Infanticide: Genetic, developmental and hormonal influences in mice

Physiology & Behavior, Vol. 27, pp. 921-927. PergamonPress and BrainResearch Publ., 1981.Printedin the U•S.A.

Infanticide: Genetic, Developmental and Hormonal Influences in Mice I BRUCE SVARE AND MARTHA MANN

D e p a r t m e n t o f Psychology, S U N Y - A l b a n y , Albany, N Y 12222 R e c e i v e d 6 M a y 1981 SVARE, B. AND M. MANN. Infanticide: Genetic, developmental and hormonal influences in mice. PHYSIOL. BEHAV. 27(5) 921-927, 1981.--DBA/2J and androgen-deficient C57BL/6J mice were examined for their response to newborn (1-3 day old) Rockland Swiss (R-S) albino mouse pups. Significantly more 70-90 day old C57BL male mice killed young as compared to similarly aged DBA males (80% vs 30% respectively). Adult, 70-90 day old, female mice of both strains typically retrieved newborn young to the nest site. Adult castration significantly reduced infanticide in males of both strains while exposure to testosterone (T)-containing silastic capsules restored it. Treatment of adult ovariectomized female mice of both strains with T-containing capsules significantly elevated the exhibition of pup killing. When tested for infanticide at 25, 35, 45, 55 or 65 days of age, few males of either strain killed young at 25 days of age. However, beginningat 35 days of age, significantly more C57BL males killed young at every age as compared to DBA males. Moreover, C57BL males exhibited an earlier developmental onset of adult-like levels of infanticide than DBA males (45 vs 65 days of age respectively). Finally, older (4.5 to 7 months of age) DBA males exhibited levels of pup-killing identical to that of younger (2 months of age) C57BL males (70%). The findings are discussed in terms of their relationship to other sexually dimophic T-dependent masculine behaviors. The potential importance of infanticide for rodent reproductive strategies and population regulation is also considered. Infanticide Ovariectomy

Inbred mice Males Females Testosterone Differentiation Population regulation

I N F A N T I C I D E , or the killing of young, and infant abuse in general have been observed in numerous species including humans, primates, rodents, insects, and fish (cf. [11, 16, 17] for recent reviews). The behavior may function to regulate population size, enhance reproductive success, optimize the postnatal rearing environment, or provide a food source (cf. [17]). Regardless, in contrast to our understanding of other forms of agonistic behavior such as the ritualized aggression observed in lactating females (maternal aggression) and the fighting seen among males (intermale aggression) and females (interfemale aggression) we know little about the factors that govern infanticide. In laboratory mice, the subjects of the present investigation, the killing of young by adults is sexually dimorphic in that males tend to exhibit the behavior whereas females do not. In Rockland-Swiss (R-S) Albino mice, approximately 35 to 50% of adult males kill conspecific young while the remaining 50-60% either ignore or are maternal toward newborns [9]. In contrast, female mice seldom exhibit infanticide (5%) and usually exhibit parental behavior including retrieval, licking, and nursing of the young. The difference between the sexes with respect to infanticide is modulated by differences in both adult (activational) and perinatal (organizational) levels of the primary androgen testosterone ~I'). Castration of adult males reduces infan-

Development

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ticide while testosterone propionate (TP) restores it with high doses more effective than low doses [13]. Also, depending upon the dose and duration of steroid exposure, 35 to 100% of female mice can be induced to kill pups by the administration of TP in adulthood [6, 28]. Male hormones also exert their effects on infanticide during the perinatal period. Adult male mice that do not kill pups (50-60%) usually respond in a maternal fashion and the longterm administration of T to these animals does not induce infanticide [13]. Also, recall that 100% of adult female mice will kill pups following chronic T exposure in adulthood [28]. Because males have been exposed to gonadal steroids during early life while females have not, the above findings suggest that perinatal hormone exposure may be having a suppressive effect upon levels of pup-killing behavior in the adult male. Recent research supports this hypothesis. Neonatal castration of male mice increases the proportion of animals exhibiting infanticide in response to adult testosterone and shortens the duration of steroid treatment needed to induce the behavior [14,21]. The later in postnatal life that castration is performed, the greater the suppression of infanticide [14]. Conversely, T treatment of neonatal female mice lowers the proportion (30-50%) of animals exhibiting infanticide in response to adult T and lengthens the duration of adult steroid treatment needed to promote the behavior [14,21]. Also, the

