Aggression persists after ovariectomy in female rats

Aggression occurs not only in males but also in females, however, under different sex-specific stimulus and endocrine conditions. After being housed with males, female rats exhibit frequent and intense aggressive behavior toward unfamiliar rats. However, the female residents primarily attack female intruder rats, while the male residents attack males and not females. Altering the hormonal condition of the intruders can modify the behavior that they provoke from the residents. Castration of the male intruders reduces aggression from male residents, but ovariectomy of the female intruders does not alter the behavior of the female residents. Treatment of the gonadectomized intruders with gonadal steroids significantly alters the response of the male residents. Resident-intruder aggressive behavior depends on the presence of the testes in the male residents but not on the ovaries or on lactation in the female residents. Even 7 weeks after ovariectomy the female residents continue to show aggressive behavior toward female intruders. In the same time period the castrated male residents show a marked decrease in aggressive and sexual behavior.     

Influences of pre- and postnatal early life environments on the inhibitory properties of familiar urine odors in male mouse aggression

For group-living animals, discriminating among individuals and chasing unfamiliar strangers away from the home range are important to protect their territory. Previously, we reported that the familiar individual information conveyed by urine results in less aggressive behavior by resident male mice toward intruders. A resident male is aggressive toward an intruding unfamiliar castrated C57BL/6J mouse (unfamiliar castrated male [UFC]), whereas there is less aggression by the resident male when the UFC is swabbed with urine collected from the resident's cage mate. Urine is affected by various factors, including the environment. In this study, we investigated the effect of 2 living environments, the early developmental environment and the adult diet, on individual information conveyed in urine. Aggressive behavior toward UFCs was lower when UFCs were swabbed with cage mate urine or urine from a cage mate's littermate that was not living with the resident male (UFCL). Litters were cross-fostered, and we examined whether the pre- or postnatal period was important for formation of individual urine odor. The resident male displayed attack bites toward UFCs that were his cage mate's littermates but were fostered by another C57BL/6J dam. In addition, a castrated male that was reared with a cage mate (sharing the same postnatal environment) but that was not his littermate was also attacked by the resident male, suggesting that littermates that share the same pre- and postnatal environments provide similar (or identical) information, which inhibits aggression. In adulthood, even after dietary changes, the resident male showed less aggression toward UFCs when the UFCs were swabbed with the cage mate's urine, which was collected before a dietary change, indicating that individual information was not affected by dietary conditions in adulthood. In a habituation-dishabituation test, resident mice could discriminate among all pairs of mouse urine from each group. These results suggest that olfactory cues containing individual information are shared among littermates, and both the pre- and postnatal environments are important for formation of the information that inhibits aggressive behavior. This individual information might differ from the odor that is used for discriminating in the habituation-dishabituation test.     

Postisolation aggression and olfactory cues.

Aggressive maternal behavior was tested by placing intruders in the home cages of 210 individually housed lactating mice 3-8 days postpartum. The intruders were of 6 types: castrated males and females, intact males and females, mothers of 3-8 day old pups, and mothers of older pups. All fights were initiated by the resident lactating female. There were significantly fewer attacks on castrated males than on intact males (p less than .001), and fewer attacks on castrated females than on intact males and females (p less than .001, p less than .01, respectively). There were no attacks on mothers of 3-8 day old pups. Attacks on older mothers were significantly more frequent than on younger mothers (p less than .01). The results indicate that maternal aggression in albino mice is strongly influenced by the hormonal and reproductive state of the intruder.     

Territorial behaviour reflects sexual status in groups of false clown anemonefish (Amphiprion ocellaris) under laboratory conditions

Anemonefishes (genus Amphiprion) are well known as protandrous sex-changing fish. They live symbiotically with sea anemones and form a social unit that consists of a breeding pair and several sexually immature individuals with ambisexual gonads. In general, the hierarchy of the social rank is strictly maintained in a group, and this hierarchy is considered to be one of the critical factors that induce sex change or sex differentiation in anemonefishes. Field observations have shown that behavioural characteristics of anemonefishes vary depending on the environment. In this study we examined the differences in territorial aggression directed at conspecific intruders according to sexual status in the false clown anemonefish, Amphiprion ocellaris, under laboratory conditions. Resident–intruder tests were conducted on groups consisting of three anemonefish: a dominant female, a second-ranked male and a subordinate ambisexual individual. Females and males showed more aggressive behaviour than did ambisexual individuals, and behaviours were specifically directed at intruders of the same sexual status, not at those of the opposite sex. Notably, the female residents displayed fierce aggressive behaviours particularly toward female intruders, whereas male residents engaged more often in side-by-side swimming with male intruders than with female or ambisexual intruders. Ambisexual intruders were threatened by all residents, rarely attacked. We observed only few aggressive acts towards tank mates. These results suggest that sexually mature resident anemonefish in a confined space, such as under laboratory conditions, perceive intruders of the same sexual status as competitors for reproductive status and thus, dominant social rank.     

