Abstract
Based on resource allocation theory, ignoring importance of immunity, and focus on growth and feed efficiency (FE) traits in breeding plans may lead to serious weakness in immune system performance. However, in poultry the adverse effects of selection for FE on the immune system are unclear. Therefore, an experiment was conducted to study the trade-off between FE and immunity using a total of 180 high-performing specialized male chickens from a commercial broiler line which were selected over 30 generations for growth (body weight gain, BWG) and FE (residual feed intake, RFI). Birds were reared for 42 d and 5 FE-related traits of the birds in the last week were considered including daily feed intake (DFI), feed conversion ratio (FCR), residual feed intake (RFI), residual BW gain (RG), and residual intake and gain (RIG). For all 180 chickens, immune system performance including humoral immune response, cell-mediated immunity (CMI), and the activity of lysozyme enzyme (L. activity) as innate immunity was measured. After ascending sort of each FE records, 10% of higher records (H-FE: N = 18) and 10% of lower records (L-FE: N = 18) were determined, and immunity between L-FE and H-FE groups were compared. Moreover, L-BWG and H-BWG were analyzed because BWG is one of components in the FE formula. Performance of the immune system was not statistically different for CMI in none of the studied FE groups. Moreover, high and low groups for DFI and BWG were not different regarding the immunity of the birds. Antibody titers against Newcastle disease virus (NDV) were different between low and high groups of FCR, RG, and RIG. Likewise, SRBC-derived antibodies were significantly different between RFI groups. Rather than humoral immunity, RIG had adversely effect on the innate immunity. Results of the present study showed that although RIG is a more appropriate indicator for FE, choosing for high RIG can weaken the performance of the both humoral and innate immune systems, while RFI had fewer adverse effects.
Key words: residual feed intake, residual intake and body weight gain, humoral immunity, cell-mediated immunity, innate immunity
INTRODUCTION
Meat-type poultry species, in particular high-performance specialized chickens (broilers), have been genetically selected for several generations to improve growth rate (GR), feed efficiency (FE), and related carcass component yields (McGovern et al., 1999; Jahan et al., 2020; Yang et al., 2020). Feed intake (FI) is a significant part of the costs of the meat-type poultry (Emamgholi Begli et al., 2018; Vaziri et al., 2022). Therefore, in recent years, much attention has been paid to the birds’ feed efficiency (Mebratie et al., 2019; Ye et al., 2020). Considering the advantages of feed efficient-birds, it is also claimed that they have less adverse environmental impact, which is of interest of modern breeding programs (Sell-Kubiak et al., 2017). The term “feed efficiency” is used in breeding programs depending on how it is calculated and defined. The most common trait is “feed conversion ratio” (FCR), which is simply derived from the ratio between a birds’ FI and their body weight gain (BWG). While FCR is mainly used by poultry nutritionists, it is of little interest from a geneticist's point of view due to its relatively low heritability (Aggrey et al., 2010; Reyer et al., 2015). Furthermore, FCR can be measured individually or most of the times for a group of the birds, whereas records of individuals are required for genetic improvement of a flock (Reyer et al., 2015; Emamgholi Begli et al., 2018). Besides, confounding effects from the relationship between FCR and its component traits (FI and BWG), and the relationship between its component traits prevent FCR from being an ideal measure of feed efficiency (Willems et al., 2013).
Net feed efficiency (NFE) has been proposed as an alternative to FCR because it describes the efficiency with which birds are arranged according to production and maintenance requirements independent of their production levels. The NFE is determined by calculating residual feed intake (RFI), residual body weight gain (RG), and residual intake and body weight gain (RIG) (Berry and Crowley, 2013; Pryce et al., 2015; Willems et al., 2019). In recent years, RFI has been considered as the most appropriate trait to describe FE (Emamgholi Begli et al., 2018). The trait RFI is a population-based computational measurement defined as the difference between the “measured FI” and the “expected FI” of an individual based on a multiple linear regression equation involving the bird's FI, metabolic weight and BWG (Van der Werf, 2004). Furthermore, RFI is moderately heritable (Mebratie et al., 2019), which is of interest to poultry geneticists. Negative values of RFI and positive values of both RG and RIG indicate feed-efficient chickens. Some studies have been conducted to investigate the effect of FE-related traits on growth traits. Possibly, slow-growing animals with relatively low feed intake are ranked as RFI-efficient animals (which is not favorable), while RG-efficient animals may have faster growth rates and relatively higher feed intake (Crowley et al., 2010). Consequently, combination of RFI and RG into RIG minimizes the likelihood of these uncertainties, while retaining independence of growth performance (Berry and Crowley, 2012, 2013). To the best of the authors’ knowledge, the effect of incorporating NFE into breeding programs on the immune performance of birds has not been studied.
