Hypothalamic levels of LHRF in male mice of differing social status and from individual housing

Swiss male mice were individually-housed or maintained in groups of 8 from weaning until 80 days of age. At this time, the grouped mice were allocated to new groups of 5–6 previously unfamiliar individuals. Identified dominants were then caged with two clearly submissive males for 1 week. At this time hypothalamic samples were taken from the dominant and one subordinate and from a number of long-term individually-housed males. A radio- immunoassay for LHRF was carried out. The levels of this hypothalamic releasing factor were significantly higher in both dominant and subordinate grouped mice than in ‘isolates’. Mice of differing social status showed comparable titres of this hormone. The results suggest that social conflict and/or disturbance augments this factor in mice irrespective of the social status achieved by individual animals.     

Effects of Dominant/Subordinate Social Status on Formalin-Induced Pain and Changes in Serum Proinflammatory Cytokine Concentrations in Mice

Current investigations regarding social stress primarily focus on the health consequences of being in stressful social hierarchies. The repetitive nature of social conflicts seems to favor an induction of hyperalgesia or hypoalgesia, both in rodents and humans. Additionally, social conflicts may affect the immune system. In order to better establish the pain and immune responses to stress, the present study implemented a sensory contact model on 32 male BALB/c mice. Subsequent to establishing a dominance/submissive social relationship, each mouse was injected with formalin (20 μl, 2%) and their pain behavior was scored and serum concentrations of proinflammatory cytokines IL-1 and IL-6, and corticosterone were also measured. Test results revealed that subordinate mice were hypoalgesic during chronic phase of formalin test compared to control and dominant mice (P<0.05). On the other hand, subordinate mice were hyperalgesic compared to dominant mice during the whole acute phase of formalin test (P<0.05). Corticosterone, IL-1 and IL-6 concentrations were much higher in serum of dominant and subordinate mice than in the control group (p<0.05). The results indicated that, although both dominant and subordinate animals displayed an increase in serum corticosterone and proinflammatory cytokines during social interactions, their response to pain perception differently was affected with the social status.     

Do Male Mice Prefer or Avoid Each Other's Company? Influence of Hierarchy, Kinship, and Familiarity

In the laboratory, individual housing of male mice who otherwise show aggression is common practice. Because mice are a social species, the question arises whether this procedure is right from the animals' point of view. This study tested the preference of subordinate animals for their dominant cagemate, and vice versa, and the preference of subordinate animals for an unknown subordinate partner. Experiments that allowed male mice with different histories to choose either an inhabited or an empty cage have shown that the mice preferred the proximity of another male over individual housing. No differences in this respect were found between dominant and subordinate males, or between littermates and nonlittermates. The preference was most obvious when mice who were previously housed together were tested. The study concludes that separation and single housing for mice are not attractive solutions for overcoming aggression in group-housed male mice and that alternative approaches, such as improving the housing conditions, should be explored as a way of tempering intermale aggression.     

Do Male Mice Prefer or Avoid Each Other's Company? Influence of Hierarchy,Kinship, and Familiarity

In the laboratory, individual housing of male mice who otherwise show aggression is common practice. Because mice are a social species, the question arises whether this procedure is right from the animals' point of view. This study tested the preference of subordinate animals for their dominant cagemate, and vice versa, and the preference of subordinate animals for an unknown subordinate partner. Experiments that allowed male mice with different histories to choose either an inhabited or an empty cage have shown that the mice preferred the proximity of another male over individual housing. No differences in this respect were found between dominant and subordinate males, or between littermates and nonlittermates. The preference was most obvious when mice who were previously housed together were tested. The study concludes that separation and single housing for mice are not attractive solutions for overcoming aggression in group-housed male mice and that alternative approaches, such as improving the housing conditions, should be explored as a way of tempering intermale aggression.     

