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Genetic correlation between serum insulin-like growth factor-1 concentration and performance and meat quality traits in Duroc pigs¹

K. Suzuki^*,2, M. Nakagawa^*, K. Katoh^*, H. Kadowaki, T. Shibata, H. Uchida, Y. Obara^* and A. Nishida^*

^* Graduate School of Agricultural Science, Tohoku University, Aoba-ku, Sendai, Miyagi Prefecture 981-8555, Japan; and Miyagi Prefecture Animal Industry Experiment Station, Iwadeyama-cho, Tamatsukuri-gun, Miyagi Prefecture 989-6445, Japan; and Miyagi Agricultural College, Hatatate, Taihaku-ku, Sendai-shi, Miyagi Prefecture 982-0215, Japan

Abstract

This study was intended to examine whether serum IGF-I concentration is appropriate for use as a physiological predictor for genetic improvement of meat production and meat quality traits in pigs. Heritabilities and genetic correlations were estimated for these traits. The Duroc breed used in this study was selected for seven generations for average daily BW gain (DG) from 30 to 105 kg of BW, loin-eye muscle area (EM), backfat thickness (BF), and intramuscular fat (IMF) content. Serum IGF-I concentration of boars and gilts at the fourth generation of selection and that of boars, gilts, and barrows from the fifth to seventh generations of selection were measured at 8 wk (IGFI-8W) for 832 animals and again at the time they reached 105 kg of BW (IGFI-105KG) for 834 animals. A multivariate REML procedure was used to estimate genetic parameters with a model incorporating generation of selection, sex, common environmental effect of litter, and individual additive genetic effects. Heritability estimates for IGFI-8W and IGFI-105KG were 0.23 ± 0.02 and 0.26 ± 0.03, respectively. The estimates of common environmental effect for IGFI-8W and IGFI-105KG were 0.20 ± 0.02 and 0.03 ± 0.01, respectively. Positive genetic correlations were estimated between IGFI-8W and DG (0.26 ± 0.08), EM (0.22 ± 0.10), and IMF (0.32 ± 0.10). Moreover, the positive genetic correlation between IGFI-105KG and EM was 0.42 ± 0.08. These results indicate that serum IGF-I concentration at an early stage of growth was effective for prediction of IMF, but it was not a reliable physiological predictor of genetic merit of meat production traits.

Key Words: Genetic Parameter • Insulin-Like Growth Factor-I • Meat Quality • Pigs • Production Traits

Introduction

Bioactive substances in blood, such as IGF-I, would be useful as selection indexes of production traits because it is easy to collect serum samples from live animals. Furthermore, concentrations measured in young animals would be especially useful for selection if they could predict future performance of animals. Insulin-like growth factor-I is secreted mainly from liver and is stimulated by GH. The main action of IGF-I is mediating GH function. It facilitates cartilage ossification and growth promotion. Use of IGF-I as a physiological criterion for genetic animal improvement is possible because IGF-I concentration increases steadily during animal growth, in contrast to the large circadian variation of GH (Scanes et al., 1987). Low-realized heritabilities of 0.15 and 0.10 for IGF-I concentration were estimated in direct selection for seven (Blair et al., 1989) and five generations (Baker et al., 1991), respectively, in mice. Those studies also reported a positive genetic correlation between BW and serum IGF-I concentration in mice. Bunter et al. (2002) reported that heritabilities for serum IGF-I concentration were in the range of 0.20 to 0.58, and that IGF-I concentration is genetically correlated with backfat depth and feed conversion ratio in pigs. Conversely, negative genetic correlations between IGF-I concentration and growth (Davis and Simmen, 1997) and backfat thickness (BF; Davis and Simmen, 2000) in beef cattle have been estimated. Notwithstanding, little is known regarding genetic correlations between IGF-I concentration and meat production traits. Therefore, this study was intended to estimate heritability of IGF-I and genetic correlations between serum IGF-I concentration and meat production traits. It also investigated whether serum IGF-I concentration is effective as a physiological criterion of selection for higher growth rate using Duroc pigs selected for meat production traits.