Considering different domestic avian species, there are several studies indicate relationship between growth performance and FE (Rekaya et al., 2013; El Moujahid el et al., 2014; Li et al., 2021), growth performance and reproduction (Barbato, 1999; Williams et al., 2002; Narinc et al., 2014), and growth performance and immune system performance (van der Most et al., 2010; Mohammadi-Tighsiah et al., 2018; Ma et al., 2022). However, studying relationship between FE and immune system has relatively received less attention (Van Eerden et al., 2004; Zerjal et al., 2021). Considering measurement of the FE and growth traits, because the bird is not directly under stress, they are easily recorded and involved in plenty of broiler breeding programs. However, in the case of the immune system performances, it is more challenging to pay attention to these traits in breeding programs due to vulnerability of commercial line birds, need to challenge birds with antigens/pathogens, and frequent blood sampling (Mohammadi-Tighsiah et al., 2018). Therefore, experimental design is necessary to investigate the effect of selection for FE and growth traits on immune system performance. Accordingly, the first objective of this study is to elucidate the trade-off between FE and immune system function (both adaptive and innate) of high-performance specialized chickens. Second, which types of net FE-related traits are nominated in breeding programs, given the importance of immunity?
MATERIALS AND METHODS
This experiment was conducted in the Poultry Research Farm (PRF) of the Faculty of Agriculture of Tarbiat Modares University, Tehran, Iran. The population investigated in this experiment belonged to a paternal line of a commercial broiler chickens that were selected for 30 generations to increase BWG and breast meat weight (BRWT), and reduce RFI. However, individual assessment of the performance of the birds' immune system was not included in the breeding program. A total of 500-day-old male broiler chickens were transferred to PRF from Arian Commercial Broiler Breeding Complex (ACBBC), located in Babolkanar, Mazandaran Province, Iran. The birds were reared in the litter system in the first 2 wk and in individual cages from the beginning of the third week until the end of the breeding period. Individual cages with dimensions of 40 × 35 × 80 cm were made in 4 floors. All the battery cages were equipped with an individual nipple drinking units, and an individual feeder for measuring the DFI. The temperature, humidity, and light were kept uniform in all parts of the hall. The cage hall was equipped with 320 individual cages and therefore only 320 birds were transferred to this hall on the 15th day. The third week was considered as the period of adaptation of the birds to the new environment, and the measurement of FE records was done from the beginning of the fourth week.
The temperature of the hall was set at 36°C for the first 24 h and 35°C for the rest of the first week. The relative humidity of 50 to 60% was also provided in the hall. Moreover, in the first 24 h, the light program was 24 h. After that, the light schedule for the first week was 23:1, the second week was 20:4, and from the third week until the end of the experiment (d 42), it was 18:6 with a constant intensity of 25 lux. The birds were fed with the starter ration in the first 2 wk, the grower ration in the third and fourth weeks, and the finisher ration in the fifth and sixth weeks. Birds had free access to feed in mesh form and water. The level of energy, protein, and other nutrients required was balanced according to the commercial broilers requirements.
Growth Performance and Feed Efficiency
Weight records at hatch (hatch weight: HW), 7, 14, 21, 28, 35 and 42 d (BW7, BW14, BW21, BW28, BW35, and BW42, respectively) were measured with a digital scale with an accuracy of 1 g. Two hours before weighing the birds, access to feed was stopped. At the beginning of the d 22, the feeders were filled with feed and weighed. In order to calculate the DFI of birds, all feeders were weighed every 24 h. Daily feed intake for each bird was calculated from the difference between the current feed weight and the previous day's feed weight. The daily weighing of the feeders continued until the end of the d 42. On d 35 and 42, traits related to FE were measured and calculated (Table 1).
Table 1.
Formula to calculate feed efficiency in broilers.
| Formula | |
|---|---|
| FCR = RDFI/RBWG | (1) |
| EDFI = b0 + b1 BW0.75 + b2 RBWG + e | (2) |
| RFI = RDFI − EDFI | (3) |
| EBWG = b0 + b1 BW0.75 + b2 RDFI + e | (4) |
| RG = RBWG − EBWG | (5) |
| RIG = RG + (−1 × RFI) | (6) |
Abbreviations: EDFI, estimated daily feed intake; FCR, feed conversion ratio; RBWG, real body weight gain; RDFI, real daily feed intake; RFI, residual feed intake; RG, residual BW gain; RIG, residual intake and gain.
Immune System Performance
Humoral (HI) and cell-mediated immune response (CMI) commonly is considered as representatives of adaptive immunity, which were evaluated in this study. As well, lysozyme activity (L. Activity) is considered as indicator of innate immunity. To identify the birds’ immunity relationship with FE, both adaptive and innate immune performances were investigated. Accordingly, 4 humoral immune responses, 1 cell-mediated immune response, and 1 innate immune function were considered. The birds vaccination were performed for bronchitis on d 0, Newcastle B1 on d 8, and Newcastle strain Lasota on d 18. No drugs/antibiotics were used during the experiment. On d 28 and 35, an amount of 0.2 mL of a 5% suspension sheep red blood cell (SRBC) in sterile phosphate buffer was injected into the breast muscle of all chickens. On the day of slaughter (43 and 44 d of age), blood was taken from the birds using sterile syringes. After transferring the samples to the laboratory, the plasma was separated and transferred to 1.5 mL microtubes. These microtubes were stored at −20°C until rest of the experiments.
