The relationship between different types of genetically defined aggressive behavior

Aggressive behavior is not a unitary trait, and different stimuli/situations elicit different kinds of aggressive behavior. According to numerous data the genotype plays a significant role in the expression of aggressive behavior. However, it remains unclear how genetic predisposition to one kind of aggression is linked with other kinds of aggressive behavior, especially pathological aggression (infanticide). Here, we report on our investigation of the expression of defensive, offensive, predatory and asocial aggression in wild rats selectively bred for 85 generations for either a high level or a lack of aggression towards humans. We found that those rats genetically predisposed to a high level of defensive aggression showed decreased social behavior and increased pathological aggressive behavior towards juvenile males. The highly aggressive rates showed a reduced latency time of attack and an increased latency time of the first social contact. Rats genetically predisposed to defensive aggression demonstrated increased predatory aggression—latency time of muricide was shorter in highly aggressive than in tame animals. At the same time, both lines of rats did not differ significantly in intermale aggression. We conclude that the data indicate a close relation between defensive, predatory and pathological aggressive behavior that allows us to suggest that similar genetic mechanisms underlie these types of aggressive behavior.     

No barriers to gene flow among sympatric polychromatic 'small'Telmatherina antoniae from Lake Matano, Indonesia

Genetic divergence, assortative courtship and intermale aggression were assessed between sympatric colour morphs of the sailfin silverside Telmatherina antoniae , endemic to Lake Matano, Indonesia. Genetic analysis using microsatellite markers showed no barriers to gene flow among T. antoniae primary colour morphs (blue and yellow) within sampling sites, sympatric populations or at the lake-wide level. Low but significant genetic differentiation was found between yellow morphs and mixed (blue–yellow) morphs. Behavioural surveys indicated assortative courtship does occur along primary colour lines; however, intermale aggression among paired and intruding male morphs appeared equal with respect to male colour. These observations support the hypothesis that males view other males as threats to their courtship regardless of their colour. This study supports recent work suggesting that assortative mating is present in T. antoniae despite a lack of reproductive isolation among colour morphs.     

Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta)

In primate species exhibiting seasonal reproduction, patterns of testosterone excretion in adult males are variable: in some species, peaks correlate with female receptivity periods and heightened male-male aggression over access to estrous females, in others, neither heightened aggression nor marked elevations in testosterone have been noted. In this study, we examined mean fecal testosterone ( f T) levels and intermale aggression in wild adult male ring-tailed lemurs residing in three groups at Beza Mahafaly Reserve, Madagascar. Results obtained from mating and post-mating season 2003 were compared to test Wingfield et al. [1990. Am Nat 136:829-846] "challenge hypothesis", which predicts a strong positive relationship between male testosterone levels and male-male competition for access to receptive females during breeding season. f T levels and rates of intermale aggression were significantly higher during mating season compared to the post-mating period. Mean f T levels and aggression rates were also higher in the first half of the mating season compared with the second half. Number of males in a group affected rates of intermale agonism, but not mean f T levels. The highest-ranking males in two of the groups exhibited higher mean f T levels than did lower-ranking males, and young males exhibited lower f T levels compared to prime-aged and old males. In the post-mating period, mean male f T levels did not differ between groups, nor were there rank or age effects. Thus, although male testosterone levels rose in relation to mating and heightened male-male aggression, f T levels fell to baseline breeding levels shortly after the early mating period, and to baseline non-breeding levels immediately after mating season had ended, offsetting the high cost of maintaining both high testosterone and high levels of male-male aggression in the early breeding period.     

Change in certain forms of aggressive behavior and the concentration of monoamines in the brain during selection of wild rats for taming

Norway rats have been selected during 20 generations by the absence of aggressive reaction to man (tamed rats). From 7 up to 20th generations of selection, different forms of aggressive behaviour (reaction to glove, intermale, shock-induced aggression and predatory aggression) were studied, and the level of noradrenaline, serotonin and its metabolite 5-hydroxyindoleacetic acid was determined in the brain. In the absence of aggressive reaction to glove in tamed rats, the shock-induced aggression considerably decreased while the predatory aggressiveness (mouse-killing behaviour) and intermale aggressiveness did not change. Beginning from 15-16th generation of selection, a higher level of the 5-hydroxyindoleacetic acid in the hypothalamus was established, in the 20th generation an increased content of serotonin was revealed in the hypothalamus and the midbrain. In some generations of selection an increased level of noradrenaline in the hypothalamus in comparison to wild rats was observed. A conclusion is made that the selection of animals by taming unequally influences different kinds of aggressiveness and is accompanied by inherited consolidated reorganization of the monoamine brain systems.     