Materials and Methods

Animals and Performance Testing Procedures

Duroc pigs used in this experiment were of a line selected for seven generations at the Miyagi Prefecture Animal Industry Experiment Station from 1995 to 2001 (Suzuki et al., 2002). Selection criteria traits were daily gain from 30 to 105 kg of BW (DG), loin-eye muscle area (EM), BF at 105 kg of BW measured by ultrasound technology, and intramuscular fat content (IMF) measured on slaughtered sib pigs. Average population size of each generation was 14 boars and 42 gilts. Gilts farrowed only once, and boars were retained for one 4- to 6-wk breeding period; therefore, a new generation was obtained each year. Pigs were weaned at 4 wk. At 8 wk, one to two male piglets (total 50 piglets) and two to four female piglets (total 100 piglets) from each litter were selected as candidates for boars and gilts based on BW at 8 wk (BW8W). At the same time, approximately 80 piglets in total, comprising mainly boars and sometimes gilts from each litter, were selected for full-sib testing in each generation. This first stage of selection was conducted within litter. Each pig’s blood was collected at the first stage of selection and BF was measured at the half body point and 2 cm away from midline by an A-mode ultrasound machine (EPOCH 2002, Panametrics Japan Co., Ltd., Tokyo, Japan) at 8 wk (BF8W). Boars for full-sib testing were subsequently castrated. The performance tests began when BW reached 30 kg and ended at 105 kg. Therefore, DG was from 30 to 105 kg of BW. Backfat thickness and EM were measured on 105-kg animals on the left side at half body length using an ultrasound (B-mode) color-scanning scope (SR-100; Kaijo Corp., Tokyo, Japan). Computer software determined EM. Feed intake was measured with boars reared individually, and feed conversion ratio (FCR) was calculated from 30 to 105 kg of BW. Blood samples also were collected from candidate boars and gilts and from two full sibs, mainly castrated full brothers at 105 kg of BW without fasting. Pigs were provided ad libitum access to a commercial diet (15% CP, 78% total digestible nutrition, 0.76 % lysine content, DM basis) during the testing periods from 30 to 105 kg of live weight. Pigs had free access to water. Boars were reared individually in performance-testing pens. Gilts and barrows were reared in growing pens and group fed in a concrete-floored building with eight pigs per pen, which provided floor space of 1.2 m² per pig.

Selection Method

The objectives of this selection were to produce an excellent Duroc line for use as terminal sires in meat production with high meat quality traits, and to supply these Duroc boars to pig farmers as commercial terminal sires. Therefore, selection was conducted without a control line at the Miyagi Prefecture Animal Industry Experiment Station in Japan. The first and second generations of selection were performed by an index selection method based on relative desired gains (Yamada et al., 1975). Traits selected for were DG, EM, BF, and IMF. Genetic and phenotypic parameters used to derive the selection criteria were obtained from the performance test data of the first and second generation, respectively. The means of DG, EM, BF, and IMF at the first generation were 865 g, 36.1 cm², 2.34 cm, and 4.3%, respectively. Relative desired gain was established as 135 g, 3.9 cm², -0.54 cm, and 0.7% for DG, EM, BF and IMF, respectively. To avoid rapid disappearance of the base generation’s genes from the population, selection was made within sires for boars and within litters for gilts at the first generation. Breeding values of DG, EM, BF, and IMF were estimated by multiple-trait, animal-model BLUP, from the third generation onward. The breeding values were calculated using the PEST3.1 program (Groeneveld and Kovac, 1990) after estimating genetic parameters by the VCE4 program (Newmaier and Groeneveld, 1998), with models of generation and sex as fixed effects and random effects of individual additive genetic effect and error. Relative economic weights of selection traits were calculated from the relative desired gain. The relative desired gains of DG, EM, BF, and IMF were established from the performance test data of the first generation as described before. The aggregate breeding values were calculated by multiplying the relative economic weights to the EBV of each trait, and the selection was executed. Approximately 15 boars and 50 gilts were selected at each generation. In each generation, inbreeding coefficients for individual pigs were computed. Based on inbreeding information, all matings were planned to minimize the rate of increase in inbreeding.

Carcass Dissection and Meat Quality Measurement

Pigs for full-sib testing (barrows and gilts) were slaughtered by manual low-voltage (200 V) electrical stunning 24 h after feed removal with free access to water. Carcasses were placed in a conventional chiller at 4°C for 24 h. Subsequently, for measuring meat quality in the LM, a 7- to 10-cm-long piece of the loin (two thoracic vertebrae sections above the last rib) was taken from the left half carcass of each pig. External loin adipose tissue was removed. Two pieces of meat, 2 x 2 x 5 cm each, were weighed and vacuum-packaged in polyethylene bags. They were then heated with a water bath of 70°C for 30 min. Then, after cooling at room temperature, two cooked pieces per animal were cut to 1 x 1 x 5 cm. We measured the tenderness (TS, kgf/cm²) with a Tensipresser (TTP-50BXII; Taketomo Electric Co., Tokyo, Japan) developed by Nakai et al. (1992). This machine was developed to accurately evaluate meat tenderness using an up and down motion to imitate chewing action. To determine IMF, two minced loin meat samples of approximately 20 g each were analyzed using the Soxhlet method.

