Genetic parameters and characterization of egg content spreading area in White Leghorn chickens

Genetic parameters and characterization of egg content spreading area in White Leghorn chickens

Genetic parameters and characterization of egg content spreading area in White Leghorn chickens Ya-Hui Gao, Xing-Hua Li, De-He Wang, Chuan-Wei Zheng, ...

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Genetic parameters and characterization of egg content spreading area in White Leghorn chickens Ya-Hui Gao, Xing-Hua Li, De-He Wang, Chuan-Wei Zheng, Zhuo-Cheng Hou, and Zhong-Hua Ning1

ABSTRACT Uncharacteristically large spreading area on a flat surface of broken egg negatively affects egg quality assessment and reduces eggs’ economic value. In this study, we investigated the heredity of the egg content spreading area as well as the relationships between the egg content spreading area and egg quality traits and properties. We measured the total egg content spreading area (TECA), outer thin albumen area (OTAA), inner thick albumen area (ITAA), yolk area (YA), and egg quality traits for 1414 newly laid eggs from 487 27-wk-old White Leghorn pure line pullets. The genetic parameters of egg content spreading areas were estimated. The phenotypic and genetic correlations between egg content spreading area and egg quality traits were analyzed. The differences in the properties of eggs with similar egg weight but markedly different TECA were also analyzed. The heritability estimates for TECA, OTAA, ITAA, and YA were low to

moderate, with values of 0.214, 0.176, 0.340, and 0.280, respectively. Egg weight was related to TECA with a phenotypic correlation of 0.450 (P < 0.01) and a genetic correlation of 0.349. A high genetic correlation (−0.731) was found between TECA and Haugh unit. In eggs with larger TECA, the weight and total solid content of outer thin albumen (OTA) and moisture content of inner thick albumen (ITA) were significantly higher, whereas the weight and total solid content of ITA was markedly lower, but no differences (P > 0.05) were found in the pH of OTA and ITA, moisture content of OTA, as well as the eggshell strength, thickness, and non-destruction and fracture deformation between eggs with similar egg weight but markedly different TECA. These results suggest that the egg content spreading area can be regulated via the direct selection strategy or indirect selection of the ratio of OTA to ITA in the breeding program.

Key words: albumen quality, egg content spreading area, egg quality, genetic parameter 2018 Poultry Science 97:3429–3434 http://dx.doi.org/10.3382/ps/pey235

INTRODUCTION Chicken eggs are important and inexpensive sources of high-quality proteins in the human diet. The egg white comprises about 60% of the whole egg by weight and it contains 9.7 to 11% superior protein (Mine, 2002). Eggs with greater interior quality are more desirable by modern consumers. It is generally agreed that consumers prefer an egg for table use which holds together well (Van Wagenen and Wilgus, 1935). If albumen spreads over a wide area, it generally indicates staleness, which is well known among consumers (Aktan, 2004). However, the variability in the egg content spreading area in fresh eggs has not been investigated comprehensively. Thus, it would be useful to determine the heredity of the egg content spreading area in order to assess whether it can be regulated in the breeding program. Leeson and Caston

 C 2018 Poultry Science Association Inc. Received December 6, 2017. Accepted May 22, 2018. 1 Corresponding author: E-mail: [email protected]

(1997) showed that offspring from hens markedly differing in albumen spreading area also had significantly different albumen spreading areas corresponding to their dams. Aktan (2011) reported that the strain and age of birds great affected the egg content spreading area. The most frequently discussed factor that affects albumen quality is the storage time. The thick albumen becomes thinner over time and the spreading area increases (Robinson and Monsey, 1972; Wells and Norris, 1987; Karoui et al., 2006). Excluding the outer thin albumen area (OTAA), the total egg content spreading area (TECA), and inner thick albumen area (ITAA) are larger in stored eggs than in fresh eggs (Aktan, 2004). On the other hand, Leeson and Caston (1997) showed that eggs with a large spreading area consistently had the best shell quality and they suggested that the large spreading area may be a consequence of selection for improved shell quality, although the relationship was not demonstrated. Few previous studies have considered the inheritance and characteristics of the content spreading area of fresh eggs. Thus, in this study, we estimated the genetic parameters associated with the egg content spreading

