N. Duijvesteijn

A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6

BackgroundIn many countries, male piglets are castrated shortly after birth because a proportion of un-castrated male pigs produce meat with an unpleasant flavour and odour. Main compounds of boar taint are androstenone and skatole. The aim of this high-density genome-wide association study was to identify single nucleotide polymorphisms (SNPs) associated with androstenone levels in a commercial sire line of pigs. The identification of major genetic effects causing boar taint would accelerate the reduction of boar taint through breeding to finally eliminate the need for castration.ResultsThe Illumina Porcine 60K+SNP Beadchip was genotyped on 987 pigs divergent for androstenone concentration from a commercial Duroc-based sire line. The association analysis with 47,897 SNPs revealed that androstenone levels in fat tissue were significantly affected by 37 SNPs on pig chromosomes SSC1 and SSC6. Among them, the 5 most significant SNPs explained together 13.7% of the genetic variance in androstenone. On SSC6, a larger region of 10 Mb was shown to be associated with androstenone covering several candidate genes potentially involved in the synthesis and metabolism of androgens. Besides known candidate genes, such as cytochrome P450 A19 (CYP2A19), sulfotransferases SULT2A1, and SULT2B1, also new members of the cytochrome P450 CYP2 gene subfamilies and of the hydroxysteroid-dehydrogenases (HSD17B14) were found. In addition, the gene encoding the ß-chain of the luteinizing hormone (LHB) which induces steroid synthesis in the Leydig cells of the testis at onset of puberty maps to this area on SSC6. Interestingly, the gene encoding the α-chain of LH is also located in one of the highly significant areas on SSC1.ConclusionsThis study reveals several areas of the genome at high resolution responsible for variation of androstenone levels in intact boars. Major genetic factors on SSC1 and SSC6 showing moderate to large effects on androstenone concentration were identified in this commercial breeding line of pigs. Known and new candidate genes cluster especially on SSC6. For one of the most significant SNP variants, the difference in the proportion of animals surpassing the threshold of consumer acceptance between the two homozygous genotypes was as much as 15.6%.

Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression

The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics. During the Industrial Revolution, Chinese breeds were imported to Europe to improve commercial traits in European breeds. Here we demonstrate the presence of introgressed Asian haplotypes in European domestic pigs and selection signatures on some loci in these regions, using whole genome sequence data. The introgression signatures are widespread and the Asian haplotypes are rarely fixed. The Asian introgressed haplotypes are associated with regions harbouring genes involved in meat quality, development and fertility. We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines. These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.

High-resolution association mapping of number of teats in pigs reveals regions controlling vertebral development

BackgroundSelection pressure on the number of teats has been applied to be able to provide enough teats for the increase in litter size in pigs. Although many QTL were reported, they cover large chromosomal regions and the functional mutations and their underlying biological mechanisms have not yet been identified. To gain a better insight in the genetic architecture of the trait number of teats, we performed a genome-wide association study by genotyping 936 Large White pigs using the Illumina PorcineSNP60 Beadchip. The analysis is based on deregressed breeding values to account for the dense family structure and a Bayesian approach for estimation of the SNP effects.ResultsThe genome-wide association study resulted in 212 significant SNPs. In total, 39 QTL regions were defined including 170 SNPs on 13 Sus scrofa chromosomes (SSC) of which 5 regions on SSC7, 9, 10, 12 and 14 were highly significant. All significantly associated regions together explain 9.5% of the genetic variance where a QTL on SSC7 explains the most genetic variance (2.5%). For the five highly significant QTL regions, a search for candidate genes was performed. The most convincing candidate genes were VRTN and Prox2 on SSC7, MPP7, ARMC4, and MKX on SSC10, and vertebrae δ-EF1 on SSC12. All three QTL contain candidate genes which are known to be associated with vertebral development. In the new QTL regions on SSC9 and SSC14, no obvious candidate genes were identified.ConclusionsFive major QTL were found at high resolution on SSC7, 9, 10, 12, and 14 of which the QTL on SSC9 and SSC14 are the first ones to be reported on these chromosomes. The significant SNPs found in this study could be used in selection to increase number of teats in pigs, so that the increasing number of live-born piglets can be nursed by the sow. This study points to common genetic mechanisms regulating number of vertebrae and number of teats.

