Research Note: Genetic parameters for egg production and clutch-related traits in indigenous Beijing-You chickens

Abstract

Egg products from indigenous chickens have growing market shares as consumers are pursuing differentiation in egg consumption. The genetic improvement in egg production performance of those breeds is crucial for increasing the economic profit. This study aimed to estimate genetic parameters for egg production and clutch-related traits in indigenous Beijing-You chickens for understanding the genetic architecture and exploring proper biological traits for selection. Data on traits including age at first egg (AFE), egg number (EN), average clutch length (ACL), maximum clutch length (MCL), number of clutches (NC) and pauses (NP), and average pause length (APL) were collected from 4 generations of purebred Beijing-You chickens based on the 43-wk and 66-wk of individual egg production record. The heritabilities, genetic and phenotypic correlations were analyzed by the DMU software with the restricted maximum likelihood method in a multivariate animal model. The results showed that the AFE of Beijing-You chickens was 174.45 d of age, and its heritability was as high as 0.62. The heritability was 0.26 for EN43 and 0.18 for EN66. The clutch traits including ACL, MCL, NC, and NP were moderate to high heritable (h² = 0.15–0.39), but APL was very low heritable (h² = 0.05). Genetic correlations were high between AFE and EN (r_{G(AFE, EN43)} = −0.79, r_{G(AFE, EN66)} = −0.39), whereas low between AFE and ACL (r_{G(AFE, ACL43)} = −0.08, r_{G(AFE, ACL66)} = 0.01) and MCL (r_{G(AFE, MCL)} = −0.07). EN had higher correlations with ACL (r_{G(EN43, ACL43)} = 0.59, r_{G(EN66, ACL66)} = 0.40) than that with MCL (r_{G(EN43, MCL43)} = 0.56, r_{G(EN66, MCL66)} = 0.32). The heritability for ACL43 (h² = 0.38) was higher than that for MCL43 (h² = 0.33). ACL43 had a positive correlation with EN66 (r_{G(ACL43, EN66)} = 0.62). These results indicated that the egg production of whole laying period could be improved by early selection for AFE and ACL at the same time in Beijing-You chickens.

INTRODUCTION

Eggs are a rich source of high-quality protein, fat, and vitamins naturally available. Besides the nutritional value, customers also pursue differentiation in the egg consumption. Eggs from some traditional breeds with distinct eggshell colors, appearance, and flavors are becoming more and more popular. Egg production in China accounted for 34% of global egg production (Horne, 2022), and around 10% of which was composed of eggs from indigenous dual-purpose chicken breeds, such as Beijing-You chickens used here. These breeds are well known for their superior egg quality including pink eggshell, higher egg yolk ratio, and flavorsome palate. They are the potential genetic resources to be recruited in professional traditional laying hens breeding. Because of the lower egg production and reproductive performance for Beijing-You chickens, the genetic selection in pure line is very necessary to improve production and reproduction efficiency and provide more economic benefits for householders.

Egg production is a comprehensive phenotype affected by several specific factors such as age at first egg (AFE), egg-laying rate, clutch traits, and oviposition interval. The traditional direct selection of egg number (EN) or egg-laying rate resulted in positive genetic progress in egg production, whereas progress went on slowly (Wolc et al., 2010). Biologically, the EN or egg-laying rate depends on the egg-laying pattern of clutches (consecutive days with eggs) and periods of pause days between them, and their length (Wang et al., 2022). Other studies claimed the advantage of selecting for clutch pattern-related traits, considering the higher genetic variability and foreseeable selective response (Wolc et al., 2019; Becot et al., 2021). AFE indicates the sexual maturation of the birds. Clutch traits including clutch and pause length, number of clutches, and pauses are characteristic of individual egg-laying patterns, and selecting for longer clutch length is beneficial to increase total egg production (Wang et al., 2022).

The estimation of genetic parameters for those egg production and clutch-related traits are substantial for understanding the genetic architecture and exploring proper biological traits for improvement of egg production. However, the information in this field is quite limited for indigenous breeds. In the present study, using the Beijing-You chicken as a representative breed, the heritability, genetic, and phenotypic correlations were estimated to provide an important basis for breeding.

