
==== Front
Poult Sci
Poult Sci
Poultry Science
0032-5791
1525-3171
Elsevier

S0032-5791(24)00777-6
10.1016/j.psj.2024.104198
104198
MANAGEMENT AND PRODUCTION
Research note: differential heterosis of spent laying hens’ carcass characteristics and meat quality in reciprocal crosses between White Leghorn and Beijing-You chickens
Yang Hanhan *1
Ni Aixin *1
Wu Yan †
Li Yunlei *
Yuan Jingwei *
Ma Hui *
Zong Yunhe *
Han Xintong *
Chen Jilan *
Sun Yanyan sunyanyan02@caas.cn
*2
⁎ State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
† Department of Poultry Science, Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Science, Wuhan 430000, China
2 Corresponding author: sunyanyan02@caas.cn
1 These authors contributed equally to this work.

08 8 2024
11 2024
08 8 2024
103 11 1041988 7 2024
5 8 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Hybridization is used extensively in commercial layer production. However, heterosis for carcass performance and meat quality of spent laying hens remains unclear, especially under the trend of extended laying cycles. In this study, indigenous Beijing-You chickens (Y) and elite White Leghorn layers (W) were selected to generate purebreds (WW and YY) and reciprocal crosses (WY and YW). Data on traits including carcass compositions, meat quality, and main nutrients for breast muscle were collected when chickens were fed to 100 wk of age. Results showed that body weight (BW) and dressed weight for WY and YW with positive heterosis were significantly higher than WW (P < 0.05). YW had the heaviest breast and thigh of 232.28 g and 278.48 g, respectively. The abdominal fat weight for WY and YW were greatly higher than that for WW (P > 0.05). The yields of carcass compositions, including the dressed yield, half eviscerated yield, eviscerated yield, breast yield and thigh yield, did not differ among the four genetic groups (P > 0.05), except for the yield of abdominal fat. The largest heterosis differences appeared in breast weight (12.26% in YW vs. −0.46% in WY) and abdominal fat yield (15.26% in YW vs. 24.55% in WY). Although BW for crossbreds were similar, the specific parts of the carcass between them were different. For meat quality, WY had negative heterosis (P < 0.05) with the lowest lightness and yellowness, whereas YW had the completely opposite trend. Neither pH1h nor pH24h values had differences among purebreds and reciprocal crossbreds (P > 0.05). The drip loss and cooking loss were 4.01%-4.77% and 15.59%-21.31% respectively among the four genetic groups. The main nutrients of breast, including moisture, crude protein, intramuscular fat and unsaturated fatty acid, did not differ for purebreds and crossbreds (P > 0.05), except for saturated fatty acid. In general, the crossbreds even at the later laying period still showed divergent heterosis on carcass performance and meat characteristics. In view of the heterosis, Beijing-You chickens can be used as the sire line in the crossbreeding to improve carcass compositions of spent hens.

Key words

heterosis
spent hen
reciprocal cross
carcass characteristics
meat quality
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pmcINTRODUCTION

With a stable growth trend in egg production, more than 6 billion laying hens are maintained globally each year (Fan and Wu, 2022). Most commercial laying hens, after completing a 1-year laying cycle, experience a decline in both egg production and egg quality, leading to their replacement. Due to differences in dietary culture, western countries use spent hens as animal feeds, pet foods or compost, while some Asian countries process spent hens into meat products for sustainability such as soup, sausage, etc., considering that they are rich in protein, vitamin, and other nutrients (Fan and Wu, 2022). Extending the laying cycle in commercial egg production has been under the spotlight in the past decade, with its potential for significant environmental, economic, and animal welfare implications (Arulnathan et al., 2024). Extending laying cycle has been explored for its effects on egg quality, bone strength (Hanlon et al., 2022), and hen physiology (Wein et al., 2020). However, limited studies have investigated the impact on carcass performance and meat quality for spent hens. In the Chinese market, the price of spent hens, influenced by meat quality, nutrients, and flavor, is a critical factor to determine farmers’ final profits. Therefore, the development of value-added spent hen products is a ponderable issue under this background.

