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Social dominance and darwinian fitness in laboratory mice: an alternative test
BEHAVIORAL BIOLOGY 16, 113-116 (1976), Abstract No. 5184
BRIEF REPORT Social Dominance and Darwinian Fitness in Laboratory Mice: An Alternative Test
A. R. KUSE and J. C. DE FRIES 1
Institute for Behavioral Genetics, University o f Colorado, BouMer, Colorado 80302 Social behavior of subjects from each of three inbred strains of mice (DBA/2, BALB/c, and C57BL) was compared to that of their derived F1 and F 2 generations in standardized living units (triads). Four males (P1, P2, F1, and F2) were placed in each of 30 triads for 7 days, and dominance hierarchies were determined. In order to assess the effect of female presence on intermale aggression, females were placed in one-half of the triads. In general, considerable heterosis for social dominance was observed, and more aggression occurred among males in triads that contained females. These results are consistent with the hypothesis that social dominance is a major component of Darwinian fitness in Mus musculus.
DeFries and McClearn (1970) suggested that social dominance among males, as indexed by the number of tail wounds in the triad paradigm, may be a major component of Darwinian fitness in house mice (Mus musculus). In each o f two experiments utilizing inbred males, over 90% of the litters were sired b y dominant animals, a finding subsequently replicated by Horn (1974) and generalized to outbred males by DeFries and McClearn (1972). Although not systematically explored in this latter study, F~ hybrid males were found to be more dominant in triads than members of inbred strains or those of a segregating population. Evidence for heterosis o f aggressive behavior by laboratory mice has also been reported by Southwick (1970). As Bmell (1964) and Roberts (1967) have discussed, most of the genetic variance for fitness characters which have been subjected to directional selection is nonadditive. Thus, if social dominance has been a major component o f Darwinian fitness during the evolution of house mice, considerable heterosis should be observed for this character; i.e., the mean social dominance of F1 hybrid males should exceed the average social dominance o f the parental strains, and the F2 generation should be intermediate between the F~ and parental means (Falconer, 1960). The primary objective o f the present comunication is to report the results o f an experiment that systematically 1This work was supported in part by NIMH Training Grant MH-11167. 113 Copyright © 1976 by Academic Press, In¢ All rights of reproduction in any form reserved.
114
KUSE AND DE FRIES
assessed the relationship between social dominance and Darwinian fitness in laboratory mice using this alternative approach. During the course of the experiment, the influence of female presence on male aggression in the triad paradigm was also ascertained. The triad apparatus is a standardized social living unit composed of three mouse cages interconnected with a Y-shaped plastic manifold. This arrangement allows subjects freedom of movement among cages throughout an experimental session and facilitates formation of social dominance hierarchies among males. Thirty triads were assembled, each containing a male from two of three inbr,~d strains (BALB/cIbg, C57BL/Ibg, or DBA/2Ibg, hereafter symbolized as B, C, and D, respectively) and from their FI and F2 hybrid generations. Thus, each of 10BC triads contained four males: a BALB/c, a C57BL, and a derived Fa a n d F2. T e n BD and 10 CD triads were correspondingly constituted. In one-half of these BC, BD, and CD triads, three outbred HS females (McClearn, Wilson, and Meredith, 1970) were included to investigate the effect of female presence on male aggression. Males were isolated 3-7 days prior to testing (66 -+ 5 days of age) and then assigned to triads at random with regard to body weight. Subjects were examined daily for number of tail wounds (skin punctures), and the average number for each male over the 7-day experimental period was used as the index of social dominance, Thus, the subject with the lowest mean number of wounds in a triad was ranked dominant, whereas that with the highest mean number was ranked lowest in the hierarchy. In addition, the average number of wounds of all males in each triad was used as a measure of intensity of aggressive interactions. Dominant animals almost invariably had no tail wounds, while subordinates had up to 25 or more. With the exception of animals that died, 25 was the maximum number of wounds assigned to any animal, since more could not be counted reliably. Whenever a death occurred, the animal was removed from the triad and assigned a daily score of 30 for the remainder of the experimental period. As shown in Table 1, the rankings support the heterosis hypothesis, i.e., F1 and F2 animals were ranked first and second, and these outbreds had significantly fewer tail wounds than inbreds (Mann-Whitney U test, Siegel, 1956) for both BC ( U = 142.5, P = 0.05) and CD (U= 99.0, P < 0.003) triad types. 2 When pooled across all three triad types, this comparison of outbreds vs inbreds was significant at the 0.0003 level of probability ( U = 1163.5). The mean number of tail wounds and the number of triads in which clearly dominant and subordinate males were found are presented in Table 2 as a function of female presence and triad type. Although all individual comparisons did not reach levels of statistical significance, an obvious trend is 2Tests of statistical significance for strain differences in the triad are only approximate, due to the impossibility of obtaining truly independent samples when subjects from different strains compete with one another.
