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The Relationship Between Plumage Color Phenotypes and the Presence of Black Melanin in the Abdomen of Broiler Chickens: Study 1
The Relationship Between Plumage Color Phenotypes and the Presence of Black Melanin in the Abdomen of Broiler Chickens: Study 1
(Received for publication January 14, 1959)
T
HE relationship between plumage color and pattern and the deposition of melanin in the skin of the shanks has been recognized for many years. A good example of such a relationship is the black shank color of the Jersey Black Giant in contrast to the yellow shank color of the Barred Plymouth Rock. The plumage color genotype of the two varieties is often the same except that genes for barring are present in the Barred Rocks in place of the genes for non-barring in the Jersey Black Giants. The barring genes present in the Barred Rock have the power to inhibit the deposition of melanin in the epidermal layer of the shank skin. The relationship of plumage color to the deposition of black melanin in the abdomen of chickens was reported by Jaap (1958). The specific location of this deposition was on the exterior muscles of the abdomen in the vicinity of the umbilicus. Jaap found that both sex and plumage genotype bore a relationship to the occurrence of melanin in this area. It was more prevalent in females. The homozygous condition of dominant white, II, had the most prominent inhibiting effect on its deposition. When the heterozygous condition of dominant white existed in the birds the presence of the genes for extended black, E, Barring, B, and Silver, S, had the next greatest inhibitive effect. In contrast to the effect of dominant white, Jaap found that the homozygous condition of recessive white appears to
promote the deposition of melanin in the abdomen. The study to be reported here arose from the trouble experienced by a producer of small roaster chickens in 1956. These birds carried the Delaware pattern and were of the genotypes eeBBSS and eeB-S-. The eviscerated chickens showed a high incidence of melanin deposits in the abdomen. These deposits often have a putrefactive appearance and the buyers of the chickens are misled into thinking decomposition is taking place. The character occurred more often in the females than the males. A considerable incidence of green shanks occurred and this character also was more prevalent in the females than in the males. This led to the consideration that the deposition of melanin in the abdomen could be associated with the sex-linked gene id. The original matings were arranged for the purpose of developing two lines of birds, one for presence of abdominal melanin and one for absence of abdominal melanin. The choice of the birds for the two lines was based on the presence or absence of the character in the parents when slaughtered. For the most part the breeds involved were the Barred Rock, Columbian Rock, White Rock and White Cornish. They were mated in many combinations and a population of many different color genotypes was produced. The plumage color and shank color phenotypes of this population were recorded.
878
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
C. M. HUNTSMAN, F. N. JEROME AND E. S. SNYDER Poultry Department, Ontario Agricultural College, Guelph, Ontario, Canada
PLUMAGE COLOR AND ABDOMINAL BLACK TABLE 1.—Prevalence and degree of abdominal melanin deposition in relation to the sexes
Sex
No. of birds
Degree of pigmentation and percentages None
Males Females
581
Trace
54.1 24.1
19.5 19.3
TABLE 3.—Prevalence and degree of abdominal melanin deposition in relation to plumage color phenotype (Experiment 1)
Sex
No. of
None
Trace
Distinct
EB
Males Females
298 179
70.5 44.1
19.8 35.8
9.7 20.1
Eb
Males Females
41 112
22.0 3.6
2.4 7.1
75.6 89.3
eB
Males Females
154 65
33.8 0.0
17.5 1.5
48.7 98.5
eb
Males Females
46 53
73.9 9.4
17.4 9.4
8.7 81.2
TABLE 2.—Prevalence and degree of abdominal melanin deposition in relation to shank color Degree of pigmentation and percentages
Shank color
Sex
No. of birds -
None
Trace
Distinct
Yellow shanks
Males Females
565 247
61.9 34.0
20.2 23.9
17.9 42.1
Green shanks
Males Females
104 241
14.4 14.5
17.3 19.1
68.3 66.4
Black shanks
Males Females
19 73
42.1 6.2
10.5 13.8
47.4 80.0