Intermale aggression of subordinate resident long-evans rats

Dominant male rats were separated from their colonies and subordinate residents were tested for aggression after a two week period. Subordinate animals showed significant increases in body weight and aggressive behavior toward intruders. Replacement of the previously dominant male led to rank reversals in three of six colonies. To assess whether two weeks of separation from the dominant male was necessary for subordinate males to exhibit aggression towards conspecifics, another intruder test was given following an additional two weeks of social housing. At the conclusion of this test, the more aggressive resident was removed and a naive intruder was immediately introduced into the colony with the subordinate male resident and again at 1, 5, and 10 day intervals. Aggressive posturing by the subordinate resident increased immediately following the removal of the dominant male, and remained at a high level throughout the subsequent intruder tests. In contrast, biting was initially low but increased steadily throughout the period of separation. These findings demonstrated that social or situational changes within a colony can greatly influence the aggression of subordinate males.     

Hormones and social behavior in the lizard, Anolis carolinensis

The purpose of this experiment was to study the effects of homologous and heterologous gonadal hormones on sexual and aggressive behavior in a reptilian species. Thirty adult male and thirty adult female lizards (Anolis carolinensis) were divided into 10 groups of six each (five groups per sex) and each group was given one of five treatments: either left intact, sham-castrated and injected with the hormone vehicle, castrated and injected with the hormone vehicle, castrated and injected with estradiol benzoate, or castrated and injected with testosterone propionate. After a week of visual isolation and daily hormone injection, animals were tested four times, twice with a stimulus animal of each sex. Females treated with estrogen were receptive, but did not court. Females treated with androgen were receptive and also courted and pursued stimulus females as frequently as males given androgen. No males in any group were receptive, and thus the female appears to be more capable of heterotypical sexual behavior than the male. Castrated males failed to court. Courtship and pursuit of stimulus females was readily stimulated in males with testosterone, and weakly stimulated by estrogen. Intact males were very aggressive, but lower levels of aggression were independent of gonadal hormones, as was subordination (head-nodding). The results for aggression and subordination are interpreted with reference to naturally-occurring Anolis behavior, and the results for sexual behavior are compared with similar experiments with mammals and birds.     

Delayed development of aggressive behavior in castrate isolated male mice

Male mice were castrated at 21–22 days of age. Intact and castrated mice were isolated to induce aggressive behavior. The incidence of fighting between paired nonisolated and isolated mice was measured at 3, 6, 12, and 23 weeks to determine the effect of time of isolation on aggressive behavior. After 3 weeks isolation, 90% of the intact isolated mice fought, but none of the castrate isolated mice fought. Aggressive behavior equivalent to that of intact isolated mice developed in the castrate mice after 23 weeks of isolation. These results suggest that the presence of gonadal androgen is important in expediting the onset of aggressive behavior in isolated mice, but its absence does not preclude its eventual development.     

Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles

We investigated in the present study the neuroendocrine correlates in intruder and resident rats of a social confrontation. Adult male Wistar rats (intruders) were introduced into the home cage of a well-trained resident to induce characteristic agonistic interactions including physical attacks prior to separation by a wire mesh. The hypothalamic-pituitary-adrenal (HPA) axis activity and the intrahypothalamic release of arginine vasopressin (AVP) were monitored via chronically implanted jugular venous catheters and microdialysis probes aimed at the hypothalamic paraventricular nucleus (PVN), respectively. Based on the behavioral data collected during the 30-min confrontation, intruders and residents were additionally classified into two different subgroups: intruders which showed almost no freezing behavior (active copers) versus those showing pronounced freezing behavior (passive copers) and residents which were either predominantly aggressive or non-aggressive. The neuroendocrine data show that social confrontation caused a significantly increased secretion of the adrenocorticotropic hormone (ACTH) into plasma in both intruder subgroups, independently of their coping strategy. In contrast, plasma ACTH in residents was increased in response to social confrontation in non-aggressive animals only, whereas aggressive residents failed to mount an ACTH response. Interestingly, plasma AVP decreased in response to social confrontation in active intruders. As measured in microdialysates, the two groups of residents and passive intruders failed to show significant changes of intra-PVN release of AVP. In contrast, an increased release of this neuropeptide within the PVN could be monitored for active intruders. The data of the present study suggest that the different interpretation of an aversive encounter results in differences in the neuroendocrine response and intrahypothalamic vasopressinergic signaling in intruders versus residents.     

Gonadal hormones modulate the display of conditioned defeat in male Syrian hamsters

It has been widely reported that gonadal hormones influence the display of aggression in Syrian hamsters; conversely, much less is known about whether gonadal hormones modulate submissive/defensive behaviors in these animals. Following social defeat, male hamsters no longer display normal territorial aggression but instead display submissive/defensive behavior in the presence of a smaller opponent, a phenomenon we have termed conditioned defeat (CD). The purpose of the present study was to examine the effect of gonadal hormones on the display of CD in male hamsters. In Experiment 1, males were castrated or sham-operated. The castrated males were significantly more submissive following social defeat relative to their intact counterparts. The increased submissive behavior in the castrated males during CD testing was particularly surprising, given the fact that they were attacked significantly less during CD training. In Experiment 2a, males were castrated and given hormone replacement. Castrated males treated with testosterone or dihydrotestosterone displayed significantly less submissive behavior following social defeat than did those treated with cholesterol or estradiol. Finally, in Experiment 2b, there was no effect of hormone replacement on aggressive behavior in non-defeated hamsters suggesting that the decrease in submissive behavior in males treated with dihydrotestosterone or testosterone is specific to being previously defeated. Taken together the data indicate that the presence of androgens reduces the display of submission in defeated male hamsters. More importantly, these findings suggest that androgens may have a protective effect against the development of depression-like or anxiety-like behaviors following exposure to an ethologically relevant stressor.     

Attractivity of male and female rats after early endocrine manipulation

Approach behavior toward males and approach behavior toward females were studied in the male rat. Adult male rats approached neonatally castrated male rats more than they approached intact males. Neonatally androgenized female rats and estrous female rats were equally approached. A preferential approach toward the androgenized female was evident when the alternative incentive was a proestrous female. These adult patterns of approach behavior appeared on Day 50 after birth. It is concluded that early endocrine manipulation influences the attractivity of the incentives.     

Variations in maternal behavior in the rat as a function of sex and gonadal state

Performance of major components of maternal care was evaluated quantitatively in several test situations for various groups of rats. Maternal behavior of concaveated ovaríectomized virgin females and castrated males was inferior on a variety of measures to that of concaveated intact virgin females. However, concaveated intact virgin females were markedly inferior to natural mothers on measures of nest building and responsiveness to an intruder. Thus, it was found that test situations other than the standard homecage test revealed previously undetected group differences and that the occurrence of pup retrieval is not a valid predictor of the performance of some major components of maternal care. In addition, it was concluded that gonadal hormones partially determine the quality of maternal responsiveness displayed by virgin females, but that gonadal hormones characteristic of the cycling female are not sufficient to increase maternal responsiveness to the level seen with natural mothers. Possible relationships between pup-induced maternal behavior and that of natural mothers are discussed.     

