Variation in aggressive behavior and anatomo-physiological correlates generated by crowding without physical contact in the house mouse

Behavioral, physiological (i.e., endocrine), and anatomical consequences of crowding in mice were studied in a situation where animals were in auditory, visual, olfactory, and tactile contact but restrained from full physical interactions, to prevent overt aggression. Males that cohabited with females undisturbed by neighboring conspecifics showed greater propensity to attack same-sex intruders and had higher plasma testosterone levels than did their “crowded” counterparts, that is, males cohabiting with females and housed adjacent to other male/female pairs. In this respect, the latter animals resembled submissive males. However, a significant increase in weight of androgen-dependent target organs (i.e., seminal vesicles and preputial glands) was found in crowded males. These data indicate that despite the observed inhibition of social aggression these males are not physiologically comparable (homologous) to male mice that experienced defeat and the stress of submission during fighting. The intriguing possibility that different conversion pathway of testosterone are accelerated, as a result of social communication, in males living in these two environments and the behavioral implications of these possibilities are discussed. Finally, the parental behavior of crowded animals, although not freely interacting with each other, was disrupted, causing a marked decrease in reproductive success. In this situation a high incidence of infanticide of their offspring by both parents was observed, whereas this behavior was virtually absent in non-crowded male/female pairs.     

Agonistic rank,aggression, social context,and testosterone in male pigtail monkeys

Two groups of pigtail monkeys were merged, a third was formed, and individual males were introduced into a group in a series of experiments examining the effects of social context upon agonistic rank, aggressive expression, and testosterone levels. In the first experiment, two heterosexual groups, containing adult males unfamiliar to the other group, were merged. The two groups fought, and the smaller group was defeated. The alpha and beta males of the defeated group were singled out for repeated attack and both showed significant drops in circulating levels of testosterone. Both males were removed from the group during the first day, but testosterone levels did not recover to baseline levels for several days. The alpha male of the victorious group, on the other hand, showed a significant rise in testosterone, which was apparent only on the day following the merger. In order to study the influence of previous social familiarity on male reception into a group, another group was formed by removing males from the victorious group and placing them in a separate enclosure. The males in the new group established a dominance hierarchy unrelated to their previous social ranks with one another. Three months later, each of the six adult males remaining in the parent group was individually introduced into the new group for one day or less. Each of the males introduced into the new group accepted a social position at the lower end of the dominance hierarchy without regard to his previous rank relationships with the host males when they were all in the parent group. Even the alpha and beta males of the parent group were relegated to low rank positions in the new group, despite having ranked over each of the host males since birth. In contrast to the aggression directed at the unfamiliar males in the first experiment, a minimum of aggression was directed to the familiar males introduced into the new group in the second experiment. Although the males introduced accepted low social ranks, it appeared that each was readily integrated into the group with a minimum of aggressive interaction during the time he was scheduled to remain in the group. There were no significant changes in circulating levels of testosterone in any of the males during the introductions of familiar males to one another.     

Effects of Early Maternal Separation on Subsequent Reproductive and Behavioral Outcomes in Male Rats

To investigate effects of maternal separation on reproductive and behavioral outcomes, male Wistar rats were separated from their mothers daily for 3 hr (maternal separation; MS) or 0 hr (control) from postnatal day (PND) 1 to 14. Timing of puberty, reproductive parameters, hormone levels, and aggressive behaviors in juvenile and adult rats were examined. Contrary to expectations, there was no effect of maternal separation on any measure of aggression. However, maternal separation altered peripubertal testosterone secretion and increased mean day of preputial separation. In addition, adult MS males demonstrated less total sexual behavior. There was no difference in sperm counts or testosterone levels at necropsy on PND 56 or in adulthood, but seminal vesicle weights were increased in adult MS rats. These results suggest that early life stress may influence hypothalamic-pituitary-gonadal axis development in males, at least during peripuberty.     

Testosterone affects gaze aversion from angry faces outside of conscious awareness

Throughout vertebrate phylogeny, testosterone has motivated animals to obtain and maintain social dominance-a fact suggesting that unconscious primordial brain mechanisms are involved in social dominance. In humans, however, the prevailing view is that the neocortex is in control of primordial drives, and testosterone is thought to promote social dominance via conscious feelings of superiority, indefatigability, strength, and anger. Here we show that testosterone administration in humans prolongs dominant staring into the eyes of threatening faces that are viewed outside of awareness, without affecting consciously experienced feelings. These findings reveal that testosterone motivates social dominance in humans in much the same ways that it does in other vertebrates: involuntarily, automatically, and unconsciously.     

