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Heritability and Repeatability of Social Aggressiveness in the Domestic Chicken1,2,3
Heritability and Repeatability of Social Aggressiveness in the Domestic Chicken1,2-3 TOORU KOMAI, J. V. CRAIG AND S. WEARDEN4 Kansas State College, Manhattan, Kansas (Received for publication July 25, 1958) INTRODUCTION
of behavior patterns in the S TUDIES chicken have been reviewed by Guhl
"This investigation was part of the Kansas contribution to the NC-47 Regional Poultry Breeding Project. 2 The Society of the Sigma Xi generously made funds available to support part-time help to allow the collection of detailed data on social behavior. 3 Contribution No. 241, Department of Poultry Husbandry and Contribution No. 40, Statistical Laboratory, Kansas Agricultural Experiment Station, Manhattan, Kansas. 4 Graduate Research Assistant and Associate Professor of Poultry Genetics, Department of Poultry Husbandry and Statistician, Statistical Laboratory, respectively.
MATERIALS AND METHODS
The birds used in this experiment and the methods of management and observations were the same as have been described by Tindell and Craig (1959). A detailed account of procedures may be obtained by examining that paper. In brief, five of the six strains used were acquired by hatching eggs obtained from commercial breeders who had been asked to supply stock from closed flocks of high egg production potential. There were three strains of White Leghorns (WL), and one each of Black Australorps (BA), Rhode Island Reds (RR), and White Plymouth Rocks (WR). The WR chicks were produced from randomly selected parents of the Kansas State College strain. All chicks were wingbanded and sexed at hatching. One group of 96 pullets were reared separately in 1956. This group consisted of 16 birds from each of the six strains. At five months of age eight pullets were randomly selected from each of the. six strains in this small flock and were placed together in one of the intermingled flocks in the laying house. All other pullets
356
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
(1953) and Wood-Gush (1955). Significant associations between individual social status and various quantitative traits associated with the well-being and productivity of the hen have been found by several investigators, including Guhl (1953) and Tindell and Craig (1959). The latter authors and King and Bray (1959) have also detected significant competition effects when strains and breeds were kept in intermingled flocks and compared with the same strains and breeds in separate flocks. Guhl (unpublished) was able to separate lines with high and low aggressiveness from the same foundation stock of White Leghorns, by selecting for these traits in both sexes over a period of a few generations. The present study was carried out in order to estimate the importance of genetic variation for social aggressiveness within each of six strains, including four breeds of chickens. A total of 288 pullets and their
131 dams supplied data for such heritability estimates. A second objective was to determine how consistent strains were in their relative aggressiveness from year to year when reared together and placed in the same pens of the laying house. Repeatability of social status of strains was calculated on the basis of the mean social rank of 16 and 24 pullets from each strain, in intermingled flocks, in the first and second years of the study, respectively.
SOCIAL AGGRESSIVENESS
heritability of social aggressiveness
(2\
Percentile social ranks were calculated for an individual "X" as follows: Percentile social rank = (A + B)/2, where A = the percentage of birds that X dominated, and B = 100% minus the percentage of birds dominating X. For heritability estimates, percentile social ranks were calculated on a withinflock, within-strain basis. A trait measured as described above has a non-normal, uniform distribution, i.e. 10% of all birds have ranks of 0-9%, 10% have ranks of 10-19%, etc. Because of this non-normal distribution the usual methods of estimating heritability based on normal variances and covariances did not appear suitable. The percentile social ranks were transformed to ordered social ranks in order to compute unbiased heritability estimates and confidence intervals by the distributionfree method of Schwartz and Wearden (1959). Thus, individuals were placed in ascending order by their percentile social rank with the least aggressive individual ranked as 1, the next more aggressive bird ranked as 2, etc. until the most aggressive bird received the highest ordered rank. It was possible to apply the Mann-Whitney "U" Test as described by Siegel (1956) to the mean difference between daughters divided according to whether their dams were in the upper or lower half of the maternal generation on the basis of the ordered social ranks within each strain. The method of computing heritability is the same as would be applied in the first generation of a selection experiment in which selection is practiced in only one sex, as follows:
