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1 BREEDING AND GENETICS Associated Effects of the Roux Plumage Color Mutation on Growth, Carcass Traits, Egg Production, and Reproduction of Japanese Quail F. MINVIELLE,*,1 E. HIRIGOYEN, and M. BOULAY *Laboratoire de Génétique Factorielle, Institut National de la Recherche Agronomique, 78352, Jouy en Josas, France, Caillor, B.P. 42, 40120, Sarbazan, France, and Syndicat des Sélectionneurs Avicoles et Aquacoles Franc ais, Station de Recherches Avicoles, 37380, Nouzilly, France ABSTRACT After two generations of introgression of with 3% lower BW and 30% less abdominal fat (AF) pad. the sex-linked recessive roux color mutation into a commercial Egg production was not influenced by the roux mutation, broiler Japanese quail line with wild-type plum- but egg weight (EW) was 2% lower. Characteristics associ- age, growth, carcass, egg laying, and reproduction of ated with the roux gene are similar to those reported for birds were evaluated and compared for all types of birds the albino mutation, except for AF, which was not tested in albino quail. The similarity of the pleiotropic effects produced (considering sex, line, and plumage). Usual sex might result from some modification that the two mutations induce in an early step of a metabolic pathway differences were obtained for BW, with larger values in females and 5% sexual dimorphism. Weights were larger involved both in coloration and in growth. From a practical breeding standpoint, the roux gene appears to be a also in the pure commercial line, which had a higher hatching rate (HR) than the introgressed birds at 17 to 19 wk of age. Roux plumage was significantly associated interesting candidate gene for auto-sexing in quail production. (Key words: Japanese quail, auto-sexing, plumage color, performances) 1999 Poultry Science 78: INTRODUCTION Of all plumage color mutations described in the Japanese quail (Coturnix coturnix japonica), only two have been localized on the Z chromosome, the imperfect albinism allelic series and the brown mutation (Somes, 1988; Cheng and Kimura, 1990). Because homozygote males and hemizygote females for either one of the recessive albino and brown genes are easily distinguished from wild-type quail at birth, those mutations may be used for auto-sexing in a crossbreeding production system with colored and wild plumage lines. In the fowl, several mutations already have been used for that purpose (Smyth, 1990), but auto-sexing may be more critical for the economic production of Japanese quail, as 1-d vent sexing is very impractical in these birds. Moreover, raising each sex separately would eliminate problems associated with the early sexual maturity and mating behavior of quail. Indeed, an albino egg laying line has been recently developed in China (Liu et al., 1991). In our laboratory, we maintain in a similar genetic background the albino gene and a form of the brown Received for publication October 16, Accepted for publication June 18, To whom correspondence should be addressed: minvielle@dga2. jouy.inra.fr 2 Caillor, B.P.42, 40120, Sarbazan, France. mutation, the roux gene (Somes, 1988), which originated in our quail colony. Because the roux plumage does not seem to be associated with the vision-related problems developed by albino quail (Lauber, 1987; Dkhissi et al., 1996) nor with its high posthatch mortality (Mérat et al., 1981), the roux mutation could be a more likely candidate gene than the albino one for auto-sexing quail. A recessive sex-linked red plumage mutation, which might indeed belong also to the brown locus, is already being used for quail production in China (Liu and Liu, 1991). In France, the major quail breeding company has started to introgress the roux mutation in a meat quail selection line, line K. However, the previous work on the albino mutation in quail emphasizes the necessity of assessing the existence and the extent of correlated effects of the roux gene on growth and egg production concurrently with the introgression process; this was the objective of the present work. MATERIALS AND METHODS Lines and Mutation The recipient line is being developed from a parental broiler quail line from Caillor 2 (line K). Line K is pedi- Abbreviation Key: AF = abdominal fat; BPBW = bled and plucked body weight; DL = dissection loss; EN1 = total egg number of quail present during the 11-wk egg laying test; EN2 = total egg number of quail put in test; EW = egg weight; FW = weight of right pectoralis mucles; HR = hatching rate; LW = leg weight 1479