The role of progesterone in pregnancy-induced aggression in mice

A series of six experiments was performed in order to explore the potential involvement of progesterone (P) in pregnancy-induced aggression (PIA) displayed by Rockland-Swiss mice toward adult male intruders. In Experiment 1, circulating levels of P and aggression were low on gestation Days 6 and 10 while both the behavior and the steroid reached peak levels by gestation Day 14. By gestation Day 18 (the day prior to parturition), serum P was at its lowest level yet aggressive behavior was still intense. Also, individual differences in the display of fighting behavior by pregnant females were not related to circulating P. Experiments 2 and 3 showed that supplemental P treatment to early pregnant female mice did not advance the onset of aggression. Experiment 4 showed that P treatment promoted the onset and elevated the incidence of aggression in virgin mice, but only in those females with intact ovaries. Experiment 5 showed that the aggressive behavior of P-stimulated virgin females was qualitatively and quantitatively different from that exhibited by pregnant mice in that the former exhibited fewer attacks and lunges than the latter. Finally, Experiment 6 showed that the removal of P from aggressive, P-stimulated virgins dramatically attenuated levels of the behavior. This contrasts sharply with the continued fighting behavior observed in late pregnant P-deficient mice. Thus, although P augments aggression in female mice it apparently is not a sufficient stimulus for producing pregnancy-like aggressive behavior.     

Responses of a plethodontid salamander to conspecific and congeneric intruders

After inhabiting their home sites for a few days, both males and females of the salamander Desmognathus monticola directed agonistic behaviour toward intruding salamanders. Resident D. monticola were significantly more aggressive toward D. fuscus intruders than toward conspecific ones, although both conspecific and congeneric intruders were frequently attacked. Responses of D. monticola residents were independent of sex, and no difference was found in the behaviour of residents toward conspecific male and female intruders. Small D. fuscus intruders were attacked and injured more frequently than similar-sized D. monticola intruders and, in general, smaller-sized salamanders were the victims of aggressive attacks more frequently than larger ones. The proportions of bites on the head and tail of intruders were similar, although injuries were much more frequent to the tail than to the head. This species-related and size-related agonistic behaviour may be functional in maintaining the spatial distribution of species in communities of Desmognathus salamanders.     

Gonadal hormones during puberty organize environment-related social interaction in the male rat

This study examined the role of gonadal androgens during puberty on the development of environment-related social interaction (SI) in male rats. SI in an unfamiliar environment versus SI in a familiar environment was evaluated in young adult rats as a function of sex and gonadal status. Intact male rats at 60 days of age exhibited a differential response to the two environments, whereas SI in intact female rats at 60 days was equivalent in the two environments. Furthermore, male rats castrated as juveniles and tested for SI at 60 days displayed a pattern of environment-related SI similar to SI in intact adult female rats. This effect of juvenile castration on SI in male rats was prevented by chronic exposure to testosterone propionate (TP) over Days 30 through 60. SI in male rats castrated in adulthood, on the other hand, was not altered either 2 or 4 weeks postcastration. The results from this study indicate that pubertal secretions of gonadal androgen(s) are necessary for the development of environment-related SI in male rats. In contrast, secretions of gonadal androgens in adulthood do not appear to be critical for the continued expression of environment-related SI, as suggested by the observation that environment-related SI in male rats remains unchanged by castration in adulthood.     

Immunoreactive beta-endorphin in the plasma, pituitary and hypothalamus of young female rats on the day of estrus and intact and chronically castrated old constant estrous female rats

Immunoreactive beta-endorphin (IR-beta-ENDO) was compared in the plasma, pituitary and hypothalamus of young female rats on the day of estrus and old constant estrous (CE) female rats, and in intact and chronically castrated old CE female rats. The concentration of IR-beta-ENDO in the plasma and the content and concentration of IR-beta-ENDO in the neurointermediate lobe of the pituitary were significantly greater in the old CE female rats than in the young female rats on the day of estrus. The content and concentration of IR-beta-ENDO in the anterior pituitary and hypothalamus were similar in the two age groups. To determine if estrogen contributed to the increase in plasma and pituitary levels of IR-beta-ENDO observed in the old animals, a group of old CE female rats were castrated and compared to sham operated control CE rats. Thirty days after castration, levels of plasma, pituitary and hypothalamic IR-beta-ENDO were comparable in the intact and the chronically castrated old female rats. These data indicate that in old CE female rats, plasma and pituitary IR-beta-ENDO are significantly increased in comparison to young female rats on the day of estrus, and that these increased levels of IR-beta-ENDO observed in old female rats do not appear to be influenced by gonadal estrogen.     

Salivary cues in the mouse: a preliminary study

Two experiments were designed to explore the possible role of mouse saliva in modulating social interactions. Experiment 1 examined the investigatory sniffing behavior of an intact male toward either another intact male or castrated male. It was found that castrates received more mouth, ears-eyes, and hind sniffing than intacts. In addition, the temporal patterning of mouth and ears-eyes sniffing was found to be different for the two stimulus conditions. The findings of Experiment 2 indicated that saliva from testosterone-treated castrates contained aggression-promoting cues relative to saliva from castrated control animals. Possible sources of the salivary chemosignal were discussed.     

Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats

Whether prenatal stress (PNS) and gonadal hormones may influence depressive behavior of rats in the forced swim test was investigated. In Experiment I, adult diestrous female rats had increased immobility, which is indicative of depression, but did not show any significant difference in the duration of struggling compared to intact adult males. In Experiment 2, the behavior of adult intact, castrated, or castrated dihydrotestosterone (DHT)- or estrogen (E2)-replaced offspring of dams that were restrained under lights for 45 min on gestational day 18 (PNS) or were not subjected to gestational stress (non-PNS, control condition) were compared. There were no effects of PNS, but DHT and E2 produced anti-depressant effects on behavior of male rats. Castration decreased struggling and increased immobility compared to intact rats. DHT or E2 replacement was able to partially reinstate struggling and immobility behavior but not to levels of intact males. In Experiment 3, behavior of PNS or control rats that were in proestrus or were ovariectomized and DHT, E2, or vehicle-replaced were compared. Ovariectomy decreased struggling and increased immobility compared to that of proestrous rats. E2 or DHT to control females increased anti-depressant struggling behavior compared to ovariectomized control or PNS rats administered vehicle, which demonstrated greater duration of struggling than did E2-primed, PNS rats. E2 or DHT administration decreased immobility of PNS and control females. These findings suggest that E2 and DHT have some anti-depressant effects but that modest PNS may alter E2's ability to alleviate some depressive behavior in female, but not male rats.     

The social interactions of adult conspecifics with an adult XY gonadal dysgenetic chacma baboon (Papio ursinus)

Two separate behavioral studies on an XY gonadal dysgenetic chacma baboon were carried out. In the first experiment the focal subject was treated identically as the control females by her adult male test partners. In contrast to the controls in this experiment the dysgenetic animal reciprocated the agonistic behaviors directed by the males toward her. In the second study intact and castrated males as well as ovariectomized females served as controls for the dysgenetic subject in tests with ovariectomized adult females. The stimulus females presented more to both classes of males than either the subject females or the gonadal dysgenetic individual, suggesting that the focal subject was treated by other female conspecifics as a female.     

Male <Emphasis Type="Italic">Betta splendends</Emphasis> are equally aggressive toward neighbors and strangers

Male Siamese fighting fish, Betta splendens, are known for their ferociousness when defending their territories against male or female conspecific intruders. The aim of this study was to investigate whether this species exhibits the dear enemy phenomenon, where territorial males would be less aggressive toward neighbors with already established territories than toward complete stranger males. In experiment 1, a male Betta was placed in an aquarium. A second male was placed in a glass jar that was fitted in one corner of the aquarium. After 24 h, a cover was placed around the jar, and then removed after 1 h. Alternatively, the jar male was replaced with a different male of a different color while the jar was covered. The frequency and duration of opercular expansion by the aquarium male were recorded. In experiment 2, two male Bettas were placed, each in a half of a large aquarium that was equally divided by a clear, perforated Plexiglas divider. After 24 h, one male (intruder) was transferred into the other male’s (resident) half. In another variation of the experiment, the intruder was a stranger male Betta that the resident male had never encountered before. The opercular expansion and duration were scored for the resident male. The results indicated that male Siamese fish reacted similarly to familiar and stranger males. This lack of dear enemy effect in Siamese fish could be due to an inability to discriminate between neighboring males and non-neighboring males. Alternatively, territorial males could be equally aggressive to all intruders because all intruders represent equal danger.     

Sexual preferences of male hamsters (Mesocricetus auratus) for conspecifics in different endocrine conditions

The behavioral responses of sexually experienced male hamsters toward a pair of anesthetized conspecifics were investigated. Males spent significantly more time licking, sniffing, and mounting neonatally and adult castrated males than intact males. Adult castrated males receiving oil injections were preferred over castrates receiving exogenous testosterone propionate (TP). Ovariectomized females were preferred over intact males, adult castrated males, or spayed females receiving exogenous TP. It was concluded that the absence of an androgen-dependent factor(s) renders an animal more sexually attractive.