Social Experience During Development and Female Offspring Aggression in Peromyscus Mice

Cross‐fostering between the highly aggressive, biparental California mouse (Peromyscus californicus) and the less aggressive, less parental white‐footed mouse (P. leucopus) influences female offspring attack latency in California mice, but not in white‐footed mice. Adult female California mice raised by white‐footed mice expressed longer attack latencies in a neutral‐arena test but not in a resident‐intruder test. One social cue that may be used by offspring to develop environmentally appropriate levels of aggression is the type of parental care during development. In California mice, a composite score of maternal behavior was positively associated with neutral‐arena aggression as indicated by decreased attack latency. In both species, paternal nest‐building was positively associated with neutral‐arena aggression and higher maternal retrieval behavior predicted higher offspring resident‐intruder aggression as indicated by decreased attack latency. Together, these results indicate that parental behavior has the potential to shape the development of attack latency in female offspring.     

The Association Between Male Offspring Aggression and Paternal and Maternal Behavior of Peromyscus Mice

Parents influence offspring aggression through genetic and non‐genetic mechanisms, although the latter are less well understood. To examine potential non‐genetic effects of parents on offspring, we cross‐fostered the highly aggressive and biparental California mouse (Peromyscus californicus) and the less aggressive, less parental white‐footed mouse (Peromyscus leucopus). In‐fostered animals within each species were used as controls. We examined associations between the foster parents’ behavior and aggression of the fostered male offspring in resident–intruder (R–I) and neutral arena aggression tests. When both species and fostering groups were combined, R–I aggression of offspring was positively associated with paternal time spent retrieving pups. In contrast, aggression in a neutral arena was negatively associated with a composite score of maternal behavior. We discuss how our findings regarding paternal retrievals may explain previously reported effects of cross‐fostering on male aggression.     

Effects of a short period of isolation in adulthood on the aggressive behavior of dominant and subordinate male mice

Male ddY mice were used to investigate the effect of a short period of isolation in adulthood on aggressive behavior. The relationship between the dominance status previous to isolation and the effect of isolation was investigated. The mice were kept in isolation for 3 weeks from 9 weeks of age, during which intruder tests were conducted once a week. They the went through an encounter test, in which the mice encountered dominant or subordinate mice in a neutral space. The number of the formerly-dominant isolated mice that attacked the intruder mice decreased at first and then increased. The latency to attack also lengthened at first and then shortened. Seven former-dominants continued to show aggression throughout the intruder The number of the formerly-subordinate isolated mice that attacked the intruder mice increased linearly. But 3 former-subordinates did not show aggression through the entire experiment. After 3 weeks isolation, the number of mice that showed aggression and the amount of aggression did not differ between the former-dominants and subordinatcs. Isolation housing was concluded to differentially affect the dominant and subordinate mice during the 3 weeks of isolation. It was also concluded to differentially affect the mice of absolute dominance and relative dominance differentially. The aggressive behavior of the isolated mice appears to occur independently of site.     

Intermale aggression of subordinate resident long-evans rats

Dominant male rats were separated from their colonies and subordinate residents were tested for aggression after a two week period. Subordinate animals showed significant increases in body weight and aggressive behavior toward intruders. Replacement of the previously dominant male led to rank reversals in three of six colonies. To assess whether two weeks of separation from the dominant male was necessary for subordinate males to exhibit aggression towards conspecifics, another intruder test was given following an additional two weeks of social housing. At the conclusion of this test, the more aggressive resident was removed and a naive intruder was immediately introduced into the colony with the subordinate male resident and again at 1, 5, and 10 day intervals. Aggressive posturing by the subordinate resident increased immediately following the removal of the dominant male, and remained at a high level throughout the subsequent intruder tests. In contrast, biting was initially low but increased steadily throughout the period of separation. These findings demonstrated that social or situational changes within a colony can greatly influence the aggression of subordinate males.     

