J. Anim Sci. 2007. 85:299-304. doi:10.2527/jas.2006-257
© 2007 American Society of Animal Science
Inbreeding trend and inbreeding depression in the Danish populations of Texel, Shropshire, and Oxford Down1
E. Norberg2 and
A. C. Sørensen
Department of Genetics and Biotechnology, Danish Institute of Agricultural Sciences, DK-8830 Tjele, Denmark
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Abstract
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The objective of this study was to analyze the development of inbreeding and estimate inbreeding depression in the Danish populations of 3 major meat type sheep breeds. The pedigrees contained 29,336 Texel, 22,838 Shropshire, and 11,487 Oxford Down. The rate of inbreeding was approximately 1% per generation for all breeds, but the rate of increase in coancestry was somewhat lower (0.45 to 0.71), indicating that more inbreeding has been accumulating than would be expected if mating was at random. Inbreeding depression for birth weight, ADG from birth until 2 mo, and litter size was estimated for all 3 breeds using a minimum of 15,000 records per trait and breed. All traits showed depression due to inbreeding of the animal itself. For most combinations of trait and breed, there was also a significant reduction of the phenotype due to inbreeding in the dam. The size of inbreeding depression was 1.2 to 2.6% of the mean, resulting in an increase in the inbreeding coefficient of the individual of 0.10, and estimates were similar for similar increases in maternal inbreeding. The rate of inbreeding in these breeds needs to be reduced in the future to avoid a further decline in birth weight, ADG, and litter size.
Key Words: inbreeding • inbreeding depression • pedigree analysis • sheep
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INTRODUCTION
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Population size and ratio of males to females are important factors that have an effect on the rate of inbreeding (
F). In addition, the practices that make breeding programs effective in generating genetic gain also contribute to an increase in F. In Denmark today, the meat sheep populations are of limited size, and commonly only a single or a few rams are used within a flock. Therefore, inbreeding is expected to increase at high rates in these populations. Associated with inbreeding is the decline in performance usually known as inbreeding depression (e.g., Falconer and Mackay, 1996
). Inbreeding depression in sheep has been found for several traits (Lamberson and Thomas, 1984). Ercanbrack and Knight (1991), Wiener et al. (1992a), and Analla et al. (1998) found inbreeding depression for lamb weights, and inbreeding depression has also been found for litter size (Ercanbrack and Knight, 1991; Wiener et al., 1992b). However, most of these studies were done on highly inbred lines.
Even though commercial production of sheep meat is not a big business in Denmark today, the use of sheep for maintaining the landscape is encouraged. To be able to manage a sustainable sheep operation, farmers are dependent on the animals reproducing and producing satisfactorily. Inbreeding is therefore an important parameter to monitor and control in breeding programs.
The aim of this paper was to present the trend in inbreeding and estimates of inbreeding depression for birth weight, ADG, and litter size in the 3 most common meat sheep breeds in Denmark: Texel, Shropshire, and Oxford Down.
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MATERIALS AND METHODS
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Animal Care and Use Committee approval was not obtained for this study because the data were obtained from an existing database (Danish Agricultural Advisory Center, Skejby).
Data
Data from 1990 to 2004 were provided by the Danish Agricultural Advisory Center, Skejby. Animals born between 2000 and 2004 with a pedigree completeness index over 5 generations (see below) of at least 0.8 were selected as a reference population to reflect the present gene pool of the breeds. Basic statistics of the data used for the pedigree analyses are given in Table 1. Pedigrees of animals in the reference population were traced as far back as possible. The degree of completeness of the pedigrees was assessed by the index proposed by Mac-Cluer et al. (1983), who established an index for pedigree completeness (PCI) to quantify the possibilities of detecting inbreeding in the pedigree:
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Table 1. Number of animals in the reference population and the entire pedigree (i.e., the reference population and all ancestors), and average pedigree completeness index of animals in the reference population
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where Csire and Cdam are contributions from the paternal and maternal lines, respectively, calculated as follows:
where ai is the proportion of known ancestors in generation i; and d is the number of generations taken into account. In this study, 5 generations were considered when calculating this index for each animal (d = 5). This index is ad hoc in the sense that a specific value cannot be translated into an expected bias in the calculated coefficient of inbreeding. However, being a harmonic mean, the index has a value of zero if 1 parent is unknown, no matter how much pedigree is known for the other parent.
The software package Inbred by Berg (2003) was used to calculate individual PCI and inbreeding coefficients (F), using the algorithm of Meuwissen and Luo (1992), and average coancestry within birth cohorts, using the algorithm of Colleau (2002). The cohort coancestry values reflect the expected inbreeding from random matings within the cohort. The rate of inbreeding and the rate of increase in coancestry per year were calculated for the time period 1996 to 2004 and multiplied by the generation interval to obtain rates per generation. The generation interval for each cohort was calculated as the average age of the parents of animals born in that year. The generation intervals presented are averages over the 4 paths, sire-son, sire-daughter, dam-son, and dam-daughter, and over birth cohorts 2000 to 2003.