Measurement of Serum IGF-I Concentration

At the first stage of selection at 8 wk of age and at the end of testing when all pigs reached 105 kg of BW, blood samples were collected from the jugular vein of pigs from the first to the seventh generation of selection. However, IGF-I was measured only for boars and gilts at the fourth generation and IGF-I of boars, gilts, and barrows was measured from the fifth to seventh generation. After centrifugal separation for 15 min at 4°C, the serum was preserved at -20°C until used for IGF-I assay. Serum samples were extracted by acid–ethanol extraction to dissociate IGF-I from binding proteins before assaying (Daughaday et al., 1980). Then IGF-I concentrations were assayed in duplicate by RIA following the double-antibody method (Kuhara et al., 1992). Intra- and interassay coefficients were 3.3 and 7.8%, respectively. Minimum detectable concentration was 20 pg/mL. Serum IGF-I concentration measured at 8 wk and that measured at 105 kg of BW were defined as IGFI-8W and IGFI-105KG, respectively. Table 1 shows the total number of IGF-I measurements.

View this table: [in this window] [in a new window]   Table 1. Number of animals, means, standard deviation, heritability, common environmental effect (c2), and phenotypic standard deviation (p) in Duroc pigs

Performance data for DG, EM, BF, BW8W, BF8W, and FCR and meat quality data for IMF and TS, and IGFI-8W and IGFI-105KG were used for the final estimation of genetic parameters. Table 1 shows the number of pigs for each measurement.

The following multiple trait animal model was used for analysis to estimate genetic parameters:

where Y_ijklm = observation for traits i; µ_i = common constant for trait i; and G_ij = fixed effect of selection generation j for trait i (this selection generation effect included the genetic effect of selection and the environmental effect at each generation); S_ik = fixed effect of sex k for trait i; c_il = random effect of common environment l of littermates for trait i; a_im = random additive genetic effect of animal m for trait i; and e_ijklm = random residual effect for trait i.

Seven generations of pedigree information of 1,642 animals with data and of 152 ancestors born before the fourth generation (total 1,794 animals) were included in this analysis. The VCE4.25 program (Neumaier and Groeneveld, 1998) was used to estimate (co)variance components and their respective standard error. Standard errors of heritability estimates and genetic correlations were also estimated with the VCE4.25 program. The GLM procedure of SAS (SAS Inst., Inc., Cary, NC) was used to obtain sex x generation least squares means of IGFI-8W and IGFI-105KG accounting for fixed effect of sex, generation, and sex x generation interaction and to test significance.

Results

Table 1 shows heritability estimates for meat production traits and serum IGF-I concentration. At the fourth generation of selection, IGF-I concentration was measured with boar and gilt candidates; from the fifth to seventh generations of selection, it was measured with these candidates and their two full sibs. Heritability estimates of IGFI-8W, IGFI-105KG, and BW8W were similar (0.23, 0.26, and 0.24, respectively). Table 1 also shows estimates of the proportion of the common environmental variance (c²). Its estimates for IGFI-8W and BW8W were higher than that for IGFI-105KG.

Table 2 presents genetic and phenotypic correlations of IGF-I concentration (IGFI-8W and IGFI-105KG) with selection traits (DG, EM, BF, and IMF), and correlated traits (TS, BW8W, BF8W, and FCR). The genetic correlation between IGFI-8W and BW8W was moderate and those between IGFI-8W and DG, EM, IMF, BF8W, and FCR were low. In addition, genetic correlations of IGFI-8W with BF and TS were low. Phenotypic correlations between them were 0.1 or less, except for correlations between IGFI-8W and BW8W, and BF8W. Although IGFI-105KG showed moderately high genetic correlations with EM and TS, it had low genetic correlations with BF, BW8W, and BF8W. In addition, the estimated genetic correlation between IGFI-8W and IGFI-105 KG was high, but the estimated phenotypic correlation was low.

Present results suggest that the heritability for serum IGF-I concentration was low and the common environmental effect on the growth performance was large in early stage of growth in pig. Blair et al. (1989) and Baker et al. (1991) reported heritability estimates of 0.15 for serum IGF-I concentration at 6 wk of age, and of 0.10 for the serum IGF-I concentration at 12 wk in mice. Bunter et al. (2002) reviewed heritability estimates ranging from 0.20 to 0.58 and pooled estimates of 0.28 and 0.32, including and excluding estimates from restricted feeding data. Hermesch et al. (2001) estimated the heritability (0.24) and common environmental effect (0.13) for juvenile IGF-I concentration at 4 wk. In addition, Cameron et al. (2003) reported a high and significant common environment variance component (0.46) for serum IGF-I concentration at 6 wk. Cameron et al. (2003) pointed out that a genetic analysis of serum IGF-I concentration data, measured at an early age, should include a common environment effect in the model to avoid overestimating heritability. If the common environmental effect had not been included in the present analysis, the estimated heritability of IGFI-8W would have been higher (0.37). Heritability is inferred to be low judging from the present result and other reports.

