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GENETICS |



* Department of Animal Science, National Chung-Hsing University, 40227 Taichung, Taiwan;
Institut National de la Recherche Agronomique, UE 997 Génétique Factorielle Avicole, 37380 Nouzilly Cedex, France; and
Institut National de la Recherche Agronomique, AgroParisTech, UMR1236 Génétique et Diversité Animales, F-78350 Jouy-en-Josas, France
1 Corresponding author: cfchen{at}dragon.nchu.edu.tw
| ABSTRACT |
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Key Words: residual feed intake naked neck gene adaptation to subtropical environment
| INTRODUCTION |
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In this paper, we investigated the effect of introducing the NA gene in a genetic background that has been optimized for feed efficiency of laying hens at moderate temperature. Since 1976, from a Rhode Island Red population, 2 divergent lines have been selected for high (R+) or low (R–) residual feed consumption at moderate temperature, based on the difference between observed feed intake and the intake predicted by a multiple regression on body weight, body weight gain, and egg mass production (Bordas and Mérat, 1984b; Bordas et al., 1992). A significant improvement of feed efficiency was obtained in the R–line due to a reduction in feed intake while maintaining egg production to a constant level (Bordas et al., 1992) as also observed in other genetic backgrounds (Katle, 1991; Luiting, 1991). The main component modified by the divergent selection was found to be the diet-induced thermogenesis, with a 75% difference between R+ and R–cockerels in the 17th generation (Gabarrou et al., 1998) and a 90% difference in the 30th generation (Swennen et al., 2007). The decreased heat production of R– laying hens was associated with reduced surface of heat dissipation areas, such as comb, wattles, and shank (Bordas and Minvielle, 1999); a low variability of rectal temperature around a mean value of 40.5°C (Bordas and Minvielle, 1997); and a rather low surface temperature, which was decreased by 2°C as compared with the R+ line (Bordas et al., 1992). In addition, the R– hens exibited a lower activity as compared with R+ hens (Gabarrou et al., 2000). Thus, a combination of the NA gene with the R– background could be expected to be profitable at moderate temperatures (decreased heat loss due to the R– background) as well as high temperatures (increased heat loss due to the NA gene).
Because heat tolerance and feed intake are critical issues for egg production in subtropical environments, a scientific cooperation program was set up between France and Taiwan to compare the performance of chosen genotypes in both countries. In the present study, the comparison involved the 3 genotypes obtained for the NA gene within the R– background.
| MATERIALS AND METHODS |
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A divergent selection for residual feed intake was initiated at Institut National de la Recherche Agronomique (INRA) in 1976 within a Rhode Island Red population (Bordas and Mérat, 1984b). The selection criterion has been food consumption adjusted for body weight, egg mass, and body weight change by multiple linear regression (Bordas et al., 1992). In 1997, the naked neck gene was introduced into the low residual feed intake line, line R–: 2 male R– were mated with 8 females, homozygous for the NA*NA mutation, which were obtained from a line selected on improved clutch length (Chen and Tixier-Boichard, 2003a). All the F1 offspring were heterozygous for the NA*NA mutation. To continue the introgression of the NA gene in the R– background, 30 heterozygote females were backcrossed to 6 male R– in consecutive generations. In 2003, at the F6 generation of introgression, 8 males and 56 females heterozygous for the NA*NA mutation were used to generate all 3 genotypes (NA*N/NA*N, NA*NA/NA*N, NA*NA/NA*NA), in 2 hatches for rearing in Taiwan and France, respectively, at 3-wk intervals.