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National Engineering Laboratory for Animal Breeding and MOA Key Laboratory of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China

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areas, before investigating the relationships between the egg content spreading area with the egg interior, external quality traits, and egg properties in White Leghorn chickens, thereby providing a better understanding of the fresh egg content spreading area.

Birds We used a pure line of White Leghorn chickens. These layers were reared by CAU Poultry Breeding Corp., Beijing, China. At the end of 2015 when this study was conducted, the White Leghorn line had been bred to the 14th generation. We selected 190 hens at random from a large population at 46 wk of age and mated them with 60 unrelated roosters (each rooster mated with 3 to 4 hens). In total, 487 pullets were obtained and used in this study. All of the hens were reared in individual cages under identical conditions and they were fed the same feed throughout the experiment. Protocols were approved by the Animal Care and Use Committee of China Agricultural University (permit number: SYXK 2007–0023).

Traits measured Cracked, soft-shelled, and double-yolked eggs were excluded during sampling. All of the measurements were conducted within 24 h after egg laying. We measured the egg weight (EW), TECA, ITAA, OTAA, yolk area (YA), albumen height (AH), Haugh unit (HU), yolk color (YC), eggshell color (ESC), eggshell breaking strength (ESS), and eggshell thickness (EST) in 1414 eggs collected during 4 consecutive days from 487 pullets at 27 wk of age. Egg weight was measured using an electronic balance with an accuracy of 0.1 g over a range of 0 to 300 g. TECA, OTAA, ITAA, and YA were measured as described by Aktan (2004, 2011). Each egg was broken gently after weighing on a horizontal non-reflective glass surface and the albumen was allowed to spread for 5 s before obtaining a digital image by Nikon D7000 digital camera. While images were shot, an accurate ruler (range: 0 to 150 mm; sensitivity: 1 mm) was placed near the spread eggs for the purpose of spatial calibration (pixel to metric unit conversion) during the digital images analysis. The images were analyzed using ImagePro Plus 6.0 software (Media Cybernetics, Rockville, MD). Eggshell color was determined as the average of 3 different shell areas (blunt, middle, and sharp ends) with a portable spectrophotometer (CM-2600d; Konica Minolta, Inc., Tokyo, Japan) and it was expressed as 3 indices: L = degree of white to black; a = degree of red to green; and b = degree of yellow to blue. A fourth value, E, was calculated as the total color difference from the standard by the equation: E = [square root of (L2 ) + (a2 ) + (b2 )], where the color was darker when

Statistical analysis Outlier values outside the mean ± 3 standard deviations (SD) were excluded. The normal distribution of each trait was tested using the one sample Kolmogorov– Smirnov test (IBM SPSS Statistics version 21, Armonk, NY). The hypothesis of a normal distribution was accepted in all cases except for ITAA. The Box–Cox transformation procedure in Minitab Statistical Software version 17 (State College, PA) was used to normalize the ITAA √ data and the transformation equation was Y = 1/ Y . SPSS software was used to obtain the means and phenotypic SDs of the traits, and to perform t-tests. The phenotypic correlations between