The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus

There is a growing body of evidence that the rapid but transient increase in male androgens, particularly testosterone (T), following a single social encounter such as a territorial intrusion occurs in a wide array of vertebrate taxa. Yet, this phenomenon, often called the Challenge Hypothesis, has rarely been investigated in females. Moreover, when studying male challenge effects, researchers have rarely investigated other hormones that can be important to the expression of aggression, such as progesterone (P4) and estradiol (E2). We conducted 10-min aggression trials using the resident-intruder paradigm in cycling female California mice, Peromyscus californicus, a species in which both sexes show territorial behavior. By comparing the hormone levels of test females to control females, we found a decrease in P(4) and the P4/T ratio, but no change in T, E2, corticosterone, E2/P4, or E2/T. Interestingly, these hormone changes were observed even when the resident was not aggressive toward the intruder, suggesting that the stimulus cueing the hormone changes was the mere presence of the intruder and not the amount of aggression displayed by the resident. Generally, T has a positive relationship with aggression, whereas P4 inhibits male and nonmaternal female aggression. Thus, decreasing the P4/T ratio following an encounter may serve to increase future aggression in females. These results suggest that females may use different hormonal mechanisms than do males to mediate aggression in a challenge situation.     

Effects of castration and home cage residency on aggressive behavior in rats

The effects of castration of both resident and intruder rats on territorial aggressive behavior were studied. The results suggest that residence in a home cage is more important than gonadal status in determining the outcome of an aggressive encounter. Resident rats were more likely to be dominant especially if they were intact. Intact residents directed less aggressive behavior toward castrated intruders than toward intact intruders. Intruder rats generally showed low levels of aggressive behavior and were only dominant when the resident had been castrated. Thus, the aggressive behavior of a male rat depends upon both his gonadal status and that of his opponent.     

Female marmosets' behavioral and hormonal responses to unfamiliar intruders

The endocrine control mechanisms for female mammalian aggression have been largely unstudied. Although it has been proposed that androgens may modulate female aggressive behavior in a similar manner to males, very little conclusive evidence exists. Previous work in male marmosets found that post‐encounter increases in testosterone (T) were dependent on the intensity of aggression displayed during the aggressive encounter. We exposed female marmosets (Callithrix kuhlii), a monogamous and biparental primate, to aggressive interactions with unfamiliar intruders. Individual female marmosets exhibited changes in T and estradiol (E₂) that are associated with aggressiveness dependent on the intensity of aggression displayed as well as their role during the encounter. Resident females exhibited increased E₂ immediately following an encounter in which they displayed high rates of aggression. If resident females received high rates of aggression from the intruder, the resident displayed increased T 24 hr following the encounter. Interestingly, if the female was an intruder in the encounter, the intensity of her aggression was associated with increased cortisol immediately following the trials, whereas received aggression was associated with increased T and E₂ immediately following the trial. Female primates do exhibit situation‐dependent changes in gonadal steroids in association with aggression that may serve to prime them for future aggressive interactions. Am. J. Primatol. 73:1072–1081, 2011. © 2011 Wiley‐Liss, Inc.     

Inter-male aggression with regard to polygynous mating system in Pampean grassland mouse, Akodon azarae (Cricetidae: Sigmodontinae)

Based on the hypothesis that, in Akodon azarae, polygyny operates through female defence, we studied inter-male aggression in order to test the following predictions: during the breeding period (1) resident males are more aggressive than intruder males in the presence of females (FP), and (2) aggressive behaviour is independent of male condition (resident or intruder) in the absence of females (FA). To test our predictions, we used the resident male behavioural response towards an intruder male in relation to FP or FA. We conducted 30 encounters in FP and 27 in FA in 0.79-m² round enclosures placed in the Espinal Reservation. Our results support the prediction that, in FP, the intensity of aggressive behaviour exhibited by males varied in relation to resident or intruder condition. Resident males showed high levels of aggression towards intruders, and intruders exhibited the greatest values of submissive behaviours with residents. In FA, the intensity of aggressive behaviour did not vary in relation to resident or intruder condition. Both resident and intruder males exhibited low aggressive behaviour and inter-male encounters resulted mainly in non interactive behaviours. Our results support the hypothesis that, in A. azarae, the polygynous mating system operates through female defence.     