MATERIALS AND METHODS

Ethical Consideration

The current study was approved by the Animal Care and Use Committee of Institute of Animal Science, Chinese Academy of Agricultural Sciences (IAS-CAAS, No. IAS2021-48) and was executed in accordance with the relevant guidelines and regulations set by Ministry of Agriculture and Rural Affairs of the People's Republic of China.

Experimental Animals

Phenotypic data was available on purebred Beijing-You chickens raised on the experimental farm of IAS-CAAS collected over 4 generations. The pedigree was used over 5 generations including a total of 4,305 birds. Hens were fed a standard commercial diet adjusted according to chicken standard feeding requirements. Each individual, from 1 to 8 wk of age, were kept in the same environment with free access to food and water following the standard brooding programs. Pullets were fed with the same diet containing 16% CP, 2,800 kcal/kg ME, 2.0% Ca, and 0.32% nonphytate P from 8 wk of age to 5% egg laying rate. 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 consisted of a systematic reduction of light ranging from 24 h at day-old to 10 h at 8 wk of age. Light was provided for 9 h throughout the growing period from 8 to 20 wk of age. Subsequently, lighting period was increased to 1 h per week in succession until 29 wk of age. The constant lighting was kept on for 16 h with lights on from 06:00 to 22:00 since 30 wk of age.

Traits Measurements

Egg production from the first egg until 66 wk of age of each individual was recorded by the customized Radio Frequency Identification-based data collection system to calculate the egg production-related traits. AFE was defined as the age of the hen laying the first egg. EN was the total number of eggs laid by each hen in a given period. Clutch traits followed a cyclical pattern, and the division and calculation were as follows (Emamgholi-Begli et al., 2019; Becot et al., 2021): the number of clutches (NC) described the number of times the hen laid eggs in succession without a break, the number of pauses (NP) represented the number of times the hen paused 1 d or several days after a consecutive laying period, average clutch length (ACL) depicted the average number of days for a clutch in each hen, maximum clutch length (MCL) characterized the maximum number of days for a clutch in each hen, and average pause length (APL) was the average number of days for halted laying in each hen.

The phenotypic values of EN and clutch traits based on the 43-wk record (EN43, NC43, NP43, ACL43, MCL43, and APL43), and 66-wk record (EN66, NC66, NP66, ACL66, MCL66, and APL66) were calculated. Outliers were removed with the triple standard deviation rule for each trait. Total individual of 1,972 hens, including 611 individuals for the first generation, 377 individuals for the second generation, 293 individuals for the third generation, and 691 individuals for the fourth generation, were kept for further analyses, thereof, the first generation only had 43-wk egg production record.

Statistical Analyses

R software (version 4.3.1) was applied to calculate phenotypic data based on the egg production record until 43 and 66 wk of age respectively, and generate descriptive statistics. Heritability, genetic and phenotypic correlations for egg production and clutch-related traits were estimated using the restricted maximum likelihood (REML) method with a multivariate animal model in the DMUAI module of the DMU software (Jensen and Madsen, 1992). The model was assumed as follows:

$$\mathit{y}=\mathbf{X}\mathit{b}+\mathbf{Z}\mathit{a}+\mathit{e}$$

where $\mathit{y}$ is a vector of observations for the traits analyzed; $\mathit{b}$ is a vector of fixed effects of generations; $\mathit{a}$ is a vector of random additive genetic effects of individual ID; $\mathit{e}$ is a vector of random residual effects; $\mathbf{X}$ and $\mathbf{Z}$ are incidence matrices combined with fixed effects and random additive genetic effects, respectively.