To determine the cellular immune response of birds, 0.1 mL of phytohemagglutinin-M (PHA-M) was injected to the membrane between the second and third toes of the right foot and 0.1 mL of sterile phosphate buffer was also injected to the membrane between the first and second toes of the left foot of birds. Before the injection and 24 h after injection, the diameter of the right and left foot-web of the birds between digit 1 and 2 was measured. The difference in the diameter of the foot membrane before and after injection was calculated, and considered as the index of the foot membrane representing the birds’ cell-mediated immune response (CMI).
The method for determining the antibody production to SRBC, immunoglobulin T titer (IgT), was microtiter hemagglutination (Mohammadi-Tighsiah et al., 2018). In order to determine the titers of immunoglobulin M and Y, in the first step, 2-mercaptoethanol was used. Then, 2-mercaptoethanol binds with immunoglobulin M (IgM) and at the end of the test, the amount of immunoglobulin Y (IgY) was calculated. From the difference of IgY from IgT, the amount of IgM was also obtained. For determination of antibody titer (IgN) against NDV, the hemagglutination inhibition (HI) test was used according to Cunningham (1971).
L. activity was measured in plasma obtained at the age of 42 d of age using the turbidity method. For this purpose, Micrococcus luteus bacterium was used (Iranian Scientific-Industrial Research Organization (ISIRO), Tehran, Iran). Bacteria were cultured according to the instructions of the ISIRO. After 24 h, the grown bacteria were collected from the surface of the culture medium using a swab and sterile phosphate buffer. Bacteria were brought to an optical density of 0.6 to 0.7 at a wavelength of 490 nm. Then, 480 μL of bacteria were mixed with 20 μL of plasma in a cuvette, and after mixing, the optical density was recorded using a spectrophotometer. Data were recorded from 0 to 300 s in 30-s intervals and the average of 11 measurements was considered as the birds’ innate immunity (L. activity).
Feed Efficiency Groups and Statistical Analysis
First, animal records were sorted in ascending order for FE performance including DFI, BWG, FCR, RFI, RG, and RIG traits. Then, 10% of the birds with the lowest FE performance (L-FE; N = 18) and 10% of the birds with the highest FE performance (H-FE; N = 18) were considered as 2 divergent groups. Only the records of the performance of 35 to 42 d of age were used to group the birds. Then, the immune system performance of the birds in L-FE and H-FE groups was statistically compared using the following model:
where is the population mean, is the birds immune system performance (humoral immunity against SRBC and NDV), cell-mediated immunity (response to PHA-M), and innate immunity (L. activity), is the FE groups (H-FE and L-FE), and is the random residual effects with mean zero and variance . The model was run 6 times for BWG and 5 different FE-related traits including DFI, FCR, RFI, RG, and RIG. Lower and higher (L and H) FE-groups were compared using the GLM procedure of Minitab software version 16 and the Tukey method.
RESULTS AND DISCUSSION
The least square means of higher and lower groups of DFI (H-DFI and L-DHI), BWG (H-BWG and L-BWG), FCR (H-FCR and L-FCR), RG (H-RG and L-RG), RFI (H-RFI and L-RFI), and RIG (H-RIG and L-RIG) on the immune system performance of birds are shown in Tables 2 to 7, respectively. To better understand, the first row of each table refers to the mean comparison of each group. The effect of grouping for DFI (Table 2) and BWG (Table 3) on the immune system performance of the broilers was not statistically significant (P > 0.05). The studied commercial line was selected for growth rate, breast meat weight, and residual feed intake, but for the immune performance of the birds, measurements were only recorded in order to the flock control against disease, and individual records were not available for breeding purposes. While the DFI and BW traits are included in the ACBBC breeding goal, it is expected that selection for improve BWG and RFI have adversely influence on the immune system performance in this population. However, in breeding programs, BWG and DFI traits are just utilized to calculate other FE-related traits (Table 1), and are not directly included in breeding program, as our population did not select for DFI. Actually, birds with high or low FI did not have significant differences in any of the humoral, cellular, and innate immune system performances. Similarly, in the case of BWG (as a growth performance), the birds with higher or lower BWG in the last week of rearing did not show statistically difference in immune system performance (Table 3). These results show that if birds with higher FI have indirectly selected due to selection for growth performance (BW and BWG), it will not have a negative effect on the function of the birds’ immune system.
Table 2.