SOCIAL DOMINANCE AND FITNESS IN MICE
115
TABLE 1 Dominance Order within Triad Types BC triads
Strain
BD triads
Mean number of tail wounds
Strain
Mean number of tail wounds
CD triads
Strain
Mean number of tail wounds
F1
0.63
F2
3.87
F1
0.27
F2
3.89
DBA
6.73
F2
0.44
BALB
5.16
F1
7.47
C57BL
2.67
C57BL
5.86
BALB
10.10
DBA
13.14
apparent in the data. More aggression occurred and more dominance hierarchies were formed in each triad type when females were present. Furthermore, when the tail-wound data were pooled across t r i a d type, this difference was highly significant ( P < 0.001). This finding of increased intermale aggression due to female presence in mice is consistent with results of other investigators who used different paradigms, cf. Goyens and Noiret (1975). The present investigation and those of DeFries and McClearn (1970, 1972) and Horn (1974) all employed laboratory mice as experimental subjects. Since data concerning the reproductive success of d o m i n a n t males derived from feral populations are currently unavailable, tests of the hypothesis that social dominance among males is a major component of Darwinian fitness in house mice are by necessity indirect. Nevertheless, evidence of heterosis for social dominance among males and increased intermale aggression due to female presence in the present study clearly support this hypothesis. TABLE 2 Effect of Female Presence on Male Aggression
Females present Triad type BC
Significance of difference in number of tail wounds
Females absent
Mean number of Number of Mean number of Number of tail wounds hierarchiesa tail wounds hierarchiesa 5.7
3
2.1
1
U
P
135
<0.07
BD
9.3
5
4.8
2
102
<0.01
CD
4.7
3
3.6
1
149
>0.10
Pooled
6.6
11
3.5
4
1159
<0.001
aNumber of triads in which dominance hierarchies were formed (five possible for each condition).
1 16
KUSE AND DE FRIES REFERENCES
Bruell, J. H. (1964). Inheritance of behavioral and physiological characters of mice and the problem of heterosis. Amer. Zool. 4, 125-138. DeFries, J. C., and McClearn, G. E: (1970). Social dominance and Darwinian fitness in the laboratory mouse. Amer. Natur. 104, 408-411. DeFries, J. C., and McClearn, G. E. (1972). Behavioral genetics and the fine structure of mouse populations. In Th. Dobzhansky, M. K. Hecht, and W. C. Steere (Eds.), "Evolutionary Biology," Vol. V, pp. 279-291. New York: Appleton-CenturyCrofts. Falconer, D. S. (1960). "Introduction to Quantitative Genetics." New York: Ronald Press. Goyens, J., and Noirot, E. (1975). Effects of cohabitation with females on aggressive behavior between male mice. Develop. Psychobiol. 8, (1), 79-84. Horn, J. M. (1974). Aggression as a component of relative fitness in four inbred strains of mice. Behav. Genet. 4, 373-381. McClearn, G. E., Wilson, J. R., and Meredith, W. (1970). The use of isogenic and heterogenic mouse stocks in behavioral research. In G. Lindzey and D. D. Thiessen (Eds.), "Contributions to Behavior-Genetic Analysis: The Mouse as a Prototype," pp. 3-22. New York: Appleton-Century-Crofts. Roberts, R. C. (i967). Some evolutionary implications of behavior. Can. J. Genet. Cytol. 9,419-435. Siegel, S. (1956). "Nonparametric Statistics for the Behavioral Sciences." New York: McGraw-Hill. Southwick, C. H. (1970). Genetic and environmental variables influencing animal aggression. In C. H. Southwick (Ed.), "Animal Aggression: Selected Readings," pp. 213-229. New York: Van Nostrand Reinhold.