Costs and benefits of maternal aggression in lactating female rhesus macaques

Data from over 400 hr of observation of mother-infant rhesus macaques indicate that during the first 12 weeks of lactation infants are at risk from other group members and that mothers use aggression as well as restraining to protect them. Maternal aggression was negatively correlated with infant restraining. High-ranking mothers reacted aggressively to individuals handling their infants more than did middle- and low-ranking mothers. Conversely, middle- and low-ranking mothers restrained their infants more than did high-ranking mothers. Maternal aggression did not vary with infant age. Maternal aggression was directed toward a higher proportion of higher-ranking adult females and their immature offspring and was more likely to be followed by counter-aggression than nonmaternal aggression, i.e. aggression not related to interactions involving the infant. Middle-and low-ranking mothers suffered higher costs in terms of retaliation than high-ranking mothers. It is argued that the occurrence and distribution of maternal aggression among species and individuals should depend on the risk posed to infants by conspecifics as well as on the characteristics of the social structure (e.g. degree of asymmetry of agonistic contests) and of the mother (e.g. her dominance rank) which may affect the probability of retaliation.     

Disruption of the vasopressin 1b receptor gene impairs the attack component of aggressive behavior in mice

Vasopressin affects behavior via its two brain receptors, the vasopressin 1a and vasopressin 1b receptors (Avpr1b). Recent work from our laboratory has shown that disruption of the Avpr1b gene reduces intermale aggression and reduces social motivation. Here, we further characterized the aggressive phenotype in Avpr1b -/- (knockout) mice. We tested maternal aggression and predatory behavior. We also analyzed the extent to which food deprivation and competition over food increases intermale aggression. We quantified defensive behavior in Avpr1b -/- mice and later tested offensive aggression in these same mice. Our results show that attack behavior toward a conspecific is consistently reduced in Avpr1b -/- mice. Predatory behavior is normal, suggesting that the deficit is not because of a global inability to detect and attack stimuli. Food deprivation, competition for food and previous experience increase aggression in both Avpr1b +/+ and -/- mice. However, in these circumstances, the level of aggression seen in knockout mice is still less than that observed in wild-type mice. Defensive avoidance behaviors, such as boxing and fleeing, are largely intact in knockout mice. Avpr1b -/- mice do not display as many 'retaliatory' attacks as the Avpr1b +/+ mice. Interestingly, when territorial aggression was measured following the defensive behavior testing, Avpr1b -/- mice typically show less initial aggressive behavior than wild-type mice, but do show a significant increase in aggression with repeated testing. These studies confirm that deficits in aggression in Avpr1b -/- mice are limited to aggressive behavior involving the attack of a conspecific. We hypothesize that Avpr1b plays an important role in the central processing that couples the detection and perception of social cues (which appears normal) with the appropriate behavioral response.     

A quantitative study of serum testosterone,sex accessory organ growth,and the development of intermale aggression in the mouse

Radioimmunoassay of serum testosterone (T) was used to characterize circulating T levels in mice from birth to sexual maturity. Until 25 days of age, serum T levels ranged from 1 to 4 ng/ml. A significant increase in T concentrations was observed in 30-day-old males, followed by a secondary rise in serum T between Days 45 and 50 of life. The latter increment was associated with the appearance of extreme individual variation in circulating T levels which was also observed in adult (120 days) males. The most rapid growth of accessory sex organs occurred between 30 and 50 days of age, the period preceding attainment of peak serum-T levels. The first incidence of intermale aggression coincided with a prepubertal rise in circulating T, but adult levels of fighting were present prior to the secondary increase in T observed between 45 and 50 days of age. Although animals involved in a fight did not differ with respect to weight of the accessory sex organs or serum T concentrations, the male that weighed more than his opponent usually won an encounter. Compared to males in encounters in which no fighting occurred, animals that won or lost an aggressive encounter showed significantly greater accessory sex organ development. While circulating T is required for the initiation and maintenance of intermale aggression, it is apparent that additional factors are related to the onset of fighting and the establishment of dominance/ subordinance relationships in mice.     