1This work was supported in part by a Research Grant from the Harry Frank Guggenheim Foundation, by Grant BNS80-08546 from NSF, and by Grant AG01319 from NIA. Portions of the data appearing here were presented at the 1981 meeting of the Behavior Genetics Association, Purchase, NY. Send repnnt requests to Dr. Bruce Svare, Department of Psychology, SUNY-Albany, 1400Washington Avenue, Albany, NY 12222. •

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C o p y r i g h t © 1981 B r a i n R e s e a r c h P u b l i c a t i o n s Inc.--0031-9384/81/110921-07502.00/0

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earlier in life that females are exposed to T, the greater the attenuation of infanticide [14]. Finally, it has been recently reported that male mice having developed in utero contiguous to two male fetuses are less likely to exhibit infanticide than are males having resided adjacent to two female fetuses [30]. It has been suggested that T produced by the fetal testes diffuses from the amniotic fluid surrounding the male across the amniotic membranes into the compartment of proximate fetuses [15]. Levels of T in the amniotic fluid surrounding females contiguous to two males have been found to be elevated [31]. If the same holds true for males contiguous to two males, the above data would agree with the findings showing that neonatal exposure to T reduces later pup-killing behavior. The above findings therefore indicate that there is an inverse relationship between perinatal T levels and infanticide. This is especially interesting in light of what is known for other sexually dimorphic T-dependent behaviors. F o r copulatory behavior and intermale aggression, early T exposure is known to facilitate later behavioral responsiveness to T while the absence of such exposure leads to a lesser degree of responsiveness (cf. [4, 8, 10]. To further study the factors that govern infanticide in mice, we have been examining the behavior in C57BL/6J and DBA/2J mice. These two strains have been selected for study since they are known to exhibit qualitative and quantitative differences in circulating T and T-dependent behaviors. C57BL males appear to be adrogen-deficient as compared to DBA males in that they have smaller testes, lower pubertal and adult circulating T levels, an unusual decrease in the yield of spermatogenesis with age, a high testicular content of esterified cholesterol, low sexual and intermale aggressive behavior, and they do not elicit the androgendependent, pheromonally mediated pregnancy block in recently inseminated females (cf. [2, 3, 5, 7, 18, 22, 23, 24, 25]). They therefore provide an ideal tool for examining genetically determined variation in testicular function and the development of infanticide. EXPERIMENT 1 In the following experiment, we explored sex and strain differences in infanticide by confronting adult male and female C57BL and DBA mice with newborn mouse pups. It was hypothesized that (1) males within each strain would kill young while females would be maternal and (2) C57BL males, by virtue of their androgen insufficiency, would exhibit lower levels of infanticide than DBA males. METHOD Inbred-derived male and female DBA/2J a.nd C57BL/6J mice were used in these experiments. The mice were born and reared in our laboratory at the State University of New York at Albany and were descendents of animals originally purchased from the Jackson Laboratory. Litters from timed-mated females were weaned at 21 days of age (Day 0 was considered the day of birth) and group housed (5-7/cage) with same sex littermates until testing. The mice were housed in 111/2 × 71/2 × 5 in. polyproylene cages, the floors of which were covered with pine shavings. The animals were provided with food (Charles River Mouse Chow) and water ad lib. The room temperature was controlled at 24___I°C and the colony room was maintained on a 12/12 hour light/dark cycle with lights on at 7:00 a.m. In the present experiment, forty male and forty female