2 1480 MINVIELLE ET AL. TABLE 1. Introgression of the roux (r) gene in the K line of Japanese quail Breeders Progeny kept as Generation Male Female next generation breeding stock of introgression K line Genotype K line Genotype K line Sex Genotype (%) (%) (%) 1 0 rr m +r r f r r 87.5 m +r r m +r and ++ f r r and r none (determination of sire s genotype) r 93.8 r 93.8 m rr f r gree-selected for high BW, and it has wild-type plumage color. In 1997, before starting introgression of the roux gene, mean 4-wk BW of the K line was 243 and 253 g in males and females, respectively (Minvielle, 1998). The roux gene is one among several major gene mutations kept and studied in quail lines at the Génétique Factorielle experimental unit. Maintained by pool breeding of 15 males and 30 females, each line is homozygous for a single mutation with a visible effect on the phenotype. Introgression and Experimental Population Introgression was completed after six generations to obtain a new line fixed for the roux gene and retaining, on average, 93.8% of the line K genome (Table 1). In a parallel manner for line K, four generations were produced contemporaneously and used in Generations 1 to 4 of the introgression. All experimental birds studied in the present work were from the second generation of introgression and were 75% K. The birds were obtained from two consecutive hatches. Both plumage colors were obtained in females, and all males were wild-type. One hatch was used for growth and carcass evaluation, and the other was used for egg laying and reproduction studies. Contemporaneous K-line birds were used as controls. Trial 1: Growth and Carcass Evaluation All birds for the growth trial were hatched on February 24, They were reared in a single room under constant lighting for 7 d; then, lighting was decreased regularly to 13 h daylight at Day 16. The temperature was decreased gradually from 35 to 23 C at Day 25. Water was available at all times. Starter feed (282 g total protein and 3,025 kcal ME/kg) was provided for ad libitum consumption up to Day 16. Birds were then provided grower feed (213 g total protein and 2,750 kcal ME/kg). At 36 d of age, plumage color was recorded. After a 2-h feed withdrawal, BW was measured prior to slaughter. Finally, the carcasses were bled, plucked, and stored overnight at 4 C. The following day, bled and plucked BW (BPBW) was obtained, and gross dissection of the carcass was carried out. Abdominal fat (AF) pads were collected and weighed. The right pectoralis major and pectoralis minor were excised from the carcass. Their total weight was recorded as the fillet weight (FW). The right leg was separated from the body at the hip joint and was weighed (LW) after the shank and the foot were removed. For each bird, precision of the dissection work was evaluated by calculating the dissection losses (DL), which were the difference (grams) between BPBW and the sum of the weights of the dissected components, including the remainder of the carcass. The origin and numbers of birds analyzed are given in Table 2. Trial 2: Egg Laying and Reproduction All birds for the egg production trial were hatched on February 17, Up to the age of 35 d, they were raised similarly to the chicks produced for the growth trial. Then, females were weighed and transferred to individual cages of five-tier egg-laying batteries maintained in a single room (16 h light:8 h dark). Temperature was maintained at 21 C. Birds were provided ad libitum access to water and to an egg layer diet (180 g total protein and 2,570 kcal ME/kg, 3.4% calcium). Egg production was monitored for 11 wk between the ages of 8 and 19 wk. Egg weight (EW) of each bird was evaluated as the average weight of normal eggs obtained in a 5-d period around 11 wk of age. Finally, experimental reproduction of those quail between 17 and 19 wk of age that were still laying eggs was carried out with tester sires chosen at random from the K line. About 50 sires were used for each female genetic group. Each sire was rotated daily among three individual egg laying cages for natural mating. All eggs were then incubated for 17 d in the same incubator (37.5 C, 55% humidity, no candling) following the 2-wk egg collection. Number of incubated eggs and number of hatched chicks were recorded for each dam, but identity of sire was not kept. Numbers of observations for each test are in Table 2. Statistical Analysis First, overall comparison of the five (growth trial) or three (egg production) types of birds obtained by considering plumage, sex, and line was done by one-way analy-
