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Influence of Heterosis and Maternal Effects on Viability in an Inter-Strain Cross of White Leghorns
POULTRY S C I E N C E November, 1 9 5 3 , Vol. 32, N o . 6
Influence of Heterosis and Maternal Effects on Viability in an Inter-Strain Cross of White Leghorns • FEED MOULTRIE, D. F. KING AND G. J. COTTIER Agricultural Experiment Station of the Alabama Polytechnic Institute, Auburn, Alabama (Received for publication February 18, 1953)
D
URING the three-year period, 19461948 inclusive, 14 strains of Single Comb White Leghorns were obtained from prominent Leghorn breeders and brought to the Alabama Agricultural Experiment Station Poultry Farm for comparative performance tests with a resistant strain of White Leghorns that was developed at this station (Sturkie, 1943; King and Cottier, 1948; Moultrie et al., 1953). Following the 1948 test, one of the introduced strains that was superior in egg production and other economic traits and about average in livability at this station was chosen for crossing with the resistant strain for the purpose of studying the performance of Fi inter-strain hybrids produced from noninbred stock. The results obtained from crossing these two strains for three consecutive years provide evidence that both heterosis and maternal effects play roles in determining viability of the inter-strain hybrids. Presentation of this evidence is the object of this report. MATERIALS AND METHODS
Strain A, or the Auburn Strain White Leghorn, was developed at the Alabama Agricultural Experiment Station. This
strain has been selected for viability since 1935 and has shown a general decrease in adult mortality of unculled pullets from 89 percent in 1935 to 17 percent in 1951. Selection in Strain A, according to the objective outlined in 1935, was primarily for resistance to fowl paralysis, since at that time paralysis accounted for a large part of the adult mortality. Later, when the mortality from paralysis was reduced considerably, the objective was expanded to include resistance to other diseases and disorders. Foundation stock for Strain A came from 11 different White Leghorn breeders of which seven were represented in the original (1935) matings; the other four strains were introduced by 1941 after which time breeding of this strain has been on a closed-flock basis. Although some close inbreeding was practiced in the early development of this strain, the mating of closely related individuals has been avoided since 1944, and the strain is not considered as an inbred line. Inbreeding coefficients for the flock produced in 1950, based on five generations of ancestors, ranged from zero to .1328 with an average of .0413. Strain D was obtained in 1948 from one of the outstanding White Leghorn breed-
935
936
F. MOULTRIE, D. F. KING AND G. J. COTTIER
ers in the United States. This strain has ranked high in many official egglaying contests during the last several years. Although excellent egg producers, pullets of Strain D, for four consecutive years (1948-1951), died during the laying period at a rate significantly higher than pullets of Strain A. Strain D also has been selected for viability since it has been at the Alabama Station and has shown an annual reduction in adult mortality of unculled pullets, having dropped from 56 percent in 1948 to 30 percent in 1951. No inbreeding has been practiced with Strain D since 1948, and the original breeder's statements concerning inbreeding lead one to believe that inbreeding was avoided prior to that time. In 1948 one case of hatching eggs purchased from the Strain-D breeder was incubated in the same machine with an equal number of eggs from Strain A. From this hatch 92 Strain-D females and 113 Strain-A females were reared and housed together until 520 days of age. The Strain-A females were obtained in approximate equal numbers from 16 Strain-A sires being used in that year, and they were considered as a random sample of Strain A. In 1949 pure Strain-A chicks and pure Strain-D chicks were sired by 12 and 8 males of the two strains, respectively, and inter-strain hybrids were sired by 4 StrainD sires each of which was mated to approximately 15 Strain-A dams. In 1950 pure Strain-A chicks and pure Strain-D chicks were sired by 10 and 8 males of the two strains, respectively. Inter-strain hybrid chicks from reciprocal crosses of the two strains were produced from 11 diallel matings in which 6 of the Strain-A sires and 5 of the StrainD sires were mated concurrently with dams of both strains. Thus, each male sired both pure-strain and hybrid progeny.
In 1951, chicks of Strains A and D were sired by 11 and 4 males of the two strains, respectively, and inter-strain hybrid chicks were produced from 4 Strain-D sires mated with Strain-A dams, as was the case in 1949. Unfortunately, reciprocal crosses were made only in 1950. In all the years covered in this report except 1948, the pure-strain and interstrain hybrid chicks were hatched over a 10-week hatching period, which was from the middle of January until the first of April. Each year the purebreds and inter-strain hybrids were housed together from one day of age until the end of their laying year, which was at 520 days of age. Natural exposure, particularly to leucosis, which at this station is quite severe (Sturkie, 1943; King and Cottier, 1948; King et al., 1952), was provided by brooding the chicks within 100 feet of adult stock until 8 weeks of age. Pullets were placed in the laying house at 155 days of age, and no culling was practiced at any time during the course of this study. It has been shown in previous reports (King and Cottier, 1948; Moultrie et al., 1953) that in general, introduced strains suffer about a 50 percent adult mortality when subjected to the severe exposure of this station, as was the case with Strain D in 1948. Strain-A females had adult mortality rates of 16, 14, and 17 percent in 1949, 1950, and 1951, respectively. During the same years, the adult mortality rates of Strain-D females were 33, 31, and 30 percent, respectively. Therefore, both strains could be considered relatively resistant. However, for the purpose of this study, Strain A was considered as the resistant and Strain D as the susceptible strain; this seems justified as there has been a significant difference in the adult mortality rates of the two strains for the period of study (1948-1951).
