Ecology and multilevel selection explain aggression in spider colonies

Progress in sociobiology continues to be hindered by abstract debates over methodology and the relative importance of within‐group vs. between‐group selection. We need concrete biological examples to ground discussions in empirical data. Recent work argued that the levels of aggression in social spider colonies are explained by group‐level adaptation. Here, we examine this conclusion using models that incorporate ecological detail while remaining consistent with kin‐ and multilevel selection frameworks. We show that although levels of aggression are driven, in part, by between‐group selection, incorporating universal within‐group competition provides a striking fit to the data that is inconsistent with pure group‐level adaptation. Instead, our analyses suggest that aggression is favoured primarily as a selfish strategy to compete for resources, despite causing lower group foraging efficiency or higher risk of group extinction. We argue that sociobiology will benefit from a pluralistic approach and stronger links between ecologically informed models and data.     

THE ROLE OF MULTILEVEL SELECTION IN THE EVOLUTION OF SEXUAL CONFLICT IN THE WATER STRIDER AQUARIUS REMIGIS

In evolution, exploitative strategies often create a paradox in which the most successful individual strategy “within” the group is also the most detrimental strategy “for” the group, potentially resulting in extinction. With regard to sexual conflict, the overexploitation of females by harmful males can yield similar consequences. Despite these evolutionary implications, little research has addressed why sexual conflict does not ultimately drive populations to extinction. One possibility is that groups experiencing less sexual conflict are more productive than groups with greater conflict. However, most studies of sexual conflict are conducted in a single isolated group, disregarding the potential for selection among groups. We observed Aquarius remigis water striders in a naturalistic multigroup pool in which individuals could freely disperse among groups. The free movement of individuals generated variation in aggression and sex‐ratio among groups, thereby increasing the importance of between‐group selection compared to within‐group selection. Females dispersed away from local aggression, creating more favorable mating environments for less‐aggressive males. Furthermore, the use of contextual analysis revealed that individual male aggression positively predicted fitness whereas aggression at the group level negatively predicted fitness, empirically demonstrating the conflict between levels of selection acting on mating aggression.     

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.     

Heightened aggressive behavior in mice with lifelong versus postweaning knockout of the oxytocin receptor

Previous work implicating the neuropeptide oxytocin (Oxt) in the neural regulation of aggression in males has been limited. However, there are reports of heightened aggression in Oxt knockout and Oxt receptor (Oxtr) knockout male mice when they are born to null mutant mothers; suggesting that intrauterine exposure to Oxt may be important to normal aggression in adulthood. To explore this, we examined aggression in two lines of Oxtr mice, a total knockout (Oxtr-/-), in which the Oxtr gene is absent from the time of conception, and a predominantly forebrain specific knockout (Oxtr FB/FB), in which the Oxtr gene is not excised until approximately 21-28days postnatally. Aggression was measured in males from both lines, as well as control littermates, using a resident-intruder behavioral test. Consistent with previous reports, male Oxtr-/- mice had elevated levels of aggression relative to controls. Oxtr FB/FB mice on the other hand displayed levels of aggression similar to control animals. In addition, following a resident-intruder test, Oxtr+/+ mice that displayed aggression had less c-fos immunoreactivity in the ventral portion of the lateral septum than those that did not. Further, Oxtr-/- mice had increased c-fos immunoreactivity in the medial amygdala relative to controls. These data suggest that Oxt may play an important role during development in the organization of the neural circuits that underlie aggressive behavior in adulthood, with its absence resulting in heightened aggression.     

Territorial Behaviour and Social Organization as a Function of the Level of Aggressiveness in Male Mice

Territoriality and social organization were examined in relation to different genetic dispositions for aggressive behaviour. The animals used in the study were male mice of the 51st and 52nd generation of selection for high (Turku Aggressive, TA) and low (Turku Non-Aggressive, TNA) levels of aggressiveness. The level of aggressiveness of the animals was assessed by means of individual tests with non-aggressive standard opponents, after which they were allowed to form individual territories in a 102 times 204 times 90 cm enclosure. TA and TNA males were placed in different enclosures. After 2 wk, when the partitions between individual pens were removed, the behaviour of the animals was observed for a 7-d period. Excessive fighting between the highly aggressive TA males occurred, resulting in the formation of dominant-subordinate relationships. A great number of attacks inflicted were found to be associated with dominance in the colony, and correlated with a high level of aggressiveness when the animals were individually tested for aggression after having been in colony environments. The level of aggressiveness of the TA males that had become subordinates had significantly decreased. The TNA males fought less and were more often found to stay in their original territory for the entire period of observation. The results suggest that different genotypes for aggression arc related to differences in territoriality and social organization in mice.     