The traits analyzed for inbreeding depression were birth weight (BrW), ADG between birth and 2 mo (DG2), and litter size (LS). Birth weight was defined as the live weight of a lamb, in kilograms, measured within 24 h of birth, and DG2 was defined as the ADG, in grams, from birth until 2 mo (weight at 2 mo was measured within ± 15 d). Litter size was recorded on the day of lambing as the total number of lambs born in a litter. Animals belonging to a flock-year class with fewer than 6 animals were omitted. Only animals with a PCI 
0.9 had data included in the estimation of inbreeding depression. A situation in which 1 great grandparent is unknown or 2 great-great grandparents are unknown results in a PCI value of 0.9. Descriptive statistics of the data used for the inbreeding depression analyses are given in Table 2.
Statistical Analyses
Univariate animal models were used for the estimation of genetic parameters, including direct and maternal additive genetic effects, common litter effects, and permanent environmental effects due to repeated observations. Regressions on F and maternal F were included in the models to estimate inbreeding depression. The correlation of coefficients of inbreeding of the individual and its dam was 0.10. This allowed reliable separation of direct and maternal inbreeding depression. Litter size was analyzed as a trait of the lamb. However, only 1 lamb selected at random from each litter was included in the analysis, as the records of the other lambs of the litter contributed no additional information. Effects included in the model differed for the 3 traits and were as follows:
where BrWijklnop = the BrW of animal o; DG2ijklmnop = the DG2 of animal o; LSjkno = the number of litter mates of animal o, including the lamb itself (i.e., litter size considered as a trait of the lamb); Si = the fixed effect of sex; FYj = fixed effect of flock-year class; LMk = the fixed effect of lambing month of ewe (grouped by month, but months July to November were pooled); NBl = the number of offspring born in litter; NA30m = the number of offspring in litter after 30 d; Pn = the fixed effect of parity of ewe; Fo = the inbreeding coefficient of animal o; Fp = the inbreeding coefficient of ewe p; b1 = the regression on Fo; b2 = the regression on Fp; adiro = the random direct additive genetic effect of animal o; amatp = random maternal additive genetic effect of animal p; pep = the random permanent environmental effect of ewe; cq = the random effect of common litter; and eijklmnop = the random residual.
Estimation of (co)variance components for all models was carried out with the AI-REML algorithm (Madsen et al., 1994; Johnson and Thompson, 1995) using the DMU-package (Madsen and Jensen, 2000). Estimated heritabilities were similar to those presented in Maxa et al. (2007), using similar models on a data set of which the data set used in this study is a subset. Therefore, discussion of variance components is not included in this paper.
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RESULTS AND DISCUSSION
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Pedigree Completeness and Trend in Inbreeding
The completeness of pedigree was high for all breeds (Figure 1). This showed that the data were suitable for pedigree analyses. Over the last decade, F was similar for the 3 breeds (Figure 2a). For Oxford Down, the level of inbreeding remained steady over the last 5 yr after a rapid increase in the preceding 5 yr. Texel had a period of approximately stable F until 1997, but F appears to have increased since then. These trends in inbreeding may reflect changes in ram use across the population as the trends were not reflected in the coancestry values, which were more stable (Figure 2b). The stable F in some periods was not due to inclusion of unknown genes because no coinciding drop in PCI could be seen for any of the breeds.
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Figure 1. Average pedigree completeness indices (PCI) for each birth cohort plotted against year of birth for Texel, Shropshire, and Oxford Down.
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Figure 2. (a) Average coefficient of inbreeding, and (b) average coancestry for each birth cohort plotted against year of birth for Texel, Shropshire, and Oxford Down.
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The distributions of inbreeding coefficients in the populations are illustrated in Figure 3. The distributions were right skewed, particularly for Shropshire. For all breeds, a proportion of animals had large inbreeding coefficients (0.25). These probably resulted from mating of full sibs, with some additional relationship of the parents due to common ancestors further back in the pedigree. Given the high completeness of the pedigrees, and the reasonably large variation in inbreeding coefficients, these data were useful for estimating inbreeding depression.
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Figure 3. Distribution of inbreeding coefficients of animals born between 1990 and 2004 for Texel, Shropshire, and Oxford Down.
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Additional results from the pedigree analyses are presented in Table 3. The average F of lambs born in 2004 ranged from about 6% in Texel to 10% in Shropshire. The difference in average coancestry coefficient among the breeds was smaller than the difference in F. Generation intervals varied between 3.1 and 3.7 yr, which was somewhat lower than found in other commercial breeds (Prod’Homme and Lauvergne, 1993; Huby et al., 2003). For all breeds the increase in F per generation was about 1%. Huby et al. (2003) analyzed the trend in inbreeding in 6 French sheep breeds and found rates no higher than 0.4% per generation in any breed. However, the depths of the pedigrees were somewhat lower than in the populations considered in this study. More important as a measure of diversity is the rate of increase in coancestry (Sørensen et al., 2005). Like the rate of inbreeding, this is a function of the past effective population size, but it is not influenced by nonrandom mating, as is the rate of inbreeding. The rate of coancestry was lower than the rate of inbreeding, which indicates that inbreeding has occurred to a higher degree than expected under random mating. Hence, the rate of inbreeding could be reduced if rams were circulated in the population. In animal breeding, it is recommended to maintain F of at most 0.5 to 1.0% per generation (FAO, 1998; Bijma, 2000). All 3 breeds investigated in this study are on the border or just above this recommendation. However, the rate of coancestry revealed that the populations only need a small restructuring in the use of rams to increase the effective population size.
