A molecular genome scan analysis to identify chromosomal regions influencing economic traits in the pig. I. Growth and body composition

Genome scans can be employed to identify chromosomal regions and eventually genes (quantitative trait loci or QTL) that control quantitative traits of economic importance. A three-generation resource family was developed by using two Berkshire grand sires and nine Yorkshire grand dams to detect QTL for growth and body composition traits in pigs. A total of 525 F₂ progeny were produced from 65 matings. All F₂ animals were phenotyped for birth weight, 16-day weight, growth rate, carcass weight, carcass length, back fat thickness, and loin eye area. Animals were genotyped for 125 microsatellite markers covering the genome. Least squares regression interval mapping was used for QTL detection. All carcass traits were adjusted for live weight at slaughter. A total of 16 significant QTL, as determined by a permutation test, were detected at the 5% chromosome-wise level for growth traits on Chromosomes (Chrs) 1, 2, 3, 4, 6, 7, 8, 9, 11, 13, 14, and X, of which two were significant at the 5% genome-wise level and two at the 1% genome-wise level (on Chrs 1, 2, and 4). For composition traits, 20 QTL were significant at the 5% chromosome-wise level (on Chrs 1, 4, 5, 6, 7, 12, 13, 14, 18), of which one was significant at the 5% genome-wise level and three were significant at the 1% genome-wise level (on Chrs 1, 5, and 7). For several QTL the favorable allele originated from the breed with the lower trait mean. Received: 29 November 2000 / Accepted: 27 March 2001     

Quantitative trait loci analysis of a Duroc commercial population highlights differences in the genetic determination of meat quality traits at two different muscles

We performed a whole‐genome scan with 110 informative microsatellites in a commercial Duroc population for which growth, fatness, carcass and meat quality phenotypes were available. Importantly, meat quality traits were recorded in two different muscles, that is, gluteus medius (GM) and longissimus thoracis et lumborum (LTL), to find out whether these traits are determined by muscle‐specific genetic factors. At the whole‐population level, three genome‐wide QTL were identified for carcass weight (SSC7, 60 cM), meat redness (SSC13, 84 cM) and yellowness (SSC15, 108 cM). Within‐family analyses allowed us to detect genome‐wide significant QTL for muscle loin depth between the 3rd and 4th ribs (SSC15, 54 cM), backfat thickness (BFT) in vivo (SSC10, 58 cM), ham weight (SSC9, 69 cM), carcass weight (SSC7, 60 cM; SSC9, 68 cM), BFT on the last rib (SSC11, 48 cM) and GM redness (SSC8, 85 cM; SSC13, 84 cM). Interestingly, there was low positional concordance between meat quality QTL maps obtained for GM and LTL. As a matter of fact, the three genome‐wide significant QTL for colour traits (SSC8, SSC13 and SSC15) that we detected in our study were all GM specific. This result suggests that QTL effects might be modulated to a certain extent by genetic and environmental factors linked to muscle function and anatomical location.     

Mapping quantitative trait loci affecting chicken body size traits via genome scanning

Body size traits reflect the condition of body development, are always mentioned when a breed is described, and are also targets in breeding programmes. In chicken, there are several reports focused on body size traits, such as shank length, tibia length or bone traits. However, no study was carried out on chest width (CW), chest depth (CD), body slope length (BL) and head width (HW) traits. In this study, genome scans were conducted on an F₂ resource population (238 F₂ individuals from 15 full‐sib families derived from an intercross of the White Plymouth Rock with the Silkies Fowl) to identify quantitative trait loci (QTL) associated with CW, CD, BL and HW from 7 to 12 weeks of age. In total, 21 significant or suggestive QTL were found that affected four body size traits. Four QTL reached 1% genome‐wide significance level: at 297 cM on GGA3 (associated with CW at 9 weeks of age), between 155 and 184 cM on GGA1 (affecting BL traits at 9 and 10 weeks of age), at 22 cM on GGA2 (related with BL traits at 12 weeks of age) and at 36 cM on GGA1 (for HW trait at 8 weeks of age).     