PNMT transgenic mice have an aggressive phenotype.

PNMT (phenylethanolamine-N-methyl-transferase) is the enzyme that catalyzes the formation of epinephrine from norepinephrine. In transgenic mice over-expressing PNMT, observations revealed a very high level of aggression compared to their background strain, C57BL/6J. To evaluate the influence of PNMT on aggression and emotionality in this transgenic line, single-sex male and female groups were independently established that consisted of either four wild-type mice or four transgenic mice overexpressing PNMT. The members of each group were littermates. Mixed single-sex groups consisting of two transgenic mice and two wild-type mice were also established. Almost no fights were observed within the female groups. In males, the transgenic line showed a significantly higher level of fighting than controls (p=0.007) and mixed male groups (p=0.02). Housing mice from the transgenic line in mixed groups with wild-type mice seems to decrease the level of aggression in the transgenic line. In conclusion, this is the first study to demonstrate a clear, significant increase in aggression arising from PNMT overexpression. This suggests an important role for central epinephrine levels in aggressive behavior.     

Impaired social recognition in male mice with repeated experience of aggression

Social recognition is crucial for many aspects of animal behavior in stabilized population. Preliminary data proposed impairment of social recognition in male mice with long experience of aggression. To check this hypothesis, experiments with male mice with different aggressive experience (during 2 and 20 days) were performed. Two types of losers were used as partners: losers with active defense reactions and losers displaying submissive postures. The enhanced aggressive motivation was found in both groups of aggressors. Mice with short aggressive experience demonstrated intensive attacks toward the active losers and decreased aggression directed to submissive losers. Mice with long aggressive experience did not change their behavior depending on a type of the partner and displayed a high level of aggression as a result of dominant aggressive motivation and impaired social recognition.     

Predatory aggression, but not maternal or intermale aggression, is associated with high voluntary wheel-running behavior in mice

Predatory (towards crickets), intermale, and maternal aggression were examined in four replicate lines of mice that had been selectively bred for high wheel-running (S) and in four random-bred control lines (C). In generation 18, individual differences in both predatory and intermale aggression were significantly consistent across four trial days, but predatory and intermale aggression were uncorrelated both at the individual level and among the eight line means. Latencies to attack crickets were significantly lower in S lines as a group. Intermale aggression, however, did not differ between S and C lines. S lines were significantly smaller in body mass, but did not differ in either testes mass or plasma testosterone. In generations 28 and 30, respectively, S and C lines did not differ in either maternal or intermale aggression. However, significant differences among the individual lines were found for maternal aggression, and one S line exhibited an extremely high mean time of aggression (>120 sec for a 5-min test). Maternal and intermale aggression were not correlated among the eight line means or at the level of individual variation. Overall, our results suggest: (1) predatory aggression and voluntary wheel-running are positively related at the genetic level; (2) predatory and intermale aggression are unrelated at a genetic level; and (3) maternal and intermale aggression are not tightly related at the genetic level. Possible relationships between predatory aggression, dopamine, and wheel-running behavior are discussed.     

Proximate perspectives on the evolution of female aggression: good for the gander,good for the goose?

Female–female aggression often functions in competition over reproductive or social benefits, but the proximate mechanisms of this apparently adaptive behaviour are not well understood. The sex steroid hormone testosterone (T) and its metabolites are well-established mediators of male–male aggression, and several lines of evidence suggest that T-mediated mechanisms may apply to females as well. However, a key question is whether mechanisms of female aggression primarily reflect correlated evolutionary responses to selection acting on males, or whether direct selection acting on females has made modifications to these mechanisms that are adaptive in light of female life history. Here, I examine the degree to which female aggression is mediated at the level of T production, target tissue sensitivity to T, or downstream genomic responses in order to test the hypothesis that selection favours mechanisms that facilitate female aggression while minimizing the costs of systemically elevated T. I draw heavily from avian systems, including the dark-eyed junco (Junco hyemalis), as well as other organisms in which these mechanisms have been well studied from an evolutionary/ecological perspective in both sexes. Findings reveal that the sexes share many behavioural and hormonal mechanisms, though several patterns also suggest sex-specific adaptation. I argue that greater attention to multiple levels of analysis—from hormone to receptor to gene network, including analyses of individual variation that represents the raw material of evolutionary change—will be a fruitful path for understanding mechanisms of behavioural regulation and intersexual coevolution.     