The prospects of selection for social genetic effects to improve welfare and productivity in livestock

Social interactions between individuals living in a group can have both positive and negative effects on welfare, productivity, and health of these individuals. Negative effects of social interactions in livestock are easier to observe than positive effects. For example, laying hens may develop feather pecking, which can cause mortality due to cannibalism, and pigs may develop tail biting or excessive aggression. Several studies have shown that social interactions affect the genetic variation in a trait. Genetic improvement of socially-affected traits, however, has proven to be difficult until relatively recently. The use of classical selection methods, like individual selection, may result in selection responses opposite to expected, because these methods neglect the effect of an individual on its group mates (social genetic effects). It has become clear that improvement of socially-affected traits requires selection methods that take into account not only the direct effect of an individual on its own phenotype but also the social genetic effects, also known as indirect genetic effects, of an individual on the phenotypes of its group mates. Here, we review the theoretical and empirical work on social genetic effects, with a focus on livestock. First, we present the theory of social genetic effects. Subsequently, we evaluate the evidence for social genetic effects in livestock and other species, by reviewing estimates of genetic parameters for direct and social genetic effects. Then we describe the results of different selection experiments. Finally, we discuss issues concerning the implementation of social genetic effects in livestock breeding programs. This review demonstrates that selection for socially-affected traits, using methods that target both the direct and social genetic effects, is a promising, but sometimes difficult to use in practice, tool to simultaneously improve production and welfare in livestock.

Maternal and social genetic effects on average daily gain of piglets from birth until weaning

The aim of this study was to investigate whether there is heritable social variation in ADG from birth until weaning in piglets. Nursing and the establishment of teat order are sources of social interaction among suckling piglets nursed by the same sow. If a heritable social effect is present, but ignored, the selected animals might be the most competitive ones with negative effects on growth of their group mates, resulting in less response to selection than expected. The social interaction model was extended with a maternal component to estimate genetic maternal and social effects. Four different animal models were compared: a basic model with a direct heritable effect only; a social model accounting for direct and social heritable effects; a maternal model with a heritable maternal effect in addition to the basic model; and a social-maternal model accounting for direct, social, and maternal heritable effects. Estimates of direct, maternal, and social heritability were 0.07, 0.06, and around 0.0007 (not significantly different from zero, SE = 0.0005), respectively. Total heritable variance, including direct, social, and maternal heritable variance and their covariances ranged from 0.07 to 0.15 of the phenotypic variation. Both maternal models were significantly better than equivalent nonmaternal models (P <or= 0.005). The social model was not significantly better than the basic model (P = 0.102), and the social-maternal model was also not significantly better than the maternal model (P = 0.486). There was no evidence for heritable social effects among piglets in a group. The generally used maternal model fit the data as well as the social-maternal model. Sufficient cross-fostering is needed to partition social and maternal variation.