some shank colors are associated with specific plumage color genotypes. Therefore, one may be concerned here with certain genes which exert a number of pleiotropic effects. Finally the data from these chickens in this experiment which exhibited colored phenotypes were assembled. The phenotypes classified were extended black, barred (EB); extended black, non-barred (Eb); restricted black, barred (eB); and restricted black, non-barred (eb). These data are presented in Table 3, and demonstrate the extreme interactions which occur between certain plumage color genotypes and sex. For example the deposition of melanin associated with the eb phenotype depends a great deal on the sex of the chicken. On the other hand the deposition associated with the EB and Eb phenotypes is not nearly so dependent on sex. Further discussion will be reserved until the data in Table 4 have been presented. Since the data presented in Tables 1, 2 and 3 arose from a number of matings, it was decided to gather another set of data from more critical matings. These matings were more critical in the sense that all parent stock were derived from a single strain of Columbian Rocks and a single strain of Barred Rocks. The two strains were mated reciprocally. Then
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
The birds were slaughtered at broiler age and the degree of melanin present in the abdomen was recorded. It was obvious at once that there was no definite association between the presence or absence of melanin in the parents and the presence or absence of the character in the offspring. In Table 1 the data on the prevalence and degree of melanin deposition in the sexes are presented. This includes all the chickens in the population. The data in Table 1 show that a considerably higher incidence of melanin pigment was present in the abdomens of the female chicks. In Table 2 the data on melanin deposition within different shank color classifications are presented. Twenty females were of uncertain classification and their data are not included in Table 2. An examination of the data presented in Table 2 shows that yellow-shanked males are relatively free of melanin deposition in the abdomen. Black-shanked females carry a high incidence of the character. Both green-shanked males and females carry a high incidence of the defect. However, it should be remembered that
Degree of pigmentation and percentages
Pheno-
Distinct 26.4 56.6
879
880
C. M . H U N T S M A N , F . N . J E R O M E AND E. S. SNYDER
TABLE 4.—Prevalence and degree of abdominal melanin deposition in relation to plumage color phenotype (Experiment Z) Degree of pigmentation a n d percentages
N o . of birds
None
Trace
Distinct
Males Females
61 49
95.1 61.2
4.9 26.5
0.0 12.3
Males Females
31 37
29.0 0.0
0.0 2.7
71.0 97.3
Males Females
23 14
73.9 0.0
4.4 0.0
21.7 100.0
Males Females
13 16
100.0 31.3
0.0 25.0
0.0 43.7
unrelated crossbred birds from each reciprocal cross were mated. The genotypes of the breeding birds in the final crosses are shown below. Mating 1 EeBb d'cr'XEeB- 9 9 Mating 2 EeBb d'cfXEeb- 9 9 The classification of data taken from the progenies of these crosses was made according to color phenotype, sex and deposition of melanin. Therefore the arrangement of d a t a coincides with that occurring in Table 3. T h e data obtained are presented in Table 4. I n general the d a t a in Table 4 confirm the interpretations made from the data of Table 3. Considering both sexes the E B phenotypes are the most free of pigment deposition in the abdomen. Sex does not influence the incidence of this deposition as greatly in the E B and E b phenotypes as in the eB and eb phenotypes. Barring in the presence of extended black tends to decrease the deposition of melanin in the abdomen while barring in the presence of restricted black tends to increase it. Since practically no green-shanked birds were present in the birds which furnished the d a t a listed in Table 4 it seems logical to assume t h a t gene id is independent of the genes responsible for abdominal melanin. An association between
Mating 1
EEbb & X EEB- 9 high prevalence low prevalence
Offspring
EEBb rj1 X EEb- 9 low prevalence high prevalence
Mating 2
EEBB o" X EEb- 9 low prevalence high prevalence
Offspring
EEBb
I n the above reciprocal crosses the character is behaving in a sex-linked fashion. However, we will examine the behaviour of barring and non-barring in combination with restricted black in the matings listed below. Mating 3
