A Genome-Wide Association Study Reveals Dominance Effects on Number of Teats in Pigs

Dominance has been suggested as one of the genetic mechanisms explaining heterosis. However, using traditional quantitative genetic methods it is difficult to obtain accurate estimates of dominance effects. With the availability of dense SNP (Single Nucleotide Polymorphism) panels, we now have new opportunities for the detection and use of dominance at individual loci. Thus, the aim of this study was to detect additive and dominance effects on number of teats (NT), specifically to investigate the importance of dominance in a Landrace-based population of pigs. In total, 1,550 animals, genotyped for 32,911 SNPs, were used in single SNP analysis. SNPs with a significant genetic effect were tested for their mode of gene action being additive, dominant or a combination. In total, 21 SNPs were associated with NT, located in three regions with additive (SSC6, 7 and 12) and one region with dominant effects (SSC4). Estimates of additive effects ranged from 0.24 to 0.29 teats. The dominance effect of the QTL located on SSC4 was negative (−0.26 teats). The additive variance of the four QTLs together explained 7.37% of the total phenotypic variance. The dominance variance of the four QTLs together explained 1.82% of the total phenotypic variance, which corresponds to one-fourth of the variance explained by additive effects. The results suggest that dominance effects play a relevant role in the genetic architecture of NT. The QTL region on SSC7 contains the most promising candidate gene: VRTN. This gene has been suggested to be related to the number of vertebrae, a trait correlated with NT.

[1]  G. Shull.  The composition of a field of maize , 1908 .

[2]  C. Davenport.  DEGENERATION, ALBINISM AND INBREEDING. , 1908, Science.

[3]  A. Bruce.  THE MENDELIAN THEORY OF HEREDITY AND THE AUGMENTATION OF VIGOR. , 1910, Science.

[4]  C. Stern.  Negative Heterosis and Decreased Effectiveness of Alleles in Heterozygotes. , 1948, Genetics.

[5]  J. King,et al.  Carcass length in the bacon pig; its association with vertebrae numbers and prediction from radiographs of the young pig. , 1960 .

[6]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[7]  B. Bereskin,et al.  Carcass Traits of Purebred Durocs and Yorkshires and their Crosses1 , 1971 .

[8]  P. Sellier.  The basis of crossbreeding in pigs; A review , 1976 .

[9]  G. Barbato.  Genetic architecture of carcass composition in chickens. , 1992, Poultry science.

[10]  J Li,et al.  Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. , 1995, Genetics.

[11]  W. Beavis.  QTL Analyses: Power, Precision, and Accuracy , 1997, Molecular Dissection of Complex Traits.

[12]  Andrew H. Paterson,et al.  Molecular Dissection of Complex Traits , 1997 .

[13]  T. Awata,et al.  Quantitative trait loci (QTL) analysis in a Meishan x Göttingen cross population. , 2000, Animal genetics.

[14]  Colin T. Whittemore,et al.  Impact of biotechnology on (cross)breeding programmes in pigs , 2000 .

[15]  M. Groenen,et al.  A whole-genome scan for quantitative trait loci affecting teat number in pigs. , 2001, Journal of animal science.

[16]  D. Pomp,et al.  Identification of quantitative trait loci affecting reproduction in pigs. , 2001, Journal of animal science.

[17]  J. L. Campo,et al.  Estimation of heritability for heterophil:lymphocyte ratio in chickens by restricted maximum likelihood. Effects of age, sex, and crossing. , 2002, Poultry science.

[18]  Robin Thompson,et al.  ASREML user guide release 1.0 , 2002 .

[19]  S. Sato,et al.  Quantitative trait loci analysis for growth and carcass traits in a Meishan x Duroc F2 resource population. , 2003, Journal of animal science.

[20]  G. Moser,et al.  Genome-wide linkage and QTL mapping in porcine F2 families generated from Pietrain, Meishan and Wild Boar crosses , 2003 .

[21]  M. Cooper,et al.  Simulating the effects of dominance and epistasis on selection response in the CIMMYT wheat breeding program using QuCim , 2004 .

[22]  D. Pomp,et al.  A genome scan for quantitative trait loci and imprinted regions affecting reproduction in pigs. , 2004, Journal of animal science.

[23]  N. Reinsch,et al.  The number of ribs and vertebrae in a Piétrain cross: variation, heritability and effects on performance traits , 2004 .

[24]  J. Noguera,et al.  QTL mapping for teat number in an Iberian-by-Meishan pig intercross. , 2005, Animal genetics.

[25]  G. Shull.  Duplicate genes for capsule-form inBursa bursa-pastoris , 2018, Zeitschrift für induktive Abstammungs- und Vererbungslehre.

[26]  T. Awata,et al.  Two quantitative trait loci on Sus scrofa chromosomes 1 and 7 affecting the number of vertebrae. , 2005, Journal of animal science.

[27]  Mark Daly,et al.  Haploview: analysis and visualization of LD and haplotype maps , 2005, Bioinform..

[28]  G. Karbani,et al.  Cancer by negative heterosis: breast and ovarian cancer excess in hybrids of inbred ethnic groups. , 2005, Medical hypotheses.

[29]  S. Sato,et al.  Identification of quantitative trait loci affecting corpora lutea and number of teats in a Meishan x Duroc F2 resource population. , 2006, Journal of animal science.

[30]  Si-wen Jiang,et al.  Detection of quantitative trait loci associated with several internal organ traits and teat number trait in a pig population. , 2007, Journal of genetics and genomics = Yi chuan xue bao.

