weaning per ewe lambing (TLWW). TLWB refers to the sum of the birth weights of all lambs born per ewe lambed and TLWW refers to the sum of the weights of all lambs weaned per ewe lambed. The characteristics of the data set used in this study are presented in Table 1. Statistical and genealogical analyses The CFC program (Sargolzaei et al. 2006) was used to calculate pedigree statistics, genetic structure analysis of the population. CFC is a software package for pedigree analysis and monitoring genetic diversity and is memory efficient and fast and applicable to very large pedigrees due to use of an indirect method, which considers the inverse of the numerator relationship matrix. The INBUPGF90 program (Aguilar and Misztal 2012) was used for calculating regular inbreeding coefficients for individuals in the pedigree. INBUPGF90 program calculates inbreeding coefficients using a recursive

Trop Anim Health Prod Table 1

Characteristics of data set for Guilan sheep Traits

No. of records No. of sires No. of dams No. of ewes with one record No. of ewes with two records No. of ewes with three records No. of ewes with four records No. of ewes with five records No. of ewes with more than five records No. of animals with both parents unknown Mean SD CV (%)

LSB

LSW

LMWLB (kg)

LMWLW (kg)

TLWB (kg)

TLWW (kg)

14,534 136 2021 4047 2113 1053 451 157 81 5285 1.05 0.23 21.90

14,534 136 2021 4047 2113 1053 451 157 81 5285 0.81 0.46 56.79

14,534 136 2021 4047 2113 1053 451 157 81 5285 3.15 0.61 19.37

14,534 136 2021 4047 2113 1053 451 157 81 5285 15.35 3.96 25.80

14,534 136 2021 4047 2113 1053 451 157 81 5285 3.28 0.81 24.70

14,534 136 2021 4047 2113 1053 451 157 81 5285 15.91 5.03 31.62

LSB litter size at birth, LSW litter size at weaning, LMWLB litter mean weight per lamb born, LMWLW litter mean weight per lamb weaned, TLWB total litter weight at birth, TLWW total litter weight at weaning, SD standard deviation, CV coefficient of variation

algorithm assuming nonzero inbreeding for unknown parents. The number of animals (in total), inbred animals, sires, dams, founders, and non-founders in the pedigree of Guilan sheep were 28,944, 43, 453, 9967, 8862, and 20,082, respectively. Also, there were totally 253 fullsib groups with average family size of 2.05 in the pedigree of Guilan 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 (05 %, respectively). The choice of fixed effects to be considered was made after testing whether the effects were statistically significant on the traits investigated with a linear fixed effects model analyzed with general linear model (GLM) procedure of SAS 9.0 program (SAS Institute 2003). After data verification, defective and doubtful records were deleted (e.g., lambs without weight records or with incomplete records of parentage or with registration numbers lower than the numbers of their parents were left out). The significance level for the inclusion of fixed effects into the model was declared at P<0.05. The models included the fixed class effects of herdyear-season of lambing, Lamb’s sex (in two classes: male and female), type of birth (in three classes: single, twin, and triplet), dam’s age at lambing (in six classes: from 2 to 7 years old) and random effect of animal. All the first-order interactions were included in the initial models. Herd-year-season of lambing was fixed effect which significantly affected on LSB. Herd-year-season of lambing, inbreeding class, and interaction between

dam’s age at lambing and inbreeding class were fixed effects which significantly affected on LSW. Lamb’s sex, type of birth, dam’s age at lambing, inbreeding class, herd-year-season of lambing, and interactions between the lamb’s sex and dam’s age at lambing, type of birth and dam age, type of birth, and inbreeding class were fixed effects which significantly affected on LMWLB. Lamb’s sex, type of birth, dam’s age at lambing, inbreeding class, herd-year-season of lambing and interaction between the lamb’s sex and inbreeding class were fixed effects which significantly affected on LMWLW. Lamb’s sex, type of birth, dam’s age at lambing, inbreeding class, herd-year-season of lambing and interactions between type of birth and the lamb’s sex, type of birth, type of birth and dam’s age at lambing, type of birth and inbreeding class, the lamb’s sex, and dam’s age at lambing were fixed class effects which significantly affected on TLWB. Lamb’s sex, type of birth, dam’s age at lambing, inbreeding class, herdyear-season of lambing, and interactions between type of birth and dam’s age at lambing, type of birth, and inbreeding class were fixed effects which significantly affected on TLWW.