Sickness and Aggressive Behavior in Dominant and Subordinate Mice*

Sick animals show a set of organized behavioral changes (sickness behavior), which is the result of a motivational re‐organization of the behavior as a whole. Sickness behavior display can be influenced by the social context. In this work, we sought to investigate the regulation of sickness behavior within a pair of mice in the presence of an intruder mouse. Dominant and subordinate mice were treated with the bacterial endotoxin lipopolysaccharide (LPS) and were challenged with the presence of an intruder mouse. LPS effects depended on ranking and social context. Even though dominant mice displayed more agonistic interaction towards the intruder, subordinate mice displayed agonistic behavior towards the intruder when their dominant companion was treated with LPS. The results show that, not only sickness behavior is differentially expressed among different social ranks, but also that sickness behavior is related to different reactions among surrounding animals. These data are relevant for a biological approach to the relation between sickness behavior and social behavior.     

Resting cortisol levels and the emergence of dominant status among male vervet monkeys

Resting serum cortisol was measured in adult male vervet monkeys (Cercopithicus aethiops sabaeus) in four different conditions: (1) among groups with unaltered group membership and established dominance hierarchies; (2) among groups from which the original dominant male had been removed and in which the remaining males competed for dominant status; (3) among newly formed groups of three unfamiliar males each of which had been the dominant male in his previous group; and (4) among groups from which a dominant male was temporarily separated and returned. In Condition 1, cortisol concentrations did not differ between dominant and subordinate males. The second condition showed that cortisol levels were highest among males who eventually emerged as the dominant male. In the third condition, however, cortisol levels did not differentiate eventually dominant from eventually subordinate males. In the last condition, cortisol levels were highest in the animals that became or remained dominant following reintroduction. These data indicate that cortisol concentration does not differ between dominant and subordinate males in stable groups and that cortisol rises during competition for dominance among familiar males.     

Pituitary-adrenocortical responses to the first dyadic encounters in male rhesus monkeys: effect of dominance relationship

Male rhesus monkeys unfamiliar with each other were paired in a cage, and blood samples were collected before and a few hours after pair formation. Adrenocorticotrophic hormone (ACTH) and cortisol levels in each blood sample were measured. Dominant-subordinate status was ascertained through two rank tests, the food competition test and the agonistic behavior test, which were performed immediately after pair formation. As a result, the dominance relationship was determined in seven pairs formed from five animals, and the differences in ACTH and cortisol values between the dominant and subordinate animal in these pairs were compared statistically. The day after the first encounter, a second encounter was conducted in randomly selected pairs of monkeys. In the first encounters, higher levels of both ACTH and cortisol were detected in dominant animals in comparison to subordinate animals. Changing the animal's partner altered the stress responses whenever the animal's dominant-subordinate status changed. The elevated levels of ACTH and cortisol in dominant animals disappeared on the day after the first encounter. In dominant animals, the pituitary-adrenocortical stress response reacts sharply to situational demands, whereas subordinate animals have a weaker response. This acute stress response is different from a chronic stress response. When the subordinate animal cannot escape, its hypothalamic-pituitary-adrenocortical axis appears to be suppressed.     

Social defeat and footshock increase body mass and adiposity in male Syrian hamsters

Obesity is a world-wide epidemic, and many factors, including stress, have been linked to this growing trend. After social stress (i.e., defeat), subordinate laboratory rats and most laboratory mice become hypophagic and, subsequently, lose body mass; the opposite is true of subordinate Syrian hamsters. After social defeat, Syrian hamsters become hyperphagic and gain body mass compared with nonstressed controls. It is unknown whether this increase in body mass and food intake is limited to subordinate hamsters. In experiment 1, we asked, do dominant hamsters increase food intake, body mass, and adiposity after an agonistic encounter? Subordinate hamsters increased food intake and body mass compared with nonstressed controls. Although there was no difference in food intake or absolute body mass between dominant and nonstressed control animals, cumulative body mass gain was significantly higher in dominant than in nonstressed control animals. Total carcass lipid and white adipose tissue (WAT) (i.e., retroperitoneal and epididymal WAT) masses were significantly increased in subordinate, but not dominant, hamsters compared with nonstressed controls. In experiment 2, we asked, does footshock stress increase food intake, body mass, and adiposity. Hamsters exposed to defeat, but not footshock stress, increased food intake relative to nonstressed controls. In animals exposed to defeat or footshock stress, body mass, as well as mesenteric WAT mass, increased compared with nonstressed controls. Collectively, these data demonstrate that social and nonsocial stressors increase body and lipid mass in male hamsters, suggesting that this species may prove useful for studying the physiology of stress-induced obesity in some humans.     