Performance-self-esteem and dominance behavior in mixed-sex dyads1

Past studies suggest that males tend to be more dominant than females in task-oriented, mixed-sex groups. It was hypothesized that one factor accounting for this sex difference is performance-self-esteem. Subjects were 44 male-female pairs (college undergraduates) who participated in a decision-making task. As predicted, female performance-self-esteem level was related to the dominance cluster of opinions, disagreements, and decision outcome scores (p < .035). Females were more dominant and males less dominant in dyads containing high performance-self-esteem females; the reverse was true in dyads containing low performance-self-esteem females. No relationship was found between male performance-self-esteem level and dominance. Also, with performance-self-esteem level controlled, no overall sex difference in dominance occurred. However, some sex differences were found in the relationships between outcome satisfaction and dominance for high and low performance-self-esteem subjects.     

Cardiovascular and testosterone responses to contested dominance in women

Examined cardiovascular and testosterone responses of dominant and submissive women to an acute stressor involving contested dominance. Twenty (10 dominant, 10 submissive) university students rated their dominance to a predefined reference group, participated in a task that involved debating with a trained technician, and were continuously provided with bogus feedback throughout the task concerning biochemical substances in their blood that purportedly covaried with dominance. Covariance analyses revealed that dominant women were much more reactive to the stressor in several cardiovascular parameters than those classified as submissive. Serum testosterone did not vary as a function of the experimental manipulation, and at each measurement point, dominant and submissive subjects had essentially identical serum levels of this hormone. Interestingly, however, baseline testosterone for the dominant group was related to changes in systolic blood pressure (i.e., gain scores computed as task response minus baseline values).     

Maternal aggression toward infanticidal males of different social status in wild house mice (Mus musculus domesticus)

Maternal aggression was examined in wild female mice (Mus musculus domesticus) derived from animals trapped in Alberta, Canada. Lactating females were tested for their behavior toward intruder males during the time of postpartum estrus while housed in a two-cage apparatus containing a defensible nest area. Prior to being used as intruders, sexually naive males were screened for their behavior toward a newborn pup (83% exhibited infanticide). Only infanticidal males were then housed in pairs and allowed to establish a dominance hierarchy. Dominance status was further verified by a urine marking test. The dominant and subordinate infanticidal males were then placed into a lactating female's cage and observed for 1 hr. The test was terminated immediately when a male began to attack the pups. Lactating females attacked the males in both groups, but subordinate males received more intense attacks than dominant males. Dominant males elicited significantly more fear/defense behavior than subordinate intruders. All of the dominant males and only one submissive male attacked the pups. Females were thus successful in blocking infanticide only by infanticidal subordinate males. Since females do not persist in attacking males with high fighting ability, one function of maternal aggression could be to assess the fighting, and resource holding, potential of a future mate. © 1994 Wiley-Liss, Inc.     

Effect of anosmia on reproduction in male and female wolves (Canis lupus)

Anosmia was produced in two female and three male wolves by transection of the olfactory peduncle and was confirmed by their inability to detect meat, urine, feces, anal-gland secretions, and fish emulsion. All operated animals continued to investigate the environment with their noses, to interact normally with other pack members, and to feed at levels which maintained presurgical body weights. No effect was found on reproductive physiology (females: estradiol or progesterone concentrations, ovulation, pregnancy or parturition; males: testosterone, testicular recrudescence or sperm numbers, motility or maturation). One anosmic female became dominant and although she urine-marked with a flexed leg, the rate was lower than typical for dominant females and perhaps contributed to her failure to pair-bond with the dominant male. One anosmic male raised-leg-urinated while competing for pack dominance and when kenneled away from other males. Precopulatory, copulatory, and maternal behavior were observed for one anosmic female and appeared normal. However, neither male that was sexually naive before surgery showed interest in proestrous or estrous females. The possibility that secondary degeneration of brain regions mediating sexual behavior was responsible for the failure of these males to respond was not supported. Not only was the lack of male sexual response the only serious deficit following transection, but the male which was sexually experienced prior to surgery did copulate successfully during his second postoperative breeding season despite continued anosmia. Chemosensory priming from female urine during the protracted proestrous phase, as well as urinary and vaginal odors during estrus, appear to be critical for induction of full sexual potency in sexually naive males. The importance of urine and vaginal secretions in the sexual response of experienced males is uncertain.     