Maternal aggression and intermale social aggression: a behavioral comparison

The aggressive behavior of alpha male rats and lactating females were each examined toward an intact adult male rat, a castrated adult male rat, an anesthetized adult male rat, a nonlactating adult female rat, an adult albino guinea pig (male or female), or an albino mouse (male or female). When in their living colony, females displayed high levels of aggressiveness toward all stimulus objects except a mouse. The aggression toward the intruding males occurred whether the female's pups were present or not. Alpha males were aggressive toward the same stimuli except an intruding female rat and a mouse. When tested in an unfamiliar colony, the males but not the females (with or without pups present) were aggressive toward an adult male rat. Half of the females but none of the males displayed defensive burying toward an anesthetized intruder. It is suggested that the attack on an adult female, the absence of attack outside of the resident colony, and the tendency to display defensive burying are features of the aggressiveness of lactating females that are fundamentally different from the aggressiveness of alpha males. The form of the aggression (lateral attack vs. lunge attack) was only quantitatively different in males and females.     

The Resident-intruder Paradigm: A Standardized Test for Aggression,Violence and Social Stress

This video publication explains in detail the experimental protocol of the resident-intruder paradigm in rats. This test is a standardized method to measure offensive aggression and defensive behavior in a semi natural setting. The most important behavioral elements performed by the resident and the intruder are demonstrated in the video and illustrated using artistic drawings. The use of the resident intruder paradigm for acute and chronic social stress experiments is explained as well. Finally, some brief tests and criteria are presented to distinguish aggression from its more violent and pathological forms.     

Female Intrasexual Territoriality and its Potential Adaptive Significance: The Pampean Grassland Mouse as an Ecological Model Species

Territorial behaviour in female small mammals has been proposed as a mechanism to defend limited ecological resources or their pups against conspecific infanticidal or predators. Female territorial behaviour very often is associated with reproductive activity due to the fact that frequency and intensity of aggression are exhibited mainly when females are pregnant or lactating. In vole and mice species, female territoriality would be a counterstrategy to prevent the killing of their pups by conspecific breeding females. To study whether female territoriality is a strategy for pups or nest defence against infanticidal breeding females, and whether time invested in nursing young affects aggressive response of mothers, we used the Pampean grassland mouse (Akodon azarae) as an ecological model species. We conducted resident–intruder tests between lactating females. Differences in residency time (48 vs. 72 h) of focal females in their home territory were also included in the analysis. In all cases, the pups of both resident and intruder mothers were placed with the nesting material from their reproductive cages. Resident mothers were always more aggressive than intruders and they were even more aggressive when they spent more time nursing their pups. Contrarily, intruder females exhibited the greatest values of submissive behaviours. Our results show that female territoriality of A. azarae would represent a strategy to protect pups from potentially infanticidal females. We discuss the extent of female intrasexual territoriality and its potential adaptive significance in relation to strategies which lead to increase their reproductive success.     

Raphe serotonin neuron‐specific oxytocin receptor knockout reduces aggression without affecting anxiety‐like behavior in male mice only