(mean rank, daughters of high dams) — (mean rank, daughters of low dams) (mean rank, high dams)
tions between pairs of birds were observed in the first and second years, respectively,
(mean rank, low dams)
Because of the relatively small number of birds per strain, confidence limits which
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
in both years were reared in large intermingled flocks. Pullets from these flocks were also randomly selected and placed in the laying house at about five months of age. Only those birds which were in obviously poor health, crippled, or showing some degree of blindness were excluded from the random selection procedure at housing time. Eight pullets were then placed in each of three intermingled flocks from each strain, i.e. a total of 24 birds represented each strain in the intermingled flocks. An additional 24 pullets of each strain were taken from the intermingled flocks in which reared and placed in single pure strain flocks. Pullets used in the second year were obtained by mating hens observed in the first year to randomly selected males of their own strains. Artificial insemination was practiced. Because of an insufficient number of chicks in the RR strain, 24 pullets hatched from dams of the same strain but received in a separate shipment from the breeder and of unknown social status were used in the second year. Twenty-four RR pullets from dams of known social rank were placed in the pure strain flock for that strain, while the pullets from dams of unknown social rank were all placed in intermingled flocks. As soon as the pullets were housed each year, they were observed for at least 24 hours per week for the first two months and 18 hours per week for the next one and onehalf months to obtain data on social interactions. Fights, pecks, threats, and avoidances were all used in estimating the social status of each pullet. Seventy-three and sixty-four percent of all possible interac-
357
358
T. KOMAI, J. V. CRAIG AND S. WEARDEN TABLE 1.—Heritability estimates for percentile and ordered social ranks of six strains with probability levels and eighty percent confidence limits
Strain
WLi WL 2 WL3 WR BA RR Means All strains WL strains WR, BA, RR
social rank
social rank
-0.28 0.36 0.66 0.05 0.25 0.79
-0.26 0.42 0.74 -0.03 0.22 0.97
0.30 0.25
0.34 0.30
0.36
0.39
Probability' level 0.22 0.11 0.01 0.46 0.26 0.01
Eighty percent confidence limits Lower
Upper
-0.76 -0.11 0.21 -0.55 -0.31 0.23
0.27 0.88 1.17 0.48 0.72 1.47
1
Probability levels of heritability estimates are based on the Mann-Whitney "U" Test of the differences between daughters of dams dominating more than or less than 50% of their own strain.
fective in changing the aggressiveness level within a strain. The mean heritability estimates of 0.25 and 0.30 for percentile and ordered social ranks of White Leghorns are in agreement with what might be expected after examination of results from Guhl's (unpublished) selection experiment. Examination of Table 2 reveals that strains tend to repeat their social standing in intermingled flocks from year to year. The repeatability estimate of 0.857 (P = TABLE 2.—Percentile and ordered social ranks of six strains in intermingled flocks in each of two years
RESULTS AND DISCUSSION The heritability estimates for social aggressiveness of the six strains in this study are presented in Table 1. Two of the estimates are clearly different from zero (P = 0.01). It may be noted, however, that the 80 percent confidence limits overlap for all heritability estimates, indicating that there is no clear evidence of differences in genetic variation for social status within the different strains. The mean intra-strain heritability estimates of 0.30 and 0.34 for percentile and ordered social ranks, respectively, indicate that selection should be ef-
Heritability estimates -,Percentile Ordered
Strain
WLi WL 2 WL 3 WR BA RR
1956-571
1957-581
Percentile Ordered social social rank rank
Percentile Ordered social social rank rank
0.63 0.56 0.43 0.56 0.46 0.29
6 44 2 44 3 1
0.65 0.56 0.30 0.65 0.43 0.41
5* 4 1 54 24 24
Repeatability of ordered social rank=0.857 (P = .065). 1 Means based on 16 and 24 pullets per strain in 1956-57 and 1957-58, respectively, less birds dying between housing and approximately eight months of age. Percentile ranks differing by less than 3 % are considered as. ties in assigning ordered ranks.