937
HETEROSIS AND MATERNAL EFFECTS ON VIABILITY TABLE 1.—Mortality of females from 1 through 15.' days of age Hybrid
Pure Year
Strain A
Strain D
Chicks No.
Mortality %
Chicks No.
Mortality %
1948 1949 1950 1951
113 1,217 718 992
28.3 16.1 24.9 11.6
92 176 333 287
47.8* 27.8* . 23.7"; 13.9
Total & av. 1949-51
2,927
16.7
796
21.1*
Ac?XD9
DcfXAQ
Chicks No.
Mortality
155
39.4
441 130 368
14.lt 16.9ft 8.7t
155
39.4
939
12.4ft
%
Chicks No.
Mortality
%
* Compared with Strain A, significantly higher at 1% level, t Compared with reciprocal cross, significantly lower at 1% level. t The difference between these values and the mid-point between the two parent strians is statistically significant to at least the 5% level.
The significant differences mentioned throughout this report were based on probabilities obtained from calculated values of chi-square (Snedecor, 1946). RESULTS
Growing Mortality. All mortality of female chicks from 1 through 155 days of age, or from hatching to housing as mature pullets, was considered as growing mortality. A summary of this mortality for the pure strains and for inter-strain hybrids is presented in Table 1. In comparing growing mortality of the pure strains, it is shown that Strain-D chicks died at a rate significantly higher than Strain A in 1948, 1949, and in the pooled results for 1949-1951 (the P value for each comparison = < . 0 1 ) . There was little difference in mortality rates of the two strains in 1950, and although the difference was not statistically significant in 1951, the mortality rate of Strain D was 2.3 percent higher than that of Strain A. In comparing growing mortality of the D X A inter-strain hybrid chicks with mortality of the chicks of the parent strains, it is evident that the hybrid chicks from this type mating died at a
rate significantly lower (to at least the 5 percent level) than the average of the mortalities of the parent strains. This difference was evident in all years of the study. If livability significantly higher than the mid-point between the parent strains is an indication of heterosis, then heterosis obviously affected viability during the growing period when the chicks were produced by mating StrainD sires with Strain-A dams. This picture becomes somewhat complicated, however, when the A X D interstrain hybrids are considered. The chicks from this type mating in 1950 had significantly higher (P<.01) growing mortality than did the chicks of the reciprocal cross of the same year. If one considers the general picture in which Strain D is thought of as susceptible and Strain A as resistant; then, there is an indication of maternal effects when comparing the reciprocal crosses of 1950. There was no indication of heterosis affecting viability in the A X D inter-strain hybrids, but it is conceivable that heterosis was involved but masked by maternal effects. Adult Mortality. All mortality of females from 156 days of age at which time pullets were housed until 520 days of
938
F. MOULTRIE, D. F. KING AND G. J. COTTIER TABLE 2.—Mortality of females from 156 through 520 days of age Pure Strain A
Year
1948 1949 1950 1951 Total & av. 1949-51
Hybrid Strain D
AcfXDP
DcfXAQ
Pullets No.
Mort. %
Pullets No.
Mort. %
Pullets. No.
Mort. %
Pullets No.
Mort. %
73 950 548 799
27.4 16.4 14.0 17.4
39 121 238 239
56.4* 32.7* 31.1* 29.7*
94
29.8
373 112 328
16.9J 17.8f 16.5t
2,297
16.2
598
30.8*
94
29.8
813
16.9ft
* Compared with Strain A, significantly higher at 1% level, t Compared with reciprocal cross, significantly lower to at least the 5% level. j The difference between these values and the mid-point between the two parent strains is statistically significant at 1% level.
age, at which time the laying year was completed, was considered as adult mortality. This mortality for the pure strains and inter-strain hybrids is summarized in Table 2. Although the general trends in adult mortality were essentially the same as during the growing period, the results in some respects were more consistent. It is shown in Table 2 that in every year of the study birds of Strain D died at a significantly higher rate than those of Strain A (P < .01). The D X A inter-strain hybrid pullets of 1949, 1951, and in pooled pullets for 1949-1951, inclusive, died at a rate significantly lower (P values<.01) than the mid-point between the two parent strains. Although the difference in 1950 was not significant, the difference of 4.8 percent between the DXA inter-strain hybrids' mortality (17.8 percent) and the mid-point between the parent strains (22.6 percent) was in the same direction as in the other years of the study. As can be noted, a smaller number of birds was housed that year than in the other years of the study; therefore, a relatively greater percentage difference would be necessary for statistical significance. These results, therefore, suggest that heterosis
affected livability of the inter-strain hybrid pullets produced by Strain-D sires and Strain-A dams. Again results were altogether different when the A X D inter-strain hybrids of 1950 were considered. Adult mortality of these pullets was significantly higher (P<.05) than mortality of pullets from the reciprocal (DXA) cross of the same year. Thus, in reciprocal crosses of these two strains, there is evidence of maternal influence on viability during both the growing and laying periods. It should be noted in Table 2 that in no instance did mortality of the inter-strain hybrids differ sifinificantly from mortality of the female line used to produce the hybrids. In both Table 1 and Table 2, the number of birds considered, with exception of the 1948 flock, included all individuals of the particular strain or inter-strain hybrids that were produced each year. Since reciprocal crosses using diallel matings were made only in 1950, all of the offspring from each sire and each dam of the flocks other than that in 1950 were either pure or hybrid. In 1950, however, 11 sires, 6 of Strain A and 5 of Strain D, were mated concurrently with dams of both strains; thus, each of these males
HETEROSIS AND MATERNAL EFFECTS ON VIABILITY
939
TABLE 3.—Adult mortality of female of spring from reciprocal diallel crosses of 1950
sired both pure and hybrid progeny. The results of these matings are given in Table 3. The chicks considered in Table 3 are exactly the same for the inter-strain hybrids, for both types of matings, as shown for 1950 in Table 2; however, the total number of purebreds involved is materially reduced as all pullets were eliminated in this comparison except those sired by the males used in reciprocal diallel matings. As previously pointed out, the reciprocal crosses differed significantly in mortality. It also is shown in Table 3 that in both crosses the inter-strain hybrids differed significantly from their half sisters sired by the same males. It is again evident in Table 3 that the Fi inter-strain hybrids differed little from the female line used in their production.