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MATERIALS AND METHODS

the E value was lower (Wei et al., 1992; Ingram et al., 2008). Eggshell breaking strength was measured using a Texture Analyser (TA.XTplus, Stable Micro Systems Ltd, Godalming, UK) and recorded automatically with TextureExponent 32 software. Eggshell thickness was measured at the equatorial region without membrane using a digital display micrometer gauge (393–741-10; Mitutoyo, Kawasaki, Japan). AH, HU, and YC were measured using a DET-6000 system (NABEL Co. Ltd, Kyoto, Japan) after obtaining an image of the egg content spreading area. To detect the differences in the properties of eggs that differed markedly in terms of TECA, 38 chickens that produced relatively small or large TECA eggs were identified according to the measurements obtained at 27 wk, whereas the EWs were similar for these chickens to avoid the effect of EW on the spreading area. We measured the EW, TECA, OTAA, ITAA, YA, ESS, eggshell non-destruction and fracture deformation (SND and SFD), and the weight, moisture content, total solid contents, and pH value for the outer thin albumen (OTA) and inner thick albumen (ITA) (OTAW and ITAW, MOTA and MITA, SOTA and SITA, pH OTA and pH ITA) in 212 eggs from 2 groups of chickens aged 60 wk. SND was measured by applying a maximum force of 10 N and SFD was measured by a continuous compression until eggshell was fractured using the Texture Analyzer. After obtaining digital images, OTA and ITA were collected separately from the dish with a syringe and kept in 2 50-mL centrifuge tubes. OTA and ITA were weighed using an electronic balance with a sensitivity of 0.01 g. The pH was measured using an HI 8424 pH meter (Hanna Instruments, Woonsocket, RI) with a sensitivity of 0.01 coupled to an HI1230B PEI body pH probe after homogenizing the OTA and ITA using a rotator for 30 min. The OTA and ITA moisture contents were calculated based on the weights of approximately 5 mL of OTA or ITA in a 6-mm diameter culture dish before and after drying using a vacuum freeze-drying system. The total solid contents of OTA and ITA were each determined as the product of the weight and moisture content.

VARIABILITY IN EGG CONTENT SPREADING AREA

Yij = μ + ai + +pej + eij , where Yij is the ij th phenotypic record of a trait, μ is the common mean, ai is the additive genetic effect for the ith individual, pej is the random permanent environmental effect, and eij is the error. The DMUAI module was applied using the average information restricted maximum likelihood algorithm. Heritability was estimated using single-trait analysis. Standard errors of heritability were calculated as described by Jensen and Madsen (2002). Genetic correlations were estimated between traits using multi-traits analysis while achieving convergence.

RESULTS AND DISCUSSION Descriptive statistics Table 1 shows the means, SDs, and coefficients of variation for the egg content spreading area and egg quality traits. The means and SDs for TECA, OTAA, ITAA, and YA were 91.94 ± 10.67, 51.06 ± 8.74, 27.86 ± 4.47, and 13.02 ± 0.78 cm2 , respectively. Similar results were obtained by Leeson and Caston (1997) who reported that the TECAs were 81.6 ± 13.2 and 98.6 ± 12.7 cm2 for compact and spreading types, respectively, in White Leghorn chickens aged 30 wk. Higher TECA, OTAA, ITAA, and YA values were reported by Aktan (2004) in fresh eggs obtained from an older Lohmann Brown layer flock (18 mo old), with values of 114.4 ± 2.09, 52.3 ± 1.58, 47.1 ± 1.14, and 15.0 ± 0.13 cm2 , respectively. The ratios of OTAA, ITAA, and YA relative to TECA were 55.54%, 30.30%, and 14.16%, respectively. With respect to the ratios of egg components to total egg by weight, they were 13.44%, 33.46%, and 29.26% for OTA, ITA, and yolk, respectively, in a White Leghorn strain (Skala and Swanson, 1962a). The mean EW, HU, and EST values obtained in this study were similar to those reported by Premavalli and Viswanathan (2004), i.e., 47.92 g, 79.16, and 0.33 mm, respectively, in White Leghorn chickens aged 26 wk. The average ESS value was 38.61 N, which could be converted to 3.86 kg/cm2 . A similar result was obtained by Hamilton et al. (1979) who reported that the ESS was 3.97 kg/cm2 in White Leghorn chickens aged 26 wk.