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
would include the true value of heritability with a probability of at least 0.80 were calculated. This probability level was used in order to attain a relatively narrow confidence interval. The relative aggressiveness of each of the six strains was estimated by calculating within-intermingled-flock percentile social ranks for individuals and then computing the mean for each strain, based on eight pullets, within each such flock. The average social rank for each strain was then taken as the mean percentile social rank from the pooled data of two intermingled flocks in the first year and three intermingled flocks in the second year of the study. The one intermingled flock assembled at hatching in the first year was not included, since it was shown by Tindell and Craig (1959) that the social ranks of the six strains varied depending on whether the flocks were assembled at hatching or at five months of age. Ordered social ranks of the strains were calculated on the basis of the percentile social ranks, with the most aggressive strain ranked as six and the least aggressive strain ranked as one. A simple rank correlation was then used to estimate the repeatability of strain performance for social dominance in the two years of the study.
SOCIAL AGGRESSIVENESS
SUMMARY
Observations of the social status of daughters and dams within six strains of four breeds were used to estimate the heritability for social aggressiveness in the do-
mestic chicken. Social aggressiveness appears to be genetically variable enough within strains (mean heritability estimates of 0.30 and 0.34) to allow effective selection. The social standing of the six strains studied had a high repeatability (0.857) indicating that differences in aggressiveness among the strains were largely determined by hereditary differences. ACKNOWLEDGMENTS
The authors are grateful to Dr. A. M. Guhl, Department of Zoology, for carefully reading the manuscript and suggesting helpful changes and to Mr. D. Tindell and Mrs. A. E. Grosse for assistance in collecting the data. REFERENCES Guhl, A. M., 19S3. Social behavior of the domestic fowl. Tech. Bull. 73, Kansas Agr. Expt. Sta. Kendall, M. G., 1948. Rank Correlation Methods. Charles Griffin and Company, London (pp. 46-49.) King, S. C , and D. F. Bray, 1959. Competition between strains of chickens in separate versus intermingled flocks. Poultry Sci. 38: 86-94. Schwartz, L., and S. Wearden, 1959. A distributionfree asymptotic method of estimating, testing and setting confidence limits for heritability. Biometrics, in press. Siegel, S., 1956. Nonparametric Statistics for the Behaviorial Sciences. McGraw-Hill, New York (pp. 190-192.) Tindell, D., and J. V. Craig, 1959. Effects of social competition on laying house performance in the chicken. Poultry Sci. 38: 95-105. Wood-Gush, D. G. M., 1955. The behavior of the domestic chicken: A review of the literature. Brit. J. An. Behav. 3 : 81-110.
NEWS AND NOTES (Continued from page 3S5) shire; R. Higgins, Hot Springs, Arkansas; and sota, St. Paul, was given an honorary life memberR. Thompson, Ellsworth, Iowa. C. W. Wampler, ship in the Federation. This honor is given to indiHarrisonburg, Virginia, and H. Beyers, Salt Lake viduals who have made an outstanding contribution City, Utah, are honorary life members. M. C. Small, to the welfare of the turkey industry. Mount Morris, Illinois, is Executive SecretaryJohn LaMont Blackham, Moroni, Utah and Treasurer. Deanna Borron, Winigan, Missouri, received the Dr. B. S. Pomeroy, Professor of Veterinary BacFederation's National Youth Achievement Awards. teriology and Public Health, University of Minne(Continued on page 372)
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
0.065, see Kendall, 1948) is large enough to indicate that differences in social aggressiveness among strains may be largely due to hereditary differences. The same conclusion was suggested by the results of Tindell and Craig (1959) who found significant differences among the heavy breeds and differences approaching significance (P = 0.15), among the WL strains, in analyzing percentile social ranks from data collected on these same birds in the first year of the experiment. Sixteen to 24 pullets constituted a sufficiently large number in this study to indicate the relative social standing of a strain in intermingled flocks. It is of interest to note, from Tables 1 and 2, that there may possibly be an inverse relationship between the social rank of a strain and the heritability of this trait, i.e. high ranking strains tended to have low heritability and vice versa. Since the 80 percent confidence limits for the heritability estimates of the six strains overlap, it is not clear whether this apparent association is meaningful. It might be hypothesized, however, that selection for aggressiveness may have inadvertently occurred in those strains showing high social rank and that such selection has tended to exhaust genetic variation for this trait.