Genome-wide identification of quantitative trait loci for carcass composition and meat quality in a large-scale White Duroc × Chinese Erhualian resource population

Carcass and meat quality traits are economically important in pigs. In this study, 17 carcass composition traits and 23 meat quality traits were recorded in 1028 F₂ animals from a White Duroc × Erhualian resource population. All pigs in this experimental population were genotyped for 194 informative markers covering the entire porcine genome. Seventy-seven genome-wide significant quantitative trait loci (QTL) for carcass traits and 68 for meat quality were mapped to 34 genomic regions. These results not only confirmed many previously reported QTL but also revealed novel regions associated with the measured traits. For carcass traits, the most prominent QTL was identified for carcass length and head weight at 57 cM on SSC7, which explained up to 50% of the phenotypic variance and had a 95% confidence interval of only 3 cM. Moreover, QTL for kidney and spleen weight and lengths of cervical vertebrae were reported for the first time in pigs. For meat quality traits, two significant QTL on SSC5 and X were identified for both intramuscular fat content and marbling score in the longissimus muscle, while three significant QTL on SSC1 and SSC9 were found exclusively for IMF. Both LM and the semimembranous muscle showed common QTL for colour score on SSC4, 5, 7, 8, 13 and X and discordant QTL on other chromosomes. White Duroc alleles at a majority of QTL detected were favourable for carcass composition, while favourable QTL alleles for meat quality originated from both White Duroc and Erhualian.     

QTL analysis of white blood cell, platelet and red blood cell-related traits in an F2 intercross between Landrace and Korean native pigs

Haematological traits play important roles in disease resistance and defence functions. The objective of this study was to locate quantitative trait loci (QTL) and the associated positional candidate genes influencing haematological traits in an F₂ intercross between Landrace and Korean native pigs. Eight blood‐related traits (six erythrocyte traits, one leucocyte trait and one platelet trait) were measured in 816 F₂ progeny. All experimental animals were genotyped with 173 informative microsatellite markers located throughout the pig genome. We report that nine chromosomes harboured QTL for the baseline blood parameters: genomic regions on SSC 1, 4, 5, 6, 8, 9, 11, 13 and 17. Eight of twenty identified QTL reached genome‐wide significance. In addition, we evaluated the KIT locus, an obvious candidate gene locus affecting variation in blood‐related traits. Using dense single nucleotide polymorphism marker data on SSC 8 and the marker‐assisted association test, the strong association of the KIT locus with blood phenotypes was confirmed. In conclusion, our study identified both previously reported and novel QTL affecting baseline haematological parameters in pigs. Additionally, the positional candidate genes identified here could play an important role in elucidating the genetic architecture of haematological phenotype variation in swine and in humans.     

Mapping and fine mapping of quantitative trait loci for the number of vertebrae in a White Duroc × Chinese Erhualian intercross resource population

The number of vertebrae is associated with body size and meat production in pigs. To identify quantitative trait loci (QTL) for the number of vertebrae, phenotypic values were measured in 1029 individuals from a White Duroc × Chinese Erhualian intercross F₂ population. A whole genome scan was performed with 194 microsatellite markers in the F₂ population. Four genome‐wide significant QTL and eight chromosome‐wide significant QTL for the number of vertebrae were identified on pig chromosomes (SSC) 1, 2, 6, 7, 10 and 12. The most significant QTL was detected on SSC7 with a confidence interval of 1 cM, explaining 42.32% of the phenotypic variance in the thoracic vertebral number. The significant QTL on SSC1, 2 and 7 confirmed previous reports. A panel of 276 animals representing seven Western and Chinese breeds was genotyped with 34 microsatellite markers in the SSC7 QTL region. No obvious selective sweep effect was observed in the tested breeds, indicating that intensive selection for enlarged body size in Western commercial breeds did not wipe out the genetic variability in the QTL region. The Q alleles for increased vertebral number originated from both Chinese Erhualian and White Duroc founder animals. A haplotype block of approximately 900 kb was found to be shared by all Q‐bearing chromosomes of F₁ sires except for one distinct Q chromosome. The critical region harbours the newly reported VRTN gene associated with vertebral number. Further investigations are required to confirm whether VRTN or two other positional candidate genes, PROX2 and FOS, cause the QTL effect.     