The Use of Cage Enrichment to Reduce Male Mouse Aggression

The complete cleaning of cages has been shown to reduce the level of intermale aggression in mice. This study investigated the effects of the addition of enrichment objects on postcage-cleaning aggression in male BALB/c mice. Enrichment objects were found to significantly reduce aggressive interactions during this period for up to 7 weeks and can make an overall economic saving to husbandry costs.     

The Use of Cage Enrichment to Reduce Male Mouse Aggression

The complete cleaning of cages has been shown to reduce the level of intermale aggression in mice. This study investigated the effects of the addition of enrichment objects on postcage-cleaning aggression in male BALB/c mice. Enrichment objects were found to significantly reduce aggressive interactions during this period for up to 7 weeks and can make an overall economic saving to husbandry costs.     

Neurobiological correlates premeditated (learned) aggression: seeking new experimental approaches]

Theoretical possibility of experimental modeling of learned (premediated) aggression developing in human after experience of aggression is considered. The sensory contact technique increases aggressiveness in male mice and allows aggressive type of behavior to be formed as a result of repeated experience of victories in daily agonistic confrontations. Some behavioral domains confirm the development of learned aggression in males similar to those in humans. The features are: repeated experience of aggression reinforced by victories; elements of learned behavior after period of confrontations; intent, measured by increase of the aggressive motivation prior agonistic confrontation; decreased emotionality estimated by parameters of open field behavior. Relevant stimuli provoke demonstration of aggression. This review summarized data on the influence of positive fighting experience in daily intermale confrontations on the behavior, neurochemistry and physiology of aggressive mice (winners). This sort of experience changes many characteristics in individual and social behaviors, these having been estimated in different tests and in varied situations. Some physiological parameters are also changed in the winners. Neurochemical data confirm the activation of brain dopaminergic systems and functional inhibition of serotonergic system in winners under influence of repeated experience of aggression. The expression of the neurochemical and behavioral changes observed in winners has been found dependent on the mouse strain and on the duration of their agonistic confrontations. Similarities in mechanisms of learned aggression in humans and mice are considered.     

Changes in male odours and urinary marking patterns due to inhibition of aggression in male mice

The effects of active inhibition of aggression on male odours and urinary marking patterns were studied in mice belonging to a highly aggressive strain the TA (Turku Aggressive), which has been developed by selective breeding through 37 generations. These males were defeated by trained fighters until they showed no aggression. Individually housed TA males served as controls. Mice from the parental or Normal Strain, which is intermediate in aggression, were exposed to the odours. The males from the Normal Strain were tested for aggression against male castrates to which urine from the two types of TA males or water had been applied. The urine from the highly aggressive control TA males evoked most aggression. The Normal males were later tested against castrates on soiled sawdust. Fewer attacks occured on sawdust soiled by the urine from the control TA males. The preferences for areas covered with soiled sawdust were also assessed. The males from the Normal Strain preferred areas soiled by the TA males trained to nonaggressiveness while the females preferred areas soiled by the highly aggressive control TA males. Subsequently the size and number of urinary marks deposited were examined. The TA males trained to nonaggressiveness voided urine in fewer but larger pools. The differences showed the same direction as those previously found between the TA and TNA strains, selectively bred for aggression and non-aggression, respectively. In mice the odour signals and urinary marking patterns seem to be correlated with the level of aggressiveness, either hereditarily determined or acquired through learning.     

Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice

In three genuses and four species of rodents, housing in winter-like short days (8L:16D) increases male aggressive behavior. In all of these species, males undergo short-day induced regression of the reproductive system. Some studies, however, suggest that the effect of photoperiod on aggression may be independent of reproductive responses. We examined the effects of photoperiod on aggressive behavior in California mice (Peromyscus californicus), which do not display reproductive responsiveness to short days. As expected, short days had no effect on plasma testosterone. Estrogen receptor alpha and estrogen receptor beta immunostaining did not differ in the lateral septum, medial preoptic area, bed nucleus of the stria terminalis, or medial amygdala. However, males housed in short days were significantly more aggressive than males housed in long days. Similar to previous work in beach mice (Peromyscus polionotus), estradiol rapidly increased aggression when male California mice were housed in short days but not when housed in long days. These data suggest that the effects of photoperiod on aggression and estrogen signaling are independent of reproductive responses. The rapid action of estradiol on aggression in short-day mice also suggests that nongenomic mechanisms mediate the effects of estrogens in short days.     