359
of behavior patterns in the S TUDIES chicken have been reviewed by Guhl
"This investigation was part of the Kansas contribution to the NC-47 Regional Poultry Breeding Project. 2 The Society of the Sigma Xi generously made funds available to support part-time help to allow the collection of detailed data on social behavior. 3 Contribution No. 241, Department of Poultry Husbandry and Contribution No. 40, Statistical Laboratory, Kansas Agricultural Experiment Station, Manhattan, Kansas. 4 Graduate Research Assistant and Associate Professor of Poultry Genetics, Department of Poultry Husbandry and Statistician, Statistical Laboratory, respectively.
MATERIALS AND METHODS
The birds used in this experiment and the methods of management and observations were the same as have been described by Tindell and Craig (1959). A detailed account of procedures may be obtained by examining that paper. In brief, five of the six strains used were acquired by hatching eggs obtained from commercial breeders who had been asked to supply stock from closed flocks of high egg production potential. There were three strains of White Leghorns (WL), and one each of Black Australorps (BA), Rhode Island Reds (RR), and White Plymouth Rocks (WR). The WR chicks were produced from randomly selected parents of the Kansas State College strain. All chicks were wingbanded and sexed at hatching. One group of 96 pullets were reared separately in 1956. This group consisted of 16 birds from each of the six strains. At five months of age eight pullets were randomly selected from each of the. six strains in this small flock and were placed together in one of the intermingled flocks in the laying house. All other pullets
356
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
(1953) and Wood-Gush (1955). Significant associations between individual social status and various quantitative traits associated with the well-being and productivity of the hen have been found by several investigators, including Guhl (1953) and Tindell and Craig (1959). The latter authors and King and Bray (1959) have also detected significant competition effects when strains and breeds were kept in intermingled flocks and compared with the same strains and breeds in separate flocks. Guhl (unpublished) was able to separate lines with high and low aggressiveness from the same foundation stock of White Leghorns, by selecting for these traits in both sexes over a period of a few generations. The present study was carried out in order to estimate the importance of genetic variation for social aggressiveness within each of six strains, including four breeds of chickens. A total of 288 pullets and their
131 dams supplied data for such heritability estimates. A second objective was to determine how consistent strains were in their relative aggressiveness from year to year when reared together and placed in the same pens of the laying house. Repeatability of social status of strains was calculated on the basis of the mean social rank of 16 and 24 pullets from each strain, in intermingled flocks, in the first and second years of the study, respectively.
SOCIAL AGGRESSIVENESS
heritability of social aggressiveness
(2\
Percentile social ranks were calculated for an individual "X" as follows: Percentile social rank = (A + B)/2, where A = the percentage of birds that X dominated, and B = 100% minus the percentage of birds dominating X. For heritability estimates, percentile social ranks were calculated on a withinflock, within-strain basis. A trait measured as described above has a non-normal, uniform distribution, i.e. 10% of all birds have ranks of 0-9%, 10% have ranks of 10-19%, etc. Because of this non-normal distribution the usual methods of estimating heritability based on normal variances and covariances did not appear suitable. The percentile social ranks were transformed to ordered social ranks in order to compute unbiased heritability estimates and confidence intervals by the distributionfree method of Schwartz and Wearden (1959). Thus, individuals were placed in ascending order by their percentile social rank with the least aggressive individual ranked as 1, the next more aggressive bird ranked as 2, etc. until the most aggressive bird received the highest ordered rank. It was possible to apply the Mann-Whitney "U" Test as described by Siegel (1956) to the mean difference between daughters divided according to whether their dams were in the upper or lower half of the maternal generation on the basis of the ordered social ranks within each strain. The method of computing heritability is the same as would be applied in the first generation of a selection experiment in which selection is practiced in only one sex, as follows:
