Effects of inbreeding on number of piglets born total , born alive and weaned in Austrian Large White and Landrace pigs

In this study records of 58 925 litters of Austrian Large White and 17 846 litters of Austrian Landrace pigs were analysed. Regression models were used to determine the effects of litter, dam and sire inbreeding on total number of born, born alive and weaned piglets in Large White and Landrace. In both populations, litter and dam inbreeding showed a negative effect on all traits. Sire inbreeding had no effect in Large White, whereas a significant positive effect was observed in Landrace. On average, inbred sires with an inbreeding coefficient of 10 % had 0.45 more piglets born total and 0.43 more piglets born alive in comparison to non-inbred sires. In a further analysis the total inbreeding coefficients of the animals were divided into two parts: »new« and »old« inbreeding. »New« inbreeding was defined as the period of the first five generations. It was shown that the observed inbreeding effects were not only caused by recent inbreeding. Reproductive performance was also affected by »old« inbreeding. Finally partial inbreeding coefficients of four important ancestors in each population were calculated to investigate if inbreeding effects are similar among these ancestors. The results revealed a varation of inbreeding effects among the four ancestors. Alleles contibuting to inbreeding depression were descendent from specific ancestors.


Introduction
The decrease in performance of offspring of matings between close relatives is known as inbreeding depression.The first scientific evidence for inbreeding depression was published by DARWIN (1876) more than a century ago.Since then, the deleterious consequences of inbreeding were documented in many species (e.g.The genetic basis of inbreeding depression is explained by two main hypotheses.The first hypothesis, the partial dominance hypothesis (DAVENPORT 1908, CROW 1952), posits inbreeding depression as being caused by the expression of deleterious recessive alleles in the homozygous state.Inbreeding increases the frequency of homozygotes and thus deleterious recessive alleles, which are hidden in heterozygotes, will become increasingly expressed.The second is the overdominance hypothesis by EAST (1908) and SHULL (1908).Here inbreeding depression is attributed to the superiority of heterozygotes over both homozygotes.The reduced frequency of heterozygotes due to inbreeding will reduce opportunities to express this overdominance.In addition a third hypothesis has been suggested, which partly explains inbreeding depression as a consequence of a breakdown of epistatic interaction between loci (TEMPLETON & READ 1994).
Inbreeding does not affect all traits to the same degree.Inbreeding depression is most servere in traits that are closely related to fitness, e.g.offspring survival and fertility (FALCONER & MACKAY 1996, DE ROSE & ROFF 1999).DE ROSE & ROFF (1999) concluded that traits less closely related to fitness (e.g.adult body weight) exhibit little or no directional dominance.Furthermore the effect of inbreeding in the same trait varies among species and populations within species (THORNHILL 1993, FRANKHAM et al. 2002).Recent studies revealed that inbreeding depression also shows variation among founders and lineages within a population (PRAY & GOODNIGHT 1995, LACY et al. 1996, RODRIGÁÑEZ et al.  1998, MIGLIOR et al. 1994, GULISIJA et al. 2006).Variability of inbreeding depression arises if founders or lineages of a population vary in number of deleterious recessive alleles (genetic load).
The objective of this study was to examine the effects of inbreeding on the important reproduction traits total number of piglets born, number of piglets born alive and number of weaned piglets in Austrian Large White and Landrace pigs by linear and quadratic regression models and by splitting inbreeding into different inbreeding coefficients (total inbreeding coefficient of litter, dam and sire, »new« and »old« inbreeding, partial inbreeding coefficient).

Performance data
Field data for reproductive performance of purebred Austrian Large White and Austrian Landrace sows were available from 1967 to February 2007.The following information was recorded for each sow: identity number, herd, parity number, identity number of service sire, date of service, date of farrowing, farrowing interval, number of piglets born total, number of piglets born alive and number of piglets weaned.Records of sows with an age at first farrowing lower than 280 days and higher than 505 days and a gestation length lower than 105 days or higher than 125 days were deleted.Additionally litter records with a farrowing interval lower than 120 days or higher than 270 days were not considered in the analysis.After data editing, 58 925 litter records from 17 784 sows and 2 880 boars for Large White and 17 846 litter records from 7 568 sows and 1 840 boars for Landrace were available.A summary of recorded data is shown in Table 1.

Pedigree data
Pedigrees of Large White and Landrace pigs contained information of animals born between 1965 and 2006.The pedigree files did not includ all progeny of the sows in the reproductive performance data.Thus dummy progeny was created to get inbreeding coefficients for the litters in such cases.The entire pedigree contained the relationship of 102 896 animals for Large White and of 52 503 animals for Landrace.