The variance components were estimated as follows:

$$E\left(\mathit{a}\right)=0,E\left(\mathit{e}\right)=0,E\left(\mathit{y}\right)=\mathbf{X}\mathit{b}$$

$$Var\left[\begin{array}{c}\mathit{a}\\ \mathit{e}\end{array}\right]=\left[\begin{array}{cc}\mathbf{A}{\mathbf{\sigma }}_{\mathit{a}}^2& 0\\ 0& \mathbf{I}{\mathbf{\sigma }}_{\mathit{e}}^2\end{array}\right]$$

where ${\mathbf{\sigma }}_{\mathit{a}}^2$ and ${\mathbf{\sigma }}_{\mathit{e}}^2$ are additive genetic variance and random residual variance, respectively; $\mathbf{A}$ and $\mathbf{I}$ are additive genetic relationship matrix and identity matrix, respectively.

The heritability ($h^2$) for egg production and clutch-related traits was calculated with the above variance components, and shown below:

$$h^2=\frac{{\sigma }_a^2}{{\sigma }_a^2+{\sigma }_e^2}$$

Genetic and phenotypic correlations between traits were estimated based on bivariate analyses.

RESULTS AND DISCUSSION

The Beijing-You chicken is a typical indigenous breed with potential for integration into commercial breeding programs following the future diversified demand for flavor and quality traits. The genetic improvement for production and reproduction performance in the purebred is therefore crucial. In the current study, genetic parameters and correlations for egg production and clutch-related traits were investigated in purebred Beijing-You chickens to understand the egg production performance and offer assistance for proper breeding program formulation.

As shown in Table 1, the average AFE was 174.45 d of age with a CV of 6.17%. The average EN increased by 85.29% from 43-wk to 66-wk egg production record. The increase, meanwhile, occurred in MCL from 10.04 d to 10.18 d, in NC from 26.15 to 57.50, and in NP from 34.01 to 79.45. The ACL calculated from the 43-wk egg production record was 3.53 d and APL was 1.37 d, whereas the former decreased to 3.00 d and the latter increased to 1.42 d when using the 66-wk record. Moreover, the CV of clutch traits were high, ranging from 26.80% for NC43 to 55.50% for MCL43.

Table 1.

The descriptive statistics, estimated variance components, and heritability for egg production and clutch-related traits of Beijing-You chickens.

Traits	N	Min	Max	Mean	SD	C.V.%	${\sigma }_a^2$	${\sigma }_e^2$	${\sigma }_p^2$	$h^2$	SE
AFE (d)	1947	142	208	174.45	10.76	6.17	72.38	44.91	117.29	0.62	0.04
EN43 (n)	1938	31	131	87.98	15.58	17.71	74.68	215.32	290.00	0.26	0.04
ACL43 (d)	1944	1.00	8.75	3.53	1.21	34.23	0.58	0.95	1.53	0.38	0.05
MCL43 (d)	1926	1	38	10.04	5.57	55.50	11.05	22.14	33.19	0.33	0.04
NC43 (n)	1959	4	47	26.15	7.01	26.80	19.78	32.69	52.47	0.38	0.04
NP43 (n)	1943	3	73	34.01	11.16	32.82	25.62	104.93	130.55	0.20	0.04
APL43 (d)	1937	1.00	5.65	1.37	0.39	28.68	0.01	0.17	0.18	0.05	0.03
EN66 (n)	1325	33	254	163.02	44.34	29.51	372.42	1658.52	2030.94	0.18	0.05
ACL66 (d)	1305	1.25	5.84	3.00	0.87	29.23	0.29	0.52	0.81	0.35	0.06
MCL66 (d)	1301	2	32	10.18	5.30	52.08	11.55	17.90	29.45	0.39	0.06
NC66 (n)	1327	6	100	57.50	18.93	32.92	87.52	270.41	357.93	0.24	0.06
NP66 (n)	1316	5	171	79.45	29.03	36.54	128.55	744.41	872.96	0.15	0.05
APL66 (d)	1310	1.00	3.59	1.42	0.40	27.81	0.01	0.18	0.19	0.04	0.04

Abbreviations: ACL43, average clutch length from 43-wk record; ACL66, average clutch length from 66-wk record; AFE, age at first egg; APL43, average pause length from 43-wk record; APL66, average pause length from 66-wk record; EN43, egg number until 43 wk of age; EN66, egg number until 66-wk of age; Max, Maximum; MCL43, maximum clutch length from 43-wk record; MCL66, maximum clutch length from 66-wk record; Min, Minimum; NC43, number of clutches from 43-wk record; NC66, number of clutches from 66-wk record; NP43, number of pauses from 43-wk record; NP66, number of pauses from 66-wk record.