BRIEF REPORT Social Dominance and Darwinian Fitness in Laboratory Mice: An Alternative Test
A. R. KUSE and J. C. DE FRIES 1
Institute for Behavioral Genetics, University o f Colorado, BouMer, Colorado 80302 Social behavior of subjects from each of three inbred strains of mice (DBA/2, BALB/c, and C57BL) was compared to that of their derived F1 and F 2 generations in standardized living units (triads). Four males (P1, P2, F1, and F2) were placed in each of 30 triads for 7 days, and dominance hierarchies were determined. In order to assess the effect of female presence on intermale aggression, females were placed in one-half of the triads. In general, considerable heterosis for social dominance was observed, and more aggression occurred among males in triads that contained females. These results are consistent with the hypothesis that social dominance is a major component of Darwinian fitness in Mus musculus.
DeFries and McClearn (1970) suggested that social dominance among males, as indexed by the number of tail wounds in the triad paradigm, may be a major component of Darwinian fitness in house mice (Mus musculus). In each o f two experiments utilizing inbred males, over 90% of the litters were sired b y dominant animals, a finding subsequently replicated by Horn (1974) and generalized to outbred males by DeFries and McClearn (1972). Although not systematically explored in this latter study, F~ hybrid males were found to be more dominant in triads than members of inbred strains or those of a segregating population. Evidence for heterosis o f aggressive behavior by laboratory mice has also been reported by Southwick (1970). As Bmell (1964) and Roberts (1967) have discussed, most of the genetic variance for fitness characters which have been subjected to directional selection is nonadditive. Thus, if social dominance has been a major component o f Darwinian fitness during the evolution of house mice, considerable heterosis should be observed for this character; i.e., the mean social dominance of F1 hybrid males should exceed the average social dominance o f the parental strains, and the F2 generation should be intermediate between the F~ and parental means (Falconer, 1960). The primary objective o f the present comunication is to report the results o f an experiment that systematically 1This work was supported in part by NIMH Training Grant MH-11167. 113 Copyright © 1976 by Academic Press, In¢ All rights of reproduction in any form reserved.
114
KUSE AND DE FRIES
assessed the relationship between social dominance and Darwinian fitness in laboratory mice using this alternative approach. During the course of the experiment, the influence of female presence on male aggression in the triad paradigm was also ascertained. The triad apparatus is a standardized social living unit composed of three mouse cages interconnected with a Y-shaped plastic manifold. This arrangement allows subjects freedom of movement among cages throughout an experimental session and facilitates formation of social dominance hierarchies among males. Thirty triads were assembled, each containing a male from two of three inbr,~d strains (BALB/cIbg, C57BL/Ibg, or DBA/2Ibg, hereafter symbolized as B, C, and D, respectively) and from their FI and F2 hybrid generations. Thus, each of 10BC triads contained four males: a BALB/c, a C57BL, and a derived Fa a n d F2. T e n BD and 10 CD triads were correspondingly constituted. In one-half of these BC, BD, and CD triads, three outbred HS females (McClearn, Wilson, and Meredith, 1970) were included to investigate the effect of female presence on male aggression. Males were isolated 3-7 days prior to testing (66 -+ 5 days of age) and then assigned to triads at random with regard to body weight. Subjects were examined daily for number of tail wounds (skin punctures), and the average number for each male over the 7-day experimental period was used as the index of social dominance, Thus, the subject with the lowest mean number of wounds in a triad was ranked dominant, whereas that with the highest mean number was ranked lowest in the hierarchy. In addition, the average number of wounds of all males in each triad was used as a measure of intensity of aggressive interactions. Dominant animals almost invariably had no tail wounds, while subordinates had up to 25 or more. With the exception of animals that died, 25 was the maximum number of wounds assigned to any animal, since more could not be counted reliably. Whenever a death occurred, the animal was removed from the triad and assigned a daily score of 30 for the remainder of the experimental period. As shown in Table 1, the rankings support the heterosis hypothesis, i.e., F1 and F2 animals were ranked first and second, and these outbreds had significantly fewer tail wounds than inbreds (Mann-Whitney U test, Siegel, 1956) for both BC ( U = 142.5, P = 0.05) and CD (U= 99.0, P < 0.003) triad types. 2 When pooled across all three triad types, this comparison of outbreds vs inbreds was significant at the 0.0003 level of probability ( U = 1163.5). The mean number of tail wounds and the number of triads in which clearly dominant and subordinate males were found are presented in Table 2 as a function of female presence and triad type. Although all individual comparisons did not reach levels of statistical significance, an obvious trend is 2Tests of statistical significance for strain differences in the triad are only approximate, due to the impossibility of obtaining truly independent samples when subjects from different strains compete with one another.