Comparing between higher and lower groups of DFI (L-DFI and H-DFI) on DFI, humoral, cell-mediated and innate immunity in male broilers.
| Traits | L-DFI | H-DFI | P value |
|---|---|---|---|
| DFI | 151.21b ± 2.43 | 226.86a ± 2.17 | 0.000 |
| IgT | 5.40 ± 0.42 | 5.43 ± 0.37 | 0.947 |
| IgY | 2.73± 0.37 | 2.95 ± 0.33 | 0.665 |
| IgM | 2.67 ± 0.24 | 2.48 ± 0.21 | 0.571 |
| IgN | 8.75 ± 0.49 | 7.83 ± 0.44 | 0.177 |
| CMI | 0.62 ± 0.07 | 0.77 ± 0.07 | 0.150 |
| L. Activity | 0.62 ± 0.01 | 0.65 ± 0.01 | 0.133 |
Abbreviations: CMI, cell-mediated immunity (mm); DFI, daily feed intake at 35 to 42 d (g); IgM, immunoglobulin M titers against SRBC (log 2); IgN, titer of immunoglobulin against NDV (log 2); IgT, total immunoglobulin against SRBC (log 2); IgY, immunoglobulin Y titers against SRBC (log 2); L. activity, activity of lysozyme enzyme (light absorption at 490 nm); L-DFI and H-DFI, the 20% of lower and higher DFI.
Means within the row followed by different letters are significantly different.
Table 7.
Comparing between higher and lower groups of RIG (L-RIG and RIG-H) on RIG, humoral, cell-mediated, and innate immunity in male broilers.
| Traits | L-RIG | H-RIG | P value |
|---|---|---|---|
| RIG | −32.51 ± 2.35b | 35.97 ± 2.43a | 0.000 |
| IgT | 5.84 ± 0.25a | 4.50 ± 0.26b | 0.001 |
| IgY | 3.28± 0.33a | 1.83 ± 0.32b | 0.004 |
| IgM | 2.56 ± 0.19 | 2.67 ± 0.19 | 0.701 |
| IgN | 8.88 ± 0.43 | 7.68 ± 0.45 | 0.065 |
| CMI | 0.59 ± 0.08 | 0.63 ± 0.08 | 0.698 |
| L. activity | 0.66 ± 0.01a | 0.63 ± 0.01b | 0.040 |
Abbreviations: CMI, cell-mediated immunity (mm); IgM, immunoglobulin M titers against SRBC (log 2); IgN, titer of immunoglobulin against NDV (log 2); IgT, total immunoglobulin against SRBC (log 2); IgY, immunoglobulin Y titers against SRBC (log 2); L. activity, activity of lysozyme enzyme (light absorption at 490 nm); L-RIG and H-RIG, the 20% of lower and higher RIG; RIG, residual intake and gain (unit).
Means within the row followed by different letters are significantly different.
Table 3.
Comparing between higher and lower groups of BWG (L-BWG and BWG -H) on BWG, humoral, cell-mediated, and innate immunity in male broilers.
| Traits | L-BWG | H-BWG | P value |
|---|---|---|---|
| BWG | 76.93b ± 2.27 | 129.61a ± 1.94 | 0.000 |
| IgT | 5.22 ± 0.42 | 5.08 ± 0.36 | 0.799 |
| IgY | 2.11± 0.37 | 2.40 ± 0.32 | 0.567 |
| IgM | 3.11 ± 0.32 | 2.68 ± 0.27 | 0.320 |
| IgN | 8.50 ± 0.67 | 7.33 ± 0.58 | 0.202 |
| CMI | 0.62 ± 0.09 | 0.78 ± 0.07 | 0.171 |
| L. Activity | 0.63 ± 0.02 | 0.66 ± 0.01 | 0.217 |
Abbreviations: BWG, bodyweight gain at 35 to 42 d (g); CMI, cell-mediated immunity (mm); IgM, immunoglobulin M titers against SRBC (log 2); IgN, titer of immunoglobulin against NDV (log 2); IgT, total immunoglobulin against SRBC (log 2); IgY, immunoglobulin Y titers against SRBC (log 2); L. activity, activity of lysozyme enzyme (light absorption at 490 nm); L-BWG and H-BWG, the 20% of lower and higher BWG.
Means within the row followed by different letters are significantly different.
While ingredients of FCR (DFI and BWG) was not significantly affected the immune system performance of broilers, the effect of FCR was significant only on the immune response of Newcastle vaccine (IgN) (Table 4) (P < 0.05). In fact, birds with a higher FCR (as an unfavorable character) also had a higher response rate to the vaccine. Adversely, the immune response against NDV will weakened due to selection of the L-FCR birds to improve economic efficiency of the flock. Regarding the response to SRBC, the numerical value of the responses was higher in H-FCR group than L-FCR group, although these differences were not statistically significant (P > 0.05). The higher immune response in birds with higher FCR was probably due to assigning the greater fraction of proteins for immunoglobulin production (Colditz, 2009; Herd, 2009). Among FE traits, FCR cannot appropriately show the balance between FE and immunity. However, including FCR in breeding programs had less negatively influence on immune system, especially of cell-mediated and innate performances.
Table 4.