' Male Strain A N 1281 P 1184 P 620 P 1076 P 1227 P 1064
Pure
Hybrid
Pullets Mortality Pullets Mortality No. % No. % 57 71 54 56 31 23
Total & av. Strain D P 2287 P 2728 P 1047 P 2264 0 2750 Total & av.
Difference
%
37.5 12.9 13.0
15 11 11 9 28 20
20.0 18.2 18.2 66.7 25.0 40.0
+0.7 + 1.3 +10.8 +29.2 +12.1 +27.0
292
18.8
94
29.8*
+11.0
26 42 52 44 31
26.9 26.2 40.4 29.5 12.9
36 42 8 10 16
16.7 21.4 12.5 10.0 18.8
-10.2 -4.8 -27.9 -19.5 +5.9
195
28.7
112
17.9f
-10.8
19.3 16.9 7.4
* Compared with pure strain from same sires, significantly higher at 5% level. t Compared with pure strain from same sires, significantly lower at 5% level.
pullets housed, whereas, only 3.8 percent of the birds of Strain A died from leucosis. The difference of 13.4 percent mortality of pullets housed is statistically significant (P<.01). Losses from leucosis among inter-strain hybrids, based on percentage of pullets housed, were within the parental mortality range. However, in birds from both types of matings (AXD and DXA), the mortality was nearer the female line.
Adult mortality of pure strains and inter-strain hybrids of the 1950 flock according to the most important causes of death is summarized in Table 4. It is evident that most of the difference in mortality of the two pure strains was due to the greater death loss from leucosis in Strain D. Mortality from this disease in Strain D was 17.2 percent of
TABLE 4.—Percentage of adult mortality due to each cause among pure strains and Fi inter-strain hybrids {1950) Hybrid
Pure Strain A
Strain D
Ac?XD9
DcfXAQ
Cause of death %of %of total pullets mortality housed Leucosis Reproductive disorders Respiratory diseases Nephritis Hepatitis Internal hemorrhage Visceral gout Miscellaneous Total
%of %of %of %of %of %of total pullets total pullets total pullets mortality housed mortality housed mortality housed
27.3 26.0 6.5 6.5 3.9 3.9 10.4 15.1
3.8 3.6 0.9 0.9 0.5 0.5 1.5 2.3
55.4 16.2 12.2 4.1 1.4 1.4 4.1 5.5
99.6
14.0
100.3
17.2* 5.0 3.8 1.3 0.4 0.4 1.3 1.7 31.1
* Compared with Strain A, significantly higher at 1% level.
42.9 17.9 17.9 7.1
12.8 5.3 5.3 2.1
50.0 20.0 10.0 5.0
—
—•
—•
—•
—
2.1
—
10.0
1.8
100.0
29.8
100.0
17.8
7.1 7.1
2.1
5.0
8.9 3.6T 1.8 0.9
—•
0.9
—
•
940
F. MOULTRIE, D. F. KING AND G. J. COTTIER
This suggests an influence of maternal effects upon resistance to leucosis. It should be noted, however, that the D X A inter-strain hybrids, again based on percentage of pullets housed, showed less mortality from each of the causes than did the A X D inter-strain hybrids, which suggests that the hybrids from the Strain-A dams possessed general viability greater than the hybrids from the reciprocal cross. DISCUSSION
The results presented in this report show that the crossing of males from a relatively susceptible strain with females from a resistant strain produced hybrids that consistently showed evidence of an effect of heterosis on viability during both the growing and laying periods. However, relatively higher mortality of birds from the reciprocal of the above cross suggests that maternal effects may be involved. Since the parent strains differed significantly in viability, livability of the D X A inter-strain hybrids excelling the mid-point between the two parent strains that has been interpreted as evidence of heterosis could have been due to maternal influence. Ghostley and Nordskog (1951) found evidence of heterosis influencing viability in strain crosses in heavy breeds; however, Hutt and Cole (1952) crossed two slightly inbred strains of White Leghorns that differed little in viability and found that the resulting hybrids consistently excelled both parent strains in hatchability, early maturity, egg production, size of eggs, and size of birds, but no consistent evidence was found to indicate that heterosis increased viability in the nybrids. Maternal effect, if operative, would not have been detected in the crosses made by Hutt and Cole as the parent strains did not differ in viabil-
ity; however, in a previous report in which lines relatively resistant and susceptible to leucosis were crossed, no evidence of maternal effects was found (Hutt and Cole, 1947). Taylor et al. (1943) reached a similar conclusion after making reciprocal crosses between strains resistant and susceptible to leucosis. In studying the heritability of resistance to death in the fowl, Lush et al. (1948), likewise found that dams had little if any more influence than the sires on the fate of their offspring. Godfrey (1952) presented evidence from which one might speculate that some type of maternal influence is involved in determining resistance of laying hens to Newcastle disease. Other characters of the domestic fowl for which maternal influence has been reported include egg weight (Waters, 1941, 1945), body weight (Hazel and Lamoreux, 1947), character of the eggshell (Taylor and Lerner, 1939), and percentage of firm albumen (Lorenz and Taylor, 1940). Reports of maternal influence in mammals as well as in forms lower than birds are too numerous to discuss here; however, it should be pointed out that in mice a specific maternal influence on resistance to leukemia has been observed by MacDowell and Richter (1935), MacDowell and Taylor (1948), Law (1952), and has been indicated by Cole and Furth (1941) and others. Since the evidence of maternal effects and heterosis presented in this report does not agree with results reported by other workers, further studies with reciprocal diallel matings seem warranted. Thus, additional matings of this type were made in 1952 and 1953 to obtain additional information on the viability of Fi inter-strain hybrids.
