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The relationship between infanticide and pregnancy block in mice
BEHAVIORAL AND NEURAL BIOLOGY
53, 277-283 (1990)
The Relationship between Infanticide and Pregnancy Block in Mice ROBERT W . ELWOOD AND HAZEL
F.
KENNEDY 1
Department of Biology, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland, United Kingdom Newly pregnant mice are more likely to exhibit pregnancy block when females exposed to infanticidal males rather than to noninfanticidal males. These data suggest that females are able to assess the risk to their future infants and adjust their reproductive tactic. Those females that did not exhibit pregnancy block in the presence of infanticidal males suffered a greater loss of pups than those in the presence of noninfanticidal males, demonstrating the advantage of pregnancy block. Females served by infanticidal or noninfanticidal males showed no difference in pregnancy block, but if the litter was produced, there was a greater loss of pups sired by infanticidal males. © 1990AcademicPress, Inc.
are
Newly pregnant female mice (Mus musculus) may fail to implant the blastocysts if exposed to strange males (Bruce, 1959, 1960), this pregnancy block being mediated by olfaction (Bruce & Parrott, 1960). The advantage to a strange male is clear, he reduces the fitness of other males while gaining the opportunity to mate with a female. Females must also have some gain, otherwise there would be selection to avoid this manipulation by males (Bronson & Coquelin, 1980). Hypotheses concerning female gain include the promotion of exogamy (Bruce & Parrott, 1960), gaining help from the new male in rearing the young (Dawkins, 1976), and gaining a mate with a higher genetic fitness (Schwagmeyer, 1979), but these have all been subject to criticism (Labor, 1981a; Huck, 1984). Another hypothesis, that females lose a small amount of parental investment by pregnancy block, in order to avoid a greater loss at a later date by having the litter destroyed by an infanticidal male (Labor, 1981a; Huck, 1982, 1984), is tested in the present study. Dominant male mice are more likely to be infanticidal than subordinates (Huck, Soltis, & Coopersmith, 1982; vom Saal & Howard, 1982) and dominant males have been shown to be more likely than subordinates to cause pregnancy block in one study (Huck, 1982) but not in another Reprint requests should be addressed to Robert Elwood. This research was funded by a grant from the SERC of the United Kingdom. 277 0163-1047/90 $3.00 Copyright © 1990 by Academic Press, Inc. All rights of reproduction in any form reserved.
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ELWOOD AND KENNEDY
similar study (Labov, 1981b). Furthermore, female hamsters are more likely to be infanticidal than males (Rowell, 1961; Marques & Valenstein, 1976) and pregnancy block is more likely in the presence of females than males (Huck, 1984; Huck, Bracken, & Lisk, 1983). These studies are cited as support for the hypothesis that females show pregnancy block when the potential for future infanticide is high (Huck, 1984). No study, however, has directly compared the effectiveness in causing pregnancy block of known infanticidal and noninfanticidal animals. Because pregnancy block imposes a loss on the female she should be expected to allow this loss only when there is a high risk of infanticide. Female mice, for example, would gain by discriminating between infanticidal and noninfanticidal males and to show pregnancy block only when exposed to the former (Labov, 1981a). This is relevant because in mice not all males are infanticidal and those that are change to being paternal after copulation and cohabitation with a pregnant female (Elwood, 1985, 1986; Soroker & Terkel, 1988). METHODS In the present experiments all males were 3-4 months old and reared in standard conditions (Elwood, 1985). They were isolated for 7-10 days prior to being screened for their infanticidal tendencies; this involved placing a single newborn pup into the home cage of the male for 10 rain. If the pup was not harmed during this period the male was classed as noninfanticidal. If the pup was harmed by the male, this was by swift bites to the head and thorax usually resulting in immediate death of the pup. Experimenter intervention, however, ensured that the pup was humanely killed within 10 s of attack. In these screening tests 20-30% of males of each strain used were infanticidal. Males used for mating were either infanticidal or noninfanticidal and these males were housed with a single female and removed from the cage when a vaginal plug indicated that copulation had occurred (Day 0); only females with a vaginal plug were used in the experiments. A novel male, either infanticidal or noninfanticidal, was placed with each female 24-48 h later and left with the female. Two experiments were conducted each with four groups in a 2 x 2 design (Table 1). In the first experiment, the female was of the albino CS 1 strain, the stud male was CS 1, and the novel male was of the brown CBA strain. In the second, the female was CBA, the stud male was CBA, and the novel was CS1. Genetically dissimilar novel males were used because these typically produce a higher incidence of pregnancy blocking than do genetically'similar males (Parkes & Bruce, 1961). The sample sizes are indicated in Table 1. Litters arriving within 22 days of the vaginal plug being located were assumed to be fathered by the original stud male (normal gestation is 19-20 days for each strain), those ap-