Comparing between higher and lower groups of FCR (L-FCR and FCR -H) on FCR, humoral, cell-mediated, and innate immunity in male broilers.
| Traits | L-FCR | H-FCR | P value |
|---|---|---|---|
| FCR | 1.58 ± 0.01b | 2.14 ± 0.01a | 0.000 |
| IgT | 4.77 ± 0.33 | 5.02 ± 0.35 | 0.606 |
| IgY | 2.05± 0.28 | 2.00 ± 0.29 | 0.902 |
| IgM | 2.72 ± 0.23 | 3.02 ± 0.24 | 0.375 |
| IgN | 7.85 ± 0.42 | 9.00 ± 0.44 | 0.051 |
| CMI | 0.66 ± 0.07 | 0.64 ± 0.08 | 0.872 |
| L. Activity | 0.63 ± 0.01 | 0.62 ± 0.01 | 0.943 |
Abbreviations: CMI, cell-mediated immunity (mm); FCR, feed conversion ratio at 65 to 42 d; IgM, immunoglobulin M titers against SRBC (log 2); IgN, titer of immunoglobulin against NDV (log 2); IgT, total immunoglobulin against SRBC (log 2); IgY, immunoglobulin Y titers against SRBC (log 2); L. activity: activity of lysozyme enzyme (light absorption at 490 nm); L-FCR and H-FCR, the 20% of lower and higher FCR.
Means within the row followed by different letters are significantly different.
For RFI groups, the IgT and IgY titers in H-RFI group (which is not economically favorable) were significantly higher than in L-RFI group (Table 5) (P < 0.05). Other immune performances were not significantly different between the 2 L- and H-RFI groups (P > 0.05). It is clear from the results of Table 5 that birds with high FI (lower FE-birds) have a higher immune system performance. In fact, the protein received from feed, instead of being converted into fibrous protein (in meat and carcass), has led to the production of globular protein (including immunoglobulins). Therefore, amino acids resources originated from food positively influence on immune performance (Colditz, 2009), than BWG. Although decreasing RFI is the goal of breeding programs to improve FE, the results of the present study showed that reducing RFI leads to a reduction in SRBC-mediated humoral immunity. In our study only the response to the Newcastle vaccine was investigated, which was not significant between RFI groups. When the goal of a breeding program is to reduce RFI, other responses of the immune system to multiple vaccines used in broilers will be considered. Research has shown that chickens with high and low RFI are regulated differently in terms of nutrient digestion, protein synthesis, lipid metabolism, molecular transport of cellular molecules, nucleotide sugar biosynthesis, glycogen metabolism, lipid uptake and transport, and absorption pathways (Zhuo et al., 2015; Abasht et al., 2019; Liu et al., 2019). It is reported that 52 genes are associated with regulation of immune system process, humoral immunity, and complement activation which are differentially expressed in L-RFI and H-RFI chickens (Liu et al., 2019). Moreover, it is demonstrated that microRNAs are regulatory function to performance of immune system related to the RFI in different breeds of chicken (Luo et al., 2015).
Table 5.
Comparing between higher and lower groups of RFI (L-RFI and RFI-H) on RFI, humoral, cell-mediated, and innate immunity in male broilers.
| Traits | L-RFI | H-RFI | P value |
|---|---|---|---|
| RFI | −22.06 ± 1.99b | 20.70 ± 1.92a | 0.000 |
| IgT | 4.89 ± 0.28b | 5.97 ± 0.27a | 0.011 |
| IgY | 2.30 ± 0.30b | 3.45 ± 0.28a | 0.010 |
| IgM | 2.59 ± 0.19 | 2.52 ± 0.19 | 0.788 |
| IgN | 8.09 ± 0.48 | 8.20 ± 0.46 | 0.869 |
| CMI | 0.64 ± 0.08 | 0.62 ± 0.08 | 0.918 |
| Lysozyme activity | 0.64 ± 0.01 | 0.67 ± 0.01 | 0.147 |
Abbreviations: CMI, cell-mediated immunity (mm); FRI-L and H-RFI, the 20% of lower and higher RFI; IgM, immunoglobulin M titers against SRBC (log 2); IgN, titer of immunoglobulin against NDV (log 2); IgT, total immunoglobulin against SRBC (log 2); IgY, immunoglobulin Y titers against SRBC (log 2); L. activity, activity of lysozyme enzyme (light absorption at 490 nm); RFI, residual feed intake (unit).
Means within the row followed by different letters are significantly different.