Heritability, repeatability, and phenotypic and genetic correlations Table 2 shows the estimated heritability and repeatability as well as the phenotypic and genetic correlations for the egg content spreading area. The heritability estimates for TECA, OTAA, ITAA, and YA were low to moderate, with values of 0.214 ± 0.069, 0.176 ± 0.064, 0.340 ± 0.095, and 0.280 ± 0.089, respectively. Compared with AH or HU, the indicators of egg interior quality traits as well, the heritabilities of the egg content spreading areas were lower, possibly due to the high variances in the measurements of the areas. The heritability estimates for AH and HU were 0.51 and 0.41, respectively (Zhang et al., 2005) and 0.55 for AH (Wolc et al., 2012). The heritability estimate for ITAA was the highest among the egg content spreading areas. TECA was highly correlated with OTAA where the phenotypic and genetic correlation coefficients were 0.908 (P < 0.01) and 0.885, respectively, thereby indicating that OTAA contributed greatly to TECA. There were high phenotypic and genetic correlations between TECA and ITAA, although they were lower than those between TECA and OTAA, which indicated a lower effect of ITA than OTA on TECA. The phenotypic correlations were low between TECA and YA, OTAA and ITAA, OTAA and YA, and ITAA and YA, whereas their genetic correlations were moderate, except for that between ITAA and YA, which had a low genetic correlation coefficient. The repeatability estimates were high for ITAA and YA, but moderate for TECA and OTAA, which suggests that it would be preferable to measure multiple eggs to achieve higher accuracy.

Phenotypic and genetic correlations with egg quality traits Table 3 shows the phenotypic correlations between the egg content spreading area and egg quality traits. The phenotypic correlations with EW were low to moderate for TECA, OTAA, and ITAA, where the correlation coefficients (P < 0.01) were 0.450, 0.359, and 0.256, respectively. Aktan (2011) reported a phenotypic correlation of 0.337 (P < 0.01) between EW and the spreading area of ITA and yolk in a commercial ATAK line aged 30 wk. There was a high phenotypic correlation of 0.670 (P < 0.01) between EW and YA. To the best of our knowledge, no other studies have determined the correlations between the egg content spreading area and EW. In terms of the relationship between the egg components weights and EW, high phenotypic correlations between total albumen weight and EW were found by Knox and Godfrey (1934) and by Skala and Swanson (1962a); Jaffe (1964) found that the phenotypic and genetic correlations between yolk weight and EW were 0.553 and 0.816, respectively, in White Leghorn pullets. We found moderate to high negative phenotypic correlations (P < 0.01) between TECA and ITAA with AH

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the egg content spreading area and egg quality traits were analyzed using Pearson’s correlation coefficients with SPSS. The genetic parameters for TECA, OTAA, ITAA, and YA were estimated using DMU version 6 software (Madsen and Jensen, 2008). The genetic correlations between spreading area and egg quality traits were analyzed as well. An animal model was constructed as follows:

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GAO ET AL. Table 1. Statistical parameters for egg content spreading area and egg quality traits. Traits 2

Standard Deviation

CV (%)

N Chickens

N Eggs

91.94 51.06 27.86 13.02 51.76 6.62 83.26 7.20 92.40 38.61 0.34

10.67 8.74 4.47 0.78 3.32 1.00 6.04 0.73 0.94 5.71 0.02

11.60 17.12 16.03 5.98 6.42 15.13 7.25 10.14 1.01 14.79 7.22

487 487 487 487 487 487 487 487 487 487 487

1414 1414 1414 1414 1414 1414 1414 1414 1414 1414 1414

TECA = total egg content spreading area; OTAA = outer thin albumen area; ITAA = inner thick albumen area; YA = yolk area; EW = egg weight; AH = albumen height; HU = Haugh unit; YC = yolk color; ESC = eggshell color; ESS = eggshell fracture strength; EST = eggshell thickness.