野生雄性成年小家鼠行为

本实验以在英格兰捕获的野生小家鼠（Ｍｕｓｍｕｓｃｕｌｕｓｄｏｍｅｓｔｉｃｕｓ）的雄性后代为材料,研究同父异母断乳鼠组和无亲缘关系断乳鼠组在鼠成年后,鼠组成员在自由活动条件下的社会行为,以及独居和亲缘关系对其行为的影响。主要结论如下：１．成年优势鼠和成年从属鼠除打斗行为有显著差别外,优势鼠的嗅底物、社会探究、尿标记等行为也显著地高于从属鼠。从属鼠接触从属鼠显著地多于优势鼠。２．在一小时观察期内,打斗行为和社会探究逐渐减少,而和睦相处行为逐渐增加。社会行为主要发生在现在初期（０—１０分钟）。３．基于非打斗行为,尤其是社会探究和接触行为,通过判别分析,可能辩别出社会等级不清楚的成年雄鼠组中谁是优势鼠,谁是从属鼠。４．独居２３小时后,社会行为中,打斗行为和社会探究均明显上升。但优势鼠的多数行为基本保持原有水平,独居主要是使从属鼠的多数行为发生了改变,并且以针对另一从属鼠为主。５．有、无亲缘关系组的个体共同生活很长一段时间后,亲缘关系依然对小家鼠行为有深刻的影响,有亲缘关系组的社会稳定性、容忍性强于无亲缘关系组。     

Subordinate Males in Harem Groups of Jamaican Fruit‐Eating Bats (Artibeus jamaicensis): Satellites or Sneaks?

In the caves of Yucatan, Mexico, the Jamaican fruit‐eating bat, Artibeus jamaicensis, forms harems consisting of four to 18 females and a dominant male that defends the group against foreign males. Large groups (>14 females) contain an additional subordinate male. In theory, subordinate males can associate with harem groups either as satellites, if they provide at least some benefits to the dominant male, or as sneaks, if they only impose costs on the dominant male. We assessed the costs and benefits of subordinate males in three removal experiments. In the first experiment, when a dominant male was removed from its group, its role was occupied by the subordinate male (in large groups) or by a foreign male (in small groups). Former subordinate males took less time to gain control of the harems and stayed longer with the groups than foreign males. In the second experiment, when a subordinate male was removed, the rate of visitation by foreign males and the number of agonistic displays by the dominant male both increased. In the third experiment, when the number of females in large groups was reduced, subordinate males spent less time with their groups and the rate of visitation by foreign males increased. However, the frequency of agonistic displays by dominant males towards subordinate males did not change. Dominant males invest large amounts of energy in defending the harems, but obtain direct and immediate benefits from the presence of subordinate males in the form of access to a larger number of females, and suffer no obvious costs. Subordinate males apparently invest little energy in defending the harems, obtain no obvious immediate benefit, but gain long‐term benefits by having priority access to vacant positions left by dominant males. Subordinate males in harem groups of the Jamaican fruit‐eating bat can be considered satellites because their presence brings immediate benefits to the dominant males.     

Effect of early androgen treatment on subsequent social behavior in heifers

Two groups of four heifers received daily injections of 0.30 mg/kg of testosterone propionate in oil for 100 days, between 3 and 6 months of age. Two other groups of four heifers of the same age received only oil and served as controls. Three to five months after the end of treatment, a series of experiments was designed to compare dominance ability, aggressiveness, and reactions associated with fear, between treated and control animals. Dominance ability, when faced with animals of the same age and social experience, is higher for treated animals than controls, 85% of them being dominant. Treated animals established dominance relationships between themselves more slowly than did control animals or mixed pairs. In all experiments treated animals fought more often than controls. Those which became subordinate fought more than those which became dominant. When subordinate, treated animals withdrew less often than control animals and frequently did not react to aggression. When dominant, treated animals were never more, and sometimes less, aggressive than controls. It is proposed that changes in social structure of organized groups and the capacity to become dominant at first encounter are due to a reduction of fear of other animals induced by androgens. The acquisition of social rank in cattle may be principally due to differences in fear or “emotionality” rather than in aggressiveness.     