Husbandry
Taiwan. On November 28, 2003, the day-old pedigree chicks were imported to Taiwan. After 10 d of quarantine, they were transferred to the experimental farm of National Chung-Hsing University (latitude 24N09, longitude 120E41). All chicks were reared in floor pens with 12 birds/m2 of floor space up to 16 wk, and pullets were beak-trimmed at 2 wk of age. The vaccines involved Mareks disease, fowl pox, Newcastle disease, infectious bronchitis, infectious bursal disease, respiratory enteritic orphan, infectious laryngotracheitis, infectious coryza, avian encephalomyelitis, and egg drop syndrome. At 17 wk of age, the pullets were housed in individual cages in an open house. The light regimen in the growth period was natural daylight, whereas a fixed lighting regimen, 14L:10D, was applied from 17 wk of age to the end of the laying test. Water and food were supplied ad libitum. The temperature and relative humidity were recorded.
France. On December 15, 2003, the full-sib chicks were hatched and reared in the experimental farm of INRA, Tours (latitude 47N23, longitude 0E41). All chicks were reared in floor pens with a 12 birds/m2 of floor space up to 17 wk. They were not beak-trimmed. The vaccines involved Mareks disease, infectious bronchitis, Gumboro, Newcastle disease, and avian encephalomyelitis. At 17 wk of age, the pullets were housed in individual cages in a windowless house. The light regimens were fixed at 10L:14D and 14L:10D in growth and laying periods, respectively. Water and food were supplied ad libitum. The temperature was controlled and monitored continuously. Relative humidity was not controlled, and the range of variation was not recorded on a daily basis but was checked from time to time.
The composition of feed is listed in Table 1
, for both environments, and Table 2
shows the average ambient temperature during the laying period.
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Body weights were measured at 6, 10, and 18 wk. Egg production was recorded daily for each hen from the first egg to 47 wk of age. For each hen, the laying rate was obtained from the ratio of egg number (whatever the egg status) to the length of the laying period. A break between ovipositions of at least 1 d was taken as the end of a clutch, and average clutch length was calculated. Egg mass and feed intake were measured between 31 and 34 wk of age, and hens were weighed at the beginning and the end of the feed intake recording period to calculate their mean body weight. Residual feed consumption was estimated from the difference between observed feed intake and predicted feed intake, which was obtained by a multiple regression equation using 3 independent variables, mean body weight, body weight variation (
BW), and total egg mass between 31 and 34 wk of age. The value 0.5 was used as the power of mean body weight, because it was close to the value corresponding to minimal variance of deviations from regression (Leeson et al., 1973; Bordas and Mérat, 1981). The measurement of anatomical traits included wattle length and shank length in both countries at 34 wk of age. In addition, rectal temperature and comb temperature were measured in Taiwan at 34 wk of age. Egg composition traits were also determined in Taiwan on 4 eggs per hen, between 33 and 34 weeks of age. Two eggs were used to record Haugh units, and 2 other eggs were used to determine the percentage of each component (yolk, albumen, shell).
Statistical Analysis
A Box-Cox power transformation was used to normalize clutch length (Chen and Tixier-Boichard, 2003a). The parameter (t) was found to be –0.15 for the transformed value of average clutch length.
The goodness of fit of the mortality was tested by using the logarithm-likelihood ratio test and comparing the observed number of the statistic with a
2 test. Genotype, environment, and their interaction effect analysis were estimated for this analysis using the model, yijk = µ + Gi + Ej + Gi x Ej + eijk, where Gi = the genotype effect for the NA gene, i = 1 to 3; Ej = the environment effect, j = 1 to 2; and Gi x Ej = the genotype by environment interaction effect. All statistical analyses were conducted by using SAS software, and the least squares means were compared with a Student t-test according to the PDIFF option of the GLM program (SAS Institute, 2002).
| RESULTS |
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The numbers and mortality during the laying period for the 3 genotypes are given in Table 3
. The experiment included 157 hens in France and 221 hens in Taiwan. The number of hens carrying the homozygous NA*NA/NA*NA genotype was unfortunately much lower than the numbers for the other 2 genotypes, due to a lower hatch-ability rate of the homozygous mutant genotype. The difference of mortality between the 2 environments was highly significant, with a much higher mortality in Taiwan, close to 11% as compared with less than 1% in France. There was no occurrence of infectious disease. On July 1, a hot wind, the foehn, caused a rise in temperature up to 40.3°C during 7 h. On that day, mortalities were 2.5, 0, and 0% for NA*N/NA*N, NA*NA/NA*N, and NA*NA/NA*NA genotypes, respectively. In spite of the absence of a null mortality for the homozygous mutant genotype on the entire laying period, there was no significant effect of the genotype, whatever the environment.