(mean rank, daughters of high dams) — (mean rank, daughters of low dams) (mean rank, high dams)
tions between pairs of birds were observed in the first and second years, respectively,
(mean rank, low dams)
Because of the relatively small number of birds per strain, confidence limits which
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
in both years were reared in large intermingled flocks. Pullets from these flocks were also randomly selected and placed in the laying house at about five months of age. Only those birds which were in obviously poor health, crippled, or showing some degree of blindness were excluded from the random selection procedure at housing time. Eight pullets were then placed in each of three intermingled flocks from each strain, i.e. a total of 24 birds represented each strain in the intermingled flocks. An additional 24 pullets of each strain were taken from the intermingled flocks in which reared and placed in single pure strain flocks. Pullets used in the second year were obtained by mating hens observed in the first year to randomly selected males of their own strains. Artificial insemination was practiced. Because of an insufficient number of chicks in the RR strain, 24 pullets hatched from dams of the same strain but received in a separate shipment from the breeder and of unknown social status were used in the second year. Twenty-four RR pullets from dams of known social rank were placed in the pure strain flock for that strain, while the pullets from dams of unknown social rank were all placed in intermingled flocks. As soon as the pullets were housed each year, they were observed for at least 24 hours per week for the first two months and 18 hours per week for the next one and onehalf months to obtain data on social interactions. Fights, pecks, threats, and avoidances were all used in estimating the social status of each pullet. Seventy-three and sixty-four percent of all possible interac-
357
358
T. KOMAI, J. V. CRAIG AND S. WEARDEN TABLE 1.—Heritability estimates for percentile and ordered social ranks of six strains with probability levels and eighty percent confidence limits
Strain
WLi WL 2 WL3 WR BA RR Means All strains WL strains WR, BA, RR
social rank
social rank
-0.28 0.36 0.66 0.05 0.25 0.79
-0.26 0.42 0.74 -0.03 0.22 0.97
0.30 0.25
0.34 0.30
0.36
0.39
Probability' level 0.22 0.11 0.01 0.46 0.26 0.01
Eighty percent confidence limits Lower
Upper
-0.76 -0.11 0.21 -0.55 -0.31 0.23
0.27 0.88 1.17 0.48 0.72 1.47
1
Probability levels of heritability estimates are based on the Mann-Whitney "U" Test of the differences between daughters of dams dominating more than or less than 50% of their own strain.
fective in changing the aggressiveness level within a strain. The mean heritability estimates of 0.25 and 0.30 for percentile and ordered social ranks of White Leghorns are in agreement with what might be expected after examination of results from Guhl's (unpublished) selection experiment. Examination of Table 2 reveals that strains tend to repeat their social standing in intermingled flocks from year to year. The repeatability estimate of 0.857 (P = TABLE 2.—Percentile and ordered social ranks of six strains in intermingled flocks in each of two years
RESULTS AND DISCUSSION The heritability estimates for social aggressiveness of the six strains in this study are presented in Table 1. Two of the estimates are clearly different from zero (P = 0.01). It may be noted, however, that the 80 percent confidence limits overlap for all heritability estimates, indicating that there is no clear evidence of differences in genetic variation for social status within the different strains. The mean intra-strain heritability estimates of 0.30 and 0.34 for percentile and ordered social ranks, respectively, indicate that selection should be ef-
Heritability estimates -,Percentile Ordered
Strain
WLi WL 2 WL 3 WR BA RR
1956-571
1957-581
Percentile Ordered social social rank rank
Percentile Ordered social social rank rank
0.63 0.56 0.43 0.56 0.46 0.29
6 44 2 44 3 1
0.65 0.56 0.30 0.65 0.43 0.41
5* 4 1 54 24 24
Repeatability of ordered social rank=0.857 (P = .065). 1 Means based on 16 and 24 pullets per strain in 1956-57 and 1957-58, respectively, less birds dying between housing and approximately eight months of age. Percentile ranks differing by less than 3 % are considered as. ties in assigning ordered ranks.