279
INFANTICIDE AND PREGNANCY BLOCK
TABLE 1 Sample Size, Females Producing Litters Sired by First and Second Males, and Those That Failed to Produce a Litter for Each of the Four Experimental Groups in the Two Experiments Litters by First and second males
N
NI-I NI-NI I-I I-NI
15 19 19 16
12 17 12 15
(80%) (89%) (63%) (94%)
3 2 6 1
0 0 1 0
NI-I NI-NI I-I I-NI
31 20 24 20
18 16 15 13
(58%) (80%) (62%) (65%)
11 4 6 4
2 0 3 3
First male
Second male
No litter
Expt 1
Expt 2
Note. NI, noninfanticidal; I, infanticidal.
pearing after this date were assumed to be fathered by the novel male. In experiment 1 the parentage of the pups could be discriminated by the eye color (which shows through the closed eyes) at birth. Pups fathered by the CBA males had dark eyes and those fathered by CS1 males were albino; this confirmed the parentage based on dates of birth. Differences in pregnancy block were inferred from differences between the groups in the number of females producing litters sired by the first male. Statistical analysis was by the Fisher exact probability tests using litters as the unit for analysis not the number of pups produced or surviving (Labov, Huck, Elwood, & Brooks, 1985).
RESULTS When just those females producing litters in experiment 1 were examined there was a significant trend for those exposed to novel infanticidal males to show more pregnancy block than those exposed to noninfanticidal males (Table 1; 9/33 vs 3/35, p = .043) and when females not producing litters were included in the analysis this remained significant (10/34 vs 3/35, p = .027). The status of the first male had no significant effect on pregnancy block. In experiment 2, there was more pregnancy blocking (35%) than in experiment 1 (17%) (p = .0186). Whether this was due to differences in the strain of females or of the novel males is not clear. When just those females producing litters were examined there was a trend for more pregnancy blocking if the novel male was infanticidal (17/50 vs 8/37, p = .153) but even if those not producing litters are included this still fails to reach conventional significance (22/55 vs 11/40, p = .147). Again the status of the first male had no effect on pregnancy block.
280
ELWOOD AND KENNEDY
The trends for pregnancy block were similar in the two experiments and examination of the combined data showed that more pregnancy blocking occurred if the novel male was infanticidal rather than noninfanticidal. This occurred when only those females producing litters were considered (28/83 vs 11/72, p = ,0065) and if females not producing litters were included as indicating pregnancy block (31/89 vs 14/75, p = .0156). There were, however, no overall effects of the status of the first male on whether or not pregnancy block occurred irrespective of how that is defined. Data on the survival of litters sired by the first male and born in the presence of the second male are available for experiment 2. There is a trend for more litters to die if the second male was classed as infanticidal (20/33 vs 12/29, p = . 104). These data concern the death of the entire litter as opposed to the survival of all or of some of the pups but does not take into account the cause of death. Some pups appeared to have been killed by bites to the head and thorax in the manner that infanticidal males kill whereas others appeared to have died for other reasons. When litters were examined for signs of such an attack (even if some pups were unharmed) then more litters showed signs of infanticide if the second male was classed as infanticidal compared to those classed as noninfanticidal (21/33 vs 8/29, p = .0045). Note that these data on litters showing signs of infanticide exclude some litters that died apparently from other causes and include some litters in which only some of the pups appeared to have been bitten whereas others survived. Curiously, there is a significant difference in the survival of litters that were fathered by infanticidal males compared to those fathered by noninfanticidal males with more litters dying if fathered by infanticidal males (20/28 vs 12/34, p = .0046). Litters whose fathers were infanticidal were more likely to show signs of having been bitten compared with those fathered by noninfanticidal males (17/28 vs 12/34, p = .041).