HETEROSIS AND MATERNAL EFFECTS ON VIABILITY SUMMARY
In three successive years, crosses were made between two noninbred strains of Single Comb White Leghorns that differed significantly in adult livability. Crosses were made, in two of the years, mating sires of the relatively susceptible strain with dams of the resistant strain; in the third year, reciprocal crosses were made. The Fx inter-strain hybrid pullets produced by susceptible sires and resistant dams consistently showed evidence of heterosis in viability during both the growing and laying periods. In the one year in which reciprocal crosses were made, the Fi inter-strain hybrid pullets produced by resistant sires and susceptible dams exhibited no evidence of heterosis in viability, but died in both the growing and laying periods at rates significantly higher than birds produced by the reciprocal cross. In no instance did adult mortality of the Fi inter-strain hybrids differ significantly from adult mortality of the female line used to produce the hybrids. Thus, it is evident from the data presented that in hybrids of the two strains maternal effects and possibly heterosis play important roles in determining viability. REFERENCES Cole, R. K., and J. Furth, 1941. Experimental studies on the genetics of spontaneous leukemia in mice. Cancer Res. 1:957-965. Ghostley, F., and A. W. Nordskog, 1951. Hybrid vigor in strain crossing and breed crossing. Poultry Sci. 30:914. Godfrey, G. F., 1952. Evidence for genetic variation in resistance to Newcastle disease in the domestic fowl. J. Heredity, 43: 22-24. Hazel, L. M., and W. F. Lamoreux, 1947. Heritability, maternal effects and nicking in relation to sexual maturity and body weight in White Leghorns. Poultry Sci. 26: 508-514.
941
Hutt, F. B., and R. K, Cole, 1947. Genetic control of lymphomatosis in the fowl. Science, 106: 379384. Hutt, F. B., and R. K. Cole, 1952. Heterosis in an inter-strain cross of White Leghorns. Poultry Sci. 31:365-374. King, D. F., and G. J. Cottier, 1948. Comparative performance of the Auburn Strain of White Leghorns. Alabama Agr. Exp. Sta. Prog. Rep. Ser. No. 38:1-4. King, D. F., R. K. Cole, F . B. Hutt and G. J. Cottier, 1952. Test in different environments of fowls genetically resistant to leucos's. Poultry Sci. 31: 1027-1029. Law, L. W., 1952. The flexed-tail-amenia gene (f) and induced leukemia in mice. J. Nat. Cancer Inst. 12: 1119-1126. Lorenz, F. W., and L. W. Taylor, 1940. The inheritance of an albumen quality characteristic of chicken eggs. J. Agr. Res. 61:293-302. Lush, J. L., W. F. Lamoureaux and L^ N . Hazel, 1948. The heritability of resistance to death in the fowl. Poultry Sci. 27: 375-388. MacDowell, E. C , and M. N . Richter, 1935. Mouse leukemia LX. The role of heredity in spontaneous cases. Arch. Path. 20: 709-724. MacDowell, E. C , and M. J. Taylor, 1948. Mouse leukemia XIII. A maternal influence that lowers the incidence of spontaneous cases. Proc. Soc. Exp. Biol. Med. 68: 571-577. Moultrie, F., D. F. King and G. J. Cottier, 1953. Fifteen years of selection for viability in White Leghorns. Poultry Sci. 32: 454-461. Snedecor, G. W., 1946, Statistical Methods. 4th Ed. The Iowa State Col. Press, Ames, Iowa. Sturkie, P. D., 1943. Five years of selection for viability in White Leghorn chickens. Poultry Sci. 22: 155-160. Taylor, L., W., and I. M., Lerner, 1939.1nheritance of eggshell thickness in White Leghorn pullets. J. Agr. Res. 58:383-396. Taylor, L. W., I. M. Lerner, K. B. DeOme and J. R. Beach, 1943. Eight years of progeny-test selection for resistance and susceptibility to lymphomatosis. Poultry Sci. 22:339-347. Waters, N . F., 1941. Genetic aspects of egg weight observed during inbreeding experiments. Poultry Sci. 20:14-27. Waters, N . F., 1945. The weight of chicken eggs as influenced by diallel crossing. Poultry Sci. 24: 81-82.