Intermale aggression in mice,selected for the cognitive trait

The data are presented on intermale aggression in mice which were selected for high scores of cognitive trait (the ability for extrapolation of movement direction) in comparison to the data of control mice performance. The changes in aggression level in the course of selection are presumably connected with anxiety level which also changed during selection generations.     

Playing to an audience: the social environment influences aggression and victory displays

Animal behaviour studies have begun to incorporate the influence of the social environment, providing new opportunities for studying signal strategies and evolution. We examined how the presence and sex of an audience influenced aggression and victory display behaviour in field-captured and laboratory-reared field crickets (Gryllus veletis). Audience type, rearing environment and their interaction were important predictors in all model sets. Thus, audience type may impose different costs and benefits for competing males depending on whether they are socially experienced or not. Our results suggest that field-captured winners, in particular, dynamically adjust their contest behaviour to potentially gain a reproductive benefit via female eavesdropping and may deter future aggression from rivals by advertising their aggressiveness and victories.     

Social Relationships among Males in Multimale Siamang Groups

I quantified social and spatial interactions among adults in 4 multimale siamang (Symphalangus syndactylus) groups to evaluate the importance of aggression and avoidance in mediating male-male relationships. Actual genetic relationships among adults are unknown, but available mitochondrial data suggest that in 3 of 4 groups, neither male was the offspring or maternal sibling of the female, whereas in the fourth group, a matrilineal relationship between the female and 1 adult male was not excluded. Rates of aggression involving male-male dyads were very low. One male-female dyad maintained closer spatial cohesion than those of other adult dyads in 3 of 4 groups. Nonetheless, all adult males spent substantial percentages of their time ≤20 m from other adults in their groups. The percentages of time that male-male dyads spent in social grooming interactions did not differ from those of male-female dyads. In 3 groups, both males copulated with the group female. While previous studies have reported high rates of aggression between adult males and subadult male group members in siamangs, my results suggest that male-male relationships in multimale groups at Way Canguk were relatively harmonious. Acceptance of multimale grouping (and in some cases sexual polyandry) suggests that the benefits outweigh the costs under some circumstances. If there was a genetic relationship between males, then tolerance of delayed dispersal and copulation with the adult female may function as a form of parental investment. Males may also benefit from multimale grouping via enhanced territorial defense or reduced costs of mate defense.     

Different effects of intensity and duration of locomotor activity on circadian period

An outstanding unresolved issue in chronobiology is how the level of locomotor activity influences length of the free-running, endogenous circadian period (tau). To address this issue, the authors studied a novel model, 4 replicate lines of laboratory house mice (Mus domesticus) that had been selectively bred for high wheel-running activity (S) and their 4 unselected control (C) lines. Previous work indicates that S mice run approximately twice as many revolutions/day and exhibit an altered dopaminergic function as compared with C mice. The authors report that S mice have a tau shorter by about 0.5 h as compared with C mice. The difference in tau was significant both under constant light (control lines: tau = 25.5 h; selected: tau = 24.9 h) and under constant dark (control lines: 23.7 h; selected: 23.4 h). Moreover, the difference remained statistically significant even when the effects of running speed and time spent running were controlled in ANCOVA. Thus, something more fundamental than just intensity or duration of wheel-running activity per se must underlie the difference in tau between the S and C lines. However, despite significant difference in total wheel-running activity between females and males, tau did not differ between the sexes. Similarly, among individuals within lines, tau was not correlated with wheel-running activity measured as total revolutions per day. Instead, tau tended to decrease with average running speed but increase with time spent running. Finally, within individuals, an increase in time spent running resulted in decreased tau in the next few days, but changes in running speed had no statistically significant effect. The distinctions between effects of duration versus intensity of an activity, as well as between the among- versus within-individual correlations, are critical to understanding the relation between locomotor activity and pace of the circadian clock.     

Neural steroid sensitivity and aggression: comparing individuals of two songbird subspecies