3 ASSOCIATED EFFECTS OF ROUX PLUMAGE MUTATION IN JAPANESE QUAIL 1481 TABLE 2. Structure of the data sets Trial 1: Growth and dissection Trial 2: Egg production and reproduction Number of quail tested Number of Mortality in Number of Origin Plumage Sire Sire quail in egg egg laying quail on (K line genome) color Sex families For BW For other traits families laying test test reproduction test (%) 100 wild-type m f wild-type m f roux f sires had both male and female K-line progeny sires had both wild-type and roux introgressed female progeny sires had both wild-type and roux introgressed female progeny. sis of variance and Duncan s test. Next, analyses of variance, including a sire effect, were carried out separately in introgressed females and in the K line, as the sires origin was different in the two groups of quail (Tables 1 and 2). Then, to study the associated effects of the roux gene, traits measured for introgressed females (75% K line, with roux or wild-type plumage) were analyzed using several linear models. For Trial 1, 36-d BW and BPBW were studied in a two-way analysis of variance, with plumage color and sire as main effects. For all dissection traits, a covariance analysis was carried out with three main effects (color, sire, and dissector) and with BPBW as the covariable. For Trial 2, a two-way analysis of variance was used to study 27-d BW, and another covariance analysis was performed with plumage color and sire as main effects; 27-d BW was used as a covariable for egg numbers (EN1 = total egg number of quail present during the 11-wk egg laying test; EN2 = total egg number of quail put in test) and EW. The same analyses were performed on data from the K line, but the effect of plumage color was then replaced in the models by the effect of sex. Because the analysis of arsine-transformed hatching rates (HP) gave the same results as with untransformed proportions, it was omitted from the Results Section. A log-linear model analysis of mortality during the egglaying test was carried out to evaluate its relationship with the plumage color and the line. All analyses were performed with the GLM, CORR, and CATMOD procedures of SAS Institute (SAS, 1988). Trial 1 RESULTS Means and significance levels are given in Table 3. Overall comparisons of BW and BPBW in the five groups by the Duncan s test showed that the K line was heavier than the introgressed population. At the same time, males were lighter than females. Similar rankings were obtained for dissection traits FW and LW, whereas DL was similar in all groups. Results for AF were somewhat different; roux females appeared to be closer to K-line males than to the other female classes for this variable. Sexual dimorphism (the percentage difference between female and male BW) was about 6% for BW and 5% for BPBW in both the K-line and the introgressed population. In introgressed birds, the well-known effect of sex on BW aside, the only significant difference remaining between least squares means when the linear model included a sire effect was for AF in females: it was 0.9 g lower in the roux carcasses (P 0.10) on a equal BPBW basis. Analysis of K-line data indicated that only FW remained different, which was larger in females (P 0.05), when data were adjusted to equal BPBW. Trial 2 Means and significance levels are listed in Table 4. At 27 d of age, BW of the three groups were different (P 0.05), with the roux quail being, respectively, 6.5 and 31.6 g lighter than the other introgressed group and the K- line females. The difference between introgressed females was maintained (P 0.001) when the effect of the sire was taken into account. Both egg number traits had higher means (P 0.05) in roux-introgressed quail than in K- line birds, and roux females had higher EN2 than the introgressed group with wild-type plumage (P 0.05). However, no significant difference in egg production remained between the two classes of introgressed