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These results are given in Table 4
. The genotype and environment significantly affected the body weight, and a genotype x environment effect was found for body weight at 10 wk only. The body weights in Taiwan were always lower than those in France. The differences in body weight between genotypes were more important in France, where the homozygous naked neck hens had always a lower body weight. Differences for body weight between genotypes were much reduced in Taiwan, being significant only at 18 wk of age between both homozygotes. Wattle length was significantly affected by genotype in both countries, but shank length was not. There was no genotype x environment effect on these traits. Wattle length was shorter in normally feathered hens than in naked neck hens, either heterozygote or homozygote carrier of the mutation. The genotype also affected the comb and rectal temperatures recorded in Taiwan. The normally feathered hens exhibited higher values for both temperature measurements. There was a clear additive and negative effect of the NA*NA mutation on rectal temperature.
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The results are given in Table 5
. Most of the egg production traits were significantly affected by the environment, but there was no significant genotype x environment effect. The laying performance was significantly decreased in Taiwan. Age at first egg was delayed by about 3 wk for all genotypes. Laying rate was decreased by about 25% for all genotypes. Figure 1
shows the laying curves for the 3 genotypes at 2 environments from the age at first egg to 44 wk. The laying curve exhibited a marked peak of egg production in France, which was not observed in Taiwan. The effect of genotype was significant for clutch length and egg weight, with a better performance for the homozygous NA*NA/NA*NA hens. The differences between genotypes for egg weight were more important in Taiwan than in France, and the genotype x environment effect approached the significance (P < 0.10).
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Feed Efficiency and Related Variables
The feed intake predicted function was as follows, with an R2 value of 0.63:
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The results are given in Table 5
. There were no significant genotype x environment effects on variables related to feed intake and production traits. Average body weight, egg mass, and feed intake were significantly lower in Taiwan than in France, but there was no effect of the environment on body weight change and on feed efficiency. Average body weight, feed intake, and residual feed intake were significantly affected by genotype, with higher values of feed intake and residual feed intake and lower values of body weight for homozygous naked neck hens.
The residual feed intake obtained from the difference between observed and predicted feed intake values differed markedly between genotypes, with positive values in hens carrying the naked neck gene. The NA*NA mutation had an additive effect, because the value for the heterozygote genotype was intermediate between the values of each homozygote. The differences between genotypes were larger in Taiwan than in France, and the genotype x environment interaction was close to significance (P < 0.10). Feed efficiency, as measured by the ratio of feed intake over egg mass, was quite variable, and differences between environments or between genotypes were not significant, but better values tended to be obtained for homozygous naked neck hens, whatever the environment.
| DISCUSSION |
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The Effect of Environment
The effect of environment was very important. All traits exhibited inferior values in Taiwan. No particular disease traits were observed, but the mortality was quite high. It seems that the genotypes did not adapt well to this new environment, which differed very much from the environment used for the selection procedure of the parental line.
