The significance of the genotype and individual behavioral characteristics for the manifestation of the dominant phenotype in mouse micropopulations]

Influence of genotype and such individual characteristics as locomotor and exploratory activity, aggressiveness and emotionality, was studied in male mice. Males F1 and males of the parent line PT had high level of social dominance. F1 had high level of aggressiveness, and low emotionality, medium level of locomotor and exploratory activity. Significance of these individual behavioural characteristics for dominant behaviour is discussed.     

Social relationships and social structure of the mound-building mouse (<Emphasis Type="Italic">Mus spicilegus</Emphasis>) in intraspecific cage groups

The social relationships of Mus spicilegus were studied in intraspecific cage groups for a month during the reproductive period to clarify the role of intraspecific aggressiveness in shaping social structure and in reproduction. The mound-building mice were captured from a wild population in northern Bulgaria. A total of 13 groups, 5 male, 4 female, and 4 male–female groups, were tested. Each group consisted of five unfamiliar adults. The experiments were carried out in 100×100-cm glass cages. The patterns of behaviour and the dominant–subordinate structure within each group were investigated. A dominance index for every individual in the group was calculated. During the period of establishment of the hierarchical structure in the groups a high level of aggressiveness was registered among individuals. About half of the subdominants and subordinates were found dead, with or without obvious marks of injury. Male–male interactions were more aggressive compared to these of females. Dominant–subordinate relationships between individuals of the same sex were observed in the mixed groups. A link between dominance rank and reproduction was established. The dominant male and the dominant female formed a pair and started to breed. Based on these findings it can be assumed that the aggressiveness of M. spicilegus is an adaptation to its life in the fields, where dominance is likely to be an essential factor in individual reproductive success. It is likely that the successful rearing of offspring in natural populations, which are exposed to strong biotic and abiotic impact, necessitates the existence of monogamous relationships. Communicated by P. Gama Mota     

Benefits and Costs of Dominance in the Angelfish Centropyge bicolor

Social groups are often structured by dominance hierarchies in which subordinates consistently defer to dominants. High‐ranking individuals benefit by gaining inequitable access to resources, and often achieve higher reproductive success; but may also suffer costs associated with maintaining dominance. We used a large‐scale field study to investigate the benefits and costs of dominance in the angelfish Centropyge bicolor, a sequential hermaphrodite. Each haremic group contains a single linear body size‐based hierarchy with the male being most dominant, followed by several females in descending size order. Compared to their subordinate females, dominant males clearly benefited from disproportionately high spawning frequencies, but bore costs in lower foraging rates and greater aggressive defence of their large territories. Within the female hierarchy, more dominant individuals benefited from higher spawning frequencies and larger home ranges, but displayed neither higher foraging rates nor spawn order priority. However, dominance in females was also linked to aggressiveness, particularly towards immediate subordinates, suggesting that females were using energetically costly aggression to maintain their high rank. We further showed by experimentally removing dominant females that the linear hierarchy was also a social queue, with subordinates growing to inherit higher rank with its attendant benefits and costs when dominants disappeared. We suggest that in C. bicolor, the primary benefit of high rank is increased reproductive success in terms of current spawning frequency and the prospect of inheriting the male position in the near future, which may be traded off against the cost of aggressively defending rank and territory.     

Evidence contradicting the notion that gonadal hormones regulate brain opiate receptors

Castration of male rats has been reported to increase brain opiate receptors by nearly 100%. We assayed brain opiate receptors with both naloxone and met-enkephalin, but found no effect of gonadectomy on the Kd or Bmax for either ligand in male or female mice or in male rats. Experiments were performed with 2 strains of mice and 3 strains of rats; mice were gonadectomized 1–7 weeks and rats were castrated 3 weeks before assay. Both washed and unwashed brain membrane preparations were used. Administration of testosterone or estrogen to intact male or female mice did not alter opiate receptors. Castration did not affect the strain or age and brain-region differences found for naloxone binding in male rats.     

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.     

The reproductive correlates of social hierarchy in laboratory male mice

In laboratory male mice the effects of social hierarchy on hormonal and spermatogenic testicular function, accessory organs and testicular weights, sexual behaviour have been investigated using an experimental model of social hierarchy, which is characterised by a minimal size (two male mice) and 5 days period of social interactions. The social rank of the partners was detected by asymmetry in aggressive behaviour. Using the experimental condition, when the both partners have no preferences for exclusive use of area we demonstrated that there were no rank differences in the number of mounts and testicular testosterone content. Nevertheless a rank asymmetry in the male sniffing behaviour towards a receptive female, weights of the testes, seminal vesicles, epididymes and the number of epididymal sperm was kept up in a stable social group. Social dominance was found to affect negatively on testicular testosterone increase in response to introduction of a receptive female and sexual attractiveness of male to a receptive female in both dominant and subordinate males. The results obtained demonstrate the impact of social hierarchy on reproduction in laboratory male mice, particular in respect of spermatogenesis and the testicular testosterone in response to a receptive female.     