quail when a sire effect was included in the model. Egg weight of roux quail was 0.3 g lower (P 0.05). This difference was maintained when the two types of introgressed females were compared. More eggs were collected from introgressed females of both types (P 0.01). Hatching rate was higher (P 0.001) in the K line, but it was not different for the two introgressed groups. Maximum likelihood analysis of mortality data yielded nonsignificant 1 df chi-square values (0.16 and 1.02, respectively) for both the effects of plumage color and line. This result indicates that neither plumage color nor line was associated with differences in adult mortality. Because correlations were homogeneous among the three groups of females, Table 5 lists only overall correlations, which were all highly significant. The negative correlations between egg number and BW corresponded to the negative (P 0.05) linear regression of EN1 on BW (b =
4 1482 MINVIELLE ET AL. TABLE 3. Means, SEM, CV, and significance for BW and carcass dissection traits from introgressed quail with a roux or a wild-type plumage and from a commercial line K Type of quail Mean Introgressed Introgressed Line K All 1 Females 2 All 3 Line K 4 Females Males Males Females Variable SEM CV CV CV Roux Wild-type Wild-type Wild-type (g) BW *** 7.4*** d c e b a Carcass weight ** 7.7*** cd c d b a Abdominal fat b 3.3 a 2.8 ab 3.3 a Weight of breast muscles * 30.7 d 31.7 c 33.0 b 35.8 a Leg weight d 24.8 c 25.9 b 26.8 a Dissection losses a 0.8 a 0.8 a 0.8 a a e Means within variables with no common superscript are different (P 0.05). 1 Analysis of variance for all quail of the experiment without sire effect in the model 2 Analysis of variance (BW) or covariance (dissection traits) for introgressed females (effect of plumage color) with a sire effect included in the model. 3 Analysis of variance for introgressed quail (effect of sex) with a sire effect included in the model. 4 Analysis of variance (BW) or covariance (dissection traits) for K-line quail (effect of sex) with a sire effect included in the model. 5 Right Pectoralis major weight + right Pectoralis minor weight. *P **P ***P P ) obtained from the analyses of covariance. Similarly, the positive correlations of EW and BW corresponded to the significant (P 0.05) regression of EW on BW (b = 0.02). DISCUSSION After two generations of introgression, there were still 26- and 30-g BW differences at 36 d in males and females, respectively, between K-line and introgressed quail. These differences resulted from the genetic makeup of the sires that were either pure K-line or F1 birds (Table 1). On the other hand, in introgressed females, all sired by F1 males, BW was 3% lighter in roux quail at 27 and 36 d (Tables 3 and 4). In roux quail, carcass weight was decreased to the same extent as BW. When the effect of the sire was taken into account, the small BW difference remained significant at 27 d but not at 36 d, almost surely because of the volume and the structure of the data sets (Table 2). Indeed, Trial 2 introgressed females, on which BW was obtained at Day 27, originated from a large number of sires, and most of them (n = 77) had both roux and wild-type progeny. Only 12 sires had both types of progeny in Trial 1 for the measure of BW at Day 36. A similar but larger plumage color-associated effect on BW was reported previously for the albino locus in Japanese TABLE 4. Means, SEM, CV, and significance for egg production and reproduction traits from introgressed quail with a roux or a wild plumage and from a commercial line K Type of quail Mean All 1 Introgressed 2 Introgressed Line K Variable SEM CV Roux Wild-type Wild-type BW at 27 d, g ** c b a Egg number of hens present (EN1) a 44.9 ab 41.7 b Egg number of hens put in test (EN2) a 40.1 b 39.6 b Egg weight (EW), g * 14.6 b 14.9 a 15.1 a INC a 5.6 a 5.1 b HR b 0.45 b 0.61 a a c Means with no common superscript are different (P 0.05). 1 Analysis of variance for all quail of the experiment without sire effect in the model. 2 Analysis of variance (BW, INC, HR) or covariance (EN1, EN2, EW) for introgressed females (effect of plumage color) with a sire effect included in the model. 3 INC = Number of eggs incubated for the hatching test from a 2-wk egg collection. 4 HR = Number of eggs hatched/number of eggs incubated from 17- to 19-wk females. *P **P 0.01.