Influence of Heterosis and Maternal Effects on Viability in an Inter-Strain Cross of White Leghorns • FEED MOULTRIE, D. F. KING AND G. J. COTTIER Agricultural Experiment Station of the Alabama Polytechnic Institute, Auburn, Alabama (Received for publication February 18, 1953)
D
URING the three-year period, 19461948 inclusive, 14 strains of Single Comb White Leghorns were obtained from prominent Leghorn breeders and brought to the Alabama Agricultural Experiment Station Poultry Farm for comparative performance tests with a resistant strain of White Leghorns that was developed at this station (Sturkie, 1943; King and Cottier, 1948; Moultrie et al., 1953). Following the 1948 test, one of the introduced strains that was superior in egg production and other economic traits and about average in livability at this station was chosen for crossing with the resistant strain for the purpose of studying the performance of Fi inter-strain hybrids produced from noninbred stock. The results obtained from crossing these two strains for three consecutive years provide evidence that both heterosis and maternal effects play roles in determining viability of the inter-strain hybrids. Presentation of this evidence is the object of this report. MATERIALS AND METHODS
Strain A, or the Auburn Strain White Leghorn, was developed at the Alabama Agricultural Experiment Station. This
strain has been selected for viability since 1935 and has shown a general decrease in adult mortality of unculled pullets from 89 percent in 1935 to 17 percent in 1951. Selection in Strain A, according to the objective outlined in 1935, was primarily for resistance to fowl paralysis, since at that time paralysis accounted for a large part of the adult mortality. Later, when the mortality from paralysis was reduced considerably, the objective was expanded to include resistance to other diseases and disorders. Foundation stock for Strain A came from 11 different White Leghorn breeders of which seven were represented in the original (1935) matings; the other four strains were introduced by 1941 after which time breeding of this strain has been on a closed-flock basis. Although some close inbreeding was practiced in the early development of this strain, the mating of closely related individuals has been avoided since 1944, and the strain is not considered as an inbred line. Inbreeding coefficients for the flock produced in 1950, based on five generations of ancestors, ranged from zero to .1328 with an average of .0413. Strain D was obtained in 1948 from one of the outstanding White Leghorn breed-
935
936
F. MOULTRIE, D. F. KING AND G. J. COTTIER
ers in the United States. This strain has ranked high in many official egglaying contests during the last several years. Although excellent egg producers, pullets of Strain D, for four consecutive years (1948-1951), died during the laying period at a rate significantly higher than pullets of Strain A. Strain D also has been selected for viability since it has been at the Alabama Station and has shown an annual reduction in adult mortality of unculled pullets, having dropped from 56 percent in 1948 to 30 percent in 1951. No inbreeding has been practiced with Strain D since 1948, and the original breeder's statements concerning inbreeding lead one to believe that inbreeding was avoided prior to that time. In 1948 one case of hatching eggs purchased from the Strain-D breeder was incubated in the same machine with an equal number of eggs from Strain A. From this hatch 92 Strain-D females and 113 Strain-A females were reared and housed together until 520 days of age. The Strain-A females were obtained in approximate equal numbers from 16 Strain-A sires being used in that year, and they were considered as a random sample of Strain A. In 1949 pure Strain-A chicks and pure Strain-D chicks were sired by 12 and 8 males of the two strains, respectively, and inter-strain hybrids were sired by 4 StrainD sires each of which was mated to approximately 15 Strain-A dams. In 1950 pure Strain-A chicks and pure Strain-D chicks were sired by 10 and 8 males of the two strains, respectively. Inter-strain hybrid chicks from reciprocal crosses of the two strains were produced from 11 diallel matings in which 6 of the Strain-A sires and 5 of the StrainD sires were mated concurrently with dams of both strains. Thus, each male sired both pure-strain and hybrid progeny.
In 1951, chicks of Strains A and D were sired by 11 and 4 males of the two strains, respectively, and inter-strain hybrid chicks were produced from 4 Strain-D sires mated with Strain-A dams, as was the case in 1949. Unfortunately, reciprocal crosses were made only in 1950. In all the years covered in this report except 1948, the pure-strain and interstrain hybrid chicks were hatched over a 10-week hatching period, which was from the middle of January until the first of April. Each year the purebreds and inter-strain hybrids were housed together from one day of age until the end of their laying year, which was at 520 days of age. Natural exposure, particularly to leucosis, which at this station is quite severe (Sturkie, 1943; King and Cottier, 1948; King et al., 1952), was provided by brooding the chicks within 100 feet of adult stock until 8 weeks of age. Pullets were placed in the laying house at 155 days of age, and no culling was practiced at any time during the course of this study. It has been shown in previous reports (King and Cottier, 1948; Moultrie et al., 1953) that in general, introduced strains suffer about a 50 percent adult mortality when subjected to the severe exposure of this station, as was the case with Strain D in 1948. Strain-A females had adult mortality rates of 16, 14, and 17 percent in 1949, 1950, and 1951, respectively. During the same years, the adult mortality rates of Strain-D females were 33, 31, and 30 percent, respectively. Therefore, both strains could be considered relatively resistant. However, for the purpose of this study, Strain A was considered as the resistant and Strain D as the susceptible strain; this seems justified as there has been a significant difference in the adult mortality rates of the two strains for the period of study (1948-1951).