High throughput analyses of epistasis for swine body dimensions and organ weights

High throughput analyses were performed to detect epistatic QTL in 17 body dimension and organ weight traits from a large F₂ pig population derived from a White Duroc and Erhualian intercross. The analyses used a nested test framework to handle multiple tests and a combined search algorithm to map epistatic QTL with empirical genome‐wide thresholds derived via prior permutation. Alternative statistical models (e.g. including vs. excluding carcass weight as a covariate) were tested to develop an in‐depth understanding of the role of epistasis in these kinds of traits. Epistasis signals were detected in only two or three traits under each statistical model studied. The interaction component of each pair of epistatic QTL explained a small proportion (0.7 to 2.1%) of the phenotypic variance in general. About half of the detected epistatic QTL pairs involved one of the two major QTL on porcine chromosomes 7 and 4. In those traits, the Erhualian allele consistently increased the phenotypes for the chromosome 7 QTL but decreased them for the chromosome 4 QTL. Models including carcass weight as covariate detected epistasis in body dimension traits whereas those excluding carcass weight found epistasis in organ weight traits. In addition, the epistasis results suggested that a QTL on chromosome 14 could be important for a number of organ weight traits. Using the high‐throughput analysis tool to examine different statistical models was essential for the generation of a complete picture of epistasis in a whole category of traits.     

Quantitative trait loci for chemical body composition traits in pigs and their positional associations with body tissues, growth and feed intake

In this study, quantitative trait loci (QTL) for chemical and physical body composition, growth and feed intake in pigs were identified in a three-generation full-sib population, developed by crossing Pietrain sires with a commercial dam line. Phenotypic data from 315 F₂ animals were available for protein and lipid deposition measured in live animals by the deuterium dilution technique at 30-, 60-, 90-, 120- and 140-kg body weight. At 140-kg body weight, carcass characteristics were measured by the AutoFOM grading system and after dissection. Three hundred and eighty-six animals from 49 families were genotyped for 51 molecular markers covering chromosomes SSC2, SSC4, SSC8, SSC9, SSC10 and SSC14. Novel QTL for protein (lipid) content at 60-kg body weight and protein (lipid) accretion from 120 to 140 kg were detected on SSC9 near several previously detected QTL for lean and fat tissue in neck, shoulder and ham cuts. Another QTL for lipid accretion was found on SSC8, closely associated with a QTL for intramuscular fat content. QTL for daily feed intake were detected on SSC2 and SSC10. The favourable allele of a QTL for food conversion ratio (FCR) on SSC2 was associated with alleles for increased lean tissue and decreased fat tissue. Because no QTL for growth rate were found in the region, the QTL for FCR is most likely due to a change in body composition. These QTL provide insights into the genomic regulation of chemical or physical body composition and its association with feed intake, feed efficiency and growth.     

On growth, fatness, and form: A further look at porcine Chromosome 4 in an Iberian × Landrace cross

A crossed population between Iberian × Landrace pigs consisting of 321 F₂, 87 F₃, and 85 backcross individuals has been analyzed to refine the number and positions of quantitative trait loci (QTL) affecting shape, growth, fatness, and meat quality traits in SSC4. A multitrait multi-QTL approach has been used. Our results suggest that carcass length and shoulder weight are affected by two loci. The first one, close to the AFABP gene, has a very strong pleiotropic effect on fatness, whereas the second one, in the interval between S0073 and S0214, also affects live weight, although to a lesser extent. This latter QTL would correspond to the FAT1 locus described initially in pigs. It seems that SSC4’s loci play an important role in redistributing total weight, and the Landrace allele increases shoulder weight and carcass length much more than ham or total weight. Furthermore, there is also strong evidence of additional loci influencing pH and color in more distant, telomeric positions.     