In Taiwan, the hens were reared in open house with natural ambient temperature and were supplied with ground water. The average daily maximal and minimal temperatures were 32.8 and 18.9°C, respectively (April to September; 22 to 47 wk of age), whereas the corresponding values were 26.6 and 19.4°C in France. Relative humidity ranged from 63 to 80% in Taiwan and from 50 to 70% in France. Thus, the ambient conditions in Taiwan were typical of a subtropical environment, with a much higher maximal temperature and a higher maximal relative humidity than in France but similar minimal values in both countries. Minimal temperature values were rather low in Taiwan at the beginning of the laying period (18.9°C), which may explain the delayed onset of lay of the naked neck hens, which are not well adapted to moderately low temperatures. By the age of 34 wk (i.e., after the peak of the laying curve), rectal temperature was much higher in Taiwan (42.2°C for normally feathered hens) than what is generally observed in France (40.5°C for the R– line). In these conditions, the decrease in laying rate, as compared with the same genotypes in France, reached about 25%, which is as severe as the decrease observed with a constant temperature of 32°C (Chen et al., 2004). Environmental factors other than temperature need to be considered in the comparison between the performance obtained in France or in Taiwan, particularly lighting regimen and the diet.
Growth rate was lower in Taiwan than in France. Because growth took place in winter, the effect of a high temperature is unlikely. Furthermore, the average body weight was rather low, which should have limited the impact of heat. The mean metabolizable energy and the mean percentage of proteins of the diet were rather similar between countries, but the diet composition was very different in terms of raw materials, with a much higher percentage of corn and the presence of fishmeal in Taiwan. The lower body weight reached at 18 wk of age by hens in Taiwan may have contributed to a delayed sexual maturity.
Differences in lighting regimen may also explain why the age at first egg was delayed by 3 wk and no marked peak of egg production could be observed in Taiwan. Natural day length exhibits less variation in Taiwan than in France. Chicks were reared in an open house from December to April, so that day length was longer at the end of the rearing period in Taiwan (close to 12 h) than in France (controlled to 10 h). Thus, the lighting stimulus when the hens were transferred into single cages was stronger in France than in Taiwan, which is likely to produce a sharper peak of egg production. Lighting plays a very important role in bird growth, development, and maturity. A constant or decreasing amount of daily light will delay sexual maturity in growing birds (Lewis, 2006).
The Effect of Naked Neck Genotype in the R– Background
In the absence of interaction, the effects of the NA mutation on egg production in Taiwan appeared to be similar to the effects described in temperate conditions within the same genetic background. Homozygosity for the naked neck gene was associated with a lower body weight. This effect of genotype on body weight was already observed in the growth period (Monnet et. al., 1979) and in the laying period (Mérat, 1986; Chen and Tixier-Boichard, 2003b) under normal ambient temperature. In spite of a lower body weight, naked neck hens had a larger egg weight and higher values for Haugh units, which is consistent with previous data (Mérat, 1986; Chen et al., 2002). The naked neck gene had a positive effect on clutch length, as previously observed (Chen and Tixier-Boichard, 2003b), but this did not result in a significantly higher laying rate. The overall laying performance was rather low, but it should be recalled here that the R– has been selected on residual feed intake at a constant production level; thus, the egg production level represents the performance of the base population established in 1976 for this line.
Regarding adaptability, wattle length was increased by the naked neck gene in the R– line, both in heterozygous and homozygous genotypes, allowing for increased heat dissipation, as previously observed by Chen et al. (2004) and Bordas et al. (1980). On the contrary, the R– line is known to exhibit a low ability of heat dissipation (Gabarrou et al., 1997, 1998; Swennen et al., 2007). In the R– line background, naked neck hens exhibited better adaptability than normally feathered hens, as shown by their body temperature. A lower body temperature of naked neck hens was observed, and the same result was reported by Chen et al. (2004), and Monnet et al. (1980) in other genetic backgrounds. The increased heat dissipation of naked neck is explained by the reduction in feather coverage in homozygous chickens. The improved heat tolerance due to the naked neck mutation may explain why the mortality of homozygous naked neck hens was null in Taiwan, in spite of the acute heat stress that lasted 1 d, but the effect of the genotype did not reach the significance level.