The White Leghorn (W) is well known as high-yield laying hens, but with lower body weight (BW) and less flavor. On the contrary, indigenous chicken breeds such as Beijing-You chickens (Y) are appreciated by consumers for their mellow meat flavor with relatively rich intramuscular fat (Chen et al., 2008). Though the Y chicken is weak in egg production, its spent hen is commonly sold as high-end products, the price of which could be 10 times of that of W chickens. Heterosis is described as the phenomenon that hybrids exhibit the superior performance to their parents with divergent genotypes. To maximize commercial and productive benefits, crossbreeding is performed to exploit the heterosis. We previously identified the heterosis for egg-laying performance based on the purebreds and crossbreds between W and Y chickens (Ni et al., 2023). However, it remains uncertain whether their crossing will enhance the carcass performance and meat quality, as well as the heterosis for laying hens with extended laying cycles. This investigation is important for breed improvement and marketing assessment. The present study therefore focused on determining the effect of hybridization on carcass characteristics, meat quality, and main nutrient contents for above-mentioned breeds at 100 wk of age.

MATERIALS AND METHODS

Ethical Consideration

This study was approved by the Animal Care and Use Committee of Institute of Animal Science, Chinese Academy of Agricultural Sciences (IAS-CAAS, No. IAS2020-12) and was in compliance with the relevant guidelines and regulations set by the Ministry of Agriculture and Rural Affairs of the People's Republic of China.

Experimental Animals

The W and Y chickens as parental lines were raised on the experimental farm of IAS-CAAS. A total of 30 cocks and 300 hens of each breed were selected to generate 4 genetic groups: (1) 30 W cocks with similar BW and good semen quality were mated with 150 W hens randomly to generate purebred offspring of WW, (2) the same 30 W cocks were mated with 150 Y hens randomly to generate crossbred offspring of WY, (3) 30 Y cocks with similar BW and good semen quality were mated with other 150 Y hens randomly to generate purebred offspring of YY, and (4) the same 30 Y cocks were mated with other 150 W hens randomly to generate crossbred offspring of YW.

All birds from the 4 genetic groups were vaccinated and housed in the same brooding pen following the standard raising program. At 19 wk of age, 290, 242, 307, and 216 hens of WW, WY, YY, and YW groups, respectively, were transferred to individual cages. During the laying period, hens were offered ad libitum water and a diet containing 16.5% CP, 2,700 kcal/kg ME, 3.5% Ca, and 0.32% nonphytate P. The lighting program was gradually increased by 1 hour per week from 8 h at 19 wk of age to 13 h at 24 wk of age, and increased by 0.5 h per week to 16 h at 30 wk of age and thereafter.

Carcass Characteristics

At 100 wk of age, 30 hens in each genetic group were selected randomly to weigh after 12 h of fasting to calculate the average live body weight of each group. A total of 10 hens with similar BW (mean ± standard deviation) in each group were selected to slaughter for carcass characteristics measurement.

Each hen was weighed and slaughtered to record carcass parameters following the standard (Ministry of Agriculture, 2004). The weights of dressed, half eviscerated, and eviscerated were measured, and the yields of those were expressed as the percentages of live body weight. Breast muscle, thigh muscle, and abdominal fat were separated and weighed. The yields of breast and thigh were expressed as the percentages of eviscerated weight. The abdominal fat yield was calculated by abdominal fat weight/ (abdominal fat weight + eviscerated weight).

Meat Quality and Main Nutrients of Breast Muscle

Meat quality was measured following the previous description (Sun et al., 2023). In short, the meat color parameters, including lightness-L*, redness-a*, and yellowness-b*, were determined within 1 h using a colorimeter (CR-400, Konica Minolta Sensing). The pH values of 3 fixed positions for the right breast muscle were measured at 1 h postmortem and 24 h at 4°C using a pH meter (HI 99163, Hanna instruments). The mean pH value of 3 positions was used as the pH of this individual. A meat sample of 1.5 cm × 1.5 cm × 3.0 cm was weighed as W1, then hung in a 50 mL centrifuge tube to avoid the touch of the wall. After 24 h at 4°C, the sample was cleaned by the tissue to remove the surface moisture and weighed as W2. The formula of drip loss was shown as follow: DripLoss(%)=W1−W2W1×100. A meat sample of 1.5 cm × 1.5 cm × 3.0 cm was weighed as W3. The food thermometer was used to monitor temperature when the sample's central temperature reached 80°C, then the meat sample was weighed as W4 after the absorbance of surface moisture by the clean tissue. The formula of cooking loss was shown as follow: CookingLoss(%)=W3−W4W3×100. The rest of breast meat samples were mixed and divided into three duplicates to analyze the moisture, crude protein, intramuscular fat, and fatty acids content according to the AOAC method (AOAC, 2019).

Statistical Analysis

Data from carcass characteristics and meat quality among purebreds and crossbreds were compared with one-way analysis of variance using the GLM procedure of SAS (version 9.4., 2016, SAS Institute Inc., Cary, NC). The results were shown as mean value and standard deviation. Significant differences among purebreds and crossbreds were analyzed by Tukey's Honestly Significant Difference test. The significance was designated as P < 0.05.