mice within each strain were used. The animals were isolated at 70-90 days of age. At 8:00 a.m. the following day ti.e., 24 hrs following isolation) the animals were tested for infanticide according to the method of Svare, Bartke and Gandelman [29]. One 1-3 day old Rockland-Swiss (R-S) Albino mouse pup was placed into each animal's cage in the corner of the cage furthest from the area occupied by the adult. (Rockland-Swiss mouse pups were used in order to provide :t standard stimulus animal (see Simon [26] for a discussion of this technique in behavior genetic experimentation)). It should also be noted that the strain and sex of the stimulus pup do not influence the incidence of infanticide in C57BL and DBA mice (Svare and Mann, unpublished observations). The pup was left in the cage for a period of 15 min (periods of testing as long as 4 hrs do not appreciably influence the incidence of infanticide in the two strains) and the adult's behavior was classified into one of the following categories: (1) Retrieve, retrieving the pup to the nest site; (2) Kill, killing and at least partially cannibalizing the pup; (3) Ignore. neither killing nor retrieving the pup. RESULTS Figure 1 shows that there were strain and sex differences in the percentage of animals that exhibited infanticide. In contrast to the low level of pup-killing observed in female mice (<13%), significantly more males within each strain tended to exhibit infanticide, X2(1)->4.4, p<0.05. Instead of exhibiting pup-killing, females within each strain retrieved newborns. More importantly, however, it is evident that, contrary to our initial speculation concerning the direction of strain differences in the exhibition of infanticide (i.e., DBA males would exhibit infanticde at higher levels than androgen-deficient C57BL males), significantly more C57BL males exhibited the behavior than did DBA males (80% vs 30% respectively, X2(1)= 14.8, p<0.001. Also, significantly more DBA males exhibited retrieval than did C57BL males, X2(1)=8.21, p <0.01. The topography of infanticide consisted of bites to the back and head of the pups and usually was followed by consumption of all or part of the newborn. Maternal retrieval typically consisted of carrying the pup to the next site followed by hovering over the pup in a nursing posture. Previous work with outbred mice has shown that the presence of gonadal hormones in adult life promotes infanticide. Castration of adult males reduces the behavior and, in a dose-dependent manner, TP restores it (cf. [14]). Also, female mice can be induced to exhibit pup-killing by exposure to TP in adulthood [6,28]. In the following experiment, we explored whether or not infanticide in inbred C57BL and DBA male and female mice is also promoted by testicular hormones. EXPERIMENT 2 METHOD At 70-75 days of age, 48 male and 28 female C57BL mice and 48 male and 28 female DBA mice were used. Within each sex and strain the animals were randomly divided into two separate groups. One group of males (N--24) and one group of females ( N = 14) within each strain were gonadectomized under ether anesthesia and implanted subcutaneously in the nape of the neck with a 10 mm silastic capsule (Dow Coming, 0.062 in. i.d.) that contained 5 mg testosterone (T) suspended in sesame oil. The ends of the capsule were sealed

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30 20 with Dow Coming Silicone Type A adhesive. This size implant was used since it previously has been shown to maintain a variety of androgen-dependent behaviors in the male mouse including infanticide and intermale aggression (cf. [1,13]). The other groups of males (N=24) and females (N= 14) within each strain were also gonadectomized but instead were implanted with a 10 mm oil-filled silastic capsule. The animals were isolated immediately following surgery as previously described. They were tested for infanticide every 10 days for a maximum of 3 tests (30 days of hormone exposure) or were terminated from testing when they exhibited killing of the neonate.

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FIG. 2. The results of Experiment 2 showing the cumulative percentage of adult 70-75 day old gonadectomized C57BL/6J and DBA/2J male and female mice that exhibited infanticide following exposure to a 10 mm length silastic implant containing testosterone (T) or oil. Following receipt of the implant, the animals were tested for their reaction toward a single (1-3 day old) Rockland-Swiss Albino mouse pup at 10 day intervals for a total of 3 tests. Each test was 15 min in duration.

RESULTS One animal died within each of the male groups leaving a total of 23 animals/group. Also, one T-treated and one oiltreated DBA female died leaving a total of 13 animals in each of those groups. Figure 2 shows the cumulative percentage of males and females that killed young as a function of strain and T or oil treatment. As seen in the figure, T-treated gonadectomized males and females within each strain killed young while their oil-treated counterparts did not, X2(I)_->4.4, p<0.05. The pup-killing behavior seen in the T-treated females was identical to that normally observed in males with biting attacks directed to the back and head of the newborns and consumption of all or part of the pup. Instead of exhibiting infanticide, oil-treated gonadectomized males and females typically retrieved young. While more T-treated C57BL males killed young as compared to steroid-treated DBA males (90% vs 60% respectively, X2 (1)=4.3, p<0.05), the strains did not differ from each other with respect to the incidence of pup-killing in the T-treated female groups (65% and 50% respectively for DBA and C57BL females). Significantly more T-treated C57BL males exhibited infanticide than similarly treated C57BL females (90% vs 50% respec-