Regarding feed efficiency, homozygous naked neck hens exhibited the highest food intake and the highest residual food intake in both environments. Yet, the feed efficiency ratio did not differ between genotypes and tended to be better, actually, in the homozygous naked neck hens. Thus, it may be suggested that the R– background limited the increase in feed intake of naked neck hens at moderate temperature, in France, where the increase represented 10% of the intake of the normally feathered hens. At a high temperature, in Taiwan, the low feed intake of the normally feathered R– line combined with the depressive effect of heat on feed intake resulted in a marked decrease in feed intake (–24%), and the total feed intake may not be sufficient to cover the protein requirements of the layers.
Indeed, the R– line, without the naked neck gene, was found to be more affected by heat stress than the high intake, R+, line (Bordas and Minvielle, 1997). This low adaptability to high temperatures may contribute to the poor performance of the R– line in Taiwan. The presence of the naked neck gene increased feed intake of R– hens in Taiwan by 22%. Thus, introducing the NA mutation in a genetic background selected for low residual feed intake appeared to be favorable in Taiwan as well as in France, as shown by the higher egg mass in homozygous carriers of the mutation.
In conclusion, the effect of introducing the naked neck gene in the R– line did improve some traits related to heat adaptation, particularly body temperature, but this did not result in better laying performance in the conditions of a subtropical environment. Clearly, other environmental factors, such as lighting regimen, also influenced greatly the laying performance. In the temperate conditions, the combination of the naked neck gene with the R– line appeared to be favorable, with a favorable trend observed on feed efficiency.
| ACKNOWLEDGMENTS |
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Received for publication January 1, 2008. Accepted for publication March 11, 2008.
| REFERENCES |
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Bordas, A., and P. Mérat. 1984a. Effects of the naked-neck gene on traits associated with egg laying in dwarf stock at two temperatures. Br. Poult. Sci. 25:195–207.[Web of Science][Medline]
Bordas, A., and P. Mérat. 1984b. Correlated responses in a selection experiment on residual feed intake of adult Rhode Island Red cock and hens. Ann. Agric. Fenn. 23:233–237.
Bordas, A., and P. Mérat. 1992. Egg production performances of hens of the NaNa (homozygous naked neck), Nana (heterozygote) and nana (normal plumage) genotype from a brown-egg dwarf (dw) line submitted to high constant temperature or to high temperature with periodic fluctuation. Arch. Geflugelkd. 56:22–27.
Bordas, A., P. Mérat, D. Sergent, and F. H. Ricard. 1978. Influence of the Na (naked neck) gene on growth, feed consumption and body composition of chicken according to environmental temperature. Ann. Genet. Sel. Anim. 10:209–231.[Web of Science]
Bordas, A., and F. Minvielle. 1997. Effects of temperature on egg laying hens from divergent lines selected on residual feed consumption. Genet. Sel. Evol. 29:279–290.[CrossRef][Web of Science]
Bordas, A., and F. Minvielle. 1999. Patterns of growth and feed intake in divergent lines of laying domestic fowl selected for residual feed consumption. Poult. Sci. 78:317–323.
Bordas, A., L. E. Monnet, and P. Mérat. 1980. Naked neck gene, laying performance and food efficiency according to temperature in the fowl. Ann. Genet. Sel. Anim. 12:343–361.[Web of Science]
Bordas, A., M. Tixier-Boichard, and P. Mérat. 1992. Direct and correlated responses to divergent selection for residual food intake in Rhode Island Red laying hens. Br. Poult. Sci. 33:741–754.[CrossRef][Web of Science][Medline]
Cahaner, A., D. Nader, and M. Gutman. 1993. Effects of plumage reducing naked neck (Na) gene on the performance of fast growing broilers at normal and high ambient temperatures. Poult. Sci. 72:767–775.[Web of Science]
Chen, C. F., A. Bordas, D. Gourichon, and M. Tixier-Boichard. 2004. Effect of high ambient temperature and naked neck genotype on performance of dwarf brown-egg layers selected for improved clutch length. Br. Poult. Sci. 45:346–354.[CrossRef][Web of Science][Medline]
Chen, C. F., A. Bordas, and M. Tixier-Boichard. 2002. Effect of high ambient temperature and naked neck genotype on egg production in purebred and crossbred dwarf brown-egg layers selected for improved clutch length. CD-ROM communication no. 18–08 in Proc. 7th World Congr. Genet. Appl. Livest. Prod., Montpellier, France.