The estimated variance components, heritabilities, and standard errors for egg production and clutch-related traits were presented in Table 1 as well. Heritability estimates for the above traits ranged from 0.04 for APL66 to 0.62 for AFE. For EN, the heritabilities were 0.26 for EN43 and 0.18 for EN66. The estimated heritabilities for ACL (h²_ACL43 = 0.38, h²_ACL66 = 0.35) and MCL (h²_MCL43 = 0.33, h²_MCL66 = 0.39) were relatively high, but that for APL waslow, being approximately 0.05. The NC (h²_NC43 = 0.38, h²_NC66 = 0.24) and NP (h²_NP43 = 0.20, h²_NP66 = 0.15) were moderate heritable.

Genetic and phenotypic correlations among egg production and clutch-related traits from 43-wk and 66-wk records were demonstrated in Table 2. Genetically, the AFE was more negatively correlated with EN43 (r_G = −0.79) than with EN66 (r_G = −0.39). In addition, AFE had weak correlations with ACL and MCL around 0, either genetically or phenotypically. The genetic correlation was -0.39 between AFE and NC43 and -0.24 between AFE and NC66. The EN43 had relatively higher correlations with ACL43 and MCL43, being 0.59 and 0.56, respectively. The EN66 showed high genetic correlation with EN43 (r_G = 0.78) and ACL43 (r_G = 0.62). Genetic correlation of ACL with MCL was significantly positive, being 0.96 for 43-wk and 0.88 for 66-wk. On the contrary, the strong association of NC with ACL and MCL were negative (r_{G(NC43, ACL43)} = −0.84, r_{G(NC43, MCL43)} = −0.86, r_{G(NC66, ACL66)} = −0.78, r_{G(NC66, MCL66)} = −0.71). The phenotypic correlations among these traits presented generally similar trends to genetic correlations.

Table 2.

The phenotypic and genetic correlations for egg production and clutch-related traits from 43-wk and 66-wk egg production record.

Traits	AFE	EN43	ACL43	MCL43	NC43	NP43	APL43	EN66	ACL66	MCL66	NC66	NP66	APL66
AFE		−0.46	−0.03	−0.07	−0.29	−0.25	0.01	−0.14	0.03	−0.05	−0.14	−0.15	−0.03
EN43	−0.79 (0.06)		0.52	0.42	0.12	−0.31	−0.52	0.71	0.36	0.42	0.19	−0.08	−0.33
ACL43	−0.08 (0.09)	0.59 (0.08)		0.77	−0.71	−0.68	−0.11	0.36	0.93	0.75	−0.42	−0.49	−0.15
MCL43	−0.07 (0.09)	0.56 (0.09)	0.96 (0.02)		−0.54	−0.46	−0.01	0.24	0.61	0.99	−0.31	−0.31	−0.08
NC43	−0.39 (0.08)	−0.09 (0.12)	−0.84 (0.04)	−0.86 (0.04)		0.64	−0.27	−0.01	−0.79	−0.61	0.67	0.56	−0.02
NP43	−0.38 (0.10)	−0.20 (0.13)	−0.86 (0.04)	−0.88 (0.06)	0.95 (0.04)		0.55	−0.23	−0.72	−0.53	0.43	0.66	0.44
APL43	0.28 (0.19)	−0.38 (0.20)	0.19 (0.23)	0.21 (0.22)	−0.53 (0.20)	−0.23 (0.30)		−0.35	−0.08	−0.06	−0.23	0.26	0.70
EN66	−0.39 (0.13)	0.78 (0.08)	0.62 (0.12)	0.44 (0.16)	−0.19 (0.16)	−0.42 (0.17)	−0.52 (0.25)		0.19	0.25	0.56	−0.21	−0.38
ACL66	0.01 (0.11)	0.49 (0.12)	0.98 (0.02)	0.86 (0.06)	−0.94 (0.03)	−0.95 (0.03)	0.69 (0.27)	0.40 (0.15)		0.63	−0.65	−0.67	−0.14
MCL66	−0.07 (0.11)	0.56 (0.11)	0.93 (0.03)	0.99 (0.01)	−0.90 (0.04)	−0.91 (0.05)	0.60 (0.27)	0.32 (0.15)	0.88 (0.04)		−0.33	−0.31	−0.03
NC66	−0.24 (0.12)	−0.05 (0.17)	−0.67 (0.11)	−0.68 (0.11)	0.88 (0.06)	0.79 (0.09)	−0.96 (0.19)	0.25 (0.17)	−0.78 (0.07)	−0.71 (0.10)		0.71	−0.22
NP66	−0.30 (0.15)	−0.20 (0.21)	−0.86 (0.11)	−0.73 (0.14)	0.96 (0.08)	0.87 (0.08)	−0.98 (0.37)	0.04 (0.22)	−0.85 (0.08)	−0.75 (0.12)	0.92 (0.06)		0.50
APL66	−0.01 (0.28)	−0.26 (0.27)	0.02 (0.25)	0.14 (0.26)	−0.23 (0.24)	−0.05 (0.30)	0.49 (0.34)	−0.67 (0.32)	0.11 (0.33)	0.17 (0.33)	−0.59 (0.36)	−0.24 (0.51)