Differences in aggressive behaviour between male mice (Mus musculus L.) in colonies of different sizes

Using cages of uniform size, colonies of three, four, five, nine and twelve unfamiliar male mice were established and observed over a 21-day period. A dominant mouse emerged in every colony, but in the two largest sizes five to six changes in dominance were recorded. The per capita aggression did not increase with colony size. There was a general linear decline in the number of attacks recorded in colony sizes nine and twelve whilst in the three smaller colony sizes the dominant showed an exponential decline in aggressiveness. Differences in hierarchical organization were interpreted in terms of the number of attacks shown by the dominant in relation to the number of subordinates present.     

Reduced aggression in AMPA-type glutamate receptor GluR-A subunit-deficient mice

The importance of AMPA-type glutamate receptors has been demonstrated in neuronal plasticity and in adaptation to drugs of abuse. We studied the involvement of AMPA receptors in social interaction and anxiety and found that in several paradigms of agonistic behavior naïve male mice deficient for the GluR-A subunit- containing AMPA receptors are less aggressive than wild-type littermates. GluR-A deficient mice and wild-type littermates exhibited similar basic behavior and reflexes as monitored by observational Irwin's test, but they tended to be less anxious in elevated plus-maze and light-dark tests. Maternal aggression or male-female encounters were not affected which suggests that male hormones are involved in the expression of suppressed aggressiveness. However, testosterone levels and brain monoamines can be excluded and found to be similar between GluR-A deficient and wild-type littermates. The reduced AMPA receptor levels caused by the lack of the GluR-A subunit, and measured by a 30% reduction in hippocampal [³H]-S-AMPA binding, seem to be the reason for suppressed male aggressiveness. When we analyzed mice with reduced number of functional AMPA receptors mediated by the genomic introduced GluR-A(Q582R) channel mutation, we observed again male-specific suppressed aggression, providing additional evidence for GluR-A subunit-containing AMPA receptor involvement in aggression.     

Social Status and Resistance to Disease in House Mice (Mus musculus): Status-related Modulation of Hormonal Responses in Relation to Immunity Costs in Different Social and Physical Environments

Unrelated and previously unfamiliar male mice were maintained in groups of six tor different periods and at different ambient temperatures. High- and low-ranking males differed in hormone-related resistance to a subsequent experimental infection with the blood protozoan Babesia microti and there were rank differences in the apparent modulation of immunodepressive hormones relative to an individual's internal, social and physical environment. Resistance to B. microti was influenced by serum concentrations of corticosterone and testosterone. Associations between aggressiveness and measures of immunocompetence and resistance were related to corticosterone concentration, but only among low rankers. Effects of testosterone on resistance were confined to high rankers but were not associated with aggressiveness, although high rankers maintained greater aggressiveness than low rankers in all experimental treatments. The effects of group duration and temperature on resistance can be interpreted in terms of changing hormone and antibody levels in relation to metabolic stress. The results emphasize the importance of interactions between underlying physiological changes in relationships between behaviour, immune function and disease.     

Effects of residence,aggressive experience and intruder familiarity on attack shown by male mice

Two groups of 12 mature male Swiss Morini strain mice were matched for aggressiveness on the basis of their response to anosmic docile male intruders after 24 h individual housing in a large defensible cage. One group was subsequently individually housed without disturbance for a further 12 days whereas the second group was exposed to a new anosmic intruder every 3 days over this same period. All mice were subsequently retested against anosmic intruders for a 10 min period. Animals which had had the opportunity to fight repeatedly showed more attack than individuals lacking such experience. A second experiment contrasted the responses of dominant isolates to the same or a different anosmic intruder, 10 min after a successful attack. Familiar intruders were attacked less vigorously than unfamiliar mice. It seems likely that the defeated mouse becomes less potent as a stimulus eliciting attack as the resident becomes habituated to it. Conversely, unfamiliar intruders evoke aggressive reactions by residents despite the prolonged fights they had had before final testing. These experiments provide little support for the appetence view of aggression in mice (i.e. the view that aggressiveness is augmented by depriving the animal of the opportunity to fight) or the view that this phenomenon is simply a consequence of “social deprivation”.     