Hormones coordinate the expression of complex phenotypes and thus may play important roles in evolutionary processes. When populations diverge in hormone‐mediated phenotypes, differences may arise via changes in circulating hormones, sensitivity to hormones or both. Determining the relative importance of signal and sensitivity requires consideration of both inter‐ and intrapopulation variation in hormone levels, hormone sensitivity and phenotype, but such studies are rare, particularly among closely related taxa. We compared males of two subspecies of the dark‐eyed junco (Junco hyemalis) for territorial aggression and associations among behaviour, circulating testosterone (T), and gene expression of androgen receptor (AR), aromatase (AROM) and oestrogen receptor α in three behaviourally relevant brain regions. Thus, we examined the degree to which evolution may shape behaviour via changes in plasma T as compared with key sex steroid binding/converting molecules. We found that the white‐winged junco (J. h. aikeni) was more aggressive than the smaller, less ornamented Carolina junco (J. h. carolinensis). The subspecies did not differ in circulating testosterone, but did differ significantly in the abundance of AR and AROM mRNA in key areas of the brain. Within populations, both gene expression and circulating T co‐varied significantly with individual differences in aggression. Notably, the differences identified between populations were opposite to those predicted by the patterns among individuals within populations. These findings suggest that hormone–phenotype relationships may evolve via multiple pathways, and that changes that have occurred over evolutionary time do not necessarily reflect standing physiological variation on which current evolutionary processes may act.     

Inbred and furious: negative association between aggression and genetic diversity in highly inbred fish

Aggressive behaviour plays an important role in securing resources, defending against predators and shaping social interactions. Although aggression can have positive effects on growth and reproductive success, it is also energetically costly and may increase injury and compromise survival. Individual genetic diversity has been positively associated with aggression, but the cause for such an association is not clear, and it might be related to the ability to recognize kin. To disentangle the relationships between genetic diversity, kinship and aggression, we quantified aggressive behaviour in a wild, self‐fertilizing fish (Kryptolebias marmoratus) with naturally variable degrees of genetic diversity, relatedness and familiarity. We found that in contrast to captive fish, levels of aggression among wild K. marmoratus are positively associated with individual homozygosity, but not with relatedness or familiarity. We suggest that the higher aggression shown by homozygous fish could be related to better kin discrimination and may be facilitated by hermaphrodite competition for scarce males, given the fitness advantages provided by outcrossing in terms of parasite resistance. It seems likely that the relationship between aggression and genetic diversity is largely influenced by both the environment and population history.     

Effect of group size on the aggression strategy of an extirpating stingless bee, Trigona spinipes

Summary. Group aggression influences communication and defense strategies in many social insect communities. Such aggression plays a particularly significant role in the lives of stingless bees, important native Neotropical pollinators, in which the battle for food resources can be deadly and critical to colony survival. However, the effects of group size on individual aggression levels and the spatio-temporal aggression strategy of communal aggressors have not been fully explored. We therefore investigated how group size affects the aggression levels and the spatio-temporal attack strategy (which body parts, and the amount of time spent in attacking each part) in close combats between Trigona spinipes foragers and a natural competitor, Melipona rufiventris. In all trials, T. spinipes foragers competitively excluded M. rufiventris foragers from nearby feeders, exhibiting four levels of aggressive behavior ranging from threat displays to prolonged grappling and decapitation. Surprisingly, aggression levels and spatial strategy corresponded to the size of group attacks. Larger groups of attackers used individually lower aggression levels than small groups of attackers. Smaller groups also attacked appendages linked to escape (legs and wings) with greater frequency than larger groups, which focused on vital central body areas (abdomen, thorax, and head). Increased aggression corresponded to increased risks for attackers and the attacked. All combatants engaging at the highest level of aggression died (100% mortality). Thus the dominance style of T. spinipes may minimize attack risk and maximize victim harm with finely tuned hostility.Received 22 May 2004; revised 18 August 2004; accepted 26 October 2004.     

Thyroid gland responses to intermale aggression in an inherently aggressive wild rat

The aim of the present investigation was to ascertain whether intermale aggression (by fighting) affects thyroid gland activity in wild rat. Following intermale aggression for three hours, thyro-follicular epithelial height was significantly decreased and colloidal content in follicular lumen increased only in the subordinate rats whereas the thyroid gland of the dominant rats was not perceptibly changed. Thus, aggression inhibits thyroid gland activity only in the subordinate rats. It is suggested that this effect may be due to psychosomatic rather than physical stress during aggression.     