Table 2. Heritability and repeatability (diagonal), genetic correlation (below the diagonal) and phenotypic correlation (above the diagonal) for egg content spreading areas. TECA

OTAA

ITAA

YA

∗∗

∗∗

∗∗

OTAA

0.214 ± 0.069 (0.495 ± 0.028) 0.885 ± 0.054

ITAA

0.638 ± 0.147

0.176 ± 0.064 (0.418 ± 0.029) 0.221 ± 0.236

YA

0.305 ± 0.225

0.235 ± 0.245

TECA

0.908

0.566

0.259

0.177∗∗

0.209∗∗

0.340 ± 0.095 (0.775 ± 0.016) 0.058 ± 0.229

0.035 0.280 ± 0.089 (0.715 ± 0.019)

Repeatabilities are shown in parentheses in the diagonal. ∗ P ≤ 0.05; ∗∗ P ≤ 0.01. TECA = total egg content spreading area; OTAA = outer thin albumen area; ITAA = inner thick albumen area; YA = yolk area.

Table 3. Phenotypic correlations between egg content spreading area and egg quality traits.

TECA OTAA ITAA YA

EW

AH

HU

YC

ESC

ESS

EST

0.450∗∗ 0.359∗∗ 0.256∗∗ 0.670∗∗

− 0.315∗∗ − 0.051 − 0.583∗∗ 0.127∗∗

− 0.437∗∗ −0.182∗∗ − 0.689∗∗ 0.007

0.020 0.055 − 0.084 0.141∗∗

− 0.065 − 0.084 0.041 − 0.185∗∗

0.028 0.020 0.013 0.087

0.148∗∗ 0.144∗∗ 0.056 0.091∗



P ≤ 0.05; ∗∗ P ≤ 0.01. TECA = total egg content spreading area; OTAA = outer thin albumen area; ITAA = inner thick albumen area; YA = yolk area; EW = egg weight; AH = albumen height; HU = Haugh unit; YC = yolk color; ESC = eggshell color; ESS = eggshell fracture strength; EST = eggshell thickness.

and HU, whereas the correlations between OTAA and YA with AH and HU were low. Similarly, Aktan (2011) reported that the phenotypic correlation between ITAA and AH was −0.525 (P < 0.01) in a commercial ATAK line aged 30 wk. The high correlations between ITAA and AH and HU were expected because all of them are dependent on ITA. The phenotypic correlations between the egg content spreading areas and YC were null expect for YA with a low positive value of 0.141 (P < 0.01). Similar to the other egg internal quality traits, the egg content spreading areas had weak phenotypic correlations with ESC, ESS, and EST. However, the phenotypic correlations between TECA and EST, OTAA and EST, and YA and ESC were highly significant. Table 4 shows the genetic correlations between the egg content spreading area and egg quality traits. The genetic correlations with EW were moderate for

TECA, ITAA, and YA, whereas the genetic correlation between OTAA and EW was low with a correlation coefficient of 0.126. The genetic correlations with AH and HU were moderate to high for TECA, OTAA, and ITAA, where they ranged from −0.515 to −0.731, whereas YA was not genetically correlated with AH and HU. The genetic correlations between the egg content spreading areas and YC were low to moderate. Unlike the phenotypic correlations, there were moderate to high negative genetic correlations between the egg content spreading areas and ESC. Eggs with darker eggshells had larger egg content spreading areas. Similar to the phenotypic correlations, there were weak genetic correlations between the egg content spreading areas and ESS. The genetic correlations with EST were moderate for TECA and OTAA with values of 0.334 and 0.450, respectively, whereas the genetic correlations with EST were weak for ITAA and YA, although

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TECA (cm ) OTAA (cm2 ) ITAA (cm2 ) YA (cm2 ) EW (g) AH (mm) HU YC ESC ESS (N) EST (mm)