SOCIAL DOMINANCE AND FITNESS IN MICE
115
TABLE 1 Dominance Order within Triad Types BC triads
Strain
BD triads
Mean number of tail wounds
Strain
Mean number of tail wounds
CD triads
Strain
Mean number of tail wounds
F1
0.63
F2
3.87
F1
0.27
F2
3.89
DBA
6.73
F2
0.44
BALB
5.16
F1
7.47
C57BL
2.67
C57BL
5.86
BALB
10.10
DBA
13.14
apparent in the data. More aggression occurred and more dominance hierarchies were formed in each triad type when females were present. Furthermore, when the tail-wound data were pooled across t r i a d type, this difference was highly significant ( P < 0.001). This finding of increased intermale aggression due to female presence in mice is consistent with results of other investigators who used different paradigms, cf. Goyens and Noiret (1975). The present investigation and those of DeFries and McClearn (1970, 1972) and Horn (1974) all employed laboratory mice as experimental subjects. Since data concerning the reproductive success of d o m i n a n t males derived from feral populations are currently unavailable, tests of the hypothesis that social dominance among males is a major component of Darwinian fitness in house mice are by necessity indirect. Nevertheless, evidence of heterosis for social dominance among males and increased intermale aggression due to female presence in the present study clearly support this hypothesis. TABLE 2 Effect of Female Presence on Male Aggression
Females present Triad type BC
Significance of difference in number of tail wounds
Females absent
Mean number of Number of Mean number of Number of tail wounds hierarchiesa tail wounds hierarchiesa 5.7
3
2.1
1
U
P
135
<0.07
BD
9.3
5
4.8
2
102
<0.01
CD
4.7
3
3.6
1
149
>0.10
Pooled
6.6
11
3.5
4
1159
<0.001
aNumber of triads in which dominance hierarchies were formed (five possible for each condition).
1 16
KUSE AND DE FRIES REFERENCES
Bruell, J. H. (1964). Inheritance of behavioral and physiological characters of mice and the problem of heterosis. Amer. Zool. 4, 125-138. DeFries, J. C., and McClearn, G. E: (1970). Social dominance and Darwinian fitness in the laboratory mouse. Amer. Natur. 104, 408-411. DeFries, J. C., and McClearn, G. E. (1972). Behavioral genetics and the fine structure of mouse populations. In Th. Dobzhansky, M. K. Hecht, and W. C. Steere (Eds.), "Evolutionary Biology," Vol. V, pp. 279-291. New York: Appleton-CenturyCrofts. Falconer, D. S. (1960). "Introduction to Quantitative Genetics." New York: Ronald Press. Goyens, J., and Noirot, E. (1975). Effects of cohabitation with females on aggressive behavior between male mice. Develop. Psychobiol. 8, (1), 79-84. Horn, J. M. (1974). Aggression as a component of relative fitness in four inbred strains of mice. Behav. Genet. 4, 373-381. McClearn, G. E., Wilson, J. R., and Meredith, W. (1970). The use of isogenic and heterogenic mouse stocks in behavioral research. In G. Lindzey and D. D. Thiessen (Eds.), "Contributions to Behavior-Genetic Analysis: The Mouse as a Prototype," pp. 3-22. New York: Appleton-Century-Crofts. Roberts, R. C. (i967). Some evolutionary implications of behavior. Can. J. Genet. Cytol. 9,419-435. Siegel, S. (1956). "Nonparametric Statistics for the Behavioral Sciences." New York: McGraw-Hill. Southwick, C. H. (1970). Genetic and environmental variables influencing animal aggression. In C. H. Southwick (Ed.), "Animal Aggression: Selected Readings," pp. 213-229. New York: Van Nostrand Reinhold.