Models
The effects of inbreeding on total number of piglets born, number of piglets born alive and weaned in Large White and Landrace were investigated with the procedure GLM of the software package SAS (SAS, Version 9.1, 2003).Different inbreeding coefficients were used to determine the effects of inbreeding.The following inbreeding coefficients and models were applied.

Total inbreeding coefficient
The overall effect of inbreeding was examined with the total inbreeding coefficient.The total inbreeding coefficient is defined as the probability that two alleles at any locus are identical by descent (WRIGHT 1922, MALÉCOT 1948).
Inbreeding coefficients were calculated with the algorithm of VANRADEN (1992) implemented in the software package PEDIG (BOICHARD 2002).
All traits were analyzed with the same model.Inbreeding coefficients of litter, dam and sire were defined as covariates.In model 1 linear regression coefficients of inbreeding were considered, whereas linear and quadratic regression coefficients were tested in model 2. Furthermore, parity number, herd-year class, farrowing season and age of the sow within parity number were included in the models.
where Yijkl is the individual observation, μ the overall mean, pni the parity number i (i = 1-11), hyj the herd-year class j (j = 1 -3 950 and 2 077 for Large White and Landrace, respectively), seasonk the farrowing season k (k = 1-6), b1-b7 regression coefficients, age(pni) the age of the sow within parity number, Fl the total inbreeding coefficient of the litter, Fd the total inbreeding coefficient of the dam, Fs the total inbreeding coefficient of the sire, εijkl the residual error.

»New« and »old« inbreeding
The differences between effects of inbreeding evolved during recent generations compared to that evolved during the more distant past were investigated.For this analysis inbreeding coefficients of litter, dam and sire were split into two parts, corresponding to the inbreeding occurring in recent generations (»new«) and that which preceded it (»old«).»New« inbreeding was defined as the period of the first five generations.
The algorithm of VANRADEN (1992) in the programme PEDIG (BOICHARD 2002) was also used to compute inbreeding coefficients from the five most recent generations (parents, grand-parents etc.) in the pedigrees.These coefficients are called »new« inbreeding.»Old« inbreeding, however, resulted from the difference of the total inbreeding coefficient taking all available pedigree information into account and the »new« inbreeding of an animal.Generally, the correlation between »new« and »old« inbreeding was below 0.3.Further »new« and »old« inbreeding coefficients of litter, dam and sire were considered separately in different models (3-5).
where Yijkl, pni, hyj, seasonk, age(pni), Fl, Fd, Fs and εijkl are defined as described above, while Fl_new is the young inbreeding of the litter, Fl_old the old inbreeding of the litter, Fd_new the young inbreeding of the dam, Fd_old the old inbreeding of the dam, Fs_new the young inbreeding of the sire, Fs_old the old inbreeding of the sire.

Partial inbreeding coefficient
To analyse whether the effects of inbreeding differ in magnitude and direction depending on the alleles' origin partial inbreeding coefficients were calculated.Inbreeding coefficients of each individual were partitioned into components due to certain ancestors.The partial inbreeding coefficient is defined as the probability that an individual is homozygous for an allele descended from a specified ancestor (LACY et al. 1996).
The The sum of the four partial inbreeding coefficients of an individual and the »rest« is equal to the total inbreeding coefficient of that individual.The »rest« is the part of the total inbreeding coefficient that will be explained by all other common ancestors.
The partial inbreeding coefficients of litter, dam and sire were again investigated using different models (6)(7)(8).The correlation between the partial inbreeding coefficients of ancestors did not exceed 0.5.
where Yijkl, pni, hyj, seasonk, age(pni), Fl, Fd, Fs and εijkl are defined as described above, while Fl_A -Fl_D is the partial inbreeding coefficient of the litter due to ancestor A-D, Fl_Rest the remaining inbreeding coefficient of the litter, Fd_A -Fd_D the partial inbreeding coefficient of the dam due to ancestor A-D, Fd_Rest the remaining inbreeding coefficient of the dam, Fs_A -Fs_D the partial inbreeding coefficient of the sire due to ancestor A-D, Fs_Rest the remaining inbreeding coefficient of the sire.

Inbreeding coefficients
Means, standard deviations and maximal values of different inbreeding coefficients for litters, dams and sires of Large White and Landrace in the reproductive performance data are shown in Table 2. Generally higher litter, dam and sire inbreeding was present in the Large White population.Mean total inbreeding coefficients ranged from 1.59 % to 2.23 % and from 0.67 % to 1.24 % for Large White and Landrace, respectively.About 45 % to 53 % of total inbreeding in Large White and 72 % to almost 80 % of total inbreeding in Landrace could be traced back to common ancestors in the first five generations (»new« inbreeding).In Large White, the important ancestors A_LW, B_LW, C_LW and D_LW were responsible for 13 % of total litter inbreeding, 12 % of total dam inbreeding and 9 % of total sire inbreeding.In case of Landrace nearly 21 % of total litter inbreeding, 20 % of total dam inbreeding and 16 % of total sire inbreeding was explained by the ancestors A_LR, B_LR, C_LR and D_LR.