Mean

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VARIABILITY IN EGG CONTENT SPREADING AREA Table 4. Genetic correlations between egg content spreading area and egg quality traits. EW TECA OTAA ITAA YA

0.349 0.126 0.413 0.553

± ± ± ±

AH 0.192 0.233 0.184 0.146

− 0.657 − 0.583 − 0.515 0.048

± ± ± ±

HU 0.212 0.280 0.183 0.272

− 0.731 − 0.562 − 0.681 − 0.063

± ± ± ±

YC 0.179 0.262 0.136 0.267

0.266 0.315 0.030 0.236

± ± ± ±

ESC 0.217 0.231 0.201 0.201

− 0.694 − 0.635 − 0.464 − 0.380

± ± ± ±

ESS 0.267 0.279 0.260 0.259

0.116 0.085 0.099 0.221

± ± ± ±

0.308 0.321 0.306 0.337

EST 0.334 0.450 0.010 0.062

± ± ± ±

0.537 0.594 0.569 0.567

all of the standard errors were high. The phenotypic and genetic correlations between ITAA and EST were consistently lower than those between OTAA and EST, possibly because OTA is immediately beneath the eggshell, and thus closer to the eggshell than ITA. Leeson and Caston (1997) found that eggs with a large spreading area also had the thickest eggshells according to deformation measurements. There appeared to be a positive relationship between the spreading area and eggshell quality considering the moderate genetic correlations of TECA and OTAA with EST.

Egg properties differences Table 5 shows the differences of egg properties between small and large TECA groups at 60 wk. TECA Table 5. Differences in egg properties between small and large TECA eggs aged 60 wk (mean ± SD). Traits

Small Group1

Large Group1

TECA (cm2 ) OTAA (cm2 ) ITAA (cm2 ) YA (cm2 ) EW (g) OTAW (g) ITAW (g) MOTA (%) MITA (%) SOTA (g) SITA (g) pH OTA pH ITA EST (mm) ESS (N) SND (um) SFD (um) N Birds N Eggs

79.8B ± 33.80B ± 31.18 ± 14.77 ± 57.83 ± 6.18B ± 20.78A ± 90.22 ± 88.49b ± 0.61B ± 2.39A ± 8.59 ± 8.36 ± 0.32 ± 25.62 ± 82.0 ± 210.7 ± 38 104

92.0A ± 43.84A ± 33.42 ± 14.70 ± 58.67 ± 8.49A ± 19.26B ± 90.40 ± 88.76a ± 0.81A ± 2.17B ± 8.56 ± 8.34 ± 0.33 ± 25.21 ± 81.6 ± 203.3 ± 38 108

10.3 8.99 4.95 0.79 3.08 1.76 2.37 0.61 0.57 0.19 0.32 0.14 0.13 0.02 5.44 13.1 30.7

12.7 8.13 7.33 0.98 3.44 1.46 1.86 0.81 0.46 0.14 0.25 0.14 0.13 0.02 6.62 12.5 36.9

1 Small and large TECA groups were identified according to the measurement of TECA aged 27 wk. TECA = total egg content spreading area; OTAA = outer thin albumen area; ITAA = inner thick albumen area; YA = yolk area; EW = egg weight; OTAW = outer thin albumen weight; ITAW = inner thick albumen weight; MOTA = moisture content of outer thin albumen; MITA = moisture content of inner thick albumen; SOTA = total solid content of outer thin albumen; SITA = total solid content of inner thick albumen; pH OTA = pH value for outer thin albumen; pH ITA = pH value for inner thick albumen; EST = eggshell thickness; ESS = eggshell fracture strength; SND = eggshell nondestruction deformation; SFD = eggshell fracture deformation. A, B Between small and large TECA eggs for each trait, means without a common superscript differ (P < 0.01). a, b Between small and large TECA eggs for each trait, means without a common superscript differ (P < 0.05).

