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Poult Sci 2008. 87:1098-1104. doi:10.3382/ps.2007-00504
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GENETICS

Estimation of Genetic Parameters for Contents of Intramuscular Fat and Inosine-5'-Monophosphate and Carcass Traits in Chinese Beijing-You Chickens1

J. L. Chen*, G. P. Zhao*, M. Q. Zheng*, J. Wen*,2 and N. Yang{dagger}

* Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100094, China; and {dagger} College of Animal Science and Technology, China Agricultural University, Beijing 100094, China

2 Corresponding author: wenj{at}iascaas.net.cn


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study was conducted to estimate genetic parameters of meat quality-related traits by a MTDFREML procedure, using 1,069 purebred Beijing-You full-sib male chickens derived from the first 2 generations of divergent selection for the percentage of intramuscular fat (IMF) and selection for increased inosine-5'-monophosphate content (IMP) in breast meat. The results show that estimated heritability of IMP was moderate (0.23), and heritability of IMF was low (0.11). Other traits with high heritabilities, ranging between 0.56 and 0.79, were BW, abdominal fat weight (AFW), breast meat yield, ratio of breast meat yield to evisceration weight (BMP), leg muscle yield, comb weight, and ratio of comb weight to BW (CWP). Moderate heritabilities for the ratio of AFW to BW (AFP) and leg muscle yield to evisceration weight were estimated, 0.24 and 0.32, respectively. Lower significant phenotypic correlations of IMP with BMP and ratio of leg muscle weight to evisceration weight were discovered (P < 0.05), whereas IMF exhibited slightly positive, though significant, phenotypic correlations with BW (0.11) and AFP (0.27). Genetic correlations of IMP with BW and CWP were negative (–0.38 and –0.62, respectively), whereas a high positive genetic correlation was found between IMP and BMP (0.57). It was found that IMF had high genetic correlations with BW (0.75) and AFW (0.66) and moderate correlations with AFP (0.32) and CWP (0.40). A low positive genetic correlation was estimated between IMP and IMF (0.27). In conclusion, both IMP and IMF contents in chicken meat have the potential to be increased through genetic selection with little or no positive effect on BW. Furthermore, close managerial control of growth rate (and BW) will be needed to assure high quality of chicken meat so that increased IMP and IMF can be obtained with less abdominal fat deposited.

Key Words: genetic parameter • inosine-5'-monophosphate • intramuscular fat • chicken


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
During the past decades, poultry breeding has been predominantly focused on increasing rate of gain, meat yield, and improving body composition. At the same time, poultry production has dramatically increased, meeting both consumer demand and commercial profit requirements desired by producers and processors. The sizeable responses in these traits to genetic selection have, however, had an effect on the taste quality of broiler chicken meat, such that it is now substantially different from meat of more traditional slow-growing chickens (Berri et al., 2001; Chen et al., 2004b, which leads consumers to seek better tasting chicken meat (Rizzi et al., 2007). This trend is particularly clear in China and some Southeast Asian countries and regions. At present, this type of chicken represents almost 50% of the market share of meat-type birds in China. As one example, the Beijing-You (B-Y) is a famous Chinese native chicken with excellent meat taste, but it has an inferior growth rate and feed conversion rate compared with the conventional broilers.

Many studies showed that inosine-5'-monophosphate (IMP) and intramuscular fat (IMF) contribute to the sensory perception of meat delicacy. Early in 1931, Kodama found that IMP was an umami substance (Kuchiba-Manabe et al., 1991). Yamaguchi (1967) evaluated the sensory effect of IMP. Chen et al. (2004c carried out a sensory test to demonstrate the effects of IMP levels added to chicken meat soup or clean water. The results showed that the umami taste score was obviously increased by adding small amounts of IMP (15 mg/g) together with monosodium glutamate (15 mg/g) compared with 200 mg/g of monosodium glutamate added alone. Inosine-5'-mono-phosphate has been widely used as a flavor enhancer to increase palatability.

Several investigations have shown that IMF contributed to sensory palatability of beef through affecting tenderness, juiciness, and flavor (Oddy et al., 2001; Thompson, 2004). Nishimura et al. (1999) reported that IMF reduced toughness of beef longissimus through physically altering the structure of connective tissue of muscle. Similar results were found in a study using pork (Schwab et al., 2006). Additionally, the juiciness and flavor of broiler meat is influenced by IMF (Chizzolini et al., 1999).