eebb cf low prevalence
X
eeB- 9 high prevalence
Offspring
eeBb c? X eeb- 9 medium prevalence high prevalence
Mating 4
eeBB cf X eeb- 9 medium prevalence high prevalence
Offspring
eeBb cf X eeB- 9 medium prevalence high prevalence
I n the reciprocal crosses illustrated in matings 3 and 4 the character behaves in a sex-limited fashion. Regardless of the fact t h a t in certain matings melanin deposition in the abdomen behaves in a sex-linked manner there still remains in those matings a sex-limited effect. For example in the offspring of Mating 2 where both sexes carry the E B phenotype and therefore carry a relatively
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
Sex
the two seemed feasible a t the s t a r t of the investigation. Because of the differential effect of barring and non-barring, depending on whether they are associated with extended black or restricted black, the character will behave a t times in a sex-linked fashion and at other times in a sex-limited manner. If one forms a hypothesis based on the d a t a of Tables 3 and 4 the results of certain crosses can be illustrated as follows.
PLUMAGE COLOR AND ABDOMINAL BLACK
1. A differential effect depending on whether the male or female sex hormone is more active in a certain chicken. 2. Some sex-linked genes which exist universally in the duplex condition in males and the simplex condition in females have an additive suppression effect on black melanin deposition. One of the most likely loci of such genes would be the gold and silver locus on the sex chromosomes. For example, either the SS, Ss or ss genotype would suppress the deposition of black melanin to a greater degree than either the S- or s- genotype. CONCLUSIONS
1. This study substantiates the conclusion of Jaap that the EB phenotype tends to suppress the deposition of abdominal melanin. It also substantiates his finding that abdominal melanin occurs more frequently in females than males. 2. Yellow-shanked males are relatively free of abdominal pigment regardless of the plumage color phenotype. In females yellow-shanked birds with the EB plum-
age color phenotype are relatively free of the character. However, yellow-shanked females of the eB and eb color phenotypes carry a high incidence of abdominal pigment. Birds of both sexes with green legs carry a high incidence. Oddly, blackshanked males are freer of the character than green-shanked males. Since Certain shank colors are the result of certain combination of plumage genes it seems most likely that a number of the associations between shank color and incidence of abdominal pigment are caused by certain combinations of plumage color genes. 3. One set of data indicate that no association exists between the presence of the gene id and the deposition of melanin in the abdomen. 4. A high interaction exists between sex and the eB phenotype and also between sex and the eb phenotype as judged by the incidence of abdominal pigment present. The interaction between sex and either the EB or Eb phenotypes is greatly reduced. 5. Based on the data presented, hypothetical crosses are arranged to show that in some crosses abdominal melanin will exhibit sex-linked inheritance while in other crosses it will behave in a sex-limited fashion. 6. The data show that while certain crosses accentuate the sex-limited behavior of the character a certain degree of this behavior is present in all the crosses. 7. Two hypotheses are suggested as an explanation for this sex-limited behavior. REFERENCES Jaap, R. G., 1958. Black abdomen—a pleiotropic effect of plumage color genes in broiler chickens. Poultry Sci. 37: 112-116. MacArthur, J. W., and J. J. Macllraith, 1946. Color sexing of day-old Brown Leghorns. Poultry Sci. 25: 180-183.
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
low incidence of the character, the females still carry it more frequently than the males. Those investigators who have worked with the wild type striping as it occurs in Brown Leghorns and Silver Dorkings have noticed a parallel situation in the behaviour of that character. The females usually carry a higher degree of black melanin in the dark-striped areas than the males. In fact, MacArthur and Macllraith (1946) used this differential in shade of striping to sex Brown Leghorn chicks with a high degree of accuracy. There would seem to be two possible explanations of such a sex-limited effect.