tively, ×2(1)=5.97, p<0.02). Finally, there was a slight tendency for an elevated level of infanticide in T-treated castrates of each strain (compare with the results of Experiment 1). The findings therefore show that infanticidal behavior in inbred mice, like outbred mice, is modulated by the presence or absence of adult testosterone. One way in which to explore the observed strain differences in levels of infanticide is to examine the ontogeny of the behavior in males. Selmanoffet al. [23] found that DBA males exhibited an earlier pubertal rise in circulating T as compared to C57BL males. Compared with androgen levels on Day 30, DBA males in their study exhibited a statistically significant pubertal increase by Day 35 while C57BL males did not experience a similar change until Day 70. In view of these finding, one might expect to see an earlier developmental onset of infanticide in male DBA mice. A crosssectional analysis was employed in the following experiment in order to examine the above hypothesis.

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FIG. 3. The results of Experiment 3 showing the percentage of 25, 35, 45, 55 and 65 day old male C57BL/6J and DBA/2J mice that killed, ignored, or retrieved a single newborn (1-3 day old) Rockland-Swiss Albino mouse pup. Following 24 hrs of isolation, separate groups of animals from each age and strain were tested for their reaction toward the newborn.

EXPERIMENT 3 METHOD

Litters of inbred C57BL and DBA male mice were generated in our laboratory as previously described. Within each strain, litters were randomly assigned to one of 5 groups, each group being differentiated by the age at which the animals were tested for infanticide. The animals were tested at either 25, 35, 45, 55 or 65 days of age. The number of animals employed at each of the above ages for each strain was 20, 20, 21, 20 and 21 respectively for DBA males and 21, 19, 21, 18 and 20 respectively for C57BL males. A single test for infanticide was conducted at the appropriate age following 24 hrs of isolation. RESULTS

Figure 3 shows the incidence of pup-killing, ignoring, and retrieval of young in 25, 35, 45, 55 and 65 day old C57BL and DBA male mice. Once again, it is evident from this portrayal that contrary to our earlier speculation, but consistent with the results of Experiment 1, C57BL males exhibited higher levels of infanticide than DBA males. With the exception of Day 25, when few animals of either strain killed young, significantly more C57BL mice exhibited infanticide at each of

the other ages tested, xZ(l)~4.3, p<0.05. In contrast to the infanticidal behavior exhibited by C57BL mice, significantly more DBA animals ignored young than did C57BL males al 35, 45 and 55 days of age, X~(1)~3.9, p.--O.05. Also, both C57BL and DBA males exhibited a significant increase in the incidence of infanticide with advancing age, X'-'(4)==21.0. p<0.01, and X2(4)=9.9, p<0.05, respectively. However-, contrary to what we expected, C57BL males exhibited an earlier development onset of pup-killing than DBA males. When compared to levels of infanticide at 25 days of age, the developmental increase attained statistical significance at Day 45 for C57BL males but not until day 65 for DBA males, X"(1)~4.6, p<0.05. Finally, the figure also shows that the incidence of ignoring declined with advancing age for both strains, X2(4)=>9.8, p<0.05. The previous findings suggest that DBA males, compared to their C57BL counterparts, exhibit a developmental lag with respect to the onset of infanticide. Although DBA males exhibited a lower incidence of the behavior than C57BL animals between 35 and 65 days of age, they none-the-less showed a significant increase in the behavior with advancing age. The question remains then as to whether or not older DBA males would ever attain the high levels of infanticide exhibited by C57BL animals, l f a developmental lag does account for the difference between C57BL and DBA males, then one might expect to observe an increase in the incidence of pup-killing in older DBA males. In the following experiment, we examined this hypothesis by testing DBA and C57BL males for infanticide at ages beyond those used in the previous experiments. EXPERIMENT 4 METHOD