5 ASSOCIATED EFFECTS OF ROUX PLUMAGE MUTATION IN JAPANESE QUAIL 1483 TABLE 5. Correlations among egg number (EN1 1 or EN2 2 ), egg weight (EW), and 27-d BW in Japanese quail Traits N Correlation EN1, EW *** EN2, EW *** EN1, 27-d BW *** EN2, 27-d BW ** EW, 27-d BW *** EW, 27-d BW *** 1 Only hens present for all 11 wk of test. 2 All hens put in test. quail, with a 14-g difference (9%) between 33-d wild type and albino females (Mérat et al., 1981). The well-known difference of body size between females and males was also observed in this work. The 5 to 6% value for sexual dimorphism on BW before and after slaughter was analogous to the values calculated from previous reports on Japanese quail lines at 28 or 35 d, but with mean BW ranging from 46 to 150 g only (Maeda et al., 1982; Marks and Washburn, 1991; Okamoto et al., 1986, 1989). However, data from recent research on a 154-g BW quail line indicated that sexual dimorphism was as high as 12 to 15% in that line at Day 35 (Yalc in et al., 1995). It appears, then, that sexual dimorphism was similar and small in the K line and in the introgressed population. Dissection losses were quite variable, but they appear to have been similar across all groups, which validates results and analyses of carcass measurements. For all dissection traits except AF, FW, and DL, significant differences of raw means and ranking of the groups obtained from the overall analysis of variance corresponded well with the results for BW, thereby indicating that body proportions were similar in all groups. However, AF, estimated on an equal carcass weight basis under the full model including the effect of the sire, was marginally lighter in the roux females. We know of no other report on the associated effect of a plumage color mutation on adiposity in Japanese quail or in poultry. In line K, the fact that FW remained 1.1 g (3%) smaller in males than in females, on a equal carcass weight basis, underlines the existence of a sex difference in muscle content that was independent of body size. Sex differences in Japanese quail carcass traits have already been reported for unadjusted values of breast muscle weight, thigh muscles, LW, and AF (Caron et al., 1990; Yalcin et al., 1995). However, they disappeared in all cases except for thigh muscles (Caron et al., 1990) when data were adjusted to equal BW. Therefore, despite overall similarity, there might be some line-specific effect of sex on body composition of Japanese quail, possibly induced by selection. The egg laying performance was comparatively lower in the K line, a frequent characteristic of broiler lines. However, because variation of egg production was high, no difference among introgressed females remained in the subsequent analyses of EN1 or EN2. On the other hand, the roux locus was associated with slightly smaller egg size. These findings parallel those reported for the albino gene (Mérat et al., 1981) for egg production and EW. The usual positive association between EW and BW in poultry was found in the present work also. However, positive phenotypic correlations of EN and EW and negative correlations between EN and BW had higher values than those reported previously (Marks, 1990) in lines of Japanese quail with smaller body size. The roux mutation did not affect hatching performances, which were similar in both introgressed groups. However, the strong effect of the dam line (100% K or 75% K) on HR was surprising. It might indicate that the decline of reproduction performances with age is much larger in the line from which the roux mutation was imported than in the K line. Indeed, HR obtained after breeding with K-line sires around the peak of egg production was above 62% in both groups (F. Minvielle, unpublished data). There are two main hypotheses to explain why roux and albino genes, two plumage color mutations located on the same chromosome, are associated with similar effects on BW and EW. These color mutations might act as visible markers of weight traits QTL positioned near them on the Z chromosome. However, linkage between the two color loci is loose (r = 0.38 ± 0.01; F. Minvielle and S. Ito, unpublished data), although it it is possible that each color locus could be linked to the same QTL lying between them. On the other hand, the two color loci might have similar pleiotropic effects at the phenotypic level through some common modification induced by the product of the mutation in metabolic pathways involved both in coloration and growth-related traits. The latter hypothesis may be more plausible, but complementary work on adiposity in albino quail would be needed to confirm definitively the convergence of pleiotropic effects. Finally, from a practical breeding standpoint, this work has shown that the roux mutation is a good candidate to develop auto-sexing quail lines, as it appears to have similar effects on growth but better early survival than the albino gene, and some favorable action on adiposity. ACKNOWLEDGMENTS Bringing our three groups together was initiated by M. Reffay, and this project was made possible by J. M. Lespez. Excellent technical assistance was provided by Anne- Franc oise Ameline, G. Coquerelle, B. Desnoues, J. L. Monvoisin, F. Seigneurin, and the staff from Caillor. The final draft of this paper was prepared when the first author was at Kagoshima University with Y. Maeda under an Invitation Research Fellowship from the Japan Society for the Promotion of Science. REFERENCES Caron, N., F. Minvielle, M. Desmarais, and L. M. Poste, Mass selection for 45-day body weight in Japanese quail: Selection response, carcass composition, cooking properties, and sensory characteristics. Poultry Sci. 69: Cheng, K. M., and M. Kimura, Mutations and major variants in Japanese quail. Pages in: Poultry Breeding and Genetics. R. D. Crawford, ed. Elsevier, Amsterdam, The Netherlands.