QTL for percentage of carcass and carcass parts in a broiler x layer cross

An F₂ experimental population, developed from a broiler layer cross, was used in a genome scan of QTL for percentage of carcass, carcass parts, shank and head. Up to 649 F₂ chickens from four paternal half‐sib families were genotyped with 128 genetic markers covering 22 linkage groups. Total map length was 2630 cM, covering approximately 63% of the genome. QTL interval mapping using regression methods was applied to line‐cross and half‐sib models. Under the line‐cross model, 12 genome‐wide significant QTL and 17 suggestive linkages for percentages of carcass parts, shank and head were mapped to 13 linkage groups (GGA1, 2, 3, 4, 5, 7, 8, 9, 11, 12, 14, 18 and 27). Under the paternal half‐sib model, six genome‐wide significant QTL and 18 suggestive linkages for percentages of carcass parts, shank and head were detected on nine chicken linkage groups (GGA1, 2, 3, 4, 5, 12, 14, 15 and 27), seven of which seemed to corroborate positions revealed by the previous model. Overall, three novel QTL of importance to the broiler industry were mapped (one significant for shank% on GGA3 and two suggestive for carcass and breast percentages on GGA14 and drums and thighs percentage on GGA15). One novel QTL for wings% was mapped to GGA3, six novel QTL (GGA1, 3, 7, 8, 9 and 27) and suggestive linkages (GGA2, 4, and 5) were mapped for head%, and suggestive linkages were identified for back% on GGA2, 11 and 12. In addition, many of the QTL mapped in this study confirmed QTL previously reported in other populations.     

Quantitative trait loci affecting growth in high growth (hg) mice

A genome-wide scan was performed in order to identify Quantitative Trait Loci (QTL) associated with growth in a population segregating high growth (hg), a partially recessive mutation that enhances growth rate and body size in the mouse. A sample of 262 hg/hg mice was selected from a C57BL/6J-hg/hg× CAST/EiJ F₂ cross and typed with 79 SSLP markers distributed across the genome. Eight significant loci were identified through interval mapping. Loci on Chromosomes (Chrs) 2 and 8 affected the growth rate of F₂ mice. Loci on Chr 2 and 11 affected growth rate and carcass lean mass (protein and ash). A locus on Chr 9 modified femur length and another one in Chr 17 affected both carcass lean mass and femur length, but none of these had significant effects on growth rate. Loci on Chrs 5 and 9 modified carcass fat content. Additive effects were positive for C57BL/6J alleles, except for the two loci affecting carcass fatness. Typing of selected markers in 274 +/+ F₂ mice revealed significant interactions between hg and other growth QTL, which were detected as changes in gene action (additive or dominant) and in allele substitution effects. Knowledge about interactions between loci, especially when major genes are involved, will help in the identification of positional candidate genes and in the understanding of the complex genetic regulation of growth rate and body size in mammals. Received: 29 June 2000 / Accepted: 22 November 2000     

Genome‐wide association study identifies quantitative trait loci affecting hematological traits in an F2 intercross between Landrace and Korean native pigs

Changes affecting the status of health and robustness can bring about physiological alterations including hematological parameters in swine. To identify quantitative trait loci (QTL) associated with eight hematological traits (one leukocyte trait, six erythrocyte traits and one platelet trait), we conducted a genome‐wide association study using the PorcineSNP60K BeadChip in a resource population derived from an intercross between Landrace and Korean native pigs. A total of 36 740 SNPs from 816 F₂ progeny were analyzed for each blood‐related trait after filtering for quality control. Data were analyzed by the genome‐wide rapid association using mixed model and regression (GRAMMAR) approach. A total of 257 significant SNPs (P < 1.36 × 10^?6) on SSC3, 6, 8, 13 and 17 were identified for blood‐related traits in this study. Interestingly, the genomic region between 17.9 and 130 Mb on SSC8 was found to be significantly associated with red blood cell, mean corpuscular volume and mean corpuscular hemoglobin. Our results include the identification of five significant SNPs within five candidate genes (KIT, IL15, TXK, ARAP2 and ERG) for hematopoiesis. Further validation of these identified SNPs could give valuable information for understanding the variation of hematological traits in pigs.     

QTL mapping for growth and carcass traits in an Iberian by Landrace pig intercross: additive,dominant and epistatic effects

Results from a QTL experiment on growth and carcass traits in an experimental F2 cross between Iberian and Landrace pigs are reported. Phenotypic data for growth, length of carcass and muscle mass, fat deposition and carcass composition traits from 321 individuals corresponding to 58 families were recorded. Animals were genotyped for 92 markers covering the 18 porcine autosomes (SSC). The results from the genomic scan show genomewide significant QTL in SSC2 (longissimus muscle area and backfat thickness), SSC4 (length of carcass, backfat thickness, loin, shoulder and belly bacon weights) and SSC6 (longissimus muscle area, backfat thickness, loin, shoulder and belly bacon weights). Suggestive QTL were also found on SSC1, SSC5, SSC7, SSC8, SSC9, SSC13, SCC14, SSC16 and SSC17. A bidimensional genomic scan every 10 cM was performed to detect interaction between QTL. The joint action of two suggestive QTL in SSC2 and SSC17 led to a genome-wide significant effect in live weight. The results of the bidimensional genomic scan showed that the genetic architecture was mainly additive or the experimental set-up did not have enough power to detect epistatic interactions.     