DISCUSSION It is clear from the above data that the status of the original stud male had no effect on the probability of pregnancy block being caused by the second. In this respect the data are similar to those reported for matings by dominant and subordinate males (Huck, 1982; Labov, 1981b) and thus do not support the hypothesis that the function of pregnancy block is concerned with obtaining a mate with a higher genetic fitness (Schwagmeyer, 1979). The failure of females to produce a litter from the first mating could be due to some failure on the part of the first male. However, because of (1) the lack of difference in pregnancy block due to the status of the first male and (2) extensive unpublished observations in this laboratory that indicate that infanticidal and noninfanticidal males have the same mating ability, the significant differences in pregnancy
INFANTICIDE AND PREGNANCY BLOCK
281
block between the four experimental groups can be ascribed only to differences in the novel males. Pregnancy block is more likely if the novel male is infanticidal thus demonstrating an ability of females to discriminate between males that impose a high or low risk to her litter should the pregnancy go to term. The data are thus fully congruent with the hypothesis that pregnancy block functions to avoid future loss of parental investment (Labov, 1981b; Huck, 1982, 1984) and are the first direct test of that hypothesis. Those litters sired by the original male but born in the presence of a novel infanticidal male suffered a greater mortality than did those born in the presence of a novel noninfanticidal male. Furthermore, the evidence suggests that this increased mortality of litters is due to infanticidal attacks on the pups. These data show the adaptive advantage of pregnancy block. Apart from demonstrating the selection pressure for the evolution of pregnancy block, however, this finding is interesting from the question of what makes male mice paternal (Elwood, 1985, 1986; Elwood & Ostermeyer, 1984; Soroker & Terkel, 1988; vom Saal, 1985). Two factors have been suggested to normally inhibit infanticide in male mice one being copulation, the other cohabitation with a pregnant female. The data from the present study show that infanticidal males that have not copulated but have cohabited with a pregnant female may remain infanticidal. It would seem, therefore, that copulation followed by cohabitation is required for a complete inhibition of infanticide and onset of paternal care. Indeed, if this were not the case, and cohabitation per se could lead to a noninfanticidal state in the male, there would be no risk to a female from a strange male and thus no advantage in pregnancy block. It should be stated that in no case was the male or the female observed being infanticidal but it is doubtful if the females are harming their own offspring because (1) this would lead to a loss in fitness, (2) more litters are lost in the presence of infanticidal males, and (3) previous studies of strange intruder males in the presence of newly parturient females have reported male, but not female, infanticide (Huck et al., 1982). The most unexpected finding of the present study is that litters fathered by infanticidal males and born in the presence of another male are less likely to survive than are those fathered by noninfanticidal males. This suggests that males discriminate between pups that were sired by infanticidal or noninfanticidal males and preferentially harm the former. However, because the strange males were introduced to the cage of the female in which the original male had also previously been housed, the strange males may be discriminating on the basis of odors from the original males rather than on some aspect of the pups. That males differ in odor has been demonstrated by the finding that pups can discriminate between urine odors of infanticidal and noninfanticidal males and produce more
282