Results and discussion Summary statistics for reproductive traits in different inbreeding classes of animals are shown in Table 2. The classes of inbreeding for all traits of this study except LSB and LSW

Trop Anim Health Prod Table 2 Distribution of records for reproductive traits in different inbreeding classes of Guilan sheep Inbreeding F=0 class Traits N (Mean±SE) LSB LSW LMWLB LMWLW TLWB TLWW

6035 (1.03±0.002a) 6035 (0.83±0.005a) 6035 (3.35±0.007a) 6035 (16.63±0.052a) 6035 (3.43±0.009a) 6035 (17.04±0.067a)

0
F>0.05

N (Mean±SE)

N (Mean±SE)

8464 (1.06±0.003a) 8464 (0.79±0.005a) 8464 (3.01±0.006b) 8464 (14.38±0.049c) 8464 (3.17±0.009b) 8464 (15.62±0.064b)

35 (1.06±0.039a) 35 (0.83±0.077a) 35 (3.08±0.095b) 35 (15.26±0.742b) 35 (3.24±0.137b) 35 (15.05±0.737b)

LSB litter size at birth, LSW litter size at weaning, LMWLB litter mean weight per lamb born, LMWLW litter mean weight per lamb weaned, TLWB total litter weight at birth, TLWW total litter weight at weaning a,b,c

The means within the same row with at least one common letter, do not have significant difference (P>0.05)

were significant (P < 0.05). The LMWLB, TLWB, and TLWW of animals within first class of inbreeding (noninbred group) were significantly higher than those of lambs belonging to the second and third classes (inbred groups) (P<0.05). There were significant differences between three classes of inbreeding on LMWLW and animals within first class of inbreeding had greater mean of the trait than two other groups (P<0.05). Inbreeding is generally associated with deterioration in growth and reproductive traits in small ruminants (Wocac 2003; Ghavi Hossein-Zadeh 2013), and level of inbreeding might be an important factor for such effects to be appeared. The effect of inbreeding on reproduction has

Table 3

Distribution of records for reproductive traits in different inbreeding classes of Guilan sheep grouped by the type of birth

Traits

LSB LSW LMWLB LMWLW TLWB TLWW

an obvious impact through fertility, pregnancy, and lambing, resulting in fewer lambs per flock (MacKinnon 2003). The inbreeding coefficient is 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; however, in this case, the accuracy is strongly determined by the incompleteness of pedigrees (Barczak et al. 2009; Eteqadi et al. 2014). The LSB and LSW of single or twin-born lambs and the LMWLB and TLWB of twin-born lambs showed no significant differences (Table 3). In addition, the LMWLW and TLWW of twin-born lambs within third class of inbreeding were significantly lower than those of twin-born lambs belonging to the first and second classes (P<0.05; Table 3). The LSB of male lambs, the LSW of male or female lambs, and the TLWB of female lambs showed no significant differences (Table 4). On the other hand, the LMWLB of male or female lambs and the LMWLW and TLWW of male lambs within first class of inbreeding (non-inbred group) were significantly greater than those of other classes (inbred groups) (P<0.05; Table 4). The regression coefficients of reproductive traits on inbreeding of lambs for a change of 1 % in inbreeding are presented in Table 5. The regression coefficient of LSB on inbreeding of all lambs for 1 % change in inbreeding was

Single

Twin

F= 0

0
F> 0.05

F= 0

0
F> 0.05

N Mean±SE N Mean±SE N

5858 1a ±0.00 4764 1a ±0.00 5858

7939 1a ±0.00 6157 1a ±0.00 7939

33 1a ±0.00 27 1a ±0.00 33

176 2a ±0.00 116 2a ±0.00 176

501 2a ±0.00 292 2a ±0.00 501

2 2a ±0.00 1 2a ±0.00 2

Mean±SE N Mean±SE N Mean±SE N Mean±SE

3.36a ±0.56 4764 16.62a ±3.64 5858 3.36a ±0.56 4764 16.62a ±3.64

3.03b ±0.58 6157 14.38c ±3.92 7939 3.03b ±0.58 6157 14.38c ±3.92

3.10b ±0.57 27 15.45b ±3.79 33 3.10b ±0.57 27 15.45b ±3.79

2.95a ±0.57 116 16.90a ±4.60 176 5.89a ±1.15 116 33.80a ±9.20

2.67a ±0.59 292 14.33a ±3.36 501 5.33a ±1.17 292 28.67a ±6.72

2.80a ±0.00 1 10.10b ±0.00 2 5.60a ±0.00 1 20.20b ±0.00

LSB litter size at birth, LSW litter size at weaning, LMWLB litter mean weight per lamb born, LMWLW litter mean weight per lamb weaned, TLWB total litter weight at birth, TLWW total litter weight at weaning a,b,c

The means within the same row with at least one common letter, do not have significant difference (P>0.05)

Trop Anim Health Prod Table 4

Distribution of records for reproductive traits in different inbreeding classes of Guilan sheep grouped by the lamb sex

Traits

LSB LSW LMWLB LMWLW TLWB TLWW

Male

N Mean±SE N Mean±SE N Mean±SE N Mean±SE N Mean±SE N Mean±SE

Female

F=0

0
F> 0.05

F= 0

0
F> 0.05

2922 1.03a ±0.18 2922 0.81a ±0.44 2922 3.37a ±0.57 2317 16.96a ±3.76 2922 3.47a ±0.75 2317 17.42a ±4.86

4001 1.07a ±0.26 4001 0.78a ±0.49 4001 3.03b ±0.60 2990 14.74b ±4.05 4001 3.20ab ±0.87 2990 15.41b ±5.26

18 1a ±0.00 18 0.78a ±0.42 18 3.11b ±0.59 14 14.93b ±2.94 18 3.11b ±0.59 14 14.93b ±2.94