values were markedly higher from large group than those from small group, showing the high consistency of spreading areas regardless of a long time interval. Similarly, Leeson and Caston (1997) reported the same trend from 22 to 66 wk in the White Leghorn hens. No difference (P > 0.05) was found in EW between the 2 groups of eggs, and thus eliminating the influence of EW on the egg content spreading area in this experiment. The differences in OTAA between the 2 groups of eggs were highly significant (P < 0.01), whereas those in ITAA and YA were not significant (P > 0.05). ITAW was significantly higher in smaller TECA eggs (20.78 vs 19.26 g); contrarily, OTAW was significantly higher in larger TECA eggs (8.49 vs 6.18 g), thereby suggesting that the OTA percentage was higher in eggs with a larger spreading area. The wide variations in the amount of OTA and ITA may be the major reasons that determine the egg content spreading area. Similar OTAW and ITAW values were reported by Skala and Swanson (1962a) and by Tharrington et al. (1999) in White Leghorn chickens. The total solid contents of OTA were higher in larger TECA eggs, whereas the total solid contents of ITA were higher in smaller TECA eggs. However, the overall solid contents of OTA and ITA did not differ between the 2 groups of eggs (3.00 vs 2.98 g). Differences in the allocation of the original magnum secretion to the various albumen layers may greatly affect the appearance of the albumen obtained after breaking eggs. The moisture contents of OTA and ITA were slightly lower in the small TECA eggs than the large TECA eggs, and the difference in the moisture contents of ITA was significant (P < 0.05) between the 2 groups of eggs. Unfortunately, we could not confirm whether the difference in the moisture contents of OTA and ITA was due to albumen secretion in the magnum or the “plumping” process in the shell gland. Both processes are involved in albumen formation, i.e., albumen secretion and “plumping” in the shell gland where water and electrolytes enter the albumen (Roberts, 2004). During the “plumping” process, the albumen weight increases to twice the original amount after egg entering the shell gland (Austic, 1977). Variations in the albumen moisture contents appear to be determined at least partly in the shell gland. The albumen pH is used widely to estimate the egg quality, where this value increases as the albumen quality degrades (Benton and Brake, 2000; Silversides and Budgell, 2004; Karoui et al., 2006; Abdel-Nour et al., 2011). In general, eggs with a large TECA are

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TECA = total egg content spreading area; OTAA = outer thin albumen area; ITAA = inner thick albumen area; YA = yolk area; EW = egg weight; AH = albumen height; HU = Haugh unit; YC = yolk color; ESC = eggshell color; ESS = eggshell fracture strength; EST = eggshell thickness.

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ACKNOWLEDGMENTS The work was supported by the National Scientific Supporting Projects of China (2015BAD03B03), National Nature Science Foundation of China (31572388), National Nature Science Foundation of China (31672409) and the Chinese Agricultural Research System (CARS-40).

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considered to exhibit greater staleness in terms of the albumen quality. However, the pH of OTA and ITA did not differ (P > 0.05) between the 2 groups of eggs, thereby indicating that the albumen quality is normal in large TECA eggs as usual. Naturally, extremely large spreading area of egg resulted from disease and food contamination was excluded. Similarly, no differences in the pH of the total albumen or ITA were found between eggs with relatively low and high egg internal quality by Conrad and Scott (1942) and Skala and Swanson (1962b), respectively. Leeson and Caston (1997) found a positive relationship between TECA and eggshell quality. However, we found no differences (P > 0.05) in EST, ESS, SND, and SFD between eggs that differed significantly in terms of TECA. In this study, we investigated the variability in the egg content spreading area in White Leghorn chickens. The heritability estimates for the egg content spreading areas were low to moderate, ranging from 0.18 to 0.34. The OTA percentage was higher in eggs with larger TECA values. In future research, it will be necessary to investigate the mechanism that controls the amounts of OTA and ITA in the magnum and shell gland of the chicken oviduct.