Three novel quantitative trait loci for skin thickness in swine identified by linkage and genome‐wide association studies

Skin is the largest organ in the pig body and plays a key role in protecting the body against pathogens and excessive water loss. Deciphering the genetic basis of swine skin thickness would enrich our knowledge about the skin. To identify the loci for porcine skin thickness, we first performed a genome scan with 194 microsatellite markers in a White Duroc × Erhualian F₂ intercross. We identified three genome‐wide significant QTL on pig chromosomes (SSC) 4, 7 and 15 using linkage analysis. The most significant QTL was found on SSC7 with a small confidence interval of ~5 cM, explaining 23.9 percent of phenotypic variance. Further, we conducted a genome‐wide association study (GWAS) using Illumina PorcineSNP60 Beadchips for the F₂ pedigree and a population of Chinese Sutai pigs. We confirmed significant QTL in the F₂ pedigree and replicated QTL on SSC15 in Chinese Sutai pigs. A meta‐analysis of GWASs on both populations detected a genomic region associated with skin thickness on SSC4. GWAS results were generally consistent with QTL mapping. Identical‐by‐descent analysis defined QTL on SSC7 in a 683‐kb region harboring an interesting candidate gene: HMGA1. On SSC15, the linkage disequilibrium analysis showed a haplotype block of 2.20 Mb that likely harbors the gene responsible for skin thickness. Our findings provide novel insights into the genetic basis of swine skin thickness, which would benefit further understanding of porcine skin function.     

Interval mapping of growth in divergent swine cross

A genomic scan of 18 swine autosomal chromosomes was constructed with 119 polymorphic microsatellite (ms) markers to identify quantitative trait loci (QTL) for 11 growth traits in the University of Illinois Meishan × Yorkshire Swine Resource Family. A significant QTL effect was found for post-weaning average daily gain (ADG) between 5.5 and 56 kg of body weight that mapped between markers SW373 and SW1301 near the telomere of Chromosome (Chr) 1 q (SSC1). This QTL effect had a nominal (pointwise) p-value of 0.000007, a genome wide p-value of 0.012, and accounted for 26% of the F₂ phenotypic variance. The same chromosome region also had significant effects on ADG between birth and 56 kg body weight (p-value = .000227), and on ADG between 35 and 56 kg (p-value = .00077). These observations suggest that a significant QTL for post-weaning growth resides on SSC1. Received: 18 May 1998 / Accepted: 6 October 1998     

A whole genome scan to detect quantitative trait loci for gestation length and sow maternal ability related traits in a White Duroc × Erhualian F2 resource population

Gestation length and maternal ability are important to improve the sow reproduction efficiency and their offspring survival. To map quantitative trait loci (QTL) for gestation length and maternal ability related traits including piglet survival rate and average body weight of piglets at weaning, more than 200 F2 sows from a White Duroc × Erhualian resource population were phenotyped. A genome-wide scan was performed with 194 microsatellite markers covering the whole pig genome. QTL analysis was carried out using a composite regression interval mapping method via QTL express. The results showed that total number of born piglets was significantly correlated with gestation length (r = -0.13, P < 0.05). Three QTL were detected on pig chromosome (SSC)2, 8 and 12 for gestation length. The QTL on SSC2 achieved the 5% genome-wide significant level and the QTL on SSC8 was consistent with previous reports. Four suggestive QTL were identified for maternal ability related traits including 1 QTL for survival rate of piglets at weaning on SSC8, 3 QTL for average body weight of piglet at weaning on SSC3, 11 and 13.     