881
(Received for publication January 14, 1959)
T
HE relationship between plumage color and pattern and the deposition of melanin in the skin of the shanks has been recognized for many years. A good example of such a relationship is the black shank color of the Jersey Black Giant in contrast to the yellow shank color of the Barred Plymouth Rock. The plumage color genotype of the two varieties is often the same except that genes for barring are present in the Barred Rocks in place of the genes for non-barring in the Jersey Black Giants. The barring genes present in the Barred Rock have the power to inhibit the deposition of melanin in the epidermal layer of the shank skin. The relationship of plumage color to the deposition of black melanin in the abdomen of chickens was reported by Jaap (1958). The specific location of this deposition was on the exterior muscles of the abdomen in the vicinity of the umbilicus. Jaap found that both sex and plumage genotype bore a relationship to the occurrence of melanin in this area. It was more prevalent in females. The homozygous condition of dominant white, II, had the most prominent inhibiting effect on its deposition. When the heterozygous condition of dominant white existed in the birds the presence of the genes for extended black, E, Barring, B, and Silver, S, had the next greatest inhibitive effect. In contrast to the effect of dominant white, Jaap found that the homozygous condition of recessive white appears to
promote the deposition of melanin in the abdomen. The study to be reported here arose from the trouble experienced by a producer of small roaster chickens in 1956. These birds carried the Delaware pattern and were of the genotypes eeBBSS and eeB-S-. The eviscerated chickens showed a high incidence of melanin deposits in the abdomen. These deposits often have a putrefactive appearance and the buyers of the chickens are misled into thinking decomposition is taking place. The character occurred more often in the females than the males. A considerable incidence of green shanks occurred and this character also was more prevalent in the females than in the males. This led to the consideration that the deposition of melanin in the abdomen could be associated with the sex-linked gene id. The original matings were arranged for the purpose of developing two lines of birds, one for presence of abdominal melanin and one for absence of abdominal melanin. The choice of the birds for the two lines was based on the presence or absence of the character in the parents when slaughtered. For the most part the breeds involved were the Barred Rock, Columbian Rock, White Rock and White Cornish. They were mated in many combinations and a population of many different color genotypes was produced. The plumage color and shank color phenotypes of this population were recorded.
878
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
C. M. HUNTSMAN, F. N. JEROME AND E. S. SNYDER Poultry Department, Ontario Agricultural College, Guelph, Ontario, Canada
PLUMAGE COLOR AND ABDOMINAL BLACK TABLE 1.—Prevalence and degree of abdominal melanin deposition in relation to the sexes
Sex
No. of birds
Degree of pigmentation and percentages None
Males Females
581
Trace
54.1 24.1
19.5 19.3
TABLE 3.—Prevalence and degree of abdominal melanin deposition in relation to plumage color phenotype (Experiment 1)
Sex
No. of
None
Trace
Distinct
EB
Males Females
298 179
70.5 44.1
19.8 35.8
9.7 20.1
Eb
Males Females
41 112
22.0 3.6
2.4 7.1
75.6 89.3
eB
Males Females
154 65
33.8 0.0
17.5 1.5
48.7 98.5
eb
Males Females
46 53
73.9 9.4
17.4 9.4
8.7 81.2
TABLE 2.—Prevalence and degree of abdominal melanin deposition in relation to shank color Degree of pigmentation and percentages
Shank color
Sex
No. of birds -
None
Trace
Distinct
Yellow shanks
Males Females
565 247
61.9 34.0
20.2 23.9
17.9 42.1
Green shanks
Males Females
104 241
14.4 14.5
17.3 19.1
68.3 66.4
Black shanks
Males Females
19 73
42.1 6.2
10.5 13.8
47.4 80.0
some shank colors are associated with specific plumage color genotypes. Therefore, one may be concerned here with certain genes which exert a number of pleiotropic effects. Finally the data from these chickens in this experiment which exhibited colored phenotypes were assembled. The phenotypes classified were extended black, barred (EB); extended black, non-barred (Eb); restricted black, barred (eB); and restricted black, non-barred (eb). These data are presented in Table 3, and demonstrate the extreme interactions which occur between certain plumage color genotypes and sex. For example the deposition of melanin associated with the eb phenotype depends a great deal on the sex of the chicken. On the other hand the deposition associated with the EB and Eb phenotypes is not nearly so dependent on sex. Further discussion will be reserved until the data in Table 4 have been presented. Since the data presented in Tables 1, 2 and 3 arose from a number of matings, it was decided to gather another set of data from more critical matings. These matings were more critical in the sense that all parent stock were derived from a single strain of Columbian Rocks and a single strain of Barred Rocks. The two strains were mated reciprocally. Then