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Table 3. Rate of inbreeding and rate of coancestry per generation from 1996 to 2004, average coefficient of inbreeding, and coancestry of lambs born in 2004, and generation interval
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Inbreeding Depression
Estimates of significant (P < 0.05) linear regressions on direct and maternal inbreeding are presented in Table 4. Inbreeding depression expressed as a percentage of the mean for a 10% increase in inbreeding coefficient is presented in Table 5. For all breeds, inbreeding affected the means of all traits significantly. For BrW, the regression on direct and maternal inbreeding was significant for all breeds. The decrease in BrW due to a 10% increase in F of the lamb ranged from 82 to 112 g, or from 2.0 to 2.6% of the mean. For an increase in F of 10% in the dam, the reduction in BrW ranged from 53 to 138 g, or 1.2 to 2.4% of the mean. These results are very similar to those reported by Lamberson and Thomas (1984) in a review that the mean effect of inbreeding in the lamb on BrW was –13 g per 1% increase and the same per 1% increase in inbreeding of the dam. The retarding effects of inbreeding of the lamb and ewe on BrW in Shropshire and Oxford Down were similar to that found by Ercanbrack and Knight (1991) for Rambouillet. They reported that the combined effect of 20% inbreeding in the dams and 25% inbreeding in the lambs reduced BrW by approximately 6%. For DG2, the regression on direct and maternal inbreeding was significant for all breeds except for the maternal inbreeding of Oxford Down. The decrease due to inbreeding ranged from 5.4 to 10.6 g, which corresponded to 2.0 to 2.4% of the mean. Analla et al. (1998) found similar values for 60-d weights of Spanish MeriNo.
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Table 4. Estimates of significant (P < 0.05) regressions on direct and maternal inbreeding, with SE in parentheses, for birth weight (BrW), ADG until 2 mo (DG2), and litter size (LS)
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Table 5. Predicted change in birth weight (BrW), ADG until 2 mo (DG2), and litter size (LS) with a 10% increase in inbreeding coefficient, expressed as percentage of the mean of the trait
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For LS the regression on direct inbreeding was significant for all 3 breeds. The direct inbreeding depression ranged from –0.019 to –0.032 lambs per lambing with a 10% increase in inbreeding, which is similar to the results of Ercanbrack and Knight (1991). Shropshire showed the lowest inbreeding depression for LS, and the effect of maternal inbreeding was not significant for this breed. Oxford Down showed the largest effect of maternal inbreeding. The literature is conflicting regarding the effect of inbreeding on fertility traits. Prod’Homme and Lauvergne (1993) found no inbreeding depression for prolificacy in a relatively highly inbred population of Merino Rambouillet. In fact, they reported increased prolificacy with increasing inbreeding, but their study confounded the increase in inbreeding with the phenotypic increase in prolificacy during a 60-yr period. The only conclusion that should be drawn from their study is that the positive effects of selection and improved management on prolificacy were larger than the negative effect of inbreeding. Analla et al. (1998) did not find a significant retarding effect of inbreeding on LS. Wiener et al. (1992a, b), in an inbreeding experiment with sheep, found negative effects of inbreeding on body weights and LS, but in their study the level of inbreeding was much higher than in our study, and therefore, the results may not be comparable. Because traits related to fitness often show inbreeding depression (Falconer and Mackay, 1996; DeRose and Roff, 1999), we expected a negative effect of direct and maternal inbreeding on LS. This was confirmed in our study, where only Shropshire did not show a significant depression due to maternal inbreeding for LS.
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IMPLICATIONS
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Inbreeding accumulated at around 1% per generation over the last decade in the Danish populations of Texel, Shropshire, and Oxford Down. There are, however, indications that only small changes to the breeding programs are required to control and even decrease this rate by circulating genetic material among flocks to a greater degree. Inbreeding was shown to negatively affect birth weight, average daily gain, and litter size in all 3 breeds. This is a major incentive for reducing the future rate of inbreeding.
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Footnotes
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1 Mike Goddard at Genetics and Genomics, Department of Primary Industries (DPI), Victoria, Australia, is acknowledged for fruitful discussions of this work during the authors stay at DPI. 
2 Corresponding author: Elise.Norberg{at}agrsci.dk
Received for publication April 24, 2006.
Accepted for publication September 20, 2006.
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LITERATURE CITED
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Abstract
INTRODUCTION