Male-female differences and the influence of neonatal and adult testosterone on intraspecies aggression in rats.

Male and female albino rats were tested for intraspecies aggression without the use of shock. In the first experiment, male pairs showed more biting attacks, offensive sideways movements, and self-grooming than did female pairs; male pairs also showed more stereotyped defensive/submissive behaviors and were wounded more frequently. The second experiment examined the effects of neonatal castration and testosterone propionate (TP) administration on fighting. Males castrated at birth attacked other males less frequently than did controls when tested with TP treatment as adults. The TP given at birth to neonatally castrated males restored attacks to control levels. Females given TP as neonates did not differ from either male or female controls. Other aggressive/defensive behaviors, however, did not show this pattern. The results suggest that while the presence of testosterone during a brief postnatal period and during adulthood is necessary for attack behavior to occur, other related behaviors may not be affected in a similar manner.     

Attack and defense in conspecific fighting in tree shrews (Tupaia belangeri)

Principles of conspecific defense have been analyzed for rodents, in which specific target sites for biting by attackers on defenders serve as an important determinant of the actions involved in both attacker and defender behavior. In an effort to determine the generality of these principles, attack and defensive behaviors and target sites for biting attack were evaluated in a nonrodent species, the tree shrew (Tupaia belangeri). Brief daily and repeated conspecific dyadic encounters between adult, socially experienced males (dominants, attackers), and adult, socially naive males (subordinates, defenders) that had been transferred into the territory of the dominants, produced a polarization of attack and defense. The dominant males showed chase, chase attack, jump attack, and biting behaviors, while the subordinates displayed flight and freezing. The vast majority of bites, as well as wounds and bruises, were on the subordinates’ backs. These patterns are very similar to those previously found in rats and mice and suggest that the organization of fighting, with targets of biting (or other painful) attack serving as an important determinant of both attacker (dominant) and defender (subordinate) behavior, may show considerable generality across nonrodent as well as rodent species. Although relatively few wounds were found after 28 days of repeated and daily encounters, the subordinate tree shrews show a variety of behavioral, neuroendocrine, and central nervous changes, indicating that they are stressed by these encounters per se. Aggr. Behav. 27:139–148, 2001. © 2001 Wiley‐Liss, Inc.     

Effects of chronic administration with high doses of testosterone propionate on behavioral and physiological parameters in mice with differing basal aggressiveness

The effects of testosterone propionate, an anabolic‐androgenic steroid, on the behavior displayed during a social encounter by gonadally intact male mice were investigated. Animals were distributed into three groups according to their attack latency in a pre‐screening test (high‐, moderate‐, and low‐ attacking mice) and each group received weekly injections of 60 or 120 mg/kg of testosterone or sesame oil for 10 weeks. Behavioral tests were then carried out. Afterwards, organs were weighed and blood samples collected in order to obtain hormonal data. Treatment had a differential impact on attack in the three groups of animals. Only the high‐attacking testosterone‐treated mice showed lower total duration of attack than their controls. Those that received 60 mg/kg spent more time exhibiting exploratory behaviors. As an index of the anabolic activity of the drug, all testosterone‐treated mice had heavier kidneys and, as an index of the androgenic activity of testosterone propionate, they had heavier seminal vesicles, lighter testes, and showed higher testosterone levels in a dose‐dependent way than their controls. Hence, the effect of treatment on peripheral physiological parameters was similar in all three groups whereas behavioral effects differed depending on basal aggressiveness, considered a characteristic of coping style. Aggr. Behav. 29:173–189, 2003. © 2003 Wiley‐Liss, Inc.     

Dexamethasone can prevent stress-related litter deficits in the golden hamster

This study was designed to examine the effects of social subordination during early pregnancy in the golden hamster (Mesocricetus auratus). Primiparous females were mated to proven breeders and stressed during early pregnancy. Females were housed singly throughout gestation except for Days 4, 5, and 6 when they were paired for 10-min intervals three times each day with another female matched for age, weight, and day of pregnancy. Within each of the pairs, one female was consistently dominant to the other. Controls were exposed to a novel area instead of a conspecific. At parturition, all pups were counted, sexed, and weighed. There were no significant differences between control and dominant females' litter sizes and sex ratios. Subordinate females produced significantly smaller litters than control or dominant dams and significantly lower sex ratios than control dams. Subordinates produced fewer males than control or dominant dams, but there were no differences in the number of females produced. The entire experiment was repeated exactly except that females received a small dosage of dexamethasone in their drinking water on Days 3-7 of pregnancy. In this second group, there were no significant reductions in mean litter size, sex ratio, or pup weights among litters born to subordinate dams. These results suggest that subordinate dams produce smaller litters via selective resorption of males in utero and that the typical adrenal response to stress mediates this response.     