Investigation of the genetic architecture of a bone carcass weight QTL on BTA6

A previous analysis of an F₂/Backcross Charolais × Holstein cross population identified the presence of a highly significant QTL on chromosome 6 (BTA6) affecting the proportion of bone in the carcass. Two closely linked QTL affected birth weight (BW) and body length at birth (BBL). In this report, the marker density around the QTL on BTA6 was increased, adding four additional microsatellite markers across the chromosome and 46 SNPs within the target QTL confidence interval. Of the SNPs, 26 were in positional candidate genes and the remaining 20 provided an even distribution of markers in the target QTL region. As a bone‐related trait, the sum of the bone weight for all the left fore‐ and hindquarter joints of the carcass was analysed. We also studied the BW and BBL. Analyses of the data substantially reduced the QTL confidence interval. No strong evidence was found that the QTL for the three traits studied are different, and we conclude that the results are consistent with a single pleiotropic QTL influencing the three traits, with the largest effects on the proportion of bone in the carcass. The analyses also suggest that none of the SNPs tested is the sole causative variant of the QTL effects. Specifically, the SNP in the NCAPG gene previously reported as a causal mutation for foetal growth and carcass traits in other cattle populations was excluded as the causal mutation for the QTL reported here. Polymorphisms located in other previously identified candidate genes including SPP1, ABCG2, IBSP, MEPE and PPARGC1A were also excluded. The results suggest that SNP51_BTA‐119876 is the polymorphism in strongest linkage disequilibrium with the causal mutation(s). Further research is required to identify the causal variant(s) associated with this bone‐related QTL.     

A genome‐wide linkage analysis for reproductive traits in F2 Large White × Meishan cross gilts

Female reproductive performance traits in pigs have low heritabilities thus limiting improvement through traditional selective breeding programmes. However, there is substantial genetic variation found between pig breeds with the Chinese Meishan being one of the most prolific pig breeds known. In this study, three cohorts of Large White × Meishan F₂ cross‐bred pigs were analysed to identify quantitative trait loci (QTL) with effects on reproductive traits, including ovulation rate, teat number, litter size, total born alive and prenatal survival. A total of 307 individuals were genotyped for 174 genetic markers across the genome. The genome‐wide analysis of the trait‐recorded F₂ gilts in their first parity/litter revealed one QTL for teat number significant at the genome level and a total of 12 QTL, which are significant at the chromosome‐wide level, for: litter size (three QTL), total born alive (two QTL), ovulation rate (four QTL), prenatal survival (one QTL) and teat number (two QTL). Further support for eight of these QTL is provided by results from other studies. Four of these 12 QTL were mapped for the first time in this study: on SSC15 for ovulation rate and on SSC18 for teat number, ovulation rate and litter size.     

Use of a large multiparent wheat mapping population in genomic dissection of coleoptile and seedling growth

Identification of alleles towards the selection for improved seedling vigour is a key objective of many wheat breeding programmes. A multiparent advanced generation intercross (MAGIC) population developed from four commercial spring wheat cultivars (cvv. Baxter, Chara, Westonia and Yitpi) and containing ca. 1000 F₂‐derived, F_6:7 RILs was assessed at two contrasting soil temperatures (12 and 20 °C) for shoot length and coleoptile characteristics length and thickness. Narrow‐sense heritabilities were high for coleoptile and shoot length (h² = 0.68–0.70), indicating a strong genetic basis for the differences among progeny. Genotypic variation was large, and distributions of genotype means were approximately Gaussian with evidence for transgressive segregation for all traits. A number of significant QTL were identified for all early growth traits, and these were commonly repeatable across the different soil temperatures. The largest negative effects on coleoptile lengths were associated with Rht‐B1b (?8.2%) and Rht‐D1b (?10.9%) dwarfing genes varying in the population. Reduction in coleoptile length with either gene was particularly large at the warmer soil temperature. Other large QTL for coleoptile length were identified on chromosomes 1A, 2B, 4A, 5A and 6B, but these were relatively smaller than allelic effects at the Rht‐B1 and Rht‐D1 loci. A large coleoptile length effect allele (a = 5.3 mm at 12 °C) was identified on chromosome 1AS despite the relatively shorter coleoptile length of the donor Yitpi. Strong, positive genetic correlations for coleoptile and shoot lengths (r_g = 0.85–0.90) support the co‐location of QTL for these traits and suggest a common physiological basis for both. The multiparent population has enabled the identification of promising shoot and coleoptile QTL despite the potential for the confounding of large effect dwarfing gene alleles present in the commercial parents. The incidence of these alleles in commercial wheat breeding programmes should facilitate their ready implementation in selection of varieties with improved establishment and early growth.