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ultrasounds when exposed to the former (Elwood, Kennedy, & Blakely, unpublished data). Further evidence of odor differences between infanticidal and noninfanticidal males comes from studies on the responses of lactating females to strange males, with infanticidal males being more likely than noninfanticidal males to be attacked (Elwood, Nesbitt, & Kennedy, unpublished data). The cause and function of this new phenomenon of preferential elimination of young sired by infanticidal males, however, are obscure and require further investigation. REFERENCES Bronson, F. H., & Coquelin, A. (1980). The modulation of reproduction by priming pheromones in house mice: Speculations on adaptive function. In D. Muller-Schwarze & R. M. Silverstein (Eds.), Chemical signals, vertebrates and aquatic invertebrates (pp. 243-265). New York: Plenum. Bruce, H. M. (1959). An exteroceptive block to pregnancy in the mouse. Nature (London), 184, 105. Bruce, H. M. (1960). A block to pregnancy in the mouse caused by proximity of strange males. Journal of Reproduction and Fertility, 1, 96-103. Bruce, H. M., & Parrott, D. M. V. (1960). Role of Olfactory sense in pregnancy block by strange males. Science, 131, 1526. Dawkins, R. (1976). The selfish gene (p. 224). Oxford: Oxford Univ. Press. Elwood, R. W. (1985). The inhibition of infanticide and the onset of paternal care in male mice, Mus musculus. Journal of Comparative Psychology, 99, 457-467. Elwood, R. W. (1986). What makes male mice paternal? Behavioral and Neural Biology, 46, 54-63. Elwood, R. W., & Ostermeyer, M. C. (1984). Does copulation inhibit infanticide in rodents? Animal Behaviour, 32, 293-305. Huck, U. W. (1982). Pregnancy block in laboratory mice as a function of male social status. Journal of Reproductive Fertility, 66, 181-184. Huck, U. W. (1984). Infanticide and the evolution of pregnancy block in rodents. In G. Hausfater & S. B. Hrdy (Eds.), Infanticide in animals and man: Comparative and evolutionary aspects. New York: Aldine. Huck, U. W., Bracken, A. C., & Lisk, R. D. (1983). Female-induced pregnancy block in the golden hamster. Behavioral and Neural Biology, 38, 190-193. Huck, U. W., Soltis, R. L.; & Coopersmith, C. B. (1982). Infanticide in male laboratory mice: Effects of social status, prior sexual experience, and basis for discrimination between related and unrelated young. Animal Behaviour, 30, 1158-1165. Labov, J. B. (1981a). Pregnancy blocking in rodents: Adaptive advantages for females. American Naturalist, 118, 361-371. Labov, J. B. (1981b). Male social status, physiology and ability to block pregnancies in female house mice (]flus musculus). Behaviour, Ecology and Sociobiology, 8, 287291. Labov, J. B., Huck, U. W., Elwood, R. W., & Brooks, R. J. (1985). Current problems in the study of infanticidal behavior of rodents. Quarterly Review of Biology, 60, 1-20. Marques, D. M., & Valenstein, E. S. (1976). Another hamster paradox: More males carry pups and fewer fill and cannibalize young than do females. Journal of Comparative Physiology and Psychology, 90, 653-657. Parkes, A. S., & Bruce, H. M. (1961). Olfactory stimuli in mammalian reproduction. Science, 134, 1049-1054. Rowell, T. E. (1961). Maternal behaviour in non-lactating golden hamsters. Animal Behaviour, 9, 11-15.
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Schwagmeyer, P. L. (1979). The Bruce effect: An evaluation of male/female advantages. American Naturalist, 114, 932-938. Soroker, V., & Terkel, J. (1988). Changes in incidence of infanticidal and parental responses during the reproductive cycle of male and female wild mice Mus musculus. Animal Behaviour, 36, 1275-1281. vom Saal, F. S. (1985). Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiology and Behaviour, 34, 7-15. vom Saal, F. S., & Howard, L. S. (1982). The regulation of infanticide and parental behavior: Implications for reproductive success in male mice. Science, 215, 12701272.