The percentage of heterosis for the above traits was calculated as the following:H%=F1‾−(PM‾+PP‾)/2(PM‾+PP‾)/2×100

where H% was the percentage of heterosis. F1‾, PM‾ and PP‾ were represented the average phenotypic value of crossbred, maternal lines and paternal lines.

The Student's t-test was performed to test the significant differences of H% (Wu and Zhang, 1983), shown below:t=F1‾−(PM‾+PP‾)/2(PM‾+PP‾)/2(2×∑(F1i−F1‾)2n−1)/[(PM‾+PP‾)×n]

where F1i was the phenotypic value of individual i from crossbreds; n was the number of each crossbred. The P-value lower than 0.05 or 0.01 were regarded as significant H% or extremely significant H%, respectively.

RESULTS AND DISCUSSION

Carcass Characteristics

Carcass composition and their muscle yield of spent laying hens are important, considering the economic factors. The carcass characteristics of purebreds and reciprocal crossbreds at 100 wk of age were presented in Table 1. The BW for YY was 2.01 kg, and significantly higher than that for WW (P < 0.05). The BW and dressed weight for YW and WY, with noticeable heterosis (P < 0.05), were also significantly higher than that for WW (P < 0.05), indicating the superiority on BW for the YY genotype. Y chickens showed strong fat deposition capacity. Abdominal fat weight for YY in our study was as high as 126.30 g, higher than that for WW (P < 0.05). The crossing between them increased the offspring's fat deposition, with high and positive heterosis of 25.22% and 21.55% for WY and YW, respectively. The eviscerated weight for WW was lower than that for YW (P < 0.05), whereas the eviscerated yields were similar, which was caused by less abdominal fat for WW. YW had the heaviest breast and thigh muscle of 232.28 g and 278.48 g, respectively, positive heterosis of which was up to 12.26% and 6.43%, respectively. Chen et al. (2007) reported a high correlation coefficient of 0.96 between breast muscle weight and BW. But comparing the four genetic groups, WY did not follow this trend, which may be affected by their sire. The yields of carcass compositions among 4 genetic groups had no significant difference (P > 0.05), except for the yield of abdominal fat. The measured values of carcass characteristics between reciprocal crossbreds had no differences (P > 0.05).Table 1 Carcass characteristics for purebred and reciprocal crossbred at 100 wk of age.

Table 1Traits	WW	YY	WY	YW	H% (WY)	H% (YW)	
Live body weight/ kg	1.83 ± 0.13b	2.01 ± 0.07a	2.04 ± 0.10a	2.05 ± 0.10a	6.62†	6.56†	
Dressed weight/ kg	1.70 ± 0.12b	1.86 ± 0.12a	1.87 ± 0.07a	1.92 ± 0.11a	4.97†	7.81†	
Dressed yield/ %	92.88 ± 3.23	92.33 ± 5.61	91.55 ± 4.11	93.71 ± 3.33	−1.14	1.19	
Half eviscerated weight/ kg	1.39 ± 0.08b	1.59 ± 0.11a	1.55 ± 0.08a	1.61 ± 0.16a	3.88†	8.04†	
Half eviscerated yield/ %	75.83 ± 2.58	78.65 ± 5.05	75.58 ± 3.35	78.56 ± 6.31	−2.15*	1.72	
Eviscerated weight/ kg	1.27 ± 0.07b	1.38 ± 0.10a	1.36 ± 0.06ab	1.42 ± 0.13a	2.74†	7.32†	
Eviscerated yield/ %	69.24 ± 2.45	68.54 ± 4.38	66.58 ± 2.66	69.55 ± 5.44	−3.35†	0.96	
Breast weight/ g	199.53 ± 19.76b	214.30 ± 32.01ab	205.96 ± 18.26ab	232.28 ± 22.66a	−0.46	12.26†	
Breast yield/ %	15.73 ± 1.11	15.49 ± 2.10	15.11 ± 1.04	16.35 ± 1.25	−3.18*	4.78†	
Thigh weight/ g	247.24 ± 19.56b	276.08 ± 23.23a	273.85 ± 21.87a	278.48 ± 31.12a	4.66*	6.43†	
Thigh yield/ %	19.52 ± 1.37	19.95 ± 0.94	20.10 ± 1.34	19.66 ± 2.45	1.88	−0.39	
Abdominal fat weight/ g	34.87 ± 13.23b	126.30 ± 30.10a	100.91 ± 30.78a	97.95 ± 35.98a	25.22†	21.55*	
Abdominal fat yield/ %	2.66 ± 0.93b	8.34 ± 1.76a	6.85 ± 1.87a	6.34 ± 1.80a	24.55†	15.26*	
a,b,c,d Different letters within the same row indicate statistical difference (P < 0.05).