Newcastle response is the only immune factor that is different between H- and L-RG groups (Table 6) (P < 0.05), which were similar to FCR (Table 4), though, while higher RG is desired, IgN in H-RG group is lower than L-RG group which is not preferable. In the case of RIG, immune system performances differences between groups were more obvious (Table 7). In L-RIG group, the values of IgT, IgY, IgN, and L. activity were higher than H-RIG group (P < 0.05). From FE's point of view, the goal is to increase RIG. However, as shown in Table 7, increase of RIG leads to the weakening of humoral and innate immunity. RIG represents both growth and RFI, which increases the former and decreases the latter. Therefore, it can be concluded that, in general, selection to increase growth efficiency and reduce feed consumption leads to weakening of the immune system. From a commercial point of view, approximately 70% of the costs of a poultry enterprise are related to feed consumption. Therefore, poultry researchers usually pay attention to the FE of birds (Aggrey et al., 2010), while probably the main purpose of their research is not directly related to the bird's nutrition (Van Eerden et al., 2004; Zerjal et al., 2021). Birds with higher body weight need to consume more feed, while the industry tries to increase the first trait (body weight), but increasing the second trait (feed consumption) is not commercially desirable. For this reason, among birds of the same age, geneticists and poultry breeders are looking for those that have reached a certain weight with less feed consumption. Results of the current study showed that focusing just on growth and FE may lead to serious decay in immune system performance. According to the resource allocation theory, while avian immune system responses are easily considered in the health category (Colditz, 2009), NFE may not be easily classified, because FI includes a set of biological processes and pathways, and interactions with the environment (Herd, 2009). Therefore, including FE in breeding programs may influence on other correlated traits, especially those traits that not included in the breeding program.
Table 6.
Comparing between higher and lower groups of RG (L-RG and RG -H) on RG, humoral, cell-mediated, and innate immunity in male broilers.
| Traits | L-RG | H-RG | P value |
|---|---|---|---|
| RG | −15.00 ± 1.03b | 17.70 ± 1.03a | 0.000 |
| IgT | 4.25 ± 0.30 | 4.68 ± 0.30 | 0.193 |
| IgY | 2.28± 0.27 | 2.02 ± 0.27 | 0.491 |
| IgM | 2.97 ± 0.22 | 2.67 ± 0.22 | 0.354 |
| IgN | 9.07 ± 0.42a | 7.82 ± 0.42b | 0.045 |
| CMI | 0.66 ± 0.08 | 0.68 ± 0.08 | 0.889 |
| Lysozyme activity | 0.63 ± 0.01 | 0.64 ± 0.01 | 0.703 |
Abbreviations: CMI, cell-mediated immunity (mm); IgM, immunoglobulin M titers against SRBC (log 2); IgN, titer of immunoglobulin against NDV (log 2); IgT, total immunoglobulin against SRBC (log 2); IgY, immunoglobulin Y titers against SRBC (log 2); L. activity, activity of lysozyme enzyme (light absorption at 490 nm); L-RG and H-RG, the 20% of lower and higher RG; RG, residual body weight gain (g).
Means within the row followed by different letters are significantly different.
Based on the RFI concept, any reduction in FI to achieve 1 unit of chicken growth performance can minimize feed costs and thereby maximize overall profitability for the poultry production system. On the other hand, bird selection for reduced RFI is associated with reduced FI sometimes with unfavorable loss of growth performance. Therefore, RIG may apparently looks better than RFI to improve both growth and FE. The distribution of energy between different functions of a bird is explained based on the theory of resource allocation. This state of balance can be disturbed through environmental instabilities or artificial selection (Siegel et al., 2009). Really, according to resource allocation theory, there is a trade-off between the categories of different traits of a bird, including maintenance, growth performance, reproduction, and health (Glazier, 2009; Siegel and Honaker, 2009). When 1 or more specific attributes are more important, it means that they are given the second priority for receiving energy, and if the received energy (here FI) is not enough or the energy above a certain limit is not received, the allocated energy given for other functions is restricted. This decrease in energy intake shows itself in the form of physiological malfunctions such as diseases, and reproductive problems. As a result, in the current study directing resources toward more growth while less input enters the system (lower FI to get FE), results in sacrificing immunity. This situation becomes harder when RIG included as FE criteria.
CONCLUSIONS
There are several FE-related traits (DFI, FCR, RFI, RG, or RIG) which may be included in the breeding programs. However, influence of these traits on immune system is unclear. None of the FE-related traits were effective on CMI of the birds. The measurements of DFI usually did not directly included in breeding programs and using FCR are controversial. Results of the present study showed that although RIG is a more appropriate indicator for FE, choosing for high RIG can weaken the performance of the both humoral and innate immune systems, while RFI had fewer adverse effects. Therefore, this study suggests RFI as a more suitable FE-related trait to be included in breeding programs, especially for flocks that the birds’ immunity have not been considered.
ACKNOWLEDGMENTS
The authors are grateful for financial assistance supported in part by the Iran National Science Foundation (project number 98012907).
DISCLOSURES
The authors have no conflicts of interest.