[31]  Yurii S. Aulchenko,et al.  BIOINFORMATICS APPLICATIONS NOTE doi:10.1093/bioinformatics/btm108 Genetics and population analysis GenABEL: an R library for genome-wide association analysis , 2022 .

[32]  H. Piepho,et al.  Genetic Basis of Heterosis for Growth-Related Traits in Arabidopsis Investigated by Testcross Progenies of Near-Isogenic Lines Reveals a Significant Role of Epistasis , 2007, Genetics.

[33]  R. Bates,et al.  Quantitative trait locus mapping in an F2 Duroc x Pietrain resource population: II. Carcass and meat quality traits. , 2008, Journal of animal science.

[34]  A. Archibald,et al.  Quantitative trait loci for production traits in pigs: a combined analysis of two Meishan x Large White populations. , 2008, Animal genetics.

[35]  P. VanRaden,et al.  Efficient methods to compute genomic predictions. , 2008, Journal of dairy science.

[36]  C. Haley,et al.  Genome-wide QTL mapping for three traits related to teat number in a White Duroc × Erhualian pig resource population , 2009, BMC Genetics.

[37]  Crossbreeding parameters of general immune response traits in White Leghorn chickens , 2008 .

[38]  Y. Billon,et al.  Detection of quantitative trait loci for teat number and female reproductive traits in Meishan × Large White F2 pigs. , 2008, Animal : an international journal of animal bioscience.

[39]  L. Moyle,et al.  Complex Epistasis for Dobzhansky–Muller Hybrid Incompatibility in Solanum , 2009, Genetics.

[40]  D. Milan,et al.  Genome-wide identification of quantitative trait loci for carcass composition and meat quality in a large-scale White Duroc x Chinese Erhualian resource population. , 2009, Animal genetics.

[41]  Denis Milan,et al.  Design of a High Density SNP Genotyping Assay in the Pig Using SNPs Identified and Characterized by Next Generation Sequencing Technology , 2009, PloS one.

[42]  L. Varona,et al.  A note on mate allocation for dominance handling in genomic selection , 2010, Genetics Selection Evolution.

[43]  Takeshi Hayashi,et al.  Identification of a second gene associated with variation in vertebral number in domestic pigs , 2011 .

[44]  M. Groenen,et al.  Combining two Meishan F2 crosses improves the detection of QTL on pig chromosomes 2, 4 and 6 , 2010, Genetics Selection Evolution.

[45]  J. Steibel,et al.  Identification of Carcass and Meat Quality QTL in an F2 Duroc × Pietrain Pig Resource Population Using Different Least-Squares Analysis Models , 2011, Front. Gene..

[46]  H. Bovenhuis,et al.  Genome-wide association of milk fatty acids in Dutch dairy cattle , 2011, BMC Genetics.

[47]  C. Haley,et al.  High throughput analyses of epistasis for swine body dimensions and organ weights. , 2011, Animal genetics.

[48]  J. Steibel,et al.  Genome-Wide Linkage Analysis of Global Gene Expression in Loin Muscle Tissue Identifies Candidate Genes in Pigs , 2011, PloS one.

[49]  J. Dekkers,et al.  Genetic improvement of the pig. , 2011 .

[50]  M. Rothschild,et al.  The genetics of the pig , 2011 .

[51]  R. Wellmann,et al.  Bayesian models with dominance effects for genomic evaluation of quantitative traits. , 2012, Genetics research.

[52]  M. Lund,et al.  Estimating Additive and Non-Additive Genetic Variances and Predicting Genetic Merits Using Genome-Wide Dense Single Nucleotide Polymorphism Markers , 2012, PloS one.

[53]  E. Wall,et al.  Genomic associations with somatic cell score in first-lactation Holstein cows. , 2012, Journal of dairy science.

[54]  M. Groenen,et al.  The Imprinted Gene DIO3 Is a Candidate Gene for Litter Size in Pigs , 2012, PloS one.

[55]  H. Bovenhuis,et al.  Genomic regions associated with bovine milk fatty acids in both summer and winter milk samples , 2012, BMC Genetics.

[56]  Bronwen L. Aken,et al.  Analyses of pig genomes provide insight into porcine demography and evolution , 2012, Nature.

[57]  M. Goddard.  Uses of genomics in livestock agriculture , 2012 .

[58]  Z. Zhang,et al.  Mapping and fine mapping of quantitative trait loci for the number of vertebrae in a White Duroc × Chinese Erhualian intercross resource population. , 2012, Animal genetics.

[59]  L. Andersson,et al.  Modelling of genetic interactions improves prediction of hybrid patterns--a case study in domestic fowl. , 2012, Genetics research.

[60]  Ming Yang,et al.  A Further Look at Porcine Chromosome 7 Reveals VRTN Variants Associated with Vertebral Number in Chinese and Western Pigs , 2013, PloS one.

[61]  B. Kinghorn,et al.  Prediction of heterosis using genome-wide SNP-marker data: application to egg production traits in white Leghorn crosses , 2013, Heredity.

[62]  Xiaolin Wu,et al.  Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era , 2012, Nucleic Acids Res..

[63]  J. Tetens,et al.  Novel Use of Derived Genotype Probabilities to Discover Significant Dominance Effects for Milk Production Traits in Dairy Cattle , 2013, Genetics.

[64]  Luis Varona,et al.  On the Additive and Dominant Variance and Covariance of Individuals Within the Genomic Selection Scope , 2013, Genetics.

[65]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[66]  M. Satoh,et al.  Including Dominance Effects in the Genomic BLUP Method for Genomic Evaluation , 2014, PloS one.