⁎ Of H% represents P < 0.05.

† Of H% represents P < 0.01.

WW = purebred offspring from White Leghorn chickens; YY = purebred offspring from Beijing-You chickens; WY = crossbred offspring from White Leghorn sires and Beijing-You chicken dams; YW = crossbred offspring from Beijing-You sires and White Leghorn chicken dams; H% = the percentage of heterosis, H%=F1‾−(PM‾+PP‾)/2(PM‾+PP‾)/2×100.

Although with similar heterosis in BW, YW showed higher heterosis than WY in dressed weight, half eviscerated weight, eviscerated weight, and breast and thigh muscle weight, except for abdominal fat weight with lower heterosis. The heterosis difference was the largest for breast weight (12.26% in YW vs. −0.46% in WY), and abdominal fat yield (15.26% in YW vs. 24.55% in WY). The BW is an overall measurement of growth, while the weight for specific parts of the carcass provides more details regarding the carcass characteristics. Mai et al. (2021) also provided the evidence that reciprocal crossbred between the layers and broilers showed different heterosis for carcass performance. Apparently, the YW crossbreds produced better carcass compositions than WY ones, in view of the higher breast muscle weight and lower abdominal fat deposition. Taken together, Y chickens were recommended to be used as the sire line of cross combination based on the results of high and positive heterosis.

A previous study reported that the improvement of meat yield and egg production at the same time was antagonistic (Ibrahim et al., 2019). Similarly, YW had better carcass compositions in the present study, whereas WY had higher egg production at 100 wk of age (Ni et al., 2023). These observations highlighted the relevance of the sire line effect on offspring's performance.

Meat Characteristics

Meat characteristics, such as color, texture, nutritional value, freshness, etc., are considered by consumers for purchase willingness. Therefore, a better understanding of meat quality for spent hens is necessary. The meat quality and main nutrients of breast muscle for purebred and reciprocal crossbred at 100 wk of age were shown in Table 2. The WY showed the lowest lightness (L*) and yellowness (b*), with negative heterosis (P < 0.05), while YW showed a completely opposite trend. Contrary to those indexes, redness (a*) of WY and YW had significantly positive heterosis (P < 0.05), higher than that of high parent (YY). The pH24h fell from 5.82 to 5.94 for the four genetic groups, within the normal range (Duclos et al., 2007). Neither pH1h nor pH24h values had differences among purebreds and reciprocal crossbreds (P > 0.05). For water holding capacity, the four groups did not show the difference in drip loss and the crossbreds did not show significant heterosis (P > 0.05). The crossing produced the phenomenon that the pH24h values for WY and YW were less than that for low parent (YY), while the drip losses were in the middle range. This finding also occurred in the cross of Sasso and Wassachie chickens (Dzungwe et al., 2024). Cooking loss increased as the temperature rose from 70°C to 90°C, which directly affected meat juiciness and tenderness (Li et al., 2013). This could be a reason for the high cooking loss (at 80°C) of the four genetic groups ranging from 15.59% to 21.31%. Unlike drip loss, the cooking loss for WY and YW showed numerically higher values than that for high parent (YY), with positive heterosis of 28.04% and 15.96% respectively. This might be caused by slaughter stress. Chen et al. (2008) found intramuscular fat had strongly positive correlation with abdominal fat weight, supporting our results that YY had the highest intramuscular fat content and the heaviest abdominal fat weight. The main nutrients of breast did not differ between purebreds and crossbreds (P > 0.05), except for saturated fatty acid. Different fatty acid contents for the four genetic groups were found in our study, which could be resulted from differences in feeding behaviors among different genetic groups. Fatty acid contents influence meat flavor and human health. Saturated fatty acid is regarded as adverse to human health. The content of saturated fatty acid did not show difference between YW and WY (P > 0.05). Compared to WW, this index for YW was significantly higher (P < 0.05), which might be affected by the sire line of Y. Moreover, some unsaturated fatty acids are relatively abundant in old hens, and made them more flavorful and nutritious (Zhang et al., 2022). WY showed positive heterosis of 3.32% for the unsaturated fatty acid content, and negative heterosis of −0.56% for the saturated fatty acid content. Although YW had relatively high fatty acid content, their intramuscular fat content is numerically lower than other groups, which may be due to the large variation of intramuscular fat content in the YW group. Above all, hybridization can improve meat quality and its nutrients to some extent.Table 2 Meat characteristics of breast muscle for purebred and reciprocal crossbred at 100 wk of age.