The effects of age and previous experience on social rank in female red junglefowl, Gallus gallus spadiceus

Social rank can influence lifetime reproductive success and therefore fitness. We examined the effects of morphology, age, previous social experience and aggressiveness on social rank in all-female flocks of red junglefowl. None of the morphological characters measured (mass, tarsus length, comb height or comb length) appeared to play a role in determining rank. Older females were not more likely to be dominant, while previous social experience and aggression levels were both important in dominance determination. Flock-experienced hens were more likely to be dominant as were more aggressive individuals. Red junglefowl females most likely use a combination of characters to establish social order in a newly formed flock. Copyright 2000 The Association for the Study of Animal Behaviour.     

Future social rank: forecasting status in the green anole (Anolis carolinensis)

Predicting the future social standing of an individual without aggressive social interaction may seem contradictory, as formation of social rank depends on agonistic interactions. In the lizard Anolis carolinensis, predicting social rank is possible using latency to eyespot formation (sympathetic darkening of postorbital skin from green to black during stressful agonistic interactions), because they form more rapidly in male lizards that become dominant. Darkened eyespots also inhibit aggressive behavior. As the timing of eyespot formation appears to be an important component of stress responsiveness and future social status, we hypothesized that a proactive disposition toward non-aggressive behavior, such as feeding and courtship, would be associated with aggressiveness. We assessed the relationship between rank and the temporal dynamics of eyespot formation, latencies to aggressive display, feeding, and reproductive behavior. Male lizards that became dominant were faster to respond to all types of stimuli tested (aggression, feeding, and courtship). The temporal dynamics of the neuroendocrine stress response appear to influence the motivation for behavioral response. Animals that recover from stress more quickly also eat, court, and fight more readily. In summary, this work suggests that latencies to aggressive, reproductive, and feeding behavior, as well as eyespot signals, are reliable predictors of future social status of individual male A. carolinensis.     

Effect of chronic administration of lithium chloride on the development of dopamine receptor sensitivity during morphine withdrawal in rats

The morphine withdrawal syndrome was studied in male Wistar rats. Spontaneous aggressiveness, enhanced apomorphine aggressiveness, lowered pain threshold and decreased dopamine turnover were observed after withdrawal of 10-day treatment with the increasing doses of morphine (30-300 mg/kg). These changes attested to the increased sensitivity of dopamine receptors. Administration of morphine in conjunction with lithium chloride in a dose of 2 mekv/kg prevented the development of dopamine receptor hypersensitivity. Also, this method did not produce the increased spontaneous and apomorphine aggressiveness or the decreased dopamine turnover. Meanwhile the pain threshold remained lowered.     

Genetic-neurochemical analysis of the role of brain catecholamines in the manifestation of dominance in male mice in micropopulations

The ability of male mice to dominate in micropopulations, in connection with brain catecholamines was studied. It was shown that the F1 obtained from breeding PT and CBA/Lac which have respectively large and small numbers of high rank males were of high level of dominance in micropopulations. Moreover, they had high levels of noradrenaline and dopamine in hippocampus, striatum and brain stem, and low--in hypothalamus.     

The production of hydrogen sulfide is regulated by testosterone and S-adenosyl-L-methionine in mouse brain

Hydrogen sulfide (H2S) is endogenously produced in the brain from L-cysteine by the enzyme cystathionine beta-synthase (CBS) and functions as a neuromodulator in the brain. H2S selectively enhances NMDA receptor-mediated responses and alters hippocampal long-term potentiation (LTP). The production of H2S is regulated by Ca2+/calmodulin-mediated pathways and is enhanced in response to neuronal excitation. In addition to this fast regulation, we describe here a slower form of the regulation of H2S production by testosterone and S-adenosyl-L-methionine (SAM), a CBS activator. Endogenous H2S in the mouse brain increases after birth, reaches a maximum level at 8 weeks and then decreases. Female brain contains less H2S than male brain at each age. A single administration of testosterone to female mice increases the endogenous H2S and SAM, which reach levels similar to those of male mice. In contrast, castration of male mice decreases the levels of testosterone, SAM and H2S in the brain. Administration of SAM once a day for 3 days increases the brain H2S without significantly changing the testosterone level. These observations suggest that testosterone can regulate the brain H2S level via changing the level of SAM.     