Effects of intracranial implants of testosterone propionate on intermale aggression in the castrated male mouse

Three experiments were conducted in order to assess the effects of intracranial implants of testosterone propionate (TP) on intermale aggression in the castrate male CF-1 mouse. In Experiment 1, seven groups received bilateral implants containing a total of 27 μg crystalline TP into the septum, neocortex, lateral ventricles, preoptic-anterior hypothalamus, hippocampus, medial reticular formation, and subcutaneously, and were tested 2 and 4 days after treatment. An eighth group received blank pellets in the brain. Animals receiving septal or lateral ventricle implants fought significantly more than other groups on trial 1. This difference had disappeared by trial 2, indicating diffusion of the hormone. The diffusion was corroborated by significant seminal vesicle growth. In Experiment 2 animals received bilateral implants of a total of 4.5 μg TP in paraffin or a blank pellet into the septum, preoptic-anterior hypothalamus, cortex, amygdala, olfactory bulbs, medial reticular formation, or subcutaneously. None of these treatments proved effective for activating aggression. Experiment 3 explored the activational effects of 10 μg of TP implanted bilaterally into the same areas as in Experiment 2, excluding the olfactory bulbs and cortex. Implants into the septum were followed by significantly increased fighting. Implants into the preoptic area were only marginally effective whereas the remaining two areas were not responsive to hormone treatment and did not differ from control animals. No seminal vesicle growth was detected as a result of the hormone treatments. These results would indicate that the septum is important in the control of androgen-dependent, intermale aggression in the male CF-1 mouse.     

Endocrine correlates of rank,reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata)

Fecal testosterone and cortisol levels in six wild male Japanese macaques (Macaca fuscata), three of high rank and three of low, were analyzed to investigate the hormonal correlates of rank, reproduction, and female-directed aggression. The study encompassed the 6-month mating season, from October 1999 to March 2000, during which time 251 fecal samples and approximately 550 h of behavioral data were collected. Dominant males were not found to differ from subordinate males in overall rates of aggressive or copulatory behavior. Likewise, testosterone excretion, which peaked in the early part of the mating season and declined gradually thereafter, did not differ significantly by rank. High-ranking males, however, were observed to excrete significantly higher levels of cortisol than low-ranking males, suggesting that dominance may carry costs. The two hormones were found to be inversely correlated in the two most dominant males, but independent in all others. Rate of noncontact aggression was significantly correlated with testosterone, while no significant relationships were observed between testosterone and contact aggression nor any aspect of copulatory behavior. These data further support the contention that social subordinance and stress are not inexorably linked, as well as suggest that elevated glucocorticoid concentrations in high-ranking males may reflect increased metabolic costs associated with dominant male reproductive strategy.     

Effect of type of opponent on aggression in male mice with particular reference to studies with antihormones

The potential influence of the type of opponent used in intermale aggression encounters to assess the actions of drugs was examined. Two experiments were carried out, one with the antiandrogen Cyproterone Acetate and the other with the antioestrogen CI-680 (both administered every three days over 25 days). In both experiments the antihormone-treated subjects encountered different opponents, namely: a) an antihormone-treated male, b) a non aggressive anosmic male or c) a vehicle-treated male. Vehicle-treated subjects also confronted a vehicle-treated or an anosmic opponent. The behaviour displayed by antihormone-treated subjects varied according to the characteristics of the partner, suggesting that the effects of drugs might be interpreted differently depending on the type of animal employed as an adversary. In fact, some of the apparently contradictory results reported in the literature seem to be consequences of the utilisation of different kinds of opponents. It is concluded that the choice of the opponent is of paramount importance in the study of drug actions on intermale aggression tests and that using more than one type of opponent can provide more complete information about the actions of particular drugs.     

Laboratory model of adaptive radiation: a selection experiment in the bank vole

In a laboratory colony of a wild rodent, the bank vole Myodes (=Clethrionomys) glareolus, a multiway artificial selection experiment was applied to mimic evolution toward high aerobic metabolism achieved during locomotor activity, predatory behavior, and ability to cope with herbivorous diet. Four lines for each of the selection directions and four unselected control lines have been maintained. After three generations of within-family selection, the maximum rate of oxygen consumption achieved during swimming was 15% higher in the selected than in the control lines (least square means, adjusted for body mass: 252.0 vs. 218.6 mL O(2)/h, P = 0.0001). When fed a low-quality diet made of dried grass, voles from the lines selected for ability to cope with herbivorous diet lost about 0.7 g less mass than voles from the control lines (-2.44 vs. -3.16 g/4 d, P = 0.008). In lines selected for predatory behavior toward crickets, proportion of "predatory" individuals was higher than in the control lines (43.6% vs. 24.9%; P = 0.045), but "time to capture" calculated for the successful trials did not differ between the lines. The experiment continues, and the selected lines of voles will provide a unique model for testing hypotheses concerning correlated evolution of complex traits.