This research was mainly intended to examine whether the IGF-I concentration measured at an early stage of growth is effective as a physiological predictor of meat production traits at a later stage of growth. Therefore, we estimated genetic and phenotypic correlations between serum IGF-I concentration and meat production and meat quality traits. Results suggest that serum IGFI-8W was a useful index of growth and fat accumulation up to 8 wk because IGFI-8W showed a moderate, positive genetic and phenotypic correlation with BW8W and BF8W. However, genetic correlations of IGFI-8W with DG, FCR, EM, BF, and TENDERNESS were lower than those with BW8 and BF8W. The present estimates of genetic correlation with these traits are different in the magnitude and direction from previously reported estimates. For growth rate, Baker et al. (1991) reported a realized genetic correlation of 0.58 and a phenotypic correlation of 0.38 between IGF-I concentration and BW at 12 wk in mice. On the other hand, Hermesch et al. (2001) estimated a genetic correlation of 0.12 ± 0.12 between IGF-I measured at 4 wk and the lifetime ADG. Bunter et al. (2002) also reported a low genetic correlation of 0.15 between IGF-I concentration measured at around 4 to 5 wk and lifetime ADG in their review. It seems that serum IGF-I concentration at an early stage of growth is not an effective physiological predictor of genetic merit for production traits during performance test. A high genetic correlation of 0.50 between backfat thickness and serum IGF-I concentration was reported (Bunter et al., 2002). However, the genetic correlation between IGFI-8W and BF at 105 kg of BW was low in the present study. The result of administering serum IGF-I to Meishan pigs (Klindt et al., 1998) was a significant increase in backfat thickness. On the other hand, Buonomo and Klindt (1993) reported that selection for increased backfat thickness of the pig increased serum IGF-2 concentration. In addition, Owens et al. (1999) reported that IGF-I controls growth of lean meat and that IGF-2 controls adipose tissue growth. In most countries, the main objectives of pig improvement have been increasing lean growth rate and decreasing backfat thickness. In contrast, moderate thickness in the dressed carcass is important in Japan. Therefore, the BF of the Duroc breed used in the present study was considered to be thick (average 2.37 cm). Apparently, the genetic difference in the fat accumulation of the pig sample used may influence the magnitude of genetic correlation. Along with backfat thickness, high genetic correlations between IGF-I concentration and FCR have been reported in pig (Bunter et al., 2002) and beef cattle (Johnston et al., 2002). The present study estimated lower genetic and phenotypic correlations. A moderate genetic correlation of 0.32 between IGFI-8W and IMF was estimated. No reports have addressed the relation between serum IGF-I concentration and meat quality traits. If IMF could be estimated from serum IGF-I concentration, such information would be important and relatively easily obtained. Duroc pigs used in present study can accumulate more intramuscular fat than other breeds or lines. Therefore, it is necessary to confirm the relationship between IGF-I and IMF with other breeds showing low intramuscular fat accumulation.

Compared with the genetic correlations of EM and TS with IGFI-8W measured at 8 wk, those with IGFI-105KG measured at an older age increased. These results suggest that serum IGF-I concentration is related to an increase in EM thickness and the amount of the lean meat. Serum IGF-I concentration of boars increased considerably from 8 wk to 105 kg of BW compared with gilts and barrows in every generation. That result suggests that the expression of IGF-I concentration is limited by other hormonal factors. Genetic correlations of BW8W, BF8W, BF at 105 kg, and FCR with IGFI-105KG were lower than with IGFI-8W. Moreover, the genetic correlations of DG and IMF with IGFI-105KG did not changed compared to those with IGFI-8W. These changes suggest that the physiological function of IGF-I depends on the animal’s age. Cameron et al. (2003) also reported that the serum IGF-I concentration measured at 6 wk was positively related with ultrasonic backfat depth and the FCR, whereas serum IGF-I concentration measured at the end of test (90 kg of BW) was negatively correlated with BF and the FCR.

Implications

A positive genetic correlation of serum insulin-like growth factor I concentration at 8 wk of age in pigs with intramuscular fat was estimated. Furthermore, a moderate genetic correlation between serum insulin-like growth factor I concentration at 105 kg of body weight and loin muscle area also was estimated. These results suggest that serum insulin-like growth factor I concentration has some relation to growth traits and meat production traits. It may be useful as an indirect selection criterion in the early growth stage to evaluate future ability of intramuscular fat accumulation in pig breeding.

Footnotes

¹ We gratefully acknowledge A. F. Parlow for the IGF-I antibody provided by NIDDK, USA, and N. D. Cameron for comments on the manuscript.

² Correspondence—phone: 81-22-717-8697; fax: 81-22-717-8697;e-mail: k1suzuki{at}bios.tohoku.ac.jp.

Received for publication August 16, 2003. Accepted for publication December 17, 2003.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Suzuki, K. Articles by Nishida, A. Search for Related Content PubMed PubMed Citation Articles by Suzuki, K. Articles by Nishida, A.