Testosterone and Linear Social Dominance Status in Captive Male Dabbling Ducks in Winter

Dominance hierarchies play an important role in avoidance and/or solving conflicts in gregarious species. In dabbling ducks (Anas species), dominance allows for feeding‐site monopolization in winter quarters where resources are generally limited. In addition, male social rank should theoretically favour access to mates. Dominance rank can be associated with morphological traits, and is often correlated with aggressiveness, a behavioural trait generally related to high testosterone levels. In this study, we investigated the existence of a winter group structure based on dominance relationships and tested for a linear hierarchy, in three species of captive male dabbling ducks (mallard Anas platyrhynchos, pintail A. acuta and wigeon A. penelope). We then analysed the relationship between dominance ranks, morphological parameters and testosterone levels measured in early (Oct.) and mid‐winter (Dec./Jan.). We found that the three male groups of the three species exhibited a linear hierarchy. Testosterone levels differed during winter and between species. Morphologic measurements, body mass and body condition were not correlated with individual dominance ranks, whereas dominant males had higher testosterone levels than subordinates. The slopes of the relationships were similar between species and winter period, but the y‐intercepts differed between species and between early and mid‐winter phases. The linear hierarchy found in the three species indicates that dominance relationships strongly structure dabbling duck groups in winter. Lack of correlation between rank and morphological characters, but correlation of rank with testosterone levels suggests that social rank is more dependent on behavioural traits such as aggressive behaviour. The differences between species and winter periods are discussed in relation to migration and wintering phenology.     

Effects of NO/cGMP signaling on behavioral changes in subordinate male crickets, Gryllus bimaculatus

After a loss against an opponent, the aggressiveness of a male cricket is significantly reduced for up to 30 minutes. This depression of aggressiveness is an important factor in the establishment and maintenance of dominance between individuals. In the present study, we investigated the functional roles of nitric oxide (NO) signaling in the depression of aggressiveness in subordinate male crickets. Pairs of male crickets, pre-injected with various NO-related reagents, were allowed to establish dominant/subordinate relationships in dyadic encounters. Opponents were separated for 15 minutes and then paired again. In second encounters, subordinate crickets pre-injected with PTIO (NO scavenger) showed agonistic behavior towards former dominant opponents. A similar effect was observed in crickets pre-injected with L-NAME (NO synthase inhibitor) or ODQ (soluble guanylate cyclase inhibitor). The effects of the latter two drugs were canceled by co-injection of NOR3 (NO donor) with L-NAME or by co-injection of 8-Br-cGMP (cGMP-analog) with ODQ. Injection of NOR3 alone prolonged the inhibition of agonistic behavior in subordinate crickets from 30 minutes to 3 hours. Our results suggest that the change in agonistic behavior observed in subordinate male crickets is closely linked to NO-mediated cGMP signaling.     

Expression in brain of amyloid precursor protein mutated in the alpha-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice.

A double mutation in the alpha-secretase site in the betaA4 region of mouse amyloid precursor protein (APP) reduced its secretion from COS cells, polarized MDCK cells and rat primary neurons. Expression of this mutant in the brain of mice, using the neuron-specific elements of the mouse Thy-1 gene promoter, resulted in transgenic mice that became progressively hyperactive, displayed seizures and died prematurely. In three different transgenic lines the severity of the phenotype was related directly to the expression levels of the transgene, estimated by both mRNA and protein levels. In addition, homozygous mice derived from each transgenic strain showed more severe symptoms which also occurred earlier in life than in heterozygotes. The observed symptoms were, however, not essentially different in the different lines. Increased aggressiveness, disturbed responses to kainic acid and N-methyl-D-aspartate, neophobia and deficiency in exploratory behavior were demonstrated in these mice. In the brain, the observed neuropathological changes included necrosis, apoptosis and astrogliosis in the hippocampus, cortex and other areas. The data demonstrate that incomplete or incorrect alpha-secretase processing of APP results in severe neurotoxicity and that this effect is expressed in a dominant manner.     

The involvement of brain 5-HT(1A)-receptors in genetically determined aggressive behavior

The hypothesis was tested that one of the critical mechanisms underlying genetically determined aggressiveness involves brain serotonin 5-HT(1A)-receptors. The expression of 5-HT(1A)-receptor mRNA in brain structures and functional correlate for 5-HT(1A)-receptors identified as 8-OH-DPAT-induced hypothermia were studied in Norway rats bred over the course of 59 generations for the low and high affective (defensive) aggressiveness with respect to man and in highly aggressive (offensive) MAO A-knockout mice (Tg8 strain). Considerable differences between the aggressive and the nonaggressive animals were shown. Agonist of 5-HT(1A)-receptor 8-OH-DPAT (0.5 mg/kg for rats and 2.0 mg/kg for mice, i.p.) produced a distinct hypothermic reaction in nonaggressive rats and mice and did not affect significantly the body temperature in aggressive animals. In aggressive rats, a significant reduction of the expression of 5-HT(1A)-receptor mRNA was found in the midbrain. In Tg8 mice, 5-HT(1A)-receptor mRNA level was increased in the frontal cortex and amygdala and not changed in the hypothalamus and the midbrain. The results provide support for the idea that brain 5-HT(1A)-receptors contribute to the genetically determined individual differences in aggressiveness.