Heritability of flavor intensity, juiciness, tenderness, and overall acceptability of beef (O’Ferrall et al., 1989) and pork (Lo et al., 1992) have been estimated. Heritability of porcine IMF was reported by Larzul et al. (1997), Knapp et al. (1997), and Fernandez et al. (2003). Increasing IMF content through genetic selection has been used to improve the meat quality of pork (Suzuki et al., 2005a,b). Very few estimates of heritability of IMF and IMP and genetic correlation between IMP and IMF and with other important body composition traits have been published. A few reports have estimated heritabilities of abdominal fat percentage and IMF percentage in meat-type broilers (Zerehdaran et al., 2004; Zhao et al., 2006).

Because of the high heritability of the yields of breast muscle (Le Bihan-Duval et al., 1998, 1999; Rance et al., 2002) and abdominal fat (Le Bihan-Duval et al., 1998; Rance et al., 2002), selection pressure to increase breast muscle yield and decrease abdominal fat have been successful.

The aim of the present study was to estimate heritabilities and phenotypic and genetic correlations for IMP, IMF, and other associated traits in a traditional Chinese meat-breed chicken, the B-Y.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Birds and Diets

Genetic parameters were estimated using 1,069 B-Y full-sib male chickens. Samples were obtained from the first 2 generations of 2 experimental populations designed for divergent selection on IMF content (+IMF and –IMF) and selection for increased IMP content (+IMP). A base population consisted of 100 males and 600 females of BY from a conservation population. From this base population, 48 males and 144 females were randomly chosen, and IMF and IMP contents were measured on their offspring (G0). Based upon the average values of IMP or IMF for each full-sib within G0, 20 males and 100 females were chosen as the founder animals of the line selected for increased IMP (+IMP) and 15 males and 65 females for each of the 2 lines divergently selected for IMF (+IMF and –IMF). Selected breeder hens were artificially inseminated twice weekly, and eggs were then collected from the third to twentieth day (1 hatch). Full-sib families were used to derive the mean family value of IMP and IMF, with a 1:3 to 1:5 ratio of males to females in each sire family. In each full family, at least 3 male chickens were randomly chosen and slaughtered at 90 d of age. The selected breeders all came from families with a mean family value for IMP above the line average and above (+IMF) or below (–IMF) the line average for IMF. No more than 3 male or female breeders were used from any selected dam family. The numbers of families and samples and measured values for the tested traits are presented later in Table 1Go.


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  		Table 1. Statistical summary of IMP, IMF, and body composition traits in selected lines of Beijing-You chickens1
 
All birds were wing-banded at 1 d of age and reared under the same conditions in stair-step caging at the experimental farm of the Institute of Animal Science, Chinese Academy of Agricultural Sciences. Feed and water were provided ad libitum until 90 d of age. All birds were fed the same corn-soybean diet, containing 12.12 MJ/kg of ME and 20% CP from 0 to 8 wk, then 11.70 MJ/kg of ME and 15% CP after 9 wk.

Sampling and Measurements

Randomly sampled birds, within families, were weighed and slaughtered at 90 d of age (the typical market time for B-Y chickens). After depilation for 3 min in water at 65°C, birds were submerged in cold water for 3 min at 15 to 20°C and then dissected immediately at room temperature (18 to 22°C). The time was controlled to about 120 min from slaying to sample storage when the samples of breast and leg muscle samples were immediately placed at –20°C.

Three male chickens from each dam line were randomly selected, slaughtered, and dissected. The comb weight (CW), breast muscle yield (BMY), leg muscle yield (LMY), and abdominal fat weight (AFW) including the adipose tissues covering the gizzard were measured and also expressed as percentages of BW (CWP and AFP), or as percentages of the eviscerated carcass weight (BMP and LMP). All traits were measured using data from G0 and G1, except for LMY and LMP (only G0).

The contents in breast muscle of IMP, its related precursors [adenosine 5'-triphosphate (ATP), adenosine diphosphate, and adenosine monophosphate], and its derivatives hypoxanthine (Hx) and inosine (HxR) were measured by HPLC (Waters515, Milford, MA), using the method of Davidek and Khan (1967). All samples were prepared and tested at room temperature (20°C). The IMP content indicates the freshness of the meat after slaughter (Davidek and Khan, 1967), and summation of IMP and its precursors and derivatives could show the genetic potential of IMP content in muscle. Therefore, IMP equivalents were derived using the following formula (Chen et al., 2004a, which normalizes each component using MW:


Formula

The content of IMF in breast muscle based on fresh meat was measured using the method of Fat or Ether Extract in Meat (AOAC, 1990).