Linear regression model
Estimates of the effects of litter, dam and sire inbreeding on total number born, number born alive and weaned piglets in Austrian Large White and Landrace pigs are presented in Table 3.In both populations inbreeding reduced the vitality of the piglets and the mothering abilities of the sow.In Large White dam inbreeding had a significant negative effect on all reproductive traits (P<0.001),whereas litter inbreeding showed a significant negative effect on number of piglets born alive (P<0.01) and number of piglets weaned (P<0.001).A similar pattern was observed for Landrace.In this population a significant negative effect of litter inbreeding on all analysed traits (P<0.01 to P<0.001) was revealed, whereas dam inbreeding had only a negative effect on number of piglets born alive (P<0.05).In total −0.19 and −0.29 piglets per 10 % increase of litter inbreeding and −0.16 and −0.21 piglets per 10 % increase of dam inbreeding were weaned in Large White and Landrace, respectively.
The inbreeding of the sire showed no significant effect on litter traits in Large White.Contrary, sire inbreeding had a significant positive effect on all reproductive traits in Landrace pigs (P<0.01 to P<0.001).Sires with an inbreeding coefficient of 10 % had on average 0.45 more piglets born total and 0.43 more piglets born alive.Subsequently, a positive effect on number of piglets weaned was observed.

Quadratic regression model
In Large White the quadratic regression coefficient was significant for dam inbreeding only (see Table 4).Inbreeding depression of the dam is decreasing slightly with increasing inbreeding.However, the difference between the linear and quadratic regression models for inbreeding coefficients up to 10 % was small.To interpret the results for inbreeding coefficients higher than 10 % correctly, it would be necessary to have more animals with inbreeding coefficients higher than 10 %.For Landrace no quadratic term turned out to be significant (data not shown).A possible reason is the lower inbreeding level detectable within the Landrace data.
In Large White, inbreeding of the sire showed no significant effect, thus sire inbreeding was excluded in subsequent analyses.

»New« and »old« inbreeding
The effects of »new« and »old« inbreeding of litter, dam and sire on reproductive performance in Large White and Landrace are shown in Tables 5 to 7.
In both populations the viability of piglets was reduced by »new« and »old« inbreeding.The estimated inbreeding depression was −0.18 and −0.23 piglets weaned per 10 % »new« litter inbreeding and −0.31 and −1.91 piglets weaned per 10 % »old« litter inbreeding in Large White and Landrace, respectively.Especially in Landrace »old« litter inbreeding had a higher impact on inbreeding depression than »new« inbreeding.In contrast, only »old« inbreeding of dams revealed a significant negative effect on all traits in Large White and Landrace.Furthermore the positive inbreeding effect of sires in the Landrace population resulted from »new« inbreeding, whereas »old« inbreeding showed a negative effect (not significant) on the traits analysed.

Partial inbreeding coefficient
An overview of means and standard deviations of inbreeding effects of four genetically important ancestors in Large White and Landrace is given in Figures 1 and 2. A difference in direction and magnitude of inbreeding effects among different ancestors in both populations could be detected.In Large White, the effects of litter and dam inbreeding due to ancestors B_LW and C_LW showed low or no inbreeding depression on all traits.However, the results were not significant.In contrast, dam inbreeding due to sire D_LW revealed a significant negative effect on reproductive performance of the sow.On average, dams with 10 % inbreeding due to D_LW had on average 2.0 piglets less born alive.In Landrace, litter inbreeding due to ancestor C_LR showed a significant negative effect on piglet viability, whereas inbreeding from D_LR reduced the mothering abilities of the sow significantly.Inbred sires in the Austrian Landrace population had on average more piglets born total and born alive.Most interestingly, sire inbreeding due to ancestor A_LR revealed a significant positive effect on number of piglets born total, whereas sires with 10 % inbreeding from C_LR had on average 1.0 less piglets born total and born alive compared to non inbred sires.