References
- Abasht B., Zhou N., Lee W.R., Zhuo Z., Peripolli E. The metabolic characteristics of susceptibility to wooden breast disease in chickens with high feed efficiency. Poult. Sci. 2019;98:3246–3256. doi: 10.3382/ps/pez183. [DOI] [PubMed] [Google Scholar]
- Aggrey S.E., Karnuah A.B., Sebastian B., Anthony N.B. Genetic properties of feed efficiency parameters in meat-type chickens. Gen. Select. Evol. 2010;42:1–5. doi: 10.1186/1297-9686-42-25. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barbato G.F. Genetic relationships between selection for growth and reproductive effectiveness. Poult. Sci. 1999;78:444–452. doi: 10.1093/ps/78.3.444. [DOI] [PubMed] [Google Scholar]
- Berry D.P., Crowley J.J. Residual intake and body weight gain: a new measure of efficiency in growing cattle. J. Anim. Sci. 2012;90:109–115. doi: 10.2527/jas.2011-4245. [DOI] [PubMed] [Google Scholar]
- Berry D.P., Crowley J.J. Cell biology symposium: genetics of feed efficiency in dairy and beef cattle. J. Anim. Sci. 2013;91:1594–1613. doi: 10.2527/jas.2012-5862. [DOI] [PubMed] [Google Scholar]
- Colditz I.G. Rauw W.M., Resource Allocation Theory Applied to Farm Animal Production. CAB International; Wallingford, UK: 2009. Allocation of resources to immune responses, Pages 192-209. [Google Scholar]
- Crowley J.J., McGee M., Kenny D.A., Crews D.H., Jr., Evans R.D., Berry D.P. Phenotypic and genetic parameters for different measures of feed efficiency in different breeds of Irish performance-tested beef bulls. J. Anim. Sci. 2010;88:885–894. doi: 10.2527/jas.2009-1852. [DOI] [PubMed] [Google Scholar]
- Cunningham, C. 1971. Page 177 in Virología práctica. Ed. Acribia, Zaragoza España.
- El Moujahid el M., Chen S., Jin S., Lu Y., Zhang D., Ji C., Yang N. Association of leptin receptor gene polymorphisms with growth and feed efficiency in meat-type chickens. Poult. Sci. 2014;93:1910–1915. doi: 10.3382/ps.2013-03674. [DOI] [PubMed] [Google Scholar]
- Emamgholi Begli H., Vaez Torshizi R., Masoudi A.A., Ehsani A., Jensen J. Genomic dissection and prediction of feed intake and residual feed intake traits using a longitudinal model in F2 chickens. Animal. 2018;12:1792–1798. doi: 10.1017/S1751731117003354. [DOI] [PubMed] [Google Scholar]
- Glazier D.S. In: Pages 22–43 in Resource Allocation Theory Applied to Farm Animal Production. Rauw W.M., editor. CAB International; Wallingford, UK: 2009. Resource allocation patterns. [Google Scholar]
- Herd R.M. In: Pages 109–189 in Resource Allocation Theory Applied to Farm Animal Production. Rauw W.M., editor. CAB International; Wallingford, UK: 2009. Residual feed intake. [Google Scholar]
- Jahan M., Maghsoudi A., Rokouei M., Faraji-Arough H. Prediction and optimization of slaughter weight in meat-type quails using artificial neural network modeling. Poult. Sci. 2020;99:1363–1368. doi: 10.1016/j.psj.2019.10.072. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li W., Zheng M., Zhao G., Wang J., Liu J., Wang S., Feng F., Liu D., Zhu D., Li Q., Guo L., Guo Y., Liu R., Wen J. Identification of QTL regions and candidate genes for growth and feed efficiency in broilers. Genet. Sel. Evol. 2021;53:13. doi: 10.1186/s12711-021-00608-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu R., Liu J., Zhao G., Li W., Zheng M., Wang J., Li Q., Cui H., Wen J. Relevance of the intestinal health-related pathways to broiler residual feed intake revealed by duodenal transcriptome profiling. Poult. Sci. 2019;98:1102–1110. doi: 10.3382/ps/pey506. [DOI] [PubMed] [Google Scholar]
- Luo C., Sun L., Ma J., Wang J., Qu H., Shu D. Association of single nucleotide polymorphisms in the microRNA miR-1596 locus with residual feed intake in chickens. Anim. Genet. 2015;46:265–271. doi: 10.1111/age.12284. [DOI] [PubMed] [Google Scholar]
- Ma H., Liang S., Wu H., Du C., Ren Z., Yang X., Yang X. Effects of in ovo feeding and dietary addition oils on growth performance and immune function of broiler chickens. Poult. Sci. 2022;101 doi: 10.1016/j.psj.2022.101815. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McGovern R.H., Feddes J.J.R., Robinson F.E., Hanson J.A. Growth performance, carcass characteristics, and the incidence of ascites in broilers in response to feed restriction and litter oiling. Poult. Sci. 1999;78:522–528. doi: 10.1093/ps/78.4.522. [DOI] [PubMed] [Google Scholar]
- Mebratie W., Madsen P., Hawken R., Rome H., Marois D., Henshall J., Bovenhuis H., Jensen J. Genetic parameters for body weight and different definitions of residual feed intake in broiler chickens. Genet. Sel. Evol. 2019;51:53. doi: 10.1186/s12711-019-0494-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mohammadi-Tighsiah A., Maghsoudi A., Bagherzadeh-Kasmani F., Rokouei M., Faraji-Arough H. Bayesian analysis of genetic parameters for early growth traits and humoral immune responses in Japanese quail. Livest. Sci. 2018;216:197–202. [Google Scholar]