3113 1.03b ±0.16 3113 0.84a ±0.41 3113 3.32a ±0.56 2564 16.33a ±3.55 3113 3.40a ±0.73 2564 16.69a ±4.51

4463 1.06ab ±0.25 4463 0.81a ±0.48 4463 2.99b ±0.59 3465 14.06b ±3.73 4463 3.15a ±0.82 3465 14.74b ±4.94

17 1.12a ±0.32 17 0.88a ±0.47 17 3.04b ±0.51 14 15.59a ±4.57 17 3.37a ±0.95 14 16.31ab ±4.44

LSB litter size at birth, LSW litter size at weaning, LMWLB litter mean weight per lamb born, LMWLW litter mean weight per lamb weaned, TLWB total litter weight at birth, TLWW total litter weight at weaning a,b

The means within the same row with at least one common letter, do not have significant difference (P>0.05)

significantly positive (0.035±0.0038; P<0.001). Therefore, LSB increased along with increase in inbreeding of lambs. The regression coefficients of LMWLB, LMWLW, TLWB, and TLWW on inbreeding of single or twin-born lambs and male or female lambs were significantly negative (P<0.001). Therefore, those traits decreased due to 1 % increase in inbreeding. Similar to the current results, Mokhtari et al. (2014) reported individual increases in inbreeding of the ewes by 1 %, significantly reduced TLWB and TLWW in Iran-Black sheep. The direct inbreeding depression in LSB per 10 % inbreeding was observed in Texel, Shropshire, and Oxford Down sheep breeds (Norberg and Sorenson 2007). Also, Prod’Homme and Lauvergne (1993) reported an increased prolificacy with increasing inbreeding in a highly inbred population of Merino Rambouillet sheep. They concluded that positive effects of selection and improved management on prolificacy traits were larger than the negative effect of Table 5

inbreeding. Rzewuska et al. (2005) did not find any inbreeding effects on ovulation rate, fertility, and litter size in a closed Booroola flock. Boujenane and Chami (1997) observed that inbreeding of the ewe had an adverse effect on LSB, LSW, and litter weight of Beni Guil ewes, as well as litter weight at 90 days of Sardi ewes, but a positive effect on LSB and LSW of Sardi ewes. It is important to note that a range of values for effects of inbreeding on individual traits have been found in different breeds and different lines within a breed. Although most estimates fall within a limited range (Lamberson and Thomas 1984), there is still much between-breed and withinbreed variation in the effect of inbreeding on a particular trait (Analla et al. 1998; Boujenane and Chami 1997; Weiner et al. 1992). The variation could be attributed to the number of detrimental alleles present in the founding population or line, in addition to differing environmental and management conditions (MacKinnon 2003).

Regression coefficients (±SE) of reproductive traits (in grams) on inbreeding of lambs for a change of 1 % in inbreeding

Traits

Single

Twin

Male

Female

All

LSB LSW LMWLB LMWLW TLWB TLWW

0 0 −0.32±0.009*** −2.20±0.073*** −0.32±0.009*** −2.20±0.073***

0 0 −0.27±0.05*** −2.59±0.41*** −0.54±0.101*** −5.18±0.817***

0.033±0.006*** −0.032±0.011** −0.34±0.014*** −2.18±0.11*** −0.26±0.019*** −1.98±0.139***

0.036±0.005*** −0.027±0.011** −0.326±0.013*** −2.218±0.094*** −0.243±0.018*** −1.910±0.123***

0.035±0.0038*** −0.029±0.0077** −0.333±0.009*** −2.21±0.071*** −0.254±0.013*** −1.95±0.093***

LSB litter size at birth, LSW litter size at weaning, LMWLB litter mean weight per lamb born, LMWLW litter mean weight per lamb weaned, TLWB total litter weight at birth, TLWW total litter weight at weaning. ***significant at P<0.001; **significant at P<0.05

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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, negative and positive inbreeding effects are mixed (Barczak et al. 2009; Eteqadi et al. 2014). The rates of inbreeding must be limited to maintain diversity at an acceptable level so that genetic variation will ensure that future animals can respond to changes in environment (Van Wyk et al. 2009). The net effect of inbreeding in a selection program is dependent on the magnitude of the selection response relative to the depression due to the accumulated inbreeding. Depending on whether genetic gain and inbreeding depression compensate for each other, the level of inbreeding might need to be accounted for in the selection process. Most breeding programs might try to minimize accumulation of inbreeding and quantify the increase by calculating the change in inbreeding per generation (Boichard et al. 1997) to limit the possible negative effect of inbreeding on productive and reproductive traits.

Conclusion Effects of inbreeding on reproductive traits in Iranian Guilan sheep was very pronounced in the flock, and inbreeding depression was generally a possible cause of the reduction in the reproductive performance of Iranian Guilan sheep until now. Both positive and negative inbreeding effects were found. Therefore, utilization of designed mating system with maximum avoidance of mating closely related animals, at the current flock, is suggested to avoid accumulation of inbreeding and appearance of its deleterious effects. Increase in number of breeding males and their more frequent replacement would help to reduce the level of inbreeding.

Conflict of interest The authors declare that they have no conflict of interest.

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