Discussion
The mean inbreeding coefficients in this study were low.In comparison, FARKAS et al. (2007) reported in their study similar inbreeding coefficients between 0.50 % to 0.89 % for Hungarian Landrace and Large White pigs.In previous studies from BERESKIN et al. (1968) and RODRIGÁÑEZ et al. (1998), who analysed experimental pig herds, the observed mean inbreeding was much higher (16.1 % to 23.1 %).The estimated inbreeding depression due to litter and dam inbreeding coefficients was low in both populations and in agreement with results by BERESKIN et al. (1968), RODRIGÁÑEZ et al. (1998), CULBERTSON et al. (1998) and FARKAS et al. (2007).The inbreeding of the sire showed no significant effect on litter traits in Large White.BERESKIN et al. (1968) also detected no significant influence of sire inbreeding on litter size.In contrast to these results, a positive sire inbreeding effect on all litter traits was observed in the Landrace population.The positive inbreeding effect is most likely caused by a better sperm quality of the inbred sires.Generally positive inbreeding effects on fitness and fertility traits are rare.SHIELDS (1982) originally called such a phenomenon »inbreeding enhancement«.LACY et al. (1996) and MARGULIS (1998) found a positive effect of dam inbreeding on offspring viability in a subspecies of the old-field mouse, Peromyscus polionotus.Furthermore BALLOU (1997) observed a significant positive effect of maternal inbreeding on neonatal survival in European bison.The increase in fitness is probably due to fixation of favourable gene complexes or epistatic relationships (TEMPELTON 1979).On the other hand, outcrossing does not always enhance fitness.Crosses between distant populations of the same species sometimes lead to significant outbreeding depression.The decline in reproductive fitness under outcrossing is usually attributed to a break up of coadapted gene complexes or favourable epistatic relationships (genetic incompatibility) (FALCONER & MACKAY 1996, EDMANDS 2007, RALLS et al. 2007).Like crossbreeding has not always beneficial effects on fitness, inbreeding is not always detrimental.
Non-linear inbreeding effects on reproductive performance were only observed for dam inbreeding in Large White.BERSKIN et al. (1968) also revealed non-linear effects of inbreeding on litter size in pigs.In recent studies with mice (ISSA & SEELAND 2001), poultry (SZWACZKOWSKI et al. 2004) and cattle (CROQUET et al. 2007) non-linear inbreeding effects on production and fitness traits were detected.Generally, the differences between linear and curvilinear regression models are very small between 0 and 10 % of inbreeding.
The observed inbreeding effects in Large White and Landrace were not only caused by recent inbreeding.Fertility is also affected by old inbreeding.In Landrace, the positive effect of sire inbreeding was caused by recent inbreeding from the first five generations.This result gives further evidence that epistatic interactions may be responsible for the positive inbreeding effect.»Old« inbreeding showed a negative effect (not significant) on the analysed traits, mating with more distant relatives may have broken up these positive interactions.In a long-term selection experiment on first-litter size in mice HINRICHS et al. (2007) also investigated differences between the effects of inbreeding in recent generations from that in the past.The analysis was repeated for different definitions of »new« and »old« inbreeding, depending on length of the »new« period.In this mouse population the »new« inbreeding was found to cause more inbreeding depression than the »old« inbreeding when at least 25 generations were classified as »new« inbreeding.
Overall inbreeding had small effects on reproductive performance in Large White and Landrace pigs.However, some differences in direction and magnitude of inbreeding effects among different ancestors were detected.Alleles contributing to inbreeding depression were descendent from specific ancestors.Variable effects of inbreeding were already reported.PRAY and GOODNIGHT (1995) revealed that inbreeding effects vary for fitness traits among lineages in the red flour beetle.LACY et al. (1996) detected heterogeneity in inbreeding effects for survival, reproduction and growth traits among different founder pairs in the old-field mouse.Also, RODRIGÁÑEZ et al. (1998) found heterogeneous effects of inbreeding on litter size in five founder lineages of Large White pigs.Recent studies in dairy cattle detected variation of inbreeding effects for production traits in different families in Canadian Holstein cows (MIGLIOR et al. 1994) and US Jersey cows (GULISIJA et al. 2006).The differences among founders and lineages in inbreeding depression indicate that relatively few deleterious alleles with major effects contribute to inbreeding depression for any one trait.This finding is especially important for endangered species and breeds, where the inbreeding level is much higher.For example, MAIGNEL and LABROUE (2001) and KOLK GEN SUNDAG et al. (2006) reported for endangered pig breeds average inbreeding coefficients between 8 and 18 %.Thus the main aim in conservation programmes is to minimize inbreeding depression.In the future may be greater emphasis could be given to the partial inbreeding components.
most important ancestors of breeding animals born between 2003 and 2006 were determined for Large White and Landrace according to BOICHARD et al. (1997) using the programme PEDIG (BOICHARD 2002).Partial inbreeding coefficients of four genetically important ancestors with low relationship were calculated with the programme GRain (BAUMUNG et al. 2006) implemented in the software package PEDIG (BOICHARD 2007).

Table 1
Means and standard deviations (SD) of the traits number of piglets born total, born alive and weaned of Large White and Landrace Mittelwerte und Standardabweichungen (SD) für die Merkmale gesamt geborene, lebend geborene und hochgezogene Ferkel für Edelschwein und Landrasse)