Improved estimation of inbreeding and kinship in pigs using optimized SNP panels

BackgroundTraditional breeding programs consider an average pairwise kinship between sibs. Based on pedigree information, the relationship matrix is used for genetic evaluations disregarding variation due to Mendelian sampling. Therefore, inbreeding and kinship coefficients are either over or underestimated resulting in reduction of accuracy of genetic evaluations and genetic progress. Single nucleotide polymorphism (SNPs) can be used to estimate pairwise kinship and individual inbreeding more accurately. The aim of this study was to optimize the selection of markers and determine the required number of SNPs for estimation of kinship and inbreeding.ResultsA total of 1,565 animals from three commercial pig populations were analyzed for 28,740 SNPs from the PorcineSNP60 Beadchip. Mean genomic inbreeding was higher than pedigree-based estimates in lines 2 and 3, but lower in line 1. As expected, a larger variation of genomic kinship estimates was observed for half and full sibs than for pedigree-based kinship reflecting Mendelian sampling. Genomic kinship between father-offspring pairs was lower (0.23) than the estimate based on pedigree (0.26). Bootstrap analyses using six reduced SNP panels (n = 500, 1000, 1500, 2000, 2500 and 3000) showed that 2,000 SNPs were able to reproduce the results very close to those obtained using the full set of unlinked markers (n = 7,984-10,235) with high correlations (inbreeding r > 0.82 and kinship r > 0.96) and low variation between different sets with the same number of SNPs.ConclusionsVariation of kinship between sibs due to Mendelian sampling is better captured using genomic information than the pedigree-based method. Therefore, the reduced sets of SNPs could generate more accurate kinship coefficients between sibs than the pedigree-based method. Variation of genomic kinship of father-offspring pairs is recommended as a parameter to determine accuracy of the method rather than correlation with pedigree-based estimates. Inbreeding and kinship coefficients can be estimated with high accuracy using ≥2,000 unlinked SNPs within all three commercial pig lines evaluated. However, a larger number of SNPs might be necessary in other populations or across lines.

The distal end of porcine chromosome 6p is involved in the regulation of skatole levels in boars

BackgroundBoar taint is an unpleasant condition of pork, mainly due to the accumulation of androstenone and skatole in male pigs at onset of puberty. This condition is the cause of considerable economic losses in the pig industry and the most common practice to control it is to castrate male piglets. Because of the economic and animal welfare concerns there is interest in developing genetic markers that could be used in selection schemes to decrease the incidence of boar taint. The Porcine 60 K SNP Beadchip was used to genotype 891 pigs from a composite Duroc sire line, for which skatole levels in fat had been collected.ResultsThe genome-wide association study revealed that 16 SNPs (single nucleotide polymorphisms) located on the proximal region of chromosome 6 were significantly associated with skatole levels. These SNPs are grouped in three separate clusters located in the initial 6 Mb region of chromosome 6. The differences observed between the homozygote genotypes for SNPs in the three clusters were substantial, including a difference of 102.8 ng/g skatole in melted fat between the homozygotes for the ALGA0107039 marker. Single SNPs explain up to 22% of the phenotypic variance. No obvious candidate genes could be pinpointed in the region, which may be due to the need of further annotation of the pig genome.ConclusionsThis study demonstrated new SNP markers significantly associated with skatole levels in the distal region of chromosome 6p. These markers defined three independent clusters in the region, which contain a low number of protein-coding genes. The considerable differences observed between the homozygous genotypes for several SNPs may be used in future selection schemes to reduce skatole levels in pigs

Backtest and novelty behavior of female and castrated male piglets, with diverging social breeding values for growth.

Pigs housed together in a group influence each others growth. Part of this effect is genetic and can be represented in a social breeding value. It is unknown, however, which traits are associated with social breeding values. The aim of this study was, therefore, to investigate whether personality and response to novelty could be associated with social breeding values for growth in piglets. Female and castrated male piglets from 80 litters, with either an estimated relative positive or negative social breeding value (+SBV or -SBV) for growth, were individually tested in a backtest and novel environment test, and group-wise in a novel object (i.e., a feeder with feed) test and human approach test. All tests were performed during the suckling period. No differences between +SBV and -SBV piglets were found for the frequency and latency of struggling and vocalizing in the backtest (at least, P > 0.30). In the novel object test, piglets with a +SBV for growth touched the feeder faster than piglets with -SBV for growth (P = 0.01) and were more frequently present near the person in the human approach test (P < 0.01). No behavioral differences between +SBV and -SBV piglets were found in the novel environment test (at least, P > 0.40), but piglets that struggled more in the backtest walked more in this test (P = 0.02). Behavior was affected by gender in each test. Female piglets were faster than castrated male piglets to start struggling in the backtest (P = 0.047). In the novel object test, females were faster than males to touch the feeder and sample the feed. In the human approach test, they were also faster than male piglets to touch a person (all, P < 0.001). Females were also more frequently present near the feeder (P < 0.001) and person (P = 0.03). In the novel environment test, female piglets explored the floor more (P = 0.046), produced less low- (P = 0.04) and high-pitched vocalizations (P = 0.02), and defecated (P = 0.08) and urinated less than male piglets (P < 0.01). It was concluded that +SBV and -SBV piglets do not differ in their response to the backtest, and only subtle differences were found in their response to novelty. More research is warranted to identify the traits underlying SBV for growth in pigs. Moreover, castrated male piglets seemed to react more fearfully to each test than female piglets.