Litters of C57BL and DBA male mice were randomly assigned to one of three groups within each strain. Each group was differentiated on the basis of the age at which the animals were tested for infanticide. The animals were tested at 2, 4.5 and 7 months of age. The number of animals used at each of the above ages for each strain was 26, 25 and 27 respectively for DBA males and 21, 26 and 26 respectively for C57BL males. RESULTS

The incidence of infanticide in 2, 4.5 and 7 month old DBA and C57BL male mice is illustrated in Fig. 4. DBA males exhibited a significantly lower level of pup-killing than C57BL males at 2 months of age, X2(1)= 11.0, p<0.001, thus supporting our previous findings. However, by 4.5 months of age, a significant increase in the level of the behavior was observed in DBA males (vs 2 months, X~(1)=6.4, p<0.02) to the extent that males of the two strains were virtually identical to each other with respect to the incidence of the behavior at 4.5 and 7 months of age (about 70% of the animals killed young). Thus, while DBA males exhibit a developmental lag in the incidence of infanticide, they apparently are not unresponsive to the factor(s) that govern(s) the behavior. GENERAL DISCUSSION It is now agreed upon by most behavioral biologists that individual differences in genotype account, at least in part, for variation in many behavioral traits observed in a particu-

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FIG. 4. The results of Experiment 4 showing the percentage of 2, 4.5 and 7 month old male C57BL/6J and DBA/2J mice that killed, ignored, or retrieved a signle newborn (1-3 day old) Rockland-Swiss Albino mouse pup. Following 24 hrs of isolation, separate groups of animals from each age and strain were tested for 15 min for their reaction toward the newborn.

lar population. Because animals within any single inbred mouse strain are virtually isogenic (i.e., genetically identical to each other), they permit a degree of genetic control which is not available in other species. Thus, the comparison of animals in any two or more strains allows for representation of a fairly large sample of the behavioral gene pool with the advantage of genetic identity inherent in inbred strains. The present findings indicate that males of the C57BL/6J and DBA/2J lines, two of the oldest and most frequently utilized inbred strains of mice in biobehavioral research, exhibit striking differences in the exhibition of an important agonistic and reproductive behavior, infanticide. Thus, the tendency to kill young, like so many other social behaviors investigated in lower animals, is modulated by genotype. According to a number of lines of research (see introductory section), C57BL male mice are androgen-deficient when compared to DBA male mice in that they have lower circulating levels of pubertal and adult testosterone (T) and exhibit lower levels of sexual and aggressive behavior. Because there is a positive relationship between levels of adult T and the activation of infanticide in the mouse [28], we originally speculated that C57BL males would probably exhibit lower levels of infanticide and a delayed onset of the behavior. To the contrary, the present findings clearly show an unex-

pected reversal of the hypothesized direction of results. When tested for their response toward standard stimulus 1-3 day old Rockland-Swiss (R-S) albino mouse pups, significantly more 70-80 day old C57BL male mice killed young as compared to similarly aged DBA males (80% vs 30% respectively). Males of the DBA strain apparently exhibit a developmental lag with respect to an onset of infanticide. When separate groups of animals from each strain were tested for pup-killing at 25, 35, 45, 55 or 65 days of age, few males of either strain killed young at 25 days of age. Beginning at 35 days of age, however, significantly more C57BL males killed young at every age as compared to DBA males. Also, C57BL males exhibited an earlier developmental onset of adult-like levels of infanticide than DBA males. When compared to levels of the behavior at 25 days of age, the developmental increase attained statistical significant by Day 45 for C57BL males but not until Day 65 for DBA males. However, DBA males do eventually attain the high levels of infanticide exhibited by C57BL animals since approximately 70% of older (4.5 to 7 months of age) DBA males were found to exhibit pup-killing. In addition, as expected from previous work with outbred mice (cf. [13,28]), we observed a sex difference within each strain in that adult 70-90 day old females rarely killed young but instead exhibited maternal retrieval. Also, as expected, the behavior was demonstrated to be modulated by the presence or absence of adult T. Adult castration prevented the appearance of infanticide in males of each strain while exposure to T-containing silastic capsules restored it. Moreover, treatment of adult ovariectomized female mice of each strain with T-containing capsules elevated the exhibition of the behavior. How T modulates infanticide in the mouse is not known, but T effects on any of the various senses, especially the olfactory system, may be important. The important question which must be addressed here concerns how genes program strain differences in infanticide. The answer to this question may reside in numerous factors, the most prominent of them being maternal environmental, situational, hormonal, and neural in nature. First, it is well-known that strain differences in rodent behaviors ranging from intermale aggression to alcohol preferences are mediated, in part, by differences in the maternal environment (cf. [19, 20, 27]). However, preliminary results from our laboratory suggest that this is not the case for infanticide. Reciprocally crossed animals exhibit low levels of the behavior regardless of the pre- and postnatal rearing environment (i.e., C57BL or DBA) and cross-fostered animals perform true to their genotype (Svare and Broida, unpublished observations). Second, although simple situational and experiential factors also may be responsible for the observed strain differences in infanticide, exploration of some of the more obvious ones has thus far failed to reduce genotypic differences. For example, extended exposure to young or confrontation with different age or strain pups has no effect on the strain difference in infanticidal behavior (Svare and Mann, unpublished observations). Third, genotypic variation in infanticide may be related to temporal differences in the secretory pattern of T during certain key developmental stages. While low adult levels of circulating T may account, in part, for observed deficits in intermale aggression and copulatory behavior exhibited by C57BL males (cf. [22, 23, 24]), differences in pubertal and adult T levels probably do not account for genotypic differences in infanticide. This follows from the fact that there is a demonstrated positive dose response relationship between T and infanticide [28] and C57BL males exhibit low circulating levels of