Mice: progesterone stimulates aggression in pregnancy-terminated females

Three experiments were conducted in order to assess the role of progesterone (P) in the aggressive behavior displayed by late pregnant Rockland-Swiss mice toward adult male intruders. In Experiment 1, hysterectomy on the 15th day of gestation reduced the aggressive behavior normally displayed by pregnant mice toward male intruders. In Experiment 2, Silastic implants of P stimulated aggression in hysterectomized mice but did not fully restore the behavior to the level of fighting normally observed in pregnant animals. In Experiment 3, aggressive behavior in P-treated hysterectomized animals was inhibited by simultaneous exposure to estradiol (E). Also, treatment with E alone did not stimulate aggression in hysterectomized mice. While pregnancy-induced aggression is promoted by P, other neuroendocrine factors may act in concert with the steroid to fully stimulate aggression in gravid mice.     

The neurochemical control of aggression and submission]

Neurochemical mechanisms of agonistic behaviour in different models of aggression are discussed. The effects of aggression and submission experience in 10 mice intermale confrontations under conditions of sensory contact on the levels of brain neurotransmitters and their metabolites were investigated in 7 brain areas. The values obtained in aggressive and control, or submissive and control, animals were compared. In this comparison neurochemical alterations specific for aggressive or submissive behaviours, or nonspecific became apparent. The long experience of victories leads to activation of dopaminergic system through DA catabolism which leads to DOPAC formation. The long experience of defeats increases the 5HT metabolism and decreases NA level in some brain areas. The dopaminergic system of Nucleus accumbens and midbrain are nonspecifically activated in both aggressive and submissive animals. The investigation of values obtained in animals with conversion of behavioural type (after defeat of previously aggressive animals and/or display of aggressive reaction by previously submissive mice) allowed to find many significant differences between aggressive, submissive and "converted" males; in particular the amygdala is the site of opposite changes in 5HT system during inversion of aggressive or submissive behaviours. The above data evidence for the specific role of transmitter systems and brain structures in maintaining or inversion of different types of agonistic behaviour.     

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.     

Indirect Genetic Effects and Housing Conditions in Relation to Aggressive Behaviour in Pigs

Indirect Genetic Effects (IGEs), also known as associative effects, are the heritable effects that an individual has on the phenotype of its social partners. Selection for IGEs has been proposed as a method to reduce harmful behaviours, in particular aggression, in livestock and aquaculture. The mechanisms behind IGEs, however, have rarely been studied. The objective was therefore to assess aggression in pigs which were divergently selected for IGEs on growth (IGEg). In a one generation selection experiment, we studied 480 offspring of pigs (Sus scrofa) that were selected for relatively high or low IGEg and housed in homogeneous IGEg groups in either barren or enriched environments. Skin lesion scores, a proxy measure of aggression, and aggressive behaviours were recorded. The two distinct IGEg groups did not differ in number of skin lesions, or in amount of reciprocal fighting, both under stable social conditions and in confrontation with unfamiliar pigs in a 24 h regrouping test. Pigs selected for a positive effect on the growth of their group members, however, performed less non-reciprocal biting and showed considerably less aggression at reunion with familiar group members after they had been separated during a 24 h regrouping test. The enriched environment was associated with more skin lesions but less non-reciprocal biting under stable social conditions. Changes in aggression between pigs selected for IGEg were not influenced by G×E interactions with regard to the level of environmental enrichment. It is likely that selection on IGEg targets a behavioural strategy, rather than a single behavioural trait such as aggressiveness.     

Studies on tube restraint-induced attack on a metal target by laboratory mice

This study examines factors influencing the attack on a metal target by laboratory ‘TO’ strain mice confined within a narrow perspex tube and contrasts this form of behaviour with attack seen in less equivocal forms of ‘aggression test’. The effects of sex, housing condition, reproductive experience, density, anosmia and castration (in the male) were systematically examined. This ‘model’ of ‘aggression’ shows few parallels with social conflict, parental defense and electroshock-induced forms of attack as none of the above manipulations influenced the level of target biting in this situation. Thus, in spite of claims that tube restraint-induced attack may show parallels with intermale aggression, the data suggest that it involves a totally different motivation.     

Changes in the sexual tendency accompanying selection for aggressiveness in the three-spined stickleback,Gasterosteus aculeatus L.*

Independent selection experiments for reduced juvenile and reduced territorial aggression levels in male three-spined sticklebacks both resulted in reduced courtship aggression levels. In the low juvenile aggression line this is accompanied by an enhanced sexual activity, but in the low territorial aggression line males display a reduced sexual activity. These results are consistent with a mutually inhibitory relationship between the aggressive and sexual tendencies, if selection for juvenile aggressiveness has only affected the aggressive tendency while selection for territorial aggressiveness has simultaneously affected the aggressive and sexual tendencies in the same direction. This is in agreement with the hormonal changes (pituitary-gonadal axis) suggested by the selection studies.