53, 277-283 (1990)
The Relationship between Infanticide and Pregnancy Block in Mice ROBERT W . ELWOOD AND HAZEL
F.
KENNEDY 1
Department of Biology, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland, United Kingdom Newly pregnant mice are more likely to exhibit pregnancy block when females exposed to infanticidal males rather than to noninfanticidal males. These data suggest that females are able to assess the risk to their future infants and adjust their reproductive tactic. Those females that did not exhibit pregnancy block in the presence of infanticidal males suffered a greater loss of pups than those in the presence of noninfanticidal males, demonstrating the advantage of pregnancy block. Females served by infanticidal or noninfanticidal males showed no difference in pregnancy block, but if the litter was produced, there was a greater loss of pups sired by infanticidal males. © 1990AcademicPress, Inc.
are
Newly pregnant female mice (Mus musculus) may fail to implant the blastocysts if exposed to strange males (Bruce, 1959, 1960), this pregnancy block being mediated by olfaction (Bruce & Parrott, 1960). The advantage to a strange male is clear, he reduces the fitness of other males while gaining the opportunity to mate with a female. Females must also have some gain, otherwise there would be selection to avoid this manipulation by males (Bronson & Coquelin, 1980). Hypotheses concerning female gain include the promotion of exogamy (Bruce & Parrott, 1960), gaining help from the new male in rearing the young (Dawkins, 1976), and gaining a mate with a higher genetic fitness (Schwagmeyer, 1979), but these have all been subject to criticism (Labor, 1981a; Huck, 1984). Another hypothesis, that females lose a small amount of parental investment by pregnancy block, in order to avoid a greater loss at a later date by having the litter destroyed by an infanticidal male (Labor, 1981a; Huck, 1982, 1984), is tested in the present study. Dominant male mice are more likely to be infanticidal than subordinates (Huck, Soltis, & Coopersmith, 1982; vom Saal & Howard, 1982) and dominant males have been shown to be more likely than subordinates to cause pregnancy block in one study (Huck, 1982) but not in another Reprint requests should be addressed to Robert Elwood. This research was funded by a grant from the SERC of the United Kingdom. 277 0163-1047/90 $3.00 Copyright © 1990 by Academic Press, Inc. All rights of reproduction in any form reserved.
278
ELWOOD AND KENNEDY
similar study (Labov, 1981b). Furthermore, female hamsters are more likely to be infanticidal than males (Rowell, 1961; Marques & Valenstein, 1976) and pregnancy block is more likely in the presence of females than males (Huck, 1984; Huck, Bracken, & Lisk, 1983). These studies are cited as support for the hypothesis that females show pregnancy block when the potential for future infanticide is high (Huck, 1984). No study, however, has directly compared the effectiveness in causing pregnancy block of known infanticidal and noninfanticidal animals. Because pregnancy block imposes a loss on the female she should be expected to allow this loss only when there is a high risk of infanticide. Female mice, for example, would gain by discriminating between infanticidal and noninfanticidal males and to show pregnancy block only when exposed to the former (Labov, 1981a). This is relevant because in mice not all males are infanticidal and those that are change to being paternal after copulation and cohabitation with a pregnant female (Elwood, 1985, 1986; Soroker & Terkel, 1988). METHODS In the present experiments all males were 3-4 months old and reared in standard conditions (Elwood, 1985). They were isolated for 7-10 days prior to being screened for their infanticidal tendencies; this involved placing a single newborn pup into the home cage of the male for 10 rain. If the pup was not harmed during this period the male was classed as noninfanticidal. If the pup was harmed by the male, this was by swift bites to the head and thorax usually resulting in immediate death of the pup. Experimenter intervention, however, ensured that the pup was humanely killed within 10 s of attack. In these screening tests 20-30% of males of each strain used were infanticidal. Males used for mating were either infanticidal or noninfanticidal and these males were housed with a single female and removed from the cage when a vaginal plug indicated that copulation had occurred (Day 0); only females with a vaginal plug were used in the experiments. A novel male, either infanticidal or noninfanticidal, was placed with each female 24-48 h later and left with the female. Two experiments were conducted each with four groups in a 2 x 2 design (Table 1). In the first experiment, the female was of the albino CS 1 strain, the stud male was CS 1, and the novel male was of the brown CBA strain. In the second, the female was CBA, the stud male was CBA, and the novel was CS1. Genetically dissimilar novel males were used because these typically produce a higher incidence of pregnancy blocking than do genetically'similar males (Parkes & Bruce, 1961). The sample sizes are indicated in Table 1. Litters arriving within 22 days of the vaginal plug being located were assumed to be fathered by the original stud male (normal gestation is 19-20 days for each strain), those ap-