Paternity and dominance loss in male breeders: the cost of helpers in a cooperatively breeding mammal

Paternity insurance and dominance tenure length are two important components of male reproductive success, particularly in species where reproduction is highly skewed towards a few individuals. Identifying the factors affecting these two components is crucial to better understand the pattern of variation in reproductive success among males. In social species, the social context (i.e. group size and composition) is likely to influence the ability of males to secure dominance and to monopolize reproduction. Most studies have analyzed the factors affecting paternity insurance and dominance tenure separately. We use a long term data set on Alpine marmots to investigate the effect of the number of subordinate males on both paternity insurance and tenure of dominant males. We show that individuals which are unable to monopolize reproduction in their family groups in the presence of many subordinate males are likely to lose dominance the following year. We also report that dominant males lose body mass in the year they lose both paternity and dominance. Our results suggest that controlling many subordinate males is energetically costly for dominant males, and those unable to support this cost lose the control over both reproduction and dominance. A large number of subordinate males in social groups is therefore costly for dominant males in terms of fitness.     

Female Preferences Based on Male Quality in House Mice: Interaction between Male Dominance Rank and t-Complex Genotype

Considerable evidence indicates that female house mice (Mus domesticus) prefer dominant over subordinate males as mates. In addition, male genotype at the t-complex seems to be an important characteristic used by females in mate choice. Specifically, female mice that carry a t-haplotype at the t-complex prefer +/+ over +/t males as mates. The purpose of the present study was to examine the relative contributions of male dominance rank and male t-complex genotype to female mating preference when both factors were systematically varied. We tested females of three genotypes (+/+, +/t, and t/t) in a preference apparatus using pairs of stimulus males varying in relative dominance status and t-complex genotype. In general, when given the choice, females preferred dominant over subordinate males regardless of the male's t-complex genotype. The preference for dominant males was manifested when both stimulus males were of the same t-complex genotype but differed in dominance rank. In addition, when forced to choose between a dominant +/+ and subordinate +/t or between a dominant +/t and subordinate +/+, females continued to prefer the dominant male. Preference for dominant males was independent of female genotype. Only when both males were dominant but differed in t-complex genotype (i.e. one male was +/+ and the other +/t) or when males were unranked (i.e. had not been used in aggressive encounters to determine dominance rank) did females carrying t-haplotypes manifest preferences for +/+ males. Quite unexpectedly, when both males were subordinate but differed in t-complex genotype, preferences of all females shifted in the direction of the +/t male. It is not clear from present data whether the propensity of females to give greater weight to male dominance rank than to t-complex genotype in choosing mates results in greater fitness. However, if these trends are found in natural populations, it would indicate that the role of mating preference in regulating the frequency of t-haplotypes in wild populations is less straightforward than had been previously thought.     

Effects of vomeronasal organ removal on the sperm motility in male mice

Odors play important roles in the communication of house mice. They release behaviors and prime changes of the physiological conditions of other individuals. In our previous study, we showed that sperm motility was lowered in the subordinate mice comparing with dominant mice. Our hypothesis is that the lowered sperm motility was due to some primer effects by odor substances derived from dominant mice. To test the hypothesis, we destroyed the vomeronasal organ (VNO) of male mice (VNX male) at 5 weeks of age and paired them with intact male mice (Experimental Group). As control group males, intact male mice were kept in pairs (Control Group). At 15 weeks of age, the sperm motility and weights of reproductive organs, and social dominance was analyzed. The subordinate VNX males were found to have high sperm motility comparable to the dominant males. It was suggested that there is male-to-male primer effects, mediated by VNO, that suppress sperm motility of the subordinate mice.     

Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice

Arginine vasopressin (AVP) and its nonmammalian homolog arginine vasotocin influence social behaviors ranging from affiliation to resident-intruder aggression. Although numerous sites of action have been established for these behavioral effects, the involvement of specific AVP cell groups in the brain is poorly understood, and socially elicited Fos responses have not been quantified for many of the AVP cell groups found in rodents. Surprisingly, this includes the AVP population in the posterior part of the medial bed nucleus of the stria terminalis (BSTMP), which has been extensively implicated, albeit indirectly, in various aspects of affiliation and other social behaviors. We examined the Fos responses of eight hypothalamic and three extra-hypothalamic AVP-immunoreactive (-ir) cell groups to copulation, nonaggressive male-male interaction, and aggressive male-male interaction in both dominant and subordinate C57BL/6J mice. The BSTMP cells exhibited a response profile that was unlike all other cell groups: from a control baseline of ∼ 5% of AVP-ir neurons colocalizing with Fos, colocalization increased significantly to ∼ 12% following nonaggressive male-male interaction, and to ∼ 70% following copulation. Aggressive interactions did not increase colocalization beyond the level observed in nonaggressive male mice. These results suggest that BSTMP neurons in mice may increase AVP-Fos colocalization selectively in response to affiliation-related stimuli, similar to findings in finches. In contrast, virtually all other cell groups were responsive to negative aspects of interaction, either through elevated AVP-Fos colocalization in subordinate animals, positive correlations of AVP-Fos colocalization with bites received, and/or negative correlations of AVP-Fos colocalization with dominance. These findings greatly expand what is known of the contributions of specific brain AVP cell groups to social behavior.     

Gender Differences in the Costs that Subordinate Group Members Impose on Dominant Males in a Cooperative Breeder

In group-living species, a dominant male's ability to monopolize reproduction, and the cost of doing so, are expected to vary with a group's gender composition. We used spawning observations of a group-living cichlid, Neolamprologus pulcher , to test this expectation. We constructed groups that contained a dominant breeding pair and either two male subordinates, one male and one female subordinate or two female subordinates. Parasitic spawning by male subordinates was more common in groups with two male subordinates than in groups with one male and one female subordinate. Female subordinates were never observed laying eggs in dominant females' clutches, but three female subordinates laid independent clutches. During spawning, frequencies of dominant male aggression towards male and female subordinates were similar. Dominant males were less aggressive during non-reproductive periods. The declines were greater for female subordinates, such that, during non-reproductive periods, dominant males were more aggressive towards male subordinates. Aggression towards each subordinate was also affected by the second subordinate's gender; the direction of that effect differed for large and small subordinates. Male subordinates approached breeding shelters less often than female subordinates, and both male and female subordinates approached shelters more frequently when the second subordinate was male. Collectively, these patterns suggest: (1) that male subordinates impose higher costs on dominant males than female subordinates do and (2) that the presence of a second male subordinate imposes additional costs beyond those of the first male subordinate. We discuss the implications of these effects for dominant and subordinate group members.     

Modulation of social behavior and dominance status by chronic pain in mice

The potential influence of pain on social behavior in laboratory animals has rarely been evaluated. Using a new assay of social behavior, the tube co‐occupancy test (TCOT), we assess propinquity—the tendency to maintain close physical proximity—in mice exposed to pain using subcutaneous zymosan or spared nerve injury as noxious stimuli. Our previous experience with the TCOT showed that outbred mouse sibling dyads show higher levels of tube co‐occupancy than stranger dyads. We find here that long‐lasting pain from spared nerve injury given to both mice in the dyad abolishes this effect of familiarity, such that strangers also display high levels of propinquity. We performed a separate experiment to assess the effect on dominance behavior of nerve injury to one or both mice of a dyad in which relative dominance status had been previously established via the confrontation tube test. We find that neuropathic pain given only to the dominant mouse reverses the relationship in male but not female mice, such that the previously subordinate mouse becomes dominant. These observations bolster the scant but growing evidence that pain can robustly affect social behavior in animals.     