Table 2Traits	WW	YY	WY	YW	H% (WY)	H% (YW)	
Meat Color							
 Lightness - L*	48.82 ± 3.31b	49.98 ± 2.98b	47.88 ± 3.13b	55.41 ± 4.38a	−3.09*	12.16†	
 Redness - a*	3.36 ± 1.15b	4.51 ± 0.98ab	5.23 ± 1.40a	5.87 ± 2.00a	32.79†	49.36†	
 Yellowness - b*	56.37 ± 9.94ab	64.10 ± 12.65ab	51.79 ± 12.34b	69.96 ± 9.92a	−14.02†	16.13†	
pH							
 pH1h	6.37 ± 0.36	6.07 ± 0.12	6.19 ± 0.33	6.07 ± 0.29	−0.54	−2.38*	
 pH24h	5.94 ± 0.22	5.88 ± 0.16	5.82 ± 0.08	5.86 ± 0.09	−1.47†	−0.81†	
Water Holding Capacity							
 Drip loss/ %	4.01 ± 1.20	4.77 ± 1.64	4.18 ± 0.73	4.37 ± 1.32	−4.85	−0.59	
 Cooking loss/ %	15.59 ± 3.72	17.70 ± 3.88	21.31 ± 6.63	19.30 ± 4.60	28.04†	15.96†	
Main Nutrients							
 Moisture/ %	73.20 ± 0.00	73.25 ± 0.35	72.20 ± 0.28	72.55 ± 0.92	−1.40	−0.92	
 Crude protein/(g/100g)	24.04 ± 0.34	24.00 ± 0.45	24.93 ± 0.64	24.70 ± 0.18	3.80	2.82	
 Intramuscular fat/(g/100g)	1.15 ± 0.21	1.25 ± 0.07	1.20 ± 0.14	1.10 ± 0.57	0.00	−8.33	
 Saturated fatty acids/(mg/g)	2.46 ± 0.14b	2.90 ± 0.17ab	2.67 ± 0.15ab	3.49 ± 0.42a	−0.56	30.22	
 Unsaturated fatty acids/(mg/g)	3.21 ± 0.22	3.42 ± 0.29	3.42 ± 0.31	4.34 ± 0.37	3.32	30.97	
 Palmitic acid (C16: 0)/(mg/g)	1.68 ± 0.11b	1.94 ± 0.05ab	1.81 ± 0.08ab	2.39 ± 0.28a	0.28	32.13	
 Stearic acid (C18: 0)/(mg/g)	0.71 ± 0.04	0.85 ± 0.07	0.76 ± 0.05	0.99 ± 0.13	−3.21	26.92	
 Oleic acid (C18: 1, cis(n9))/(mg/g)	1.08 ± 0.01b	1.24 ± 0.13ab	1.21 ± 0.11ab	1.63 ± 0.16a	4.10	40.82	
 Linoleic acid (C18: 2, cis(n6))/(mg/g)	1.31 ± 0.07	1.16 ± 0.11	1.26 ± 0.13	1.52 ± 0.04	1.83	22.92*	
a,b,c,d different letters within the same row indicate statistical difference (P < 0.05).

⁎ Of H% represents P < 0.05.

† Of H% represents P < 0.01.

WW = purebred offspring from White Leghorn chickens; YY = purebred offspring from Beijing-You chickens; WY = crossbred offspring from White Leghorn sires and Beijing-You chicken dams; YW = crossbred offspring from Beijing-You sires and White Leghorn chicken dams; H% = the percentage of heterosis, H%=F1‾−(PM‾+PP‾)/2(PM‾+PP‾)/2×100.

In summary, this study demonstrated the divergent heterosis for carcass characteristics, meat quality, and main nutrients of breast in reciprocal crossbreds between an elite egg-laying line like W and an indigenous line like Y. The YW crossbred plays an important role in the increase of the carcass related weights and fatty acids content.

DISCLOSURES

None of the authors have any conflict of interest to declare.

ACKNOWLEDGMENTS

Financial support of this study was provided by China Agriculture Research System of MOF and MARA (CARS-40 ), and the Agricultural Science and Technology Innovation Program (ASTIP-IAS-16 ). The authors express great gratitude to Hongwei Wang and Chao Chen (IAS-CAAS) for their assistance with raising animals.
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