Phenotypic correlations are above the diagonal and genetic correlations are below the diagonal with standard errors in parentheses.

Abbreviations: ACL43, average clutch length from 43-wk record; ACL66, average clutch length from 66-wk record; AFE, age at first egg; APL43, average pause length from 43-wk record; APL66, average pause length from 66-wk record; EN43, egg number until 43 wk of age; EN66, egg number until 66-wk of age; MCL43, maximum clutch length from 43-wk record; MCL66, maximum clutch length from 66-wk record; NC43, number of clutches from 43-wk record; NC66, number of clutches from 66-wk record; NP43, number of pauses from 43-wk record; NP66, number of pauses from 66-wk record.

The indigenous breeds are expected to be kept for egg production until no later than 66 wk of age due to the sharp decrease in performance afterward. However, improving persistence of laying and prolonging the laying cycle is under breeders’ eager concerns, in order to reduce cost during the brooding stage and lessen the environmental burden. The EN43 is normally employed as a selection criterion for genetic improvement of egg production in the pure lines based on its genetic correlation with the egg production of the whole laying period. The high genetic correlation between EN43 and EN66 indicated that selecting for higher EN43 was of great value to increase EN66. The larger additive variance and residual variance were estimated for EN66 than EN43 because phenotypic variance increased with the number of laying times from 43 to 66-wk of age. However, the estimated heritability for EN at a late age (EN66) is lower than that of EN43, indicating that the proportion of residual variance for EN66 increased due to dramatic environmental variation in the late production period. Liu et al. (2019) also reported that the heritability for EN till 23 wk was as high as 0.53, but that for EN till 80 wk was as low as 0.09 in the purebred Rhode Island Red (RIR) line, supporting the similar downward trend of heritability with aging as found in our results. This inspires that the refined rearing condition for later egg production period is important, in order to achieve an extension of efficient laying period. For selection, the high genetic correlation between EN43 and EN66 indicates the feasibility of improving the whole laying period performance by selection for traits estimated at an early age.