Behavioral effects of testosterone in relation to social rank in the male rabbit

The role of gonadal androgens in favoring the adaptation to environmental pressure, including social organization, is well known. In the rabbit, testosterone administration increases marking behavior, and its level can be affected by agonistic interaction. In this experiment, we studied the effect of subcutaneous administration of testosterone propionate (TP) (3 mg/d for 6 days) in male rabbits belonging to the same social group (6 groups of 4 animals). In 2 additional groups (4 animals each), males were injected with almond oil. The animals were observed for 6 days in seminatural conditions, then treated with TP (or oil) and observed for another 6 days. The dominant/subordinate frequency ratio of behavioral patterns was used to rank the animals. The testosterone plasma concentration was correlated with agonistic behavior after the first period of social interaction. A significant increase of marking, digging, and defensive activity was observed after TP administration in all animals independent of rank, whereas this increase was not present in animals treated with oil. Agonistic and interactive behaviors increased significantly after TP treatment only in the first‐ranking animals. This indicates the influence of social rank in the modification of behaviors involving interactions among subjects Aggr. Behav. 29:269–278, 2003. © 2003 Wiley‐Liss, Inc.     

Testosterone prevents synaptic loss in the perineal motoneuron pool in the spinal cord in male rats exposed to chronic stress

Chronic stress is known to induce disorders of reproductive neuroendocrine functions. Motoneurons of the spinal nucleus of the bulbocavernosus (SNB) in male rats play an important role in copulatory behavior. In the present study, it was examined whether chronic stress would alter synaptic organization of the SNB motoneurons and whether androgen would modify the changes under chronic stress. Five male rats were under restraint stress for 5 days per week for 3 weeks, and five males implanted subcutaneously with Silastic capsules containing testosterone were also exposed to stress. Five males served as unstressed controls. After 3 weeks of restraint stress, cholera toxin-horseradish peroxidase (CT-HRP) was injected into the bulbocavernosus muscles and animals were killed 2 days later. The spinal cords containing the SNB were dissected, processed with a modified tetramethylbenzidine (TMB) method for visualization of retrogradely transported CT-HRP, and examined ultrastructurally. Neuronal structures apposing the membranes of 150 SNB motoneurons (total for three groups) were analyzed by measuring the percentage of somatic membranes covered by synaptic contacts. The mean percentage of somatic membranes covered by synapses in males exposed to chronic stress was significantly less than that in controls or stressed males treated with testosterone. Size and number of synaptic contacts per unit length of somatic membranes in males exposed to stress were also significantly less than those in controls or stressed males treated with testosterone. There was no significant difference in any of the parameters between controls and stressed males treated with testosterone. Changes in plasma levels of testosterone showed the same profile as changes in the synaptic contacts. These results suggest that the SNB motoneurons of male rats exposed to chronic stress retain a considerable synaptic plasticity in response to androgen, and that androgen treatment can rescue the SNB system in male rats when under chronic restraint stress.     

Aggressive behavior of adult bank voles (Clethrionomys glareolus) towards conspecifics

Male and female bank voles reared in different conditions were investigated for their aggressiveness in order to show how social factors modify intermale and interfemale behavior. Singly reared males or females were paired with a tested animal for 10 min. The number of attacks and the accumulative attack times of singly reared males were higher than for females reared in similar conditions. The differences were not, however, statistically significant due to the variation among tested animals. There were significant differences in aggressiveness of females reared in various conditions before the test. Most attacks were observed in females reared with intact males. In this group, the accumulative attack time was significantly higher than that of singly reared, grouped females, or females kept with castrated or castrated-testosterone-treated males. Also, the aggression of males was affected by breeding. Both the number of attacks and the accumulative attack times were elevated in intact males kept with females. Housing of males in groups and castration significantly decreased the number of attacks of these animals. Injection of testosterone increased aggression in castrated males. It is suggested that olfactory signals in bank voles released by males increase aggression in females and the female's signals stimulate male behavior.     