- Narinc D., Karaman E., Aksoy T., Firat M.Z. Genetic parameter estimates of growth curve and reproduction traits in Japanese quail. Poult. Sci. 2014;93:24–30. doi: 10.3382/ps.2013-03508. [DOI] [PubMed] [Google Scholar]
- Pryce J.E., Gonzalez-Recio O., Nieuwhof G., Wales W.J., Coffey M.P., Hayes B.J., Goddard M.E. Hot topic: definition and implementation of a breeding value for feed efficiency in dairy cows. J. Dairy Sci. 2015;98:7340–7350. doi: 10.3168/jds.2015-9621. [DOI] [PubMed] [Google Scholar]
- Rekaya R., Sapp R.L., Wing T., Aggrey S.E. Genetic evaluation for growth, body composition, feed efficiency, and leg soundness. Poult. Sci. 2013;92:923–929. doi: 10.3382/ps.2012-02649. [DOI] [PubMed] [Google Scholar]
- Reyer H., Hawken R., Murani E., Ponsuksili S., Wimmers K. The genetics of feed conversion efficiency traits in a commercial broiler line. Sci. Rep. 2015;5:16387. doi: 10.1038/srep16387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sell-Kubiak E., Wimmers K., Reyer H., Szwaczkowski T. Genetic aspects of feed efficiency and reduction of environmental footprint in broilers: a review. J. Appl. Gen. 2017;58:487–498. doi: 10.1007/s13353-017-0392-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siegel P.B., Honaker C.F. Impact of genetic selection for growth and immunity on resource allocations. J. Appl. Poult. Res. 2009;18:125–130. [Google Scholar]
- Siegel P.B., Honaker C.F., Rauw W.M. In: Pages 230-242. Resource Allocation Theory Applied to Farm Animal Production. Rauw W.M., editor. CAB International; Wallingford, UK: 2009. Selection for high production in poultry. [Google Scholar]
- van der Most P.J., de Jong B., Parmentier H.K., Verhulst S. Trade-off between growth and immune function: a meta-analysis of selection experiments. Funct. Ecol. 2010;25:74–80. [Google Scholar]
- Van der Werf J. Is it useful to define residual feed intake as a trait in animal breeding programs? Aust. J. Exp. Agric. 2004;44:405–409. [Google Scholar]
- Van Eerden E., Van Den Brand H., Parmentier H.K., De Jong M.C., Kemp B. Phenotypic selection for residual feed intake and its effect on humoral immune responses in growing layer hens. Poult. Sci. 2004;83:1602–1609. doi: 10.1093/ps/83.9.1602. [DOI] [PubMed] [Google Scholar]
- Vaziri E., Maghsoudi A., Feizabadi M., Faraji-Arough H., Rokouei M. Scientometric evaluation of 100-year history of poultry science (1921-2020) Poult. Sci. 2022;101 doi: 10.1016/j.psj.2022.102134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willems O.W., Miller S.P., Wood B.J. Assessment of residual body weight gain and residual intake and body weight gain as feed efficiency traits in the turkey (Meleagris gallopavo) Genet. Sel. Evol. 2013;45:26. doi: 10.1186/1297-9686-45-26. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willems O.W., Miller S.P., Wood B.J. Aspects of selection for feed efficiency in meat producing poultry. World's Poult. Sci. J. 2019;69:77–88. [Google Scholar]
- Williams S.M., Price S.E., Siegel P.B. Heterosis of growth and reproductive traits in fowl. Poult. Sci. 2002;81:1109–1112. doi: 10.1093/ps/81.8.1109. [DOI] [PubMed] [Google Scholar]
- Yang L., Wang X., He T., Xiong F., Chen X., Chen X., Jin S., Geng Z. Association of residual feed intake with growth performance, carcass traits, meat quality, and blood variables in native chickens. J. Anim. Sci. 2020;98:1–11. doi: 10.1093/jas/skaa121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ye S., Chen Z., Zheng R., Diao S., Teng J., Yuan X., Zhang H., Chen Z., Zhang X., Li J., Zhang Z. New insights from imputed whole-genome sequence-based genome-wide association analysis and transcriptome analysis: the genetic mechanisms underlying residual feed intake in chickens. Front. Genet. 2020;11:243. doi: 10.3389/fgene.2020.00243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zerjal T., Hartle S., Gourichon D., Guillory V., Bruneau N., Laloe D., Pinard-van der Laan M.H., Trapp S., Bed'hom B., Quere P. Assessment of trade-offs between feed efficiency, growth-related traits, and immune activity in experimental lines of layer chickens. Genet. Sel. Evol. 2021;53:44. doi: 10.1186/s12711-021-00636-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhuo Z., Lamont S.J., Lee W.R., Abasht B. RNA-Seq analysis of abdominal fat reveals differences between modern commercial broiler chickens with high and low feed efficiencies. PLoS One. 2015;10 doi: 10.1371/journal.pone.0135810. [DOI] [PMC free article] [PubMed] [Google Scholar]