937
HETEROSIS AND MATERNAL EFFECTS ON VIABILITY TABLE 1.—Mortality of females from 1 through 15.' days of age Hybrid
Pure Year
Strain A
Strain D
Chicks No.
Mortality %
Chicks No.
Mortality %
1948 1949 1950 1951
113 1,217 718 992
28.3 16.1 24.9 11.6
92 176 333 287
47.8* 27.8* . 23.7"; 13.9
Total & av. 1949-51
2,927
16.7
796
21.1*
Ac?XD9
DcfXAQ
Chicks No.
Mortality
155
39.4
441 130 368
14.lt 16.9ft 8.7t
155
39.4
939
12.4ft
%
Chicks No.
Mortality
%
* Compared with Strain A, significantly higher at 1% level, t Compared with reciprocal cross, significantly lower at 1% level. t The difference between these values and the mid-point between the two parent strians is statistically significant to at least the 5% level.
The significant differences mentioned throughout this report were based on probabilities obtained from calculated values of chi-square (Snedecor, 1946). RESULTS
Growing Mortality. All mortality of female chicks from 1 through 155 days of age, or from hatching to housing as mature pullets, was considered as growing mortality. A summary of this mortality for the pure strains and for inter-strain hybrids is presented in Table 1. In comparing growing mortality of the pure strains, it is shown that Strain-D chicks died at a rate significantly higher than Strain A in 1948, 1949, and in the pooled results for 1949-1951 (the P value for each comparison = < . 0 1 ) . There was little difference in mortality rates of the two strains in 1950, and although the difference was not statistically significant in 1951, the mortality rate of Strain D was 2.3 percent higher than that of Strain A. In comparing growing mortality of the D X A inter-strain hybrid chicks with mortality of the chicks of the parent strains, it is evident that the hybrid chicks from this type mating died at a
rate significantly lower (to at least the 5 percent level) than the average of the mortalities of the parent strains. This difference was evident in all years of the study. If livability significantly higher than the mid-point between the parent strains is an indication of heterosis, then heterosis obviously affected viability during the growing period when the chicks were produced by mating StrainD sires with Strain-A dams. This picture becomes somewhat complicated, however, when the A X D interstrain hybrids are considered. The chicks from this type mating in 1950 had significantly higher (P<.01) growing mortality than did the chicks of the reciprocal cross of the same year. If one considers the general picture in which Strain D is thought of as susceptible and Strain A as resistant; then, there is an indication of maternal effects when comparing the reciprocal crosses of 1950. There was no indication of heterosis affecting viability in the A X D inter-strain hybrids, but it is conceivable that heterosis was involved but masked by maternal effects. Adult Mortality. All mortality of females from 156 days of age at which time pullets were housed until 520 days of
938
F. MOULTRIE, D. F. KING AND G. J. COTTIER TABLE 2.—Mortality of females from 156 through 520 days of age Pure Strain A
Year
1948 1949 1950 1951 Total & av. 1949-51
Hybrid Strain D
AcfXDP
DcfXAQ
Pullets No.
Mort. %
Pullets No.
Mort. %
Pullets. No.
Mort. %
Pullets No.
Mort. %
73 950 548 799
27.4 16.4 14.0 17.4
39 121 238 239
56.4* 32.7* 31.1* 29.7*
94
29.8
373 112 328
16.9J 17.8f 16.5t
2,297
16.2
598
30.8*
94
29.8
813
16.9ft
* Compared with Strain A, significantly higher at 1% level, t Compared with reciprocal cross, significantly lower to at least the 5% level. j The difference between these values and the mid-point between the two parent strains is statistically significant at 1% level.
age, at which time the laying year was completed, was considered as adult mortality. This mortality for the pure strains and inter-strain hybrids is summarized in Table 2. Although the general trends in adult mortality were essentially the same as during the growing period, the results in some respects were more consistent. It is shown in Table 2 that in every year of the study birds of Strain D died at a significantly higher rate than those of Strain A (P < .01). The D X A inter-strain hybrid pullets of 1949, 1951, and in pooled pullets for 1949-1951, inclusive, died at a rate significantly lower (P values<.01) than the mid-point between the two parent strains. Although the difference in 1950 was not significant, the difference of 4.8 percent between the DXA inter-strain hybrids' mortality (17.8 percent) and the mid-point between the parent strains (22.6 percent) was in the same direction as in the other years of the study. As can be noted, a smaller number of birds was housed that year than in the other years of the study; therefore, a relatively greater percentage difference would be necessary for statistical significance. These results, therefore, suggest that heterosis
affected livability of the inter-strain hybrid pullets produced by Strain-D sires and Strain-A dams. Again results were altogether different when the A X D inter-strain hybrids of 1950 were considered. Adult mortality of these pullets was significantly higher (P<.05) than mortality of pullets from the reciprocal (DXA) cross of the same year. Thus, in reciprocal crosses of these two strains, there is evidence of maternal influence on viability during both the growing and laying periods. It should be noted in Table 2 that in no instance did mortality of the inter-strain hybrids differ sifinificantly from mortality of the female line used to produce the hybrids. In both Table 1 and Table 2, the number of birds considered, with exception of the 1948 flock, included all individuals of the particular strain or inter-strain hybrids that were produced each year. Since reciprocal crosses using diallel matings were made only in 1950, all of the offspring from each sire and each dam of the flocks other than that in 1950 were either pure or hybrid. In 1950, however, 11 sires, 6 of Strain A and 5 of Strain D, were mated concurrently with dams of both strains; thus, each of these males
HETEROSIS AND MATERNAL EFFECTS ON VIABILITY
939
TABLE 3.—Adult mortality of female of spring from reciprocal diallel crosses of 1950
sired both pure and hybrid progeny. The results of these matings are given in Table 3. The chicks considered in Table 3 are exactly the same for the inter-strain hybrids, for both types of matings, as shown for 1950 in Table 2; however, the total number of purebreds involved is materially reduced as all pullets were eliminated in this comparison except those sired by the males used in reciprocal diallel matings. As previously pointed out, the reciprocal crosses differed significantly in mortality. It also is shown in Table 3 that in both crosses the inter-strain hybrids differed significantly from their half sisters sired by the same males. It is again evident in Table 3 that the Fi inter-strain hybrids differed little from the female line used in their production.