Genetic Analysis

Because there were only 2 generations in this study and no differing lines in G0, G0 was considered to be 1 line and was used, together with the 3 lines in G1, to estimate genetic parameters.

Descriptive statistics were obtained from the univariate procedure of SAS software (SAS Institute, 1999). An animal model was used to estimate the genetic parameters of IMP, IMF, and carcass-related traits. The animal model was constructed as follows:


Formula

where yij = the observation of the chicken; µ = the population mean; Li = the fixed effect of the line (i = 1,2...4); aij = the random direct genetic effect of chicken k; and eij = the random residual effect.

The same model was used for all traits. One-trait and then 2-trait analyses were used to estimate heritabilities, and the final heritabilities were estimated as the means of results of the 2 analyses. Multivariate analyses were used to estimate genetic and phenotypic correlations between any 2 traits. Heritabilities of AFW, BMY, LMY, and CW were estimated using BW as a covariable. Parameter estimates were obtained using the MTDFREML software (Boldman et al., 1995). Initial values were set as genetic and environmental estimates from the results of the 1-trait analysis and random covariance values. Then the 2-trait analyses were run to a 10–9 level of convergence criterion. Cold starts were again run to the same level of convergence with initial values from the former 2-trait analysis results until a –2log-likelihood did not change in the first 3 decimal positions. Two or 3 cold restarts from converged estimates, holding the same converged F-value, were made to examine the convergence to a global maximum instead of a local maximum.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Description of Traits

The statistical summary of IMP, IMF, and carcass-related traits is provided in Table 1Go. Values of most traits in G1 were higher (P < 0.05 or P < 0.01) than those in G0, except for CW and CWP. In G1, the IMP content was highest in the +IMP line and was higher (3.9%, P < 0.05) than that of the –IMF line. The IMF content was highest in the +IMF line, which was 15.1% higher (P < 0.05) than that of the –IMF line and 5.8% higher than the +IMP line (P > 0.05). Compared with the –IMF line, BW, AFW, AFP, BMY, and BMP were higher (P < 0.05) in the +IMF line. The CW was increased in the +IMP line (P < 0.05), but it was decreased in the –IMF line (P < 0.05). The CWP was decreased in all selected lines in G1.

Genetic Parameters

The heritabilities, genetic and phenotypic correlations between IMP and IMF content, and the measured body traits are shown in Table 2Go. Breast muscle percentage had the highest estimated heritability (0.79) of all the traits measured, followed by the heritabilities of CWP, AFW, CW, LMY, BMY, and BW (ranging from 0.56 to 0.68); the heritabilites of IMP, AFP, and LMP were moderate (ranging from 0.23 to 0.39), whereas the heritability of IMF was the lowest (0.11).


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  		Table 2. Genetic and phenotypic correlations between IMP and IMF content and the measured body traits
 
Lower phenotypic correlations of IMP and IMF with the other traits were discovered. Only IMF showed a relatively higher phenotypic correlation (0.27) with AFP.

Negative genetic correlation estimates were found between IMP and BW (–0.38) and between IMP and CWP (–0.62), but a high positive genetic correlation (0.57) existed between IMP and BMP. Intramuscular fat was found to have a highly positive genetic correlation with BW (0.75) and AFW (0.66), with moderately positive genetic correlations with AFP (0.32) and CWP (0.40), and a low genetic correlation with CW (0.20). The genetic correlation between IMP and IMF was also low (0.27).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Heritability Estimates

The heritability of chicken meat quality traits has, until now, been less intensively studied than those of carcass quality. A study by Le Bihan-Duval et al. (2001) reported heritabilities of pH, meat color, and drip loss in chicken meat. Most estimates of heritabilities of IMF and meat flavor characteristics are available for beef and pork. Larzul et al. (1997) estimated the heritability of porcine IMF at 0.44, and similar results were obtained by Knapp et al. (1997) and Fernandez et al. (2003). The estimate of the heritability of IMF in the present study is much lower than above, and it is lower than that of Zhao et al. (2006) using a Chinese quality chicken line (Jingxing 100), but is close to the estimates for broilers (Zerehdaran et al., 2004). Zhao et al. (2007) additionally reported that IMF in breast muscle was increased by 11.8% after 5 generations of selection. Therefore, IMF is a moderate genetically influenced trait that can be improved by continuous family selection.

The current estimated heritability values for BW, AFW, BMY, and BMP were higher than or close to the previously published estimates for broiler chickens (Le Bihan-Duval et al., 1998; Zerehdaran et al., 2004; Norris and Ngambi, 2006). This is not surprising given that the B-Y chicken breed has not been heavily selected for BMY or AFY. The low heritability of AFP found here contrasts with estimates (ranging from 0.45 to 0.85) reported by Le Bihan-Duval et al. (1998), Rance et al. (2002), and Zerehdaran et al. (2004).This might result from the higher variation in BW of B-Y chickens, which have not been subjected to much systematic selection. High estimated heritabilities were found here for LMY, CW, and CWP and moderate heritability for LMP, traits for which few estimates have been reported in the studies of others.

Although the heritabilities of IMP and IMF are not as high as those for other traits, both traits may still respond to selection. Because heritability of IMP is slightly higher, selection for increased IMP should result in a quicker response than would selection for IMF. However, it is important to note that IMF had a large phenotypic variability (CV nearly 30%), and this large variability should facilitate genetic improvement.

Correlations Between IMP and Other Traits

Few published estimates exist of phenotypic and genetic correlations between IMP and body composition traits. Phenotypic correlation between IMP and BW was moderately negative (–0.29 to –0.45) in several Chinese local chickens (Chen et al., 2002), but no significant phenotypic correlation was found in the present study. As noted earlier, the study of Chen et al. (2002) involved many fewer birds at a range of ages. The present study has found significant phenotypic correlations between IMP and BMP and LMP, also between IMF and AFP (all positive), and a negative genetic correlation between IMP and BW. This finding could explain why fast-growing chickens have lower IMP (Chen et al., 2004b, perhaps contributing to reduced flavor. This disparity between growth rate and IMP content of breast muscle was observed when B-Y chickens were compared with fast-growing broilers. The contents of IMP in breast muscle in B-Y were 1.23, 1.18, and 1.30 times values for Arbor Acres chickens at 28, 56, and 90 d, respectively, and 20% higher when adjusted for BW (Chen et al., 2004a) These findings suggest that the potential exists to increase the growth rate of native chickens without too stringent an effect on IMP. Our study did show a rather high genetic correlation between IMP and breast muscle percentage (0.57), implying that selection for IMP content will also increase muscle yield. Further study is needed to confirm such a prediction.

Correlations Between IMF and Abdominal Fat Percentage

Efforts to increase desirable traits in livestock must take into account genetic correlations between traits, including the less desirable ones. The higher IMF content is helpful in increasing the tenderness and flavor of meat, which is expected by consumers, but the increased abdominal fat is a waste of feed resources and therefore is not desirable. Zerehdaran et al. (2004) found low genetic correlations between AFW and IMF percentage (0.02) and between abdominal fat percentage and BW (0.13) in broilers. However, a high positive genetic correlation (0.87) was found between BW and IMF content at 7 wk of age. We estimated a similarly high genetic correlation between BW and content of IMF in breast muscle based on fresh meat at 90 d of age (0.75). It is possible, therefore, that BW could be increased by genetic selection without sacrificing the content of intramuscular fat. However, because of the equally high genetic correlation between IMF and AFW (0.66) in the B-Y strain, selection for BW could cause a correlated increase in AFW along with IMF. Intramuscular fat and abdominal fat percentage are heavily affected by diet and energy level. In general, diets with a ME level or a high energy:protein ratio promote energy retention as fat (Swennen et al., 2004). To some extent, more energy provided translates to higher IMF and abdominal fat percentage. However, IMF and abdominal fat deposition occurs with different developmental patterns. For the meat-type chicken, IMF typically accumulates during the rearing and growing periods, and further fat accretion in muscle slows during the finishing period (Chen et al., 2004b). Conversely, AFW increases rapidly after chickens enter the finishing phase. This difference in ontogeny most likely reflects differences in genetic control. Because IMF has major effect on meat quality and tenderness, efforts to increase or maintain IMF without modifying AFW will be aided by information about genes underlying IMF, or associated genetic markers.

These genetic correlation estimates could aid in selection efforts for other genotypes of meat-type chickens including some other Chinese native chicken breeds and commercial broilers, which have a similar pattern of fat deposition.

Relationship of Sexual Maturity with IMP and IMF

Chicken meat flavor and delicacy are related to the sexual maturity of the animal; taste and flavor improve after maturity (Chen, 2001). Moderately positive genetic correlation between IMP and CW was found in the present study. Determination of maturity is a key factor for selection of quality chicken in China, and development of secondary sex characteristics is an important indication of maturity (Chen, 2001). Zhao et al. (2007) found that ovarian weight at 90 d of age was increased after 5 generations of selection for IMF content in chicken breast muscle. A study by Zhang (2001) estimated negative genetic and phenotypic correlations between comb area and AFW or AFP in 12-wk-old male chickens. In contrast, in females, the phenotypic correlation between these traits was positive, and selection for 12-wk comb area tended to decrease fatness in males (P = 0.046) while increasing it in hens (P = 0.718). The present study using male chickens revealed a moderate positive genetic correlation between CWP and IMF (rA = 0.40), but there was no significant phenotypic correlation. Zelenka et al. (1986) found that fat deposits were heavier and percentages of fat were higher in laying than in nonlaying pullets, which meant that there was some relationship between body fat and sexual maturity for the chickens. Although the results of these experiments differ, the studies show a link between sexual maturity and fat deposition, an important aspect of meat flavor. Thus, further investigation of this relationship is warranted.

Relationship of Conventional Meat Quality Traits with IMP or IMF

Conventional meat quality traits include pH, tenderness, color, and drip loss, as well as sensory characteristics such as flavor, oral sensation, and acceptability. Inosine-5'-monophosphate and IMF are implicated in the development of these traits. Inosine-5'-monophosphate content is well known to contribute to food flavor and is also linked with initial pH value. Muscle uses glycogen stores for ATP regeneration (Duclos et al., 2007), and ATP is degraded to adenosine diphosphate, adenosine mono-phosphate, and IMP, step by step, in less than 24 h at 20 to 21°C (Chen et al., 2004c) and pH decreased from around 6.2 to 6.5 at 15 min postmortem to normal ultimate pH around 5.8 at 24 h postmortem (Duclos et al., 2007). Perhaps there is a relationship between IMP content and changes in pH after slaughter, but it should be studied further. Intramuscular fat affects tenderness of meat through altering connective tissue structure in muscle (Nishimura et al., 1999) and contributes to flavor, oral sensation, and acceptability (Devol et al., 1988).

We have found no previous estimate of correlations between IMP and IMF. These traits appear to be fairly independent given the low genetic correlation (rA = 0.27) and nearly null phenotypic correlation found here. Both should thus be included in the selection indices, because responses to selection should be independent of each other. Selecting for increased IMF should contribute to an indirect response for increased BW, whereas the response should be in the opposite direction for IMP. Both indirect responses should at least partially offset each other so that global indirect effects on BW should be low.

In conclusion, genetic parameters of IMP, IMF, and other important meat quality traits were estimated here in male B-Y chickens. inosine-5'-monophosphate was found to have a moderate heritability and may thus be modified by selection. Heritability of IMF was lower but still may be slowly modified by selection, which should improve meat quality. Simultaneously, close control of growth rate of commercial chickens through nutritional management is important in assuring a good quality of chicken meat, by increasing accumulation of IMP and IMF and decreasing abdominal fat deposition. The results of this study will help to increase desirable meat quality traits in B-Y chickens as well as other breeds and provides further insight into the hereditary mechanisms underlying meat quality traits of chickens. Because IMF influences meat quality and tenderness, efforts to increase or maintain IMF without modifying AFW will be aided by information about genes or genetic markers associated with IMF.


   ACKNOWLEDGMENTS
 
We thank Catherine Beaumont for her comments and suggestions and corrections. We are grateful to W. Bruce Currie, Liu Gui-Sheng, and Li Ji-Zhi for their linguistic revision of the manuscript. We also thank the People’s Republic of China, Ministry of Science and Technology, for financial support.


   FOOTNOTES
 
1 Supported by the following grants: National Key Technology R&D Program (2006BAD01A00) and National High-Tech R&D Program (2006AA10Z1D8). Back

Received for publication December 14, 2007. Accepted for publication February 25, 2008.


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 DISCUSSION
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