Growth performance and carcass traits in pigs selected for indirect genetic effects on growth rate in two environments

Production traits such as growth rate may depend on the social interactions between group members. These social interactions may be partly heritable and are referred to as indirect genetic effects (IGE) or social, associative, or competitive genetic effects. Indirect genetic effects may contribute to heritable variation in traits and can therefore be used to increase the response to selection. This, however, has hardly been tested by selection experiments. Our objective was to determine the effects of 1 generation of selection on IGE for growth (IGEg) in pigs on ADG, BW, ADFI, feed efficiency, and postmortem measurements. Sires (n = 24) and dams (n = 64) were selected to create a high vs. low contrast for IGEg in the offspring (n = 480). The IGE difference was 2.8 g ADG per pen mate, corresponding to 14 g higher ADG in high IGEg offspring compared to low IGEg offspring when housed in groups of 6 (i.e., (6 - 1) × 2.8 = 14). Male (barrows) and female (gilts) offspring were housed in groups of 6 of the same IGEg classification, in either barren concrete pens or pens enriched with straw and wood shavings (n = 80 pens). Pigs were followed from birth to slaughter. Data were analyzed in a mixed model with pen as random factor. There was no difference in ADG between high and low IGEg pigs during the finishing period (wk 10 to 23). Opposite to expectations, high IGEg tended to have a 17 g lower ADG from weaning to slaughter (P = 0.08), which was caused by a higher BW of low IGEg pigs in wk 5 (P = 0.008). This led to a 2.3 kg lower carcass weight (P = 0.02) and 2.2 mm less muscle depth for high IGEg pigs (P = 0.03). High IGEg pigs had a higher stomach wall damage score (P = 0.01). Pigs on straw had a 25 g lower ADG during finishing (P = 0.03) and less stomach wall damage (P < 0.001). Fewer interventions against harmful behavior were required in high IGEg pigs. The unexpected results regarding IGEg may be due to several reasons. Despite initial power calculations showing good power, the IGEg contrast between groups may have been too small. Moreover, measures that were taken to limit harmful behavior may have had a substantial role. Harmful behavior such as tail biting may affect ADG and might underlie the effects of selection on IGEg in pigs. Research under commercial circumstances, where harmful behavior is likely to be more profound, may give more accurate insight into the benefits of selecting for IGEg.

A genome-wide association study reveals a novel candidate gene for sperm motility in pigs

Sperm motility is one of the most widely used parameters in order to evaluate boar semen quality. However, this trait can only be measured after puberty. Thus, the use of genomic information appears as an appealing alternative to evaluate and improve selection for boar fertility traits earlier in life. With this study we aimed to identify SNPs with significant association with sperm motility in two different commercial pig populations and to identify possible candidate genes within the identified QTL regions. We performed a single-SNP genome-wide association study using genotyped animals from a Landrace-based (L1) and a Large White-based (L2) pig populations. For L1, a total of 602 animals genotyped for 42,551 SNPs were used in the association analysis. For L2, a total of 525 animals genotyped for 40,890 SNPs were available. After the association analysis, a false discovery rate q-value ≤0.05 was used as the threshold for significant association. No SNPs were significantly associated with sperm motility in L1, while six SNPs on Sus scrofa chromosome 1 (position 117.26-119.56Mb) were significant in L2. The mitochondrial methionyl-tRNA formyltransferase (MTFMT) gene, which affects translation efficiency of proteins in sperm cells, was identified as a putative candidate gene. The significant markers identified in this study may be useful to enhance the genetic improvement of sperm motility by selection of boars at an earlier age under a marker assisted selection strategy.