Serotonin and oxytocin influence aggressive and anxiety‐like behaviors, though it is unclear how the two may interact. That the oxytocin receptor is expressed in the serotonergic raphe nuclei suggests a mechanism by which the two neurotransmitters may cooperatively influence behavior. We hypothesized that oxytocin acts on raphe neurons to influence serotonergically mediated anxiety‐like, aggressive and parental care behaviors. We eliminated expression of the oxytocin receptor in raphe neurons by crossing mice expressing Cre recombinase under control of the serotonin transporter promoter (Slc6a4) with our conditional oxytocin receptor knockout line. The knockout mice generated by this cross are normal across a range of behavioral measures: there are no effects for either sex on locomotion in an open‐field, olfactory habituation/dishabituation or, surprisingly, anxiety‐like behaviors in the elevated O and plus mazes. There was a profound deficit in male aggression: only one of 11 raphe oxytocin receptor knockouts showed any aggressive behavior, compared to 8 of 11 wildtypes. In contrast, female knockouts displayed no deficits in maternal behavior or aggression. Our results show that oxytocin, via its effects on raphe neurons, is a key regulator of resident‐intruder aggression in males but not maternal aggression. Furthermore, this reduction in male aggression is quite different from the effects reported previously after forebrain or total elimination of oxytocin receptors. Finally, we conclude that when constitutively eliminated, oxytocin receptors expressed by serotonin cells do not contribute to baseline anxiety‐like behaviors or maternal care.     

Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor beta knockout (betaERKO) male mice

Estrogen, as an aromatized metabolite of testosterone, has a facilitatory effect on male aggressive behavior in mice. Two subtypes of estrogen receptors, alpha (ER-alpha) and beta (ER-beta), in the brain are known to bind estrogen. Previous studies revealed that the lack of ER-alpha gene severely reduced the induction of male aggressive behavior. In contrast, mice that lacked the ER-beta gene tended to be more aggressive than wild type (WT) control mice, although the behavioral effects of ER-beta gene disruption were dependent on their social experience. These findings lead us to hypothesize that estrogen may facilitate aggression via ER-alpha whereas it may inhibit aggression via ER-beta. In the present study, we further investigated the role of ER-beta in the regulation of aggressive behavior by examining developmental changes starting at the time of first onset, around the age of puberty. Aggressive behaviors of ER-beta gene knockout (betaERKO) mice were examined in three different age groups, puberty, young-adult, and adult. Each mouse was tested every other day for three times in a resident-intruder paradigm against olfactory bulbectomized intruder mice and their trunk blood was collected for measurements of serum testosterone after the completion of the study. Overall, betaERKO mice were significantly more aggressive than WT. These genotype differences were more pronounced in puberty and young adult age groups, but not apparent in the adult age group, in which betaERKO mice were less aggressive than those in two younger age groups. Serum testosterone levels of betaERKO mice were significantly higher than those of WT mice only in the pubertal age group, but not in young adult (when betaERKO mice were still significantly more aggressive than WT mice) and adult (when no genotype differences in aggression were found) age groups. These results suggest that ER-beta mediated actions of gonadal steroids may more profoundly be involved in the inhibitory regulation of aggressive behavior in pubertal and young adult mice.     

Sex-specific interactions between aggressive and sexual behavior in the rat: Effects of testosterone and progesterone

The influence of progesterone on sexual and aggressive behaviors during aggressive encounters was investigated in pairs of TP-treated male and female rats. Gonadectomized females, chronically injected with testosterone propionate (TP), showed low but consistent levels of feminine sexual behavior which alternated with aggression. Progesterone when given in addition to TP facilitated receptive and proceptive behaviors, but reduced levels of aggression. In TP-treated males, levels of aggression were the same as observed in TP-treated females. However, TP-treated males seldomly showed sexual behavior during aggressive encounters and additional treatment with progesterone did not affect their behavior. After the aggression tests, animals were tested in a social preference test in which an ovariectomized female cage mate and the opponent from the aggressive encounter served as incentives. Positive correlations between levels of aggression and social preference for an opponent were found in both sexes, although correlations only reached statistical significance when progesterone was given in addition to TP. These correlations were found in both sexes, despite the fact that group analysis revealed pronounced sex differences in social preference: males preferred to spend their time near ovariectomized female cage mates, whereas females divided their time equally among female cage mates and opponents.     

Two Sides of the Same Coin? Consistency in Aggression to Conspecifics and Predators in a Female Songbird

Different forms of aggression have traditionally been treated