AFE is a direct indicator of onset of sexual maturation of female chickens. Although altered with environmental factors such as lighting, variation of AFE is determined by genetic background. Highly intensive selection for total egg production in some productive layer lines, such as RIR and White Leghorn (WL), may result in early and uniform sexual maturation around 150 d of age (Wolc et al., 2019; Shi et al., 2023). It is noticed that the less productive indigenous chickens without any selection pressure showed varied AFE: it is as early as 124 d of age for Ningdu Sanhuang chickens (Xu et al., 2011) and 157 d of age for Suken chickens (Li et al., 2019). Therefore, the early AFE is a necessary but not sufficient condition for high egg production in the whole laying period. The AFE for Beijing-You chickens estimated in this study (174.45 d ± 10.76 d) was very similar to the result in the same line reported by Wang et al. (2022). In general, Beijing-You chickens showed late sexual maturity characteristics among indigenous chickens. The genetic selection for earlier AFE, therefore, is expected to improve the egg production performance. AFE was reported as a moderate to high heritable trait in previous literatures, ranging from 0.22 to 0.55 (Wolc et al., 2010; Emamgholi Begli et al., 2019; Liu et al., 2019; Wolc et al., 2019). Our estimated heritability for AFE was as high as 0.62 for Beijing-You chickens, showing that the genetic variance played a dominant role. This may have resulted from the fact that Beijing-You chickens were not under intensive selection for AFE or total egg production. These results also indicated that genetic improvement for early AFE by selection can be anticipated. Besides, AFE showed a stronger negative genetic correlation with EN43 than that with EN66 (−0.79 vs. −0.39). Therefore, AFE can be chosen as a selection indicator to improve early egg production effectively, whereas the egg production during the late laying cycle needs to be lifted by selection for an alternative trait indicating the laying persistence.

Besides AFE, the improvement of successive or persistent egg production is also substantial. The indigenous chickens normally show lower egg-laying peaks and inability to maintain the peak for a long time. Evaluation of clutch traits, which represent the sequence of oviposition and its rhythm, can provide more insight into the difference between productive and inferior layers than EN and laying rate (Wolc et al., 2010). Moreover, the crossbred between indigenous breeds and elite layer line WL showed negative heterosis for ACL (Wang et al., 2022). The better understanding of inheritance and promoting its application for selection in pure lines is therefore important. The declining tendency for ACL and increasing tendency for NC and NP as age advances (43 wk vs. 66 wk) may account for the sharp decline in laying rate. Except for APL, other clutch traits including ACL, MCL, NC, and NP were moderate heritable in Beijing-You chickens, ranging from 0.15 to 0.39. But for highly productive Rhode Island White hens, heritabilities of NC, ACL, and MCL calculated from 64-wk record were 0.23, 0.23, and 0.11, respectively (Wolc et al., 2010), which are lower than our NC66, ACL66, and MCL66. These results indicate that the indigenous breeds are holding higher genetic variation for these traits and that the variation in the elite layer lines may be eroded by intense selection for production. The heritability for ACL and MCL from 43-wk and 66-wk were higher than that for EN43 and EN66, respectively. The genetic correlation between EN and ACL was overall higher than that between EN and MCL, indicating that ACL is better than MCL to improve EN. Furthermore, a high correlation was found between ACL43 and EN66. Taken together, ACL43 is a better indirect selection indicator for improvement in EN through the whole laying period in purebred Beijing-You chickens.

Interestingly, low correlations between AFE and clutch traits were found in this study, either genetically or phenotypically. In turkeys, AFE was negatively correlated with ACL (r_G = −0.39) and MCL (r_G = −0.44) (Emamgholi Begli et al., 2019). These findings support the feasibility to select earlier AFE and longer ACL at the same time, to increase EN in breeding programs for Beijing-You chickens. Moreover, formulating a proper selection index with the inclusion of AFE and ACL, according to actual economic benefits, deserves further investigation for more comprehensive genetic improvement.

In this study, genetic parameters for egg production and clutch-related traits were estimated in an indigenous chicken breed. The results showed that AFE and clutch traits were medium-high heritable, except for APL. The genetic correlations between EN and AFE were highly negative. Meanwhile, EN had higher positive correlations with ACL than that with MCL. More importantly, genetic correlations between AFE and clutch traits were very low. Therefore, increasing EN in indigenous chicken breeds like Beijing-You chickens can be achieved by early selection of AFE and ACL at the same time to implement comprehensive breeding improvement.