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
would include the true value of heritability with a probability of at least 0.80 were calculated. This probability level was used in order to attain a relatively narrow confidence interval. The relative aggressiveness of each of the six strains was estimated by calculating within-intermingled-flock percentile social ranks for individuals and then computing the mean for each strain, based on eight pullets, within each such flock. The average social rank for each strain was then taken as the mean percentile social rank from the pooled data of two intermingled flocks in the first year and three intermingled flocks in the second year of the study. The one intermingled flock assembled at hatching in the first year was not included, since it was shown by Tindell and Craig (1959) that the social ranks of the six strains varied depending on whether the flocks were assembled at hatching or at five months of age. Ordered social ranks of the strains were calculated on the basis of the percentile social ranks, with the most aggressive strain ranked as six and the least aggressive strain ranked as one. A simple rank correlation was then used to estimate the repeatability of strain performance for social dominance in the two years of the study.
SOCIAL AGGRESSIVENESS
SUMMARY
Observations of the social status of daughters and dams within six strains of four breeds were used to estimate the heritability for social aggressiveness in the do-
mestic chicken. Social aggressiveness appears to be genetically variable enough within strains (mean heritability estimates of 0.30 and 0.34) to allow effective selection. The social standing of the six strains studied had a high repeatability (0.857) indicating that differences in aggressiveness among the strains were largely determined by hereditary differences. ACKNOWLEDGMENTS
The authors are grateful to Dr. A. M. Guhl, Department of Zoology, for carefully reading the manuscript and suggesting helpful changes and to Mr. D. Tindell and Mrs. A. E. Grosse for assistance in collecting the data. REFERENCES Guhl, A. M., 19S3. Social behavior of the domestic fowl. Tech. Bull. 73, Kansas Agr. Expt. Sta. Kendall, M. G., 1948. Rank Correlation Methods. Charles Griffin and Company, London (pp. 46-49.) King, S. C , and D. F. Bray, 1959. Competition between strains of chickens in separate versus intermingled flocks. Poultry Sci. 38: 86-94. Schwartz, L., and S. Wearden, 1959. A distributionfree asymptotic method of estimating, testing and setting confidence limits for heritability. Biometrics, in press. Siegel, S., 1956. Nonparametric Statistics for the Behaviorial Sciences. McGraw-Hill, New York (pp. 190-192.) Tindell, D., and J. V. Craig, 1959. Effects of social competition on laying house performance in the chicken. Poultry Sci. 38: 95-105. Wood-Gush, D. G. M., 1955. The behavior of the domestic chicken: A review of the literature. Brit. J. An. Behav. 3 : 81-110.
NEWS AND NOTES (Continued from page 3S5) shire; R. Higgins, Hot Springs, Arkansas; and sota, St. Paul, was given an honorary life memberR. Thompson, Ellsworth, Iowa. C. W. Wampler, ship in the Federation. This honor is given to indiHarrisonburg, Virginia, and H. Beyers, Salt Lake viduals who have made an outstanding contribution City, Utah, are honorary life members. M. C. Small, to the welfare of the turkey industry. Mount Morris, Illinois, is Executive SecretaryJohn LaMont Blackham, Moroni, Utah and Treasurer. Deanna Borron, Winigan, Missouri, received the Dr. B. S. Pomeroy, Professor of Veterinary BacFederation's National Youth Achievement Awards. teriology and Public Health, University of Minne(Continued on page 372)
Downloaded from http://ps.oxfordjournals.org/ at University of Hong Kong on May 11, 2015
0.065, see Kendall, 1948) is large enough to indicate that differences in social aggressiveness among strains may be largely due to hereditary differences. The same conclusion was suggested by the results of Tindell and Craig (1959) who found significant differences among the heavy breeds and differences approaching significance (P = 0.15), among the WL strains, in analyzing percentile social ranks from data collected on these same birds in the first year of the experiment. Sixteen to 24 pullets constituted a sufficiently large number in this study to indicate the relative social standing of a strain in intermingled flocks. It is of interest to note, from Tables 1 and 2, that there may possibly be an inverse relationship between the social rank of a strain and the heritability of this trait, i.e. high ranking strains tended to have low heritability and vice versa. Since the 80 percent confidence limits for the heritability estimates of the six strains overlap, it is not clear whether this apparent association is meaningful. It might be hypothesized, however, that selection for aggressiveness may have inadvertently occurred in those strains showing high social rank and that such selection has tended to exhaust genetic variation for this trait.
359