279
INFANTICIDE AND PREGNANCY BLOCK
TABLE 1 Sample Size, Females Producing Litters Sired by First and Second Males, and Those That Failed to Produce a Litter for Each of the Four Experimental Groups in the Two Experiments Litters by First and second males
N
NI-I NI-NI I-I I-NI
15 19 19 16
12 17 12 15
(80%) (89%) (63%) (94%)
3 2 6 1
0 0 1 0
NI-I NI-NI I-I I-NI
31 20 24 20
18 16 15 13
(58%) (80%) (62%) (65%)
11 4 6 4
2 0 3 3
First male
Second male
No litter
Expt 1
Expt 2
Note. NI, noninfanticidal; I, infanticidal.
pearing after this date were assumed to be fathered by the novel male. In experiment 1 the parentage of the pups could be discriminated by the eye color (which shows through the closed eyes) at birth. Pups fathered by the CBA males had dark eyes and those fathered by CS1 males were albino; this confirmed the parentage based on dates of birth. Differences in pregnancy block were inferred from differences between the groups in the number of females producing litters sired by the first male. Statistical analysis was by the Fisher exact probability tests using litters as the unit for analysis not the number of pups produced or surviving (Labov, Huck, Elwood, & Brooks, 1985).
RESULTS When just those females producing litters in experiment 1 were examined there was a significant trend for those exposed to novel infanticidal males to show more pregnancy block than those exposed to noninfanticidal males (Table 1; 9/33 vs 3/35, p = .043) and when females not producing litters were included in the analysis this remained significant (10/34 vs 3/35, p = .027). The status of the first male had no significant effect on pregnancy block. In experiment 2, there was more pregnancy blocking (35%) than in experiment 1 (17%) (p = .0186). Whether this was due to differences in the strain of females or of the novel males is not clear. When just those females producing litters were examined there was a trend for more pregnancy blocking if the novel male was infanticidal (17/50 vs 8/37, p = .153) but even if those not producing litters are included this still fails to reach conventional significance (22/55 vs 11/40, p = .147). Again the status of the first male had no effect on pregnancy block.
280
ELWOOD AND KENNEDY
The trends for pregnancy block were similar in the two experiments and examination of the combined data showed that more pregnancy blocking occurred if the novel male was infanticidal rather than noninfanticidal. This occurred when only those females producing litters were considered (28/83 vs 11/72, p = ,0065) and if females not producing litters were included as indicating pregnancy block (31/89 vs 14/75, p = .0156). There were, however, no overall effects of the status of the first male on whether or not pregnancy block occurred irrespective of how that is defined. Data on the survival of litters sired by the first male and born in the presence of the second male are available for experiment 2. There is a trend for more litters to die if the second male was classed as infanticidal (20/33 vs 12/29, p = . 104). These data concern the death of the entire litter as opposed to the survival of all or of some of the pups but does not take into account the cause of death. Some pups appeared to have been killed by bites to the head and thorax in the manner that infanticidal males kill whereas others appeared to have died for other reasons. When litters were examined for signs of such an attack (even if some pups were unharmed) then more litters showed signs of infanticide if the second male was classed as infanticidal compared to those classed as noninfanticidal (21/33 vs 8/29, p = .0045). Note that these data on litters showing signs of infanticide exclude some litters that died apparently from other causes and include some litters in which only some of the pups appeared to have been bitten whereas others survived. Curiously, there is a significant difference in the survival of litters that were fathered by infanticidal males compared to those fathered by noninfanticidal males with more litters dying if fathered by infanticidal males (20/28 vs 12/34, p = .0046). Litters whose fathers were infanticidal were more likely to show signs of having been bitten compared with those fathered by noninfanticidal males (17/28 vs 12/34, p = .041).