' Male Strain A N 1281 P 1184 P 620 P 1076 P 1227 P 1064
Pure
Hybrid
Pullets Mortality Pullets Mortality No. % No. % 57 71 54 56 31 23
Total & av. Strain D P 2287 P 2728 P 1047 P 2264 0 2750 Total & av.
Difference
%
37.5 12.9 13.0
15 11 11 9 28 20
20.0 18.2 18.2 66.7 25.0 40.0
+0.7 + 1.3 +10.8 +29.2 +12.1 +27.0
292
18.8
94
29.8*
+11.0
26 42 52 44 31
26.9 26.2 40.4 29.5 12.9
36 42 8 10 16
16.7 21.4 12.5 10.0 18.8
-10.2 -4.8 -27.9 -19.5 +5.9
195
28.7
112
17.9f
-10.8
19.3 16.9 7.4
* Compared with pure strain from same sires, significantly higher at 5% level. t Compared with pure strain from same sires, significantly lower at 5% level.
pullets housed, whereas, only 3.8 percent of the birds of Strain A died from leucosis. The difference of 13.4 percent mortality of pullets housed is statistically significant (P<.01). Losses from leucosis among inter-strain hybrids, based on percentage of pullets housed, were within the parental mortality range. However, in birds from both types of matings (AXD and DXA), the mortality was nearer the female line.
Adult mortality of pure strains and inter-strain hybrids of the 1950 flock according to the most important causes of death is summarized in Table 4. It is evident that most of the difference in mortality of the two pure strains was due to the greater death loss from leucosis in Strain D. Mortality from this disease in Strain D was 17.2 percent of
TABLE 4.—Percentage of adult mortality due to each cause among pure strains and Fi inter-strain hybrids {1950) Hybrid
Pure Strain A
Strain D
Ac?XD9
DcfXAQ
Cause of death %of %of total pullets mortality housed Leucosis Reproductive disorders Respiratory diseases Nephritis Hepatitis Internal hemorrhage Visceral gout Miscellaneous Total
%of %of %of %of %of %of total pullets total pullets total pullets mortality housed mortality housed mortality housed
27.3 26.0 6.5 6.5 3.9 3.9 10.4 15.1
3.8 3.6 0.9 0.9 0.5 0.5 1.5 2.3
55.4 16.2 12.2 4.1 1.4 1.4 4.1 5.5
99.6
14.0
100.3
17.2* 5.0 3.8 1.3 0.4 0.4 1.3 1.7 31.1
* Compared with Strain A, significantly higher at 1% level.
42.9 17.9 17.9 7.1
12.8 5.3 5.3 2.1
50.0 20.0 10.0 5.0
—
—•
—•
—•
—
2.1
—
10.0
1.8
100.0
29.8
100.0
17.8
7.1 7.1
2.1
5.0
8.9 3.6T 1.8 0.9
—•
0.9
—
•
940
F. MOULTRIE, D. F. KING AND G. J. COTTIER
This suggests an influence of maternal effects upon resistance to leucosis. It should be noted, however, that the D X A inter-strain hybrids, again based on percentage of pullets housed, showed less mortality from each of the causes than did the A X D inter-strain hybrids, which suggests that the hybrids from the Strain-A dams possessed general viability greater than the hybrids from the reciprocal cross. DISCUSSION
The results presented in this report show that the crossing of males from a relatively susceptible strain with females from a resistant strain produced hybrids that consistently showed evidence of an effect of heterosis on viability during both the growing and laying periods. However, relatively higher mortality of birds from the reciprocal of the above cross suggests that maternal effects may be involved. Since the parent strains differed significantly in viability, livability of the D X A inter-strain hybrids excelling the mid-point between the two parent strains that has been interpreted as evidence of heterosis could have been due to maternal influence. Ghostley and Nordskog (1951) found evidence of heterosis influencing viability in strain crosses in heavy breeds; however, Hutt and Cole (1952) crossed two slightly inbred strains of White Leghorns that differed little in viability and found that the resulting hybrids consistently excelled both parent strains in hatchability, early maturity, egg production, size of eggs, and size of birds, but no consistent evidence was found to indicate that heterosis increased viability in the nybrids. Maternal effect, if operative, would not have been detected in the crosses made by Hutt and Cole as the parent strains did not differ in viabil-
ity; however, in a previous report in which lines relatively resistant and susceptible to leucosis were crossed, no evidence of maternal effects was found (Hutt and Cole, 1947). Taylor et al. (1943) reached a similar conclusion after making reciprocal crosses between strains resistant and susceptible to leucosis. In studying the heritability of resistance to death in the fowl, Lush et al. (1948), likewise found that dams had little if any more influence than the sires on the fate of their offspring. Godfrey (1952) presented evidence from which one might speculate that some type of maternal influence is involved in determining resistance of laying hens to Newcastle disease. Other characters of the domestic fowl for which maternal influence has been reported include egg weight (Waters, 1941, 1945), body weight (Hazel and Lamoreux, 1947), character of the eggshell (Taylor and Lerner, 1939), and percentage of firm albumen (Lorenz and Taylor, 1940). Reports of maternal influence in mammals as well as in forms lower than birds are too numerous to discuss here; however, it should be pointed out that in mice a specific maternal influence on resistance to leukemia has been observed by MacDowell and Richter (1935), MacDowell and Taylor (1948), Law (1952), and has been indicated by Cole and Furth (1941) and others. Since the evidence of maternal effects and heterosis presented in this report does not agree with results reported by other workers, further studies with reciprocal diallel matings seem warranted. Thus, additional matings of this type were made in 1952 and 1953 to obtain additional information on the viability of Fi inter-strain hybrids.
