SNP- and haplotype-based genome-wide association studies for growth, carcass, and meat quality traits in a Duroc multigenerational population

Abstract

Background: The aim of the present study was to compare the power of single nucleotide polymorphism (SNP)-based genome-wide association study (GWAS) and haplotype-based GWAS for quantitative trait loci (QTL) detection, and to detect novel candidate genes affecting economically important traits in a purebred Duroc population comprising seven-generation pedigree. First, we performed a simulation analysis using real genotype data of this population to compare the power (based on the null hypothesis) of the two methods. We then performed GWAS using both methods and real phenotype data comprising 52 traits, which included growth, carcass, and meat quality traits.

Results: In total, 836 animals were genotyped using the Illumina PorcineSNP60 BeadChip and 14 customized SNPs from regions of known candidate genes related to the traits of interest. The power of SNP-based GWAS was greater than that of haplotype-based GWAS in a simulation analysis. In real data analysis, a larger number of significant regions was obtained by SNP-based GWAS than by haplotype-based GWAS. For SNP-based GWAS, 23 genome-wide significant SNP regions were detected for 17 traits, and 120 genome-wide suggestive SNP regions were detected for 27 traits. For haplotype-based GWAS, 6 genome-wide significant SNP regions were detected for four traits, and 11 genome-wide suggestive SNP regions were detected for eight traits. All genome-wide significant SNP regions detected by haplotype-based GWAS were located in regions also detected by SNP-based GWAS. Four regions detected by SNP-based GWAS were significantly associated with multiple traits: on Sus scrofa chromosome (SSC) 1 at 304 Mb; and on SSC7 at 35-39 Mb, 41-42 Mb, and 103 Mb. The vertnin gene (VRTN) in particular, was located on SSC7 at 103 Mb and was significantly associated with vertebrae number and carcass lengths. Mapped QTL regions contain some candidate genes involved in skeletal formation (FUBP3; far upstream element binding protein 3) and fat deposition (METTL3; methyltransferase like 3).

Conclusion: Our results show that a multigenerational pig population is useful for detecting QTL, which are typically segregated in a purebred population. In addition, a novel significant region could be detected by SNP-based GWAS as opposed to haplotype-based GWAS.

Keywords: Duroc pigs; Haplotype-based GWAS; Known candidate genes; Production traits; SNP-based GWAS.

Fig. 1

Power to achieve 5 % genome-wide significance in simulation analysis. The x-axis indicates QTL heritability and the y-axis represents the power to detect QTL. Results of varying minor allele frequency (MAF) categories (low and high) and models (SNP-based and haplotype-based genome-wide association studies) are shown

Fig. 2

Power to achieve 5 % genome-wide significance within different ranges around selected QTL in simulation analysis. The y-axis represents the power to detect QTL. The results of the SNP-based genome-wide association study (GWAS) in high and low minor allele frequency (MAF) scenarios and those of haplotype-based GWAS in a high MAF scenario are shown. Three different ranges around the selected QTL were evaluated. QTL ± 0.5 Mb: The region ranged from ±0.5 Mb apart from the selected QTL. QTL ± 0.5–1.0 Mb: The region ranged from ±0.5 to 1.0 Mb apart from the selected QTL. QTL ± 1.0–2.0 Mb: The region ranged from ±1.0 to 2.0 Mb apart from the selected QTL

Fig. 3

Trait associations across genomic regions analyzed by SNP-based and haplotype-based genome-wide association studies (GWAS). Each row represents a trait, and each column, a genomic region containing SNPs that are genome-wide suggestively or significantly associated with a trait. Only traits with at least one associated SNP and SNPs associated with at least one trait are shown. Each summary shows the results of growth traits (a) carcass traits (b) and meat quality traits (c). SSC, Sus scrofa chromosome; DG, Average daily gain; LEA, Ultrasound loin muscle area; BF, Ultrasound backfat thickness; HEIGHT, Height at withers; FW, Front width; CW, Chest width; CD, Chest depth; CC, Circumference of chest; CCB at F(/R) 30(/105), Circumference of cannon bone at front (/Rear) (at 30 kg/105 kg); SCORE at F(/R) 30(/105), Front (/Rear) leg score at 30 kg (/105 kg); CL, Carcass length; CL1, Carcass length I; CL2, Carcass length II; CL3, Carcass length III; CT, Carcass thickness; TVN, Thoracic vertebrae number; LVN, Lumbar vertebrae number; BSFT, Subcutaneous fat thickness (Back); LSFT, Subcutaneous fat thickness (Loin); 45r, carcass cross section at fourth–fifth rib; HBL, carcass cross section at half-body length; LEA at 45r, Longissimus muscle area at 45r; LEA at HBL, Longissimus muscle area at HBL; IFA at 45r, Intermuscular fat area at 45r; ALLFA at 45r, All fat area of 45r; SFA at HBL, Subcutaneous fat area at HBL; IFA at HBL, Intermuscular fat area at HBL; ALLFA at HBL, All fat area at HBL; MOS, Moisture; IMF, Intramuscular fat; PROT, Protein; COOK, Cooking loss; WHC, Centrifugal water-holding capacity; SF, Shear force value; M-a*, Redness of longissimus muscle; M-b*, Yellowness of longissimus muscle; F-L*, Lightness of subcutaneous fat; F-a*, Redness of subcutaneous fat; F-b*, Yellowness of subcutaneous fat

Fig. 4

Regional plots of several loci associated with 13 traits. The x-axis indicates the Mb, and the y-axis indicates -log₁₀ (p-value). Gene loci and their strands were annotated based on Sscrofa10.2 assembly from the Ensemble database (http://asia.ensembl.org/Sus_scrofa/Info/Index?db=core). Dashed line indicates the threshold of the Bonferroni 5 % genome-wide significance level. a Plots in chromosome 1 (304.2–305.0 Mb) for average daily gain (DG), backfat thickness (BF), chest width (CW), and circumference of chest (CC). b Plots in chromosome 7 (102.8–103.9 Mb) for Carcass length (CL), Carcass length I (CL1), Carcass length II (CL2), Carcass length III (CL3), and Thoracic vertebrae number (TVN). c Plots in chromosome 7 (34.2–42.5 Mb) for circumference of cannon bone at front (CCB at F105), circumference of cannon bone at rear (CCB at R105), Subcutaneous fat area of carcass cross section at half-body length (SFA at HBL), and All fat area of carcass cross section at half-body length (ALLFA at HBL)