DISCUSSION It is clear from the above data that the status of the original stud male had no effect on the probability of pregnancy block being caused by the second. In this respect the data are similar to those reported for matings by dominant and subordinate males (Huck, 1982; Labov, 1981b) and thus do not support the hypothesis that the function of pregnancy block is concerned with obtaining a mate with a higher genetic fitness (Schwagmeyer, 1979). The failure of females to produce a litter from the first mating could be due to some failure on the part of the first male. However, because of (1) the lack of difference in pregnancy block due to the status of the first male and (2) extensive unpublished observations in this laboratory that indicate that infanticidal and noninfanticidal males have the same mating ability, the significant differences in pregnancy
INFANTICIDE AND PREGNANCY BLOCK
281
block between the four experimental groups can be ascribed only to differences in the novel males. Pregnancy block is more likely if the novel male is infanticidal thus demonstrating an ability of females to discriminate between males that impose a high or low risk to her litter should the pregnancy go to term. The data are thus fully congruent with the hypothesis that pregnancy block functions to avoid future loss of parental investment (Labov, 1981b; Huck, 1982, 1984) and are the first direct test of that hypothesis. Those litters sired by the original male but born in the presence of a novel infanticidal male suffered a greater mortality than did those born in the presence of a novel noninfanticidal male. Furthermore, the evidence suggests that this increased mortality of litters is due to infanticidal attacks on the pups. These data show the adaptive advantage of pregnancy block. Apart from demonstrating the selection pressure for the evolution of pregnancy block, however, this finding is interesting from the question of what makes male mice paternal (Elwood, 1985, 1986; Elwood & Ostermeyer, 1984; Soroker & Terkel, 1988; vom Saal, 1985). Two factors have been suggested to normally inhibit infanticide in male mice one being copulation, the other cohabitation with a pregnant female. The data from the present study show that infanticidal males that have not copulated but have cohabited with a pregnant female may remain infanticidal. It would seem, therefore, that copulation followed by cohabitation is required for a complete inhibition of infanticide and onset of paternal care. Indeed, if this were not the case, and cohabitation per se could lead to a noninfanticidal state in the male, there would be no risk to a female from a strange male and thus no advantage in pregnancy block. It should be stated that in no case was the male or the female observed being infanticidal but it is doubtful if the females are harming their own offspring because (1) this would lead to a loss in fitness, (2) more litters are lost in the presence of infanticidal males, and (3) previous studies of strange intruder males in the presence of newly parturient females have reported male, but not female, infanticide (Huck et al., 1982). The most unexpected finding of the present study is that litters fathered by infanticidal males and born in the presence of another male are less likely to survive than are those fathered by noninfanticidal males. This suggests that males discriminate between pups that were sired by infanticidal or noninfanticidal males and preferentially harm the former. However, because the strange males were introduced to the cage of the female in which the original male had also previously been housed, the strange males may be discriminating on the basis of odors from the original males rather than on some aspect of the pups. That males differ in odor has been demonstrated by the finding that pups can discriminate between urine odors of infanticidal and noninfanticidal males and produce more
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