HETEROSIS AND MATERNAL EFFECTS ON VIABILITY SUMMARY
In three successive years, crosses were made between two noninbred strains of Single Comb White Leghorns that differed significantly in adult livability. Crosses were made, in two of the years, mating sires of the relatively susceptible strain with dams of the resistant strain; in the third year, reciprocal crosses were made. The Fx inter-strain hybrid pullets produced by susceptible sires and resistant dams consistently showed evidence of heterosis in viability during both the growing and laying periods. In the one year in which reciprocal crosses were made, the Fi inter-strain hybrid pullets produced by resistant sires and susceptible dams exhibited no evidence of heterosis in viability, but died in both the growing and laying periods at rates significantly higher than birds produced by the reciprocal cross. In no instance did adult mortality of the Fi inter-strain hybrids differ significantly from adult mortality of the female line used to produce the hybrids. Thus, it is evident from the data presented that in hybrids of the two strains maternal effects and possibly heterosis play important roles in determining viability. REFERENCES Cole, R. K., and J. Furth, 1941. Experimental studies on the genetics of spontaneous leukemia in mice. Cancer Res. 1:957-965. Ghostley, F., and A. W. Nordskog, 1951. Hybrid vigor in strain crossing and breed crossing. Poultry Sci. 30:914. Godfrey, G. F., 1952. Evidence for genetic variation in resistance to Newcastle disease in the domestic fowl. J. Heredity, 43: 22-24. Hazel, L. M., and W. F. Lamoreux, 1947. Heritability, maternal effects and nicking in relation to sexual maturity and body weight in White Leghorns. Poultry Sci. 26: 508-514.
941
Hutt, F. B., and R. K, Cole, 1947. Genetic control of lymphomatosis in the fowl. Science, 106: 379384. Hutt, F. B., and R. K. Cole, 1952. Heterosis in an inter-strain cross of White Leghorns. Poultry Sci. 31:365-374. King, D. F., and G. J. Cottier, 1948. Comparative performance of the Auburn Strain of White Leghorns. Alabama Agr. Exp. Sta. Prog. Rep. Ser. No. 38:1-4. King, D. F., R. K. Cole, F . B. Hutt and G. J. Cottier, 1952. Test in different environments of fowls genetically resistant to leucos's. Poultry Sci. 31: 1027-1029. Law, L. W., 1952. The flexed-tail-amenia gene (f) and induced leukemia in mice. J. Nat. Cancer Inst. 12: 1119-1126. Lorenz, F. W., and L. W. Taylor, 1940. The inheritance of an albumen quality characteristic of chicken eggs. J. Agr. Res. 61:293-302. Lush, J. L., W. F. Lamoureaux and L^ N . Hazel, 1948. The heritability of resistance to death in the fowl. Poultry Sci. 27: 375-388. MacDowell, E. C , and M. N . Richter, 1935. Mouse leukemia LX. The role of heredity in spontaneous cases. Arch. Path. 20: 709-724. MacDowell, E. C , and M. J. Taylor, 1948. Mouse leukemia XIII. A maternal influence that lowers the incidence of spontaneous cases. Proc. Soc. Exp. Biol. Med. 68: 571-577. Moultrie, F., D. F. King and G. J. Cottier, 1953. Fifteen years of selection for viability in White Leghorns. Poultry Sci. 32: 454-461. Snedecor, G. W., 1946, Statistical Methods. 4th Ed. The Iowa State Col. Press, Ames, Iowa. Sturkie, P. D., 1943. Five years of selection for viability in White Leghorn chickens. Poultry Sci. 22: 155-160. Taylor, L., W., and I. M., Lerner, 1939.1nheritance of eggshell thickness in White Leghorn pullets. J. Agr. Res. 58:383-396. Taylor, L. W., I. M. Lerner, K. B. DeOme and J. R. Beach, 1943. Eight years of progeny-test selection for resistance and susceptibility to lymphomatosis. Poultry Sci. 22:339-347. Waters, N . F., 1941. Genetic aspects of egg weight observed during inbreeding experiments. Poultry Sci. 20:14-27. Waters, N . F., 1945. The weight of chicken eggs as influenced by diallel crossing. Poultry Sci. 24: 81-82.