6 1484 MINVIELLE ET AL. Dkhissi, O., E. Chanut, C. Versaux-Botteri, F. Minvielle, J. H. Trouvier, and J. Nguyen-Legras, Changes in retinal dopaminergic cells and dopamine rythmic metabolism during the development of a glaucoma-like disorder in quails. Invest. Ophthalmol. Vis. Sci. 37: Lauber, J. K., Review: Light induced avian glaucoma as an animal model for human primary glaucoma. J. Ocul. Pharmacol. 3: Liu, Y., and Y. Liu, Quail s autosexing strain. Page 100 in: Proceedings of the World Quail Conference. USSR National Branch of the WPSA, Tartu, Estonia. Liu, M., W. Shen, and Yang, Breeding for a line of recessive sex-linked white quails. Pages in: Proceedings of the World Quail Conference. USSR national branch of the WPSA, Tartu, Estonia. Maeda, Y., H. Kawasaki, and T. Hashiguchi, Genetic parameters of feed efficiency in the Japanese quail. Jpn. J. Zootech. Sci. 53: Marks, H., Genetics of egg production in other galliforms. Pages in: Poultry Breeding and Genetics. R. D. Crawford, ed., Elsevier, Amsterdam, The Netherlands. Marks, H. L., and K. W. Washburn, Body, abdominal fat, and testes weights, and line by sex interactions in Japanese quail divergently selected for plasma cholesterol response to adrenocorticotropin. Poultry Sci. 70: Mérat, P., A. Bordas, F. Jonon, and A. Perramon, Effets quantitatifs associés augène albinos lié au sexe chez la caille japonaise. Ann. Génét. Sél. Anim. 13: Minvielle, F., Genetics and breeding of Japanese quail for production around the world. Pages in: Proceedings of the 6th Asian Pacific Poultry Congress, Japan Branch of the WPSA, Nagoya, Japan. Okamoto, S., S. Kobayashi, and T. Matsuo, Live body weight and carcass characteristics of 6-week of age Japanese quail. Bull. Fac. Agric. Saga Univ. 60:9 16. Okamoto, S., S. Kobayashi, and T. Matsuo, Feed conversion to body weight gain and egg production in large and small Japanese quail lines selected for 6-week body weight. Jpn. Poult. Sci. 26: SAS Institute, SAS User s Guide: Statistics. SAS Institute Inc., Cary, NC. Smyth, J. R., Genetics of plumage, skin and eye pigmentation in chickens. Pages in: Poultry Breeding and Genetics. R. D. Crawford, ed. Elsevier, Amsterdam, The Netherlands. Somes, R. G., International Registry of Poultry Genetics Stocks. University of Connecticut, Storrs, CT. Yalc in, S., I. Oguz, and S. Otles, Carcase characteristics of quail (Coturnix coturnix japonica) slaughtered at different ages. Br. Poult. Sci. 36:
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