Redness enhances perceived aggression, dominance and attractiveness in men's faces

In a range of non-human primate, bird and fish species, the intensity of red coloration in males is associated with social dominance, testosterone levels and mate selection. In humans too, skin redness is associated with health, but it is not known whether - as in non-human species - it is also associated with dominance and links to attractiveness have not been thoroughly investigated. Here we allow female participants to manipulate the CIELab a* value (red-green axis) of skin to maximize the perceived aggression, dominance and attractiveness of photographs of men's faces, and make two findings. First, participants increased a* (increasing redness) to enhance each attribute, suggesting that facial redness is perceived as conveying similar information about a male's qualities in humans as it does in non-human species. Second, there were significant differences between trial types: the highest levels of red were associated with aggression, an intermediate level with dominance, and the least with attractiveness. These differences may reflect a trade-off between the benefits of selecting a healthy, dominant partner and the negative consequences of aggression.     

Factors influencing sexual performance in male rhesus monkeys.

A 5-yr retrospective study of the sexual behavior of eight adult male rhesus monkeys showed that sexual vigor declined over the years but testosterone levels in peripheral vein plasma did not. Two prospective experiments were then carried out on these males during the sixth year. (a) The four poorest performers were injected daily for 28 days with testosterone propionate (1 mg/kg of body weight). There was no significant increase in level of performance, and behavior was not correlated with plasma levels of testosterone either before or 24 hr after the last hormone injection. (b) All eight males were exposed to novel nonspecific sensory stimulation during tests of sexual behavior. Eight different adult male rhesus strangers-present in the room but not in the test cage-were used as stimuli, one for each experimental test. Sexual behavior during experimental and control tests did not differ.     

Role reversal changes during the ontogeny of play fighting in male rats: Attack vs. defense

From weaning until sexual maturity, the rates at which young male rats hold each other supine during play fighting appear to become progressively asymmetrical. These changes have been previously thought to reflect an initial lack of dominance and a later development of dominance-subordinance relationships. In this paper it is shown that pairs of male rats exhibit asymmetries in playful attack and playful defense throughout development. The changes, resulting in greater asymmetry of pinning rates, are shown to result from age-dependent changes in defensive tactics; the relationship, therefore, remains constant while the form of the behavior changes. Furthermore, it is not the animals showing the highest rates of playful attack who become dominant in older ages.     

Females in charge: Effects of sex of subordinate and romantic attachment status upon self-ratings of dominance

Female, male, and mixed-sex dyads in which one member was assigned the leader role interacted and rated their own dominance throughout the interaction. The effects of gender and romantic attachment status (whether one has an exclusive dating partner or is “unattached” and free to go out with someone new) upon these self-ratings of dominance within the interaction were examined. The results showed that both leaders and subordinates perceived female leaders to be less dominant than male leaders. In addition, members of mixed-sex pairs rated themselves as less dominant than did those in same-sex pairs. Female leaders paired with males rated themselves least dominant and unattached female leaders interacting with males rated themselves least dominant of all. Female subordinates rated themselves as less dominant when with male leaders than when with female leaders, while the effect of the gender of the leader was insignificant for male subordinates. The results are discussed as evidence of a role conflict created by the contradictory roles of “dominant” leader and “subordinate” female, roles described by the sex role stereotypes prevalent in our culture.     

Rank order in pairs of communally nursing female mice (Mus musculus domesticus) and Maternal Aggression Towards Conspecific Intruders of Differing Sex

This study examined social behavior between pairs of unfamiliar lactating females, with litters of the same age, at different periods after parturition (3, 7, and 17 days). Tests were generally followed by the formation of communal rearing nests, and subsequent maternal attack on intruders of differing sex was assessed. In all three intervals lactating females showed ritualized attack with formation of clear dominance-subordination relationships before combining litters into communal nests. The dominant females in 90% of cases started to retrieve alien pups into their nests. Agonistic behavior and communal nest formation were most rapid when pups were around 3 days old. Maternal attack on conspecific intruders was mainly displayed by the dominant lactating females. Male and female intruders were equally attacked (in terms of frequency and intensity of attack), but there was less such aggression when pups were around 17 days of age. Nevertheless the topography of biting attack employed against female and male conspecific intruders was different. Females were attacked using a strategy avoiding bites to the head and ventral surface (indicative of “offensive” behavior) whereas males were severely bitten on vulnerable body regions (indicative of “defensive” behavior).