Chen, C. F., and M. Tixier-Boichard. 2003a. Estimation of genetic variability and selection response for clutch length in dwarf brown-egg layers carrying or not the naked neck gene. Genet. Sel. Evol. 35:219–238.[CrossRef][Web of Science][Medline]
Chen, C. F., and M. Tixier-Boichard. 2003b. Correlated response to long-term selection for clutch length in dwarf brown-egg layers carrying or not the naked neck gene. Poult. Sci. 83:709–720.
Deaton, J. W., F. N. Reece, and B. D. Lott. 1984. Effect of differing temperature cycles on broiler performance. Poult. Sci. 63:612–615.[Web of Science][Medline]
Deeb, N., and A. Cahaner. 2001. Genotype-by-environment interaction with broiler genotypes differing in growth rate. 1. The effects of high ambient temperature and naked-neck genotype on lings differing in genetic background. Poult. Sci. 80:695–702.
Gabarrou, J. F., P. A. Geraert, N. François, S. Guillaumin, M. Picard, and A. Bordas. 1998. Energy balance of laying hens selected on residual food consumption. Br. Poult. Sci. 39:79–89.[CrossRef][Web of Science][Medline]
Gabarrou, J. F., P. A. Geraert, M. Picard, and A. Bordas. 1997. Diet-induced thermogenesis in cockerels is modulated by genetic selection for high or low residual feed intake. J. Nutr. 127:2371–2376.
Gabarrou, J. F., P. A. Geraert, J. Williams, L. Ruffier, and N. Rideau. 2000. Glucose-insulin relations and thyroid status of cockerels selected for high or low residual food consumption. Br. J. Nutr. 83:645–651.[Web of Science][Medline]
Katle, J. 1991. Selection for efficiency of feed utilisation in laying hens: Causal factors for variation in residual food consumption. Br. Poult. Sci. 32:955–969.[CrossRef][Web of Science]
Leeson, S., D. Lewis, and D. H. Shrimpton. 1973. Multiple linear regression equations for the prediction of food intake of laying fowl. Br. Poult. Sci. 14:595–608.[CrossRef][Web of Science][Medline]
Lewis, P. D. 2006. A review of lighting for broiler breeders. Br. Poult. Sci. 47:393–404.[CrossRef][Web of Science][Medline]
Luiting, P. 1991. Metabolic differences between White Leghorns selected for high and low residual feed consumption. Br. Poult. Sci. 32:763–782.[CrossRef][Web of Science][Medline]
Mérat, P. 1986. Potential usefulness of the Na (naked neck) gene in poultry production. Worlds Poult. Sci. J. 42:124–142.[CrossRef][Web of Science]
Monnet, L. E., A. Bordas, and P. Mérat. 1979. Naked neck gene and growth performance of chicks according to ambient temperature. Ann. Genet. Sel. Anim. 11:397–412.[Web of Science]
Monnet, L. E., A. Bordas, and P. Mérat. 1980. Naked neck gene, body weight and anatomical and physiological traits of pullets and adult hens according to ambient temperature. Ann. Genet. Sel. Anim. 6:17–28.
SAS Institute. 2002. The SAS System for Windows. Release 9.1. SAS Inst. Inc., Cary, NC.
Swennen, Q., P. J. Verhulst, A. Collin, A. Bordas, K. Verbeke, G. Vansant, E. Decuypere, and J. Buyse. 2007. Further investigations on the role of diet-induced thermogenesis in the regulation of feed intake in chickens: Comparison of adult cockerels of lines selected for high or low residual feed intake. Poult. Sci. 86:1960–1971.
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