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T and a rapid developmental onset of the behavior while DBA males experience the converse (i.e., high T and a developmental lag). Because our previous work [21] as well as that of others [13,30] shows that high levels of circulating T during perinatal life suppresses infanticide, the most parsimonious interpretation of the present findings is that the rapid developmental onset of pup-killing in C57BL males may be related to deficiencies in T secretion during perinatal life. Thus, in spite of the fact that C57BL male mice exhibit low pubertal and adult ~ levels, they are highly sensitive to their own androgens at least with respect to infanticide. Conversely, by virtue of their greater exposure to T perinatally, DBA males may be less sensitive to the infanticidepromoting qualities of T but more responsive to its aggression and libido-promoting characteristics. Thus, for DBA males, one would predict that only extended developmental exposure to the steroid would overcome their presumed lack of responsiveness to its infanticide-promoting quality. Our findings demonstrating that older DBA males (>4.5 months of age) exhibit C57BL-like levels of infanticide would seem to fit this interpretation. Fourth, we cannot rule out the possiblity that strain differences in infanticide may be mediated by the manner in which genes modulate the impact of T on the other T-dependent processes in central neural tissue. Differential turnover rates and/or relative levels of a variety of neurotransmitters, enzymes, and other hormones, as well as differential aromatization and/or reduction of T may account for the present strain differences. It is interesting to speculate as to what impact infanticide and genotypic variation in the behavior may have upon both individuals and entire populations. Hrdy I16,17] has pro-

posed that the behavior in male primates may serve an important reproductive strategy. In the case of H o n u m a t t langurs, males frequently are known to kill young that are being cared for by females, thus increasing the male's reproductive success at the expense of the former leader (presumably the father of the infant killed), the mother and the infant. Infanticide would seem to be an optimum strategy tbr the male since female langurs begin ovulating soon after the young are removed. If one assumes that the usurping male is stronger than the dead infants' father, the distribution of the usuper's genes would benefit the population over the long run. Whether or not the above explanation for infanticide is also suitable for the mouse is purely speculative at this time. It is interesting to note, however, that the androgen-deficienl C57BL male mouse is incapable of eliciting the testosterone-dependent, pheromonally mediated pregnancy block in recently inseminated females I51. In view of this deficit, high levels of infanticide would appear to be one of the few alternative strategies available to the C57BL male. Thus, the behavior may have evolved in this strain as a compensatory mechanism in order to ensure male reproductive success. Finally, in a population context, genotypic variation in infanticide would seem to have important implications. Under conditions of high population density, it would be of obvious value to have selection for " h i g h " infanticide genes. Conversely, when population density is low, it would be advantageous to have selection for "'low" infanticide genes. While overly simplistic in nature, the above explanation may be one mechanism whereby rodent populations can control their numbers and reproductive fitness.

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