A Trouble Shared Is a Trouble Halved: Social Context and Status Affect Pain in Mouse Dyads

In mice behavioral response to pain is modulated by social status. Recently, social context also has been shown to affect pain sensitivity. In our study, we aimed to investigate the effects of interaction between status and social context in dyads of outbred CD-1 male mice in which the dominance/submission relationship was stable. Mice were assessed for pain response in a formalin (1% concentration) test either alone (individually tested-IT), or in pairs of dominant and subordinate mice. In the latter condition, they could be either both injected (BI) or only one injected (OI) with formalin. We observed a remarkable influence of social context on behavioral response to painful stimuli regardless of the social status of the mice. In the absence of differences between OI and IT conditions, BI mice exhibited half as much Paw-licking behavior than OI group. As expected, subordinates were hypoalgesic in response to the early phase of the formalin effects compared to dominants. Clear cut-differences in coping strategies of dominants and subordinates appeared. The former were more active, whereas the latter were more passive. Finally, analysis of behavior of the non-injected subjects (the observers) in the OI dyads revealed that dominant observers were more often involved in Self-grooming behavior upon observation of their subordinate partner in pain. This was not the case for subordinate mice observing the pain response of their dominant partner. In contrast, subordinate observers Stared at the dominant significantly more frequently compared to observer dominants in other dyads. The observation of a cagemate in pain significantly affected the observer''s behavior. Additionally, the quality of observer''s response was also modulated by the dominance/submission relationship.     

Dominance‐related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees

It is well established that spatial memory is dependent on the hippocampus in both mammals and birds. As memory capacity can fluctuate on a temporal basis, it is important to understand the mechanisms mediating such changes. It is known that early memory‐dependent experiences in young animals result in hippocampal enlargement and in increased neurogenesis, including cell proliferation and neuron survival. It is less clear, however, whether temporal changes in spatial memory are also associated with changes in hippocampal anatomy and cell proliferation in fully grown and experienced adult animals. In a previous study, we experimentally demonstrated that socially subordinate mountain chickadees (Poecile gambeli) showed inferior spatial memory performance compared to their dominant group mates, in the absence of significant differences in baseline corticosterone levels. Here we investigated whether these differences in memory between dominant and subordinate birds were associated with changes in the hippocampus. Following memory tests, chickadees were injected with 5‐bromo‐2′‐deoxyuridine to label dividing cells and sacrificed 2 days after the injections. We found no significant differences in volume or the total number of neurons in the hippocampal formation between dominant and subordinate chickadees, but subordinate birds had significantly lower cell proliferation rates in the ventricular zone adjacent to both the hippocampus and mesopallium compared to the dominants. Individuals, which performed better on spatial memory tests tended to have higher levels of cell proliferation. These results suggest that social status can affect cell proliferation rates in the ventricular zone and support the hypothesis that neurogenesis might be involved in memory function in adult animals. © 2004 Wiley Periodicals, Inc. J Neurobiol, 2005     

Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees

It is well established that spatial memory is dependent on the hippocampus in both mammals and birds. As memory capacity can fluctuate on a temporal basis, it is important to understand the mechanisms mediating such changes. It is known that early memory-dependent experiences in young animals result in hippocampal enlargement and in increased neurogenesis, including cell proliferation and neuron survival. It is less clear, however, whether temporal changes in spatial memory are also associated with changes in hippocampal anatomy and cell proliferation in fully grown and experienced adult animals. In a previous study, we experimentally demonstrated that socially subordinate mountain chickadees (Poecile gambeli) showed inferior spatial memory performance compared to their dominant group mates, in the absence of significant differences in baseline corticosterone levels. Here we investigated whether these differences in memory between dominant and subordinate birds were associated with changes in the hippocampus. Following memory tests, chickadees were injected with 5-bromo-2'-deoxyuridine to label dividing cells and sacrificed 2 days after the injections. We found no significant differences in volume or the total number of neurons in the hippocampal formation between dominant and subordinate chickadees, but subordinate birds had significantly lower cell proliferation rates in the ventricular zone adjacent to both the hippocampus and mesopallium compared to the dominants. Individuals, which performed better on spatial memory tests tended to have higher levels of cell proliferation. These results suggest that social status can affect cell proliferation rates in the ventricular zone and support the hypothesis that neurogenesis might be involved in memory function in adult animals.