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
The birds were slaughtered at broiler age and the degree of melanin present in the abdomen was recorded. It was obvious at once that there was no definite association between the presence or absence of melanin in the parents and the presence or absence of the character in the offspring. In Table 1 the data on the prevalence and degree of melanin deposition in the sexes are presented. This includes all the chickens in the population. The data in Table 1 show that a considerably higher incidence of melanin pigment was present in the abdomens of the female chicks. In Table 2 the data on melanin deposition within different shank color classifications are presented. Twenty females were of uncertain classification and their data are not included in Table 2. An examination of the data presented in Table 2 shows that yellow-shanked males are relatively free of melanin deposition in the abdomen. Black-shanked females carry a high incidence of the character. Both green-shanked males and females carry a high incidence of the defect. However, it should be remembered that
Degree of pigmentation and percentages
Pheno-
Distinct 26.4 56.6
879
880
C. M . H U N T S M A N , F . N . J E R O M E AND E. S. SNYDER
TABLE 4.—Prevalence and degree of abdominal melanin deposition in relation to plumage color phenotype (Experiment Z) Degree of pigmentation a n d percentages
N o . of birds
None
Trace
Distinct
Males Females
61 49
95.1 61.2
4.9 26.5
0.0 12.3
Males Females
31 37
29.0 0.0
0.0 2.7
71.0 97.3
Males Females
23 14
73.9 0.0
4.4 0.0
21.7 100.0
Males Females
13 16
100.0 31.3
0.0 25.0
0.0 43.7
unrelated crossbred birds from each reciprocal cross were mated. The genotypes of the breeding birds in the final crosses are shown below. Mating 1 EeBb d'cr'XEeB- 9 9 Mating 2 EeBb d'cfXEeb- 9 9 The classification of data taken from the progenies of these crosses was made according to color phenotype, sex and deposition of melanin. Therefore the arrangement of d a t a coincides with that occurring in Table 3. T h e data obtained are presented in Table 4. I n general the d a t a in Table 4 confirm the interpretations made from the data of Table 3. Considering both sexes the E B phenotypes are the most free of pigment deposition in the abdomen. Sex does not influence the incidence of this deposition as greatly in the E B and E b phenotypes as in the eB and eb phenotypes. Barring in the presence of extended black tends to decrease the deposition of melanin in the abdomen while barring in the presence of restricted black tends to increase it. Since practically no green-shanked birds were present in the birds which furnished the d a t a listed in Table 4 it seems logical to assume t h a t gene id is independent of the genes responsible for abdominal melanin. An association between
Mating 1
EEbb & X EEB- 9 high prevalence low prevalence
Offspring
EEBb rj1 X EEb- 9 low prevalence high prevalence
Mating 2
EEBB o" X EEb- 9 low prevalence high prevalence
Offspring
EEBb
I n the above reciprocal crosses the character is behaving in a sex-linked fashion. However, we will examine the behaviour of barring and non-barring in combination with restricted black in the matings listed below. Mating 3
eebb cf low prevalence
X
eeB- 9 high prevalence
Offspring
eeBb c? X eeb- 9 medium prevalence high prevalence
Mating 4
eeBB cf X eeb- 9 medium prevalence high prevalence
Offspring
eeBb cf X eeB- 9 medium prevalence high prevalence
I n the reciprocal crosses illustrated in matings 3 and 4 the character behaves in a sex-limited fashion. Regardless of the fact t h a t in certain matings melanin deposition in the abdomen behaves in a sex-linked manner there still remains in those matings a sex-limited effect. For example in the offspring of Mating 2 where both sexes carry the E B phenotype and therefore carry a relatively
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
Sex
the two seemed feasible a t the s t a r t of the investigation. Because of the differential effect of barring and non-barring, depending on whether they are associated with extended black or restricted black, the character will behave a t times in a sex-linked fashion and at other times in a sex-limited manner. If one forms a hypothesis based on the d a t a of Tables 3 and 4 the results of certain crosses can be illustrated as follows.
PLUMAGE COLOR AND ABDOMINAL BLACK
1. A differential effect depending on whether the male or female sex hormone is more active in a certain chicken. 2. Some sex-linked genes which exist universally in the duplex condition in males and the simplex condition in females have an additive suppression effect on black melanin deposition. One of the most likely loci of such genes would be the gold and silver locus on the sex chromosomes. For example, either the SS, Ss or ss genotype would suppress the deposition of black melanin to a greater degree than either the S- or s- genotype. CONCLUSIONS
1. This study substantiates the conclusion of Jaap that the EB phenotype tends to suppress the deposition of abdominal melanin. It also substantiates his finding that abdominal melanin occurs more frequently in females than males. 2. Yellow-shanked males are relatively free of abdominal pigment regardless of the plumage color phenotype. In females yellow-shanked birds with the EB plum-
age color phenotype are relatively free of the character. However, yellow-shanked females of the eB and eb color phenotypes carry a high incidence of abdominal pigment. Birds of both sexes with green legs carry a high incidence. Oddly, blackshanked males are freer of the character than green-shanked males. Since Certain shank colors are the result of certain combination of plumage genes it seems most likely that a number of the associations between shank color and incidence of abdominal pigment are caused by certain combinations of plumage color genes. 3. One set of data indicate that no association exists between the presence of the gene id and the deposition of melanin in the abdomen. 4. A high interaction exists between sex and the eB phenotype and also between sex and the eb phenotype as judged by the incidence of abdominal pigment present. The interaction between sex and either the EB or Eb phenotypes is greatly reduced. 5. Based on the data presented, hypothetical crosses are arranged to show that in some crosses abdominal melanin will exhibit sex-linked inheritance while in other crosses it will behave in a sex-limited fashion. 6. The data show that while certain crosses accentuate the sex-limited behavior of the character a certain degree of this behavior is present in all the crosses. 7. Two hypotheses are suggested as an explanation for this sex-limited behavior. REFERENCES Jaap, R. G., 1958. Black abdomen—a pleiotropic effect of plumage color genes in broiler chickens. Poultry Sci. 37: 112-116. MacArthur, J. W., and J. J. Macllraith, 1946. Color sexing of day-old Brown Leghorns. Poultry Sci. 25: 180-183.
Downloaded from http://ps.oxfordjournals.org/ at Kokusai Hoken Keikakugaku (UNIV OF TOKYO) on May 15, 2015
low incidence of the character, the females still carry it more frequently than the males. Those investigators who have worked with the wild type striping as it occurs in Brown Leghorns and Silver Dorkings have noticed a parallel situation in the behaviour of that character. The females usually carry a higher degree of black melanin in the dark-striped areas than the males. In fact, MacArthur and Macllraith (1946) used this differential in shade of striping to sex Brown Leghorn chicks with a high degree of accuracy. There would seem to be two possible explanations of such a sex-limited effect.
881