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Investigation on muscle fiber types and meat quality and estimation of their heritability and correlation coefficients with each other in four pig populations

Min Yan

orcid.org/0009-0005-7070-0250

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Longyun Li,

Longyun Li

orcid.org/0000-0001-8385-9918

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Yizhong Huang,

Yizhong Huang

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Xi Tang,

Xi Tang

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Yujie Shu,

Yujie Shu

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Dengshuai Cui,

Dengshuai Cui

orcid.org/0009-0008-2927-4319

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Chuangang Yu,

Chuangang Yu

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Yongqiang Hu,

Yongqiang Hu

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Junwu Ma,

Junwu Ma

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Shijun Xiao,

Corresponding Author

Shijun Xiao

[email protected]

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

Correspondence

Shijun Xiao and Yuanmei Guo, National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, 330045, China.

Email: [email protected] and [email protected]

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Yuanmei Guo,

Corresponding Author

Yuanmei Guo

[email protected]

orcid.org/0000-0003-0381-9647

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

Correspondence

Email: [email protected] and [email protected]

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Min Yan,

Min Yan

orcid.org/0009-0005-7070-0250

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

Search for more papers by this author

Longyun Li,

Longyun Li

orcid.org/0000-0001-8385-9918

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Yizhong Huang,

Yizhong Huang

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Xi Tang,

Xi Tang

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Yujie Shu,

Yujie Shu

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Dengshuai Cui,

Dengshuai Cui

orcid.org/0009-0008-2927-4319

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Chuangang Yu,

Chuangang Yu

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Yongqiang Hu,

Yongqiang Hu

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Junwu Ma,

Junwu Ma

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

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Shijun Xiao,

Corresponding Author

Shijun Xiao

[email protected]

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

Correspondence

Email: [email protected] and [email protected]

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Yuanmei Guo,

Corresponding Author

Yuanmei Guo

[email protected]

orcid.org/0000-0003-0381-9647

National Key Laboratory for Pig Genetic Improvement and Germplasm Innovation, Ministry of Science and Technology of China, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China

Correspondence

Email: [email protected] and [email protected]

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First published: 01 February 2024

https://doi.org/10.1111/asj.13915

Citations: 3

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Abstract

The aim of this study was to investigate the muscle fiber types and meat quality in four populations and estimate the heritability and correlation coefficients of those traits in Shanxia long black pig (SX). In this study, a total of 318 pigs were recorded for 16 traits of the muscle fiber types and meat quality in four populations, including 256 individuals from the new breed SX. The population had a significant effect on all recorded traits, and the meat quality of the Lulai black pig was better than the remaining populations. The heritability (h²) of meat quality traits was from 0.06 (pH at 24 h) to 0.47 (shearing force), and the muscle fiber types belonged to the traits with low to medium heritability. The density of total fiber had the highest h² (0.40), while the percentage of type IIA had the lowest h² (0.04). Most traits are phenotypically correlated with each other, but only a small proportion of traits are genetically correlated with each other. None fiber type genetically correlated with meat quality significantly, because the genetic correlation coefficients had large standard errors. These results provided some insights into genetic improvements for the meat quality in pig breeds and also indicated that the parameters of muscle fiber characteristics can explain parts of the variation in meat quality.

1 INTRODUCTION

China is the largest pork producer and is also the largest pork market in the world (Lim & Grohn, 2021). In the past, the pursuit of pig production traits has led to a decline in meat quality. With the improvement of people's living standards, the demand for high-quality meat has been steadily growing in recent years. In addition, genetic improvement of meat quality can effectively reduce meat processing losses and benefit the pig industry (Ma et al., 2014). Therefore, meat quality is becoming more and more important in swine breeding programs (Dransfield et al., 2005; Jiang et al., 2019; Khanal et al., 2019). Meat quality is measured postmortem, so it is difficult to phenotype enough individuals to increase the selection intensity. In addition, the heritability of meat quality is low to medium. Therefore, the genetic improvement of pork meat quality is inefficient using an ordinary breeding program. Chinese indigenous breeds have high meat quality, but they grow slowly, which hinders their industrialization (Jiang et al., 2011). Commercial breeds, such as Duroc, Landrace, and Yorkshire, provide the major part of pork in China, but they fail to meet the demand of consumers for meat quality (Huang et al., 2020). New breeds have been bred by crossing Chinese indigenous pigs with commercial breeds to integrate their merits. Shanxia long black pig is bred as a paternal strain with large body size, high meat quality, and fast growth rate (Li et al., 2021).

Meat quality is a complex economic trait, and it is also an indicator of acceptability or preference for consumers (Cheng et al., 2017). Marbling, pH, meat color, and shear force are the major intrinsic factors influencing meat quality (Calvo et al., 2017; Lee et al., 2021; Park et al., 2022; Rincker et al., 2008). Marbling has positive influences on tenderness (usually measured with shear force), flavor, juiciness, and overall appearance of pork (Cannata et al., 2010; Kim et al., 2010; Scheffler et al., 2011). The pH reflects the extent of muscle glycolysis postmortem, and the more muscle glycogen has been hydrolyzed, the lower the pH is. Meat color is the most intuitive and predominant impression of consumers in the purchasing process. In addition, muscle fiber characteristics is also an important factor in meat quality (Klont et al., 1998).

Skeletal muscle is the main component of carcass, accounting for about 40–60% of body mass, and its basic structural unit is the muscle fiber (Hakimov et al., 2009). The number, diameter, and type of each muscle fiber can be determined through enzyme histochemical staining of the muscle thermostatic frozen section (Paciello & Papparella, 2009). After having been stained with myosin ATPase and oxidative metabolism enzyme activity, muscle fibers are classified as type I (slow-twitch, oxidative), type IIA (fast-twitch, oxidative glycolytic), and type IIB (fast-twitch, glycolytic) according to the size, color, and glycogen and lipid contents (Karlsson et al., 1999; Kim et al., 2013). In general, type I fiber has the smallest diameter and abundant mitochondrial content; type IIB fiber has the largest diameter and lower mitochondrial content; and type IIA fiber has an intermediate size with a greater lipid and myoglobin content than type IIB fibers (Essén-Gustavsson et al., 1992; Klont et al., 1998). Many studies have reported that the number of muscle fibers influences muscle growth potential and meat quality (Rehfeldt & Kuhn, 2006; Ryu & Kim, 2005). A total number of fibers (FN) positively correlated with pH at 45 min postmortem, and negatively correlated with drip loss in pigs (Lee et al., 2010; Rehfeldt et al., 2000). Compared to the individuals from larger litter sizes, piglets with few littermates had a lower FN during prenatal development (Rehfeldt et al., 2008). Increasing the proportion of type I fiber could decrease the rate and extent of pH decline and meat lightness, and improve water holding capacity in pigs (Choi et al., 2006). The density and total number of type IIB fibers related to rapid glycolysis of glycogen, because the concentration of glycogen was high in the type IIB fibers (Ryu & Kim, 2005). The total number of type IIB fibers positively correlated with the intramuscular fat content, which was the major intrinsic factor influencing meat quality (Henckel et al., 1997).

To improve meat quality, the heritability and genetic correlations of meat quality and muscle fiber traits were the essential prerequisites. The aim of this study was to investigate the meat quality and muscle fiber characteristics in four populations and estimate their heritability and genetic correlations in Shanxia long black pigs, paving the road to genetic improvement of those traits in pigs.

2 MATERIALS AND METHODS

All pigs were treated according to the guidelines for the care and use of experimental animals issued by the Ministry of Agriculture and Rural Affairs of China. The Animal Care and Use Committee of Jiangxi Agricultural University specifically approved this study.

2.1 Animals

A total of 106 barrows and 212 gilts from four populations were used in this study. The 4 populations were Shanxia long black pig (SX, derived from a cross between Berkshire boars and Licha black pig sows), Lulai black pig (LL), a cross (DS) between Duroc boars and SX sows, and an intercross (SL) between SX and LL, and 256, 10, 30, and 22 pigs were randomly selected from the 4 populations, respectively. The 256 Shanxia black pigs were from the same generation, and they were the offspring of 24 boars (10.67 ± 3.14 per boar) and 119 sows (2.15 ± 0.57 per sow). All the pigs were raised at Jiangxi Huaxi Pig Breeding Company Limited (Dingnan County, Jiangxi province, China) with the same feeding and management conditions. Pigs were raised in a solid concrete floor pen and accessed to a corn-soybean meal diet and fresh water ad libitum. Each pen housed about 10 pigs (1.25m²/pig).

2.2 Sampling

The pigs were transported to a commercial abattoir in four batches when their body weights were around 105 ± 10 kg. After an overnight fasting, they were stunned by an electrical circuit and then bled. When the head, legs, tail, and viscera had been removed, the carcass was split into halves longitudinally. For each pig, Longissimus dorsi muscle sample for histochemical analysis was dissected from the tenth thoracic vertebra on the right-side carcass within half an hour postmortem. The muscle sample was placed on a piece of A4 PVC binding cover, and a 2 × 0.5 × 0.5 cm³ sample was taken along the muscle fiber direction. To prevent muscle tissue from adhering to the tube wall and fixing the orientation of the muscle fibers, the sample was placed on a 2.5 cm long × 0.8 cm wide × 0.1 mm thick plastic film, and then the sample together with the plastic film was put into a sampling tube numbered in advance (Huang et al., 2017). The tube has 14 inlet holes: each on the cap and bottom, and the remaining 12 on the wall. The inlet holes facilitate the flow velocity of liquid nitrogen next to the tissue and reduce the formation of ice crystals. The sample was quickly submerged in liquid nitrogen using 25 cm tweezers in the pre-cooled Styrofoam cooler for 10 s, and then stored at −80°C for histochemical analysis.

2.3 Meat quality

Meat pH at 45 min (pH_45min) and 24 h (pH_24h) postmortem were measured using a Delta 320 pH meter (Mettler-Toledo International Inc., USA) with an insertion glass electrode (Metrohm, Switzerland). The meat color was measured on the muscle surface using a CM-2600d/2500d Minolta Chromameter (Tokyo, Japan) with an 8-mm measuring port and D65 illuminant, and lightness (L*) and redness (a*) were recorded (Gil et al., 2003). According to the standards of the National Pork Producers Council (NPPC, 2000), the marbling score (from 1 = devoid to 10 = overly abundant) was evaluated for the longissimus dorsi muscle at 24 h postmortem and meat color score (from 1 = pale to 6 = dark) was evaluated at 45 min and 24 h postmortem. A piece of fresh meat, which was prepared using a standard cylindrical sampler, was placed at the shear plate of tenderness meter (C-LM3B; China) for shearing operation. The sample was sheared at a speed of 5 mm/s perpendicular to the fiber longitudinal orientation, and the shearing force was recorded in Newtons. Repeated the procedure three times, and the shearing force was the average of the three values.

2.4 Histochemical analysis

Each sample was sliced into 7 μm transverse serial sections with a cryostat (CM1950; Leica, Germany) at −24°C, and each section was fixed on a glass slide. The slides with sections were stained following the method described in Cerisuelo et al. (2007) with some modifications. The sections were stained 45 min for succinate dehydrogenase (SDH) activity after acid (pH 4.17) pre-incubation for about 10 min. Then, they were stained with a myofibrillar ATPase activity. They were incubated for the histochemical demonstration of myosin adenosine triphosphatase (mATPase) for 30 min in an alkaline (pH 9.40) incubation condition. For each individual, a staining section was selected randomly for photographing, and more than five 10 × bright fields were taken photos with a Nikon microscope (Nikon, Japan) (Cai et al., 2023; Huang et al., 2022). The photos were used to count the number of muscle fibers for each type.

Approximately 600 fibers per sample were counted to analyze the muscle fiber characteristics. The number of muscle fibers for each type was counted directly, and its ratio was the fiber number of this type to the total number of all types. The total number of fibers was equal to the product of the total fiber density and the loin-eye area (cm²). Fiber density was the average number of muscle fibers per cm².

2.5 Genotyping and quality control

Shanxia long black pigs were genotyped for 51,368 SNPs using the CC1 Porcine SNP50K BeadChip, which was designed by Jiangxi Agricultural University (Jiangxi, China) and manufactured by Illumina Company (Illumina, USA). The SNPs with minor allele frequencies (MAF) ≥ 0.05 and call rate ≥90% on autosomal chromosomes were used for subsequent analyses.

2.6 Statistical analysis

Except for the genetic correlation and heritability analysis, all statistical analyses were performed using R (R4.0.2) software. We fitted population, sex, and slaughter batch as fixed effects in a linear model using the lm function in R, and then performed an analysis of variance to test whether the population and sex had effects on recorded traits using the Anova function in the car package. Least square means were compared to test the differences among populations and between sexes, and the multiple comparisons were corrected with a Tukey method in the lsmean package. The statistic model is shown as follows:

y_{ijkl} = μ + {sex}_{i} + {population}_{j} + {batch}_{k} + e_{ijkl} .

where y_ijkl and e_ijkl are the phenotype and residual of lth individual with ith sex, jth population, and kth batch, respectively; μ is the total mean; sex_i is the effect of ith sex; population_j is the effect of jth population; batch_k is the effect of kth batch.

The heritability of recorded traits was estimated in Shanxia long black pig using GCTA (Yang et al., 2013). For each trait, the following single-trait animal model is used to estimate the variance components:

y = Xβ + g + ε .

where y, β, g, and ε are the vectors of the phenotype, covariates of sex and batch, polygenic random effect, and residual, respectively; X is the incidence matrices of β. Var(y) = H

σ_{g}^{2}

+ I

σ_{ε}^{2}

, H is the genomic relationship matrix (GRM) estimated using all autosomal SNPs, I is an identity matrix,

σ_{g}^{2}

and

σ_{ε}^{2}

are the additive and residual variances, respectively. The heritability is the quotient of

σ_{g}^{2}

divided by the sum of

σ_{g}^{2}

and

σ_{ε}^{2}

(Yang et al., 2011).

The phenotypic residuals (e_ijkl), which were mentioned above, were used to calculate (cor.test function of R) the phenotypic correlation coefficients between each pair of traits. The genetic correlation coefficients were calculated from a two-traits model using HIBLUP (Yin et al., 2023) only in Shanxia long black pig. The linear mixed model formula is shown in the following:

[\begin{matrix} y_{1} \\ y_{2} \end{matrix}] = [\begin{matrix} X_{1} & 0 \\ 0 & X_{2} \end{matrix}] [\begin{matrix} β_{1} \\ β_{2} \end{matrix}] + [\begin{matrix} a_{1} \\ a_{2} \end{matrix}] + [\begin{matrix} e_{1} \\ e_{2} \end{matrix}],

where subscript 1 and 2 indicate trait 1 and trait 2, respectively; y, β, a, and e are the vectors of observed values, fixed effects of sex and batch, random polygenetic effects, and residuals, respectively; X is the incidence matrices of β. Variance and covariance components were calculated assuming

[\begin{matrix} a_{1} \\ a_{2} \end{matrix}]

~ N(0, H ⊗ G) and

[\begin{matrix} e_{1} \\ e_{2} \end{matrix}]

~ N(0, I ⊗ R), where G, H, I, and R are the matrices of genetic variance–covariance, genomic relationship, identity, and residual variance–covariance, respectively. Because the pedigrees of Shanxia black pigs could be tracked back for only a few generations, and the additive relationship matrix based on the pedigrees was inaccurate. Therefore, the SNP-based GRM was used in this study. The GRM is calculated using the following formula:

H = \frac{{ZZ}^{'}}{tr (Z Z^{'}) / n}

where Z is the numeric coded genotype matrix with a dimension of n × m, n is the number of individuals, m is the number of markers, and tr is the trace of the matrix (Yang et al., 2010).

3 RESULTS

3.1 Meat quality

Population had a significant effect on all recorded traits of meat quality, the order of meat quality in the four populations was LL > SL > SX ≈ DS (Table 1). There was no significant difference of pH_45min among the populations except that pH_45min in SL was higher than SX. Lightness (L*) at 45 min (L^*_45min) and at 24 h (L^*_24h) were greater in DS than the remaining populations, and they were also greater in SX than SL and LL, but no significant difference between SL and LL. There was no difference in pH_24h and shearing force between SL and LL and between DS and SX, but pH_24h in SL and LL were higher than DS and SX. Meat color score at 24 h (Color_24h) and redness (a*) at 24 h (a^*_24h) were significantly different between each pair of the four populations, their descending order was LL > SL > SX > DS in the four populations. Marbling score at 24 h (Marbling_24h) was highest in LL, and it was also higher in SL than SX, but no significant difference among populations.

TABLE 1. Least square means of meat quality in each population.

Trait	Population^†	Female		Male		All^§
Trait	Population^†	N	LSMean ± S.E.^‡	N	LSMean ± S.E.	N	LSMean ± S.E.
pH at 45 min	DS	14	6.49 ± 0.066	16	6.42 ± 0.061	30	6.48 ± 0.057^AB
	LL	4	6.46 ± 0.125	6	6.40 ± 0.102	10	6.56 ± 0.087^AB
	SL	9	6.51 ± 0.081	13	6.50 ± 0.067	22	6.64 ± 0.065^A
	SX	185	6.38 ± 0.021^a	71	6.30 ± 0.032^b	256	6.34 ± 0.019^B
L* at 45 min	DS	14	47.7 ± 0.538	16	47.8 ± 0.503	30	47.4 ± 0.611^A
	LL	4	41.0 ± 1.017	6	41.8 ± 0.831	10	41.5 ± 0.945^C
	SL	9	41.6 ± 0.903	13	43.0 ± 0.751	22	42.5 ± 0.700^C
	SX	185	44.4 ± 0.228^b	71	45.3 ± 0.357^a	256	44.9 ± 0.203^B
pH at 24 h	DS	14	5.52 ± 0.017	16	5.51 ± 0.016	30	5.40 ± 0.0397^B
	LL	4	5.75 ± 0.101	6	5.81 ± 0.083	10	5.76 ± 0.0614^A
	SL	9	5.70 ± 0.083	13	5.74 ± 0.069	22	5.69 ± 0.0455^A
	SX	185	5.43 ± 0.015	71	5.44 ± 0.023	256	5.44 ± 0.0132^B
Color score at 24 h	DS	14	2.43 ± 0.148	16	2.59 ± 0.138	30	2.36 ± 0.184^D
	LL	4	4.75 ± 0.310	6	4.17 ± 0.253	10	4.69 ± 0.285^A
	SL	9	3.72 ± 0.327	13	3.35 ± 0.272	22	3.79 ± 0.211^B
	SX	185	2.94 ± 0.068	71	2.83 ± 0.106	256	2.88 ± 0.061^C
Marbling score at 24 h	DS	14	1.89 ± 0.198	16	2.03 ± 0.185	30	2.35 ± 0.168^BC
	LL	4	4.75 ± 0.695	6	4.58 ± 0.567	10	4.49 ± 0.260^A
	SL	9	3.06 ± 0.289	13	3.23 ± 0.240	22	3.00 ± 0.193^B
	SX	185	1.82 ± 0.058^b	71	2.07 ± 0.091^a	256	1.94 ± 0.056^C
L* at 24 h	DS	14	53.4 ± 0.634	16	55.1 ± 0.593	30	54.2 ± 0.844^A
	LL	4	42.7 ± 1.009	6	43.3 ± 0.824	10	44.7 ± 1.306^C
	SL	9	44.6 ± 1.310	13	44.3 ± 1.090	22	46.0 ± 0.968^C
	SX	185	49.4 ± 0.318	71	49.6 ± 0.497	256	49.5 ± 0.280^B
a* at 24 h	DS	14	0.48 ± 0.273	16	0.50 ± 0.255	30	0.31 ± 0.310^D
	LL	4	7.21 ± 0.865	6	6.10 ± 0.706	10	6.40 ± 0.480^A
	SL	9	3.26 ± 0.542	13	2.47 ± 0.451	22	2.65 ± 0.356^B
	SX	185	1.08 ± 0.112	71	1.40 ± 0.175	256	1.20 ± 0.103^C
Shearing force	DS	14	55.4 ± 1.85	16	51.7 ± 1.73	30	51.2 ± 1.77^B
	LL	4	70.9 ± 3.86	6	62.9 ± 3.15	10	67.3 ± 2.73^A
	SL	9	64.6 ± 3.70	13	60.9 ± 3.08	22	63.6 ± 2.02^A
	SX	185	54.7 ± 0.62	71	53.7 ± 0.97	256	54.0 ± 0.59^B

^† SX: Shanxia long black pig; LL: Lulai Black pig; DS: a cross between Duroc boars and SX sows; SL: an intercross between SX and LL.
^‡ Means with different lower letters indicate significant (P < 0.05) difference between sexes.
^§ Means with different upper letters indicate significant (P < 0.05) differences among populations.

All meat quality traits were not different between castrated males and gilts except for pH_45min, L_45min and Marbling_24h in SX. Except pH_45min of gilts higher than castrated males, the other two traits of gilts were lower than castrated males.

3.2 Muscle fiber characteristics

Each type of muscle fiber was clearly shown as a staining section in Figure 1. Muscle fiber characteristics of longissimus dorsi muscle were significantly different among populations (Table 2). Total number of fibers (FN) in DS, SL, and SX were not significantly different, but significantly more than LL. Percentage of type I fiber (Percent_I) was more in LL than in the remaining populations, and it was also more in DS than SX. Percentage of type IIA fiber (Percent_IIA) was significantly higher in LL than in the other three populations, and it was also higher in SL and SX than DS. Percentage of type IIB fiber (Percent_IIB) was greater in SX than SL and LL, and it was also greater in DS and SL than LL. Density of type I fiber (Dens_I) was significantly different among the four populations except for DS, in which Dens_I was no different from those in SL and SX. Density of type IIA fiber (Den_IIA) was significantly higher in LL, SL, and SX than DS, and the density of type IIB fiber (Dens_IIB) was higher in SL and SX than DS and LL. Density of FN (Dens_FN) was greater in SL than DS and LL, and it was also greater in SX than DS.

Details are in the caption following the image — **FIGURE 1**
Open in figure viewer PowerPoint

A representative cross-section of *longissimus dorsi* muscle of Shanxia long black pig stained for myosin ATPase after pre-incubation in pH 4.20, the arrows indicate the different muscle fiber types (fiber type I, fiber type IIA, and fiber type IIB). Scale bar indicates 100 μm.

TABLE 2. The least square means of muscle fiber types in each population.

Trait	Population^†	Female		Male		All^§
Trait	Population^†	N	LSMean ± S.E.^‡	N	LSMean ± S.E.	N	LSMean ± S.E.
Total number of fibers	DS	14	2,057,694 ± 86,055	16	1,902,089 ± 80,497	30	2,128,271 ± 100036^A
	LL	4	1,415,476 ± 207,274	6	1,317,940 ± 169,239	10	1,303,573 ± 154765^B
	SL	9	2,047,070 ± 162,514	13	2,269,823 ± 135,220	22	2,124,165 ± 114667^A
	SX	185	2,315,641 ± 36774^a	71	2,151,198 ± 57581^b	256	2,241,593 ± 33167^A
Percentage of type I	DS	14	0.112 ± 0.0069	16	0.107 ± 0.0065	30	0.109 ± 0.0065^B
	LL	4	0.150 ± 0.0295	6	0.157 ± 0.0241	10	0.154 ± 0.0101^A
	SL	9	0.109 ± 0.0144	13	0.093 ± 0.0120	22	0.099 ± 0.0075^BC
	SX	185	0.082 ± 0.0022	71	0.078 ± 0.0034	256	0.080 ± 0.0022^C
Percentage of type IIA	DS	14	0.082 ± 0.0070	16	0.085 ± 0.0066	30	0.086 ± 0.0065^C
	LL	4	0.173 ± 0.0361	6	0.159 ± 0.0295	10	0.162 ± 0.0101^A
	SL	9	0.140 ± 0.0099	13	0.119 ± 0.0082	22	0.125 ± 0.0075^B
	SX	185	0.115 ± 0.0022	71	0.123 ± 0.0034	256	0.118 ± 0.0022^B
Percentage of type IIB	DS	14	0.806 ± 0.0051	16	0.809 ± 0.0048	30	0.805 ± 0.0080^AB
	LL	4	0.677 ± 0.0523	6	0.684 ± 0.0427	10	0.684 ± 0.0123^C
	SL	9	0.751 ± 0.0166	13	0.788 ± 0.0138	22	0.776 ± 0.0091^B
	SX	185	0.803 ± 0.0025	71	0.799 ± 0.0039	256	0.802 ± 0.0026^A
Density of type I	DS	14	4,236 ± 272	16	3,925 ± 255	30	3,994 ± 303^BC
	LL	4	6,612 ± 1,174	6	5,528 ± 959	10	6,140 ± 468^A
	SL	9	4,571 ± 655	13	4,632 ± 545	22	4,784 ± 347^B
	SX	185	3,667 ± 104	71	3,563 ± 162	256	3,604 ± 100^C
Density of type IIA	DS	14	3,107 ± 278	16	3,097 ± 260	30	2,990 ± 400^B
	LL	4	7,370 ± 957	6	5,336 ± 781	10	6,249 ± 619^A
	SL	9	6,371 ± 643	13	5,878 ± 535	22	6,182 ± 459^A
	SX	185	5,259 ± 147^b	71	5,800 ± 231^a	256	5,473 ± 133^A
Density of type IIB	DS	14	30,789 ± 1,034	16	29,670 ± 967	30	29,052 ± 1515^B
	LL	4	29,902 ± 4,936	6	25,693 ± 4,031	10	29,475 ± 2343^B
	SL	9	34,615 ± 3,018	13	39,065 ± 2,511	22	39,350 ± 1736^A
	SX	185	36,128 ± 539	71	37,113 ± 844	256	36,585 ± 502^A
Density of total fibers	DS	14	38,132 ± 1,176	16	36,692 ± 1,100	30	36,037 ± 1848^C
	LL	4	43,884 ± 5,482	6	36,557 ± 4,476	10	41,864 ± 2860^BC
	SL	9	45,557 ± 3,539	13	49,575 ± 2,945	22	50,317 ± 2119^A
	SX	185	45,053 ± 666	71	46,476 ± 1,043	256	45,663 ± 613^AB

^† SX: Shanxia long black pig; LL: Lulai Black pig; DS: a cross between Duroc boars and SX sows; SL: an intercross between SX and LL.
^‡ Means with different lower letters indicate significant (P < 0.05) difference between sexes.
^§ Means with different upper letters indicate significant (P < 0.05) difference among populations.

Sex had no significant effect on all muscle fiber types except FN and Dens_IIA in SX. FN was more in gilts than castrated males, but Dens_IIA was more in castrated males than gilts.

3.3 Heritability

The heritability of meat quality and muscle fiber types was estimated in SX (Table 3). Among meat quality traits, the shearing force had the highest h² (0.47), while pH_24h had the lowest h² (0.06). Both L_24h and Marbling_24h had the same h² (0.45), and the same for L_45min and L_24h (h² = 0.41). The h² of pH_45min, Color_24h, and a_24h were 0.28, 0.26, and 0.15, respectively.

TABLE 3. Estimated heritability of meat quality and muscle fiber types in Shanxia long black pig.

Trait	Additive variance	Environmental variance	h²	S.E.
pH at 45 min	0.0184	0.0464	0.28	0.13
L* at 45 min	3.2200	4.5600	0.41	0.14
pH at 24 h	0.0019	0.0311	0.06	0.11
Color score at 24 h	01880	0.5410	0.26	0.12
Marbling score at 24 h	0.2930	0.3540	0.45	0.12
L* at 24 h	6.3800	7.8500	0.45	0.13
a* at 24 h	0.3170	1.7400	0.15	0.11
Shearing force	28.800	32.600	0.47	0.11
Total number of muscle fiber	3.79e+10	1.76e+11	0.18	0.12
Percentage of type I	6.10e-05	8.27e-04	0.07	0.10
Percentage of type IIA	3.89e-05	8.15e-4	0.04	0.11
Percentage of type IIB	1.90e-04	1.14e-03	0.14	0.11
Density of type I	1.83e+05	1.78e+06	0.09	0.12
Density of type IIA	5.14e+05	2.12e+06	0.20	0.12
Density of type IIB	1.62e+07	2.57e+07	0.39	0.11
Density of total fiber	2.39e+07	3.66e+07	0.40	0.11

The heritability of muscle fiber types was not greater than 0.40 and belonged to low-to-moderate heritability. Dens_FN had the highest h² (0.40), followed by Dens_IIB (0.39). The h² of Dens_IIA, FN, and Percent_IIB were 0.20, 0.18, and 0.14, respectively. The h² of Dens_I, Percent_I, and Percent_IIA were less than 0.1, they were 0.09, 0.07, and 0.04, respectively.

3.4 Genetic and phenotypic correlations

The phenotypic and genetic correlation coefficients between the recorded traits were presented in the upper and lower triangles of Table 4 and Figure S1, respectively.

TABLE 4. Phenotypic and genetic correlation coefficients of meat quality and muscle fiber types in Shanxia long black pig.

Trait	FN	Percent_I	Percent_IIA	Percent_IIB	Dens_I	Dens_IIA	Dens_IIB	Dens_FN	pH_45min	L*_45min	pH_24h	Color_24h	Marbling_24h	L*_24h	a*_24h	Shearing force
FN		−0.15 ± 0.06	−0.07 ± 0.06	0.17 ± 0.05	0.22 ± 0.05	0.35 ± 0.05	0.65 ± 0.04	0.65 ± 0.04	0.10 ± 0.06	−0.09 ± 0.06	−0.19 ± 0.05	−0.07 ± 0.06	−0.21 ± 0.05	0.08 ± 0.06	−0.18 ± 0.05	−0.16 ± 0.05
Percent_I	−0.36 ± 0.42		−0.19 ± 0.05	−0.65 ± 0.04	0.83 ± 0.03	−0.33 ± 0.05	−0.38 ± 0.05	−0.25 ± 0.05	0.20 ± 0.05	−0.08 ± 0.06	0.06 ± 0.06	0.15 ± 0.06	0.20 ± 0.05	−0.05 ± 0.06	0.25 ± 0.05	0.10 ± 0.06
Percent_IIA	−0.06 ± 0.47	0.14 ± 0.88		−0.62 ± 0.04	−0.19 ± 0.05	0.79 ± 0.03	0.01 ± 0.06	0.15 ± 0.06	0.00 ± 0.06	−0.17 ± 0.05	0.02 ± 0.06	0.17 ± 0.05	0.16 ± 0.06	−0.11 ± 0.06	0.32 ± 0.05	0.11 ± 0.06
Percent_IIB	0.28 ± 0.42	−0.87 ± 0.22	−0.58 ± 0.54		−0.52 ± 0.05	−0.35 ± 0.05	0.29 ± 0.05	0.08 ± 0.06	−0.16 ± 0.06	0.19 ± 0.05	−0.06 ± 0.06	−0.26 ± 0.05	−0.28 ± 0.05	0.13 ± 0.06	−0.45 ± 0.05	−0.17 ± 0.05
Dens_I	0.26 ± 0.31	0.10 ± 0.51	−0.67 ± 0.39	0.24 ± 0.47		−0.02 ± 0.06	0.15 ± 0.06	0.28 ± 0.05	0.23 ± 0.05	−0.11 ± 0.06	0.04 ± 0.06	0.15 ± 0.06	0.11 ± 0.06	−0.06 ± 0.06	0.22 ± 0.05	0.08 ± 0.06
Dens_IIA	0.96 ± 0.15	−0.30 ± 0.46	−0.07 ± 0.60	0.25 ± 0.49	0.22 ± 0.49		0.58 ± 0.05	0.69 ± 0.04	0.04 ± 0.06	−0.18 ± 0.05	−0.02 ± 0.06	0.15 ± 0.06	0.04 ± 0.06	−0.10 ± 0.06	0.24 ± 0.05	0.05 ± 0.06
Dens_IIB	0.75 ± 0.11	−0.14 ± 0.40	−0.50 ± 0.41	0.33 ± 0.38	0.72 ± 0.22	0.80 ± 0.18		0.97 ± 0.01	0.07 ± 0.06	−0.06 ± 0.06	−0.04 ± 0.06	0.01 ± 0.06	−0.10 ± 0.06	−0.02 ± 0.06	−0.03 ± 0.06	−0.01 ± 0.06
Dens_FN	0.77 ± 0.09	−0.15 ± 0.40	−0.50 ± 0.41	0.34 ± 0.38	0.73 ± 0.22	0.81 ± 0.17	0.99 ± 0.00		0.10 ± 0.06	−0.11 ± 0.06	−0.03 ± 0.06	0.07 ± 0.06	−0.05 ± 0.06	−0.05 ± 0.06	0.06 ± 0.06	0.02 ± 0.06
pH_45min	0.10 ± 0.33	0.02 ± 0.52	0.07 ± 0.57	−0.04 ± 0.51	−0.07 ± 0.43	0.14 ± 0.46	0.06 ± 0.32	0.06 ± 0.31		−0.39 ± 0.05	0.11 ± 0.06	−0.01 ± 0.06	0.10 ± 0.06	0.00 ± 0.06	0.02 ± 0.06	0.20 ± 0.05
L*_45min	−0.04 ± 0.32	0.09 ± 0.51	−0.28 ± 0.52	0.06 ± 0.47	0.29 ± 0.41	−0.07 ± 0.43	0.10 ± 0.30	0.11 ± 0.30	−0.28 ± 0.35		−0.11 ± 0.06	−0.47 ± 0.05	−0.06 ± 0.06	0.51 ± 0.05	−0.31 ± 0.05	−0.10 ± 0.06
pH_24h	−0.44 ± 0.43	0.44 ± 0.64	0.49 ± 0.68	−0.56 ± 0.53	−0.16 ± 0.53	−0.38 ± 0.51	−0.33 ± 0.40	−0.34 ± 0.39	−0.04 ± 0.56	−0.14 ± 0.50		0.42 ± 0.05	0.29 ± 0.05	−0.48 ± 0.05	−0.01 ± 0.06	0.17 ± 0.05
Color_24h	−0.16 ± 0.30	0.08 ± 0.47	0.13 ± 0.49	−0.11 ± 0.46	−0.09 ± 0.37	−0.13 ± 0.39	−0.13 ± 0.28	−0.14 ± 0.28	−0.18 ± 0.38	−0.44 ± 0.28	0.39 ± 0.37		0.31 ± 0.05	−0.72 ± 0.04	0.47 ± 0.05	0.13 ± 0.06
Marbling_24h	−0.43 ± 0.32	0.39 ± 0.50	0.31 ± 0.58	−0.43 ± 0.47	−0.12 ± 0.43	−0.40 ± 0.44	−0.36 ± 0.32	−0.36 ± 0.31	−0.11 ± 0.45	0.13 ± 0.44	0.57 ± 0.38	0.18 ± 0.38		−0.16 ± 0.05	0.37 ± 0.05	0.21 ± 0.05
L*_24h	0.20 ± 0.32	−0.04 ± 0.56	−0.24 ± 0.52	0.14 ± 0.52	0.09 ± 0.39	0.19 ± 0.39	0.17 ± 0.30	0.18 ± 0.29	0.24 ± 0.42	0.54 ± 0.27	−0.62 ± 0.31	−0.73 ± 0.16	−0.18 ± 0.43		−0.27 ± 0.05	−0.13 ± 0.06
a*_24h	−0.40 ± 0.34	0.42 ± 0.52	0.31 ± 0.63	−0.45 ± 0.50	−0.33 ± 0.44	−0.32 ± 0.44	−0.41 ± 0.29	−0.42 ± 0.29	−0.28 ± 0.49	−0.13 ± 0.42	0.32 ± 0.58	0.40 ± 0.34	0.45 ± 0.40	−0.26 ± 0.40		0.17 ± 0.05
Shearing force	−0.41 ± 0.33	0.13 ± 0.57	0.31 ± 0.52	−0.23 ± 0.52	−0.06 ± 0.40	−0.37 ± 0.38	−0.26 ± 0.30	−0.27 ± 0.30	−0.12 ± 0.42	−0.05 ± 0.38	0.43 ± 0.43	0.11 ± 0.36	0.14 ± 0.46	−0.30 ± 0.35	0.04 ± 0.47

Note: The phenotypic and genetic correlations ± standard errors were presented in the upper and lower triangles, respectively; italic: p < 0.05 and blod: p < 0.01.

All fiber types correlated with each other in phenotype except for four pairs, which were Percent_IIA with FN and Dens_IIB, between Dens_I and Dens_IIA, and between Percent_IIB and Dens_NF. The strongest phenotypic correlation was between Dens_IIB and Dens_FN, and the correlation coefficient between them was 0.97 (P < 0.0001). Most meat quality traits were also in correlation with each other, and the strongest phenotypic correlation was between Color_24h and L*_24h (r = −0.72, P < 0.0001). All fiber types also correlated with at least one meat quality trait except for Dens_FN, and the strongest correlation was between Percent_IIB and a^*_24h (r = −0.45, P < 0.0001).

Most genetic correlation coefficients were not significant because of their large standard errors, especially the correlation coefficients between fiber types and meat quality, none was significant. FN was in positive and strong correlation with Dens_IIA (r_g = 0.96, P < 0.0001) and Dens_IIB (r_g = 0.75, P < 0.0001), and Percent_I correlated with Percent_IIB (r_g = −0.87, P < 0.0001) negatively and strongly. Except for no correlation between Dens_I and Dens_IIA, the four fiber densities were in positive and strong correlation with each other. For meat quality, except for L*_24h correlated with L*_45min (r_g = 0.54, P < 0.05), pH_24h (r_g = −0.62, P < 0.05), and Color_24h (r_g = −0.73, P < 0.01), all meat quality traits did not correlate with each other in genetics significantly.

4 DISCUSSION

The aim of the present study was to investigate muscle fiber types and meat quality in four pig populations and estimate their heritability, phenotypic, and genetic correlation coefficients in Shanxia long black pig. The genetic parameters, estimated in this study, would be used to improve meat quality traits.

4.1 Meat quality among four populations

Many researches have investigated the influence of marbling score or intramuscular fat deposition on the flavor and tenderness of longissimus dorsi muscle in pigs (Brewer et al., 2001; Hocquette et al., 2010). Marbling_24h were 1.94, 2.35, 3.00, and 4.49 in SX, DS, SL, and LL, respectively, greater than 1.57 reported by Lee et al. (2022) in Jeju black pigs. Lulai black pigs had a strong ability of fat deposition, and they deposited fat not only under the skin but also in muscle. Therefore, Marbling_24h of LL was the highest among the four populations. The pH plays a vital role in the protein denaturation of muscle, and it has been reported in association with meat color and drip loss (Fischer, 2007). pH_24h ranged from 5.40 to 5.76 in this study, and it was similar to those reported by Ryu et al. (2008). Warner-Bratzler shear force was the most common method to measure meat tenderness (Fernández-Barroso et al., 2020; Honikel, 1997; Tejerina et al., 2012), so it was used in this study. Shearing force was higher in this study than those reported previously, since the diameter of the meat sample was larger than that of the standard method to reduce the measuring error.

4.2 Muscle characteristics among four breeds

Muscle characteristics, particularly fiber types and their ratios, play an indispensable role in meat quality (Gondret et al., 2005). Among the four populations, Percent_IIA was highest (16.2%) in SL and lowest (8.6%) in DS, but FN was highest (2241593) in SX and lowest (1303573) in LL. This result indicates that Percent_IIA only contributes a small proportion to FN (Ryu et al., 2004). Percent_IIB was lowest (68.4%) in LL and highest (80.5%) in DS, and meat quality was also best in LL and poorest in DS. It is consistent that low Percent_IIB would be beneficial to meat quality (Lefaucheur, 2010). Low pH_24h was in SX and DS probably caused by high Percent_IIB, because the type IIB fiber was related to produce lactic acid through rapid glycolysis of muscle glycogen (Fernandez et al., 1995). Fiber type composition was significantly different among populations, and type IIB fibers were a major component of muscle, in consistent with the results reported by Kim et al. (2014).

4.3 The impact of muscle fibers on meat quality

The fiber types influenced the meat quality in pigs (Lee et al., 2010; Ryu & Kim, 2006). For example, pH of Berkshire pigs was high due to high Percent_I (10.69%) and low Percent_IIB (80.29%) (Ryu et al., 2008). In this study, the same tendency was observed. Among the four populations, pH_24h of LL was the highest because its Percent_I was the highest (15.4%) and its Percent_IIB was the lowest (68.4%) in LL. FN has been reported to have a positive correlation with the growth potential of lean tissue (Kim et al., 2008), for example, LL had the lowest FN, and its lean meat content was the lowest, but only increasing FN would not be a good strategy to improve lean meat content (Kim et al., 2008; Lefaucheur, 2010). Small areas and high density of muscle fibers were consistent with high meat quality (Choi et al., 2006; Qi et al., 2019). Lulai black pig had the highest fiber density, and its meat quality was the best; while DS had the lowest fiber density, and its meat quality was the worst.

4.4 Heritability of recorded traits in SX

The heritability of muscle fiber types was from 0.04 to 0.40 in SX, similar to those (0.05 to 0.43) reported previously (Lee et al., 2022). The heritability of the meat quality traits ranged from 0.06 to 0.47 in SX, consistent with the results of previous studies (from 0.13 to 0.55) (Miar et al., 2014). Most muscle fiber types and meat quality traits exhibited low-to-moderate heritability, and this indicated that it is difficult to improve those traits through standard selection practices.

4.5 Phenotypic and genetic correlation in Shanxia long black pig

Phenotypic and genetic correlation analyses were performed only in SX, and Percent_IIB positively correlated to L^*_45min (r = 0.19) and L^*_24h (r = 0.13), in agreement with the light color of this type of fiber (Larzul et al., 1997). Percent_IIA negatively correlated with L^*_45min (r = −0.17) and L^*_24h (r = −0.11), this was consistence with the results reported by Ryu and Kim (2005): lightness of meat was increasing with decreasing of Percent_IIA. The correlation between FN and pH_24h was −0.19, indicating that selection for increased FN could decrease pH_24h and have a detrimental effect on pork quality due to the lower ultimate pH, this was consistent with the result that a high FN would be exhibiting an adverse effects on meat quality (Rehfeldt & Kuhn, 2006). Percent_I positively correlated to Marbling_24h (r = 0.20), it was consistent with that total number of type I was positively correlated to the fat content and prone to the production of dark, firm and dry meat (Hwang et al., 2010; Ozawa et al., 2000). Therefore, it is beneficial to maintain meat quality with a suitable amount of total number of type I. Percent_IIB negatively correlated to pH_45min (r = −0.16), SX had the lower ultimate pH with the higher total number of type IIB among the four populations, in consistent with the result that a higher proportion of type IIB fibers may be more prone to lower ultimate pH (Solomon et al., 1998). Our results showed either increasing the proportion of type I fiber or the number of type IIB fibers alone had a detrimental effect on meat quality, indicating that the appropriate proportion of type I and type IIB fibers would be a direction to ensure the meat quality of pork. Kim et al. (2013) reported pigs with a higher or lower Dens_IIB also had a higher or lower Dens_I, in consistent with the result of the present genetic correlation study: Dens_I positively correlated to Dens_IIB (r_g = 0.72). There are only a small number of studies reported the relationship between muscle fiber density and meat quality traits, and additional research is needed to further investigate.

ACKNOWLEDGMENTS

We thank Professor Lusheng Huang for his contribution to the design and conception of the study, revision of the manuscript, and financial and human resources support of the present work. This study was financially supported by National Key Research and Development Program of China (2021YFD1200801), Jiangxi Joint Key Project of Pig Improvement (2022JXCQZY01) and the National Natural Science Foundation of China (31972542).

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

Supporting Information

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Citing Literature

Volume95, Issue1

January/December 2024

e13915

Investigation on muscle fiber types and meat quality and estimation of their heritability and correlation coefficients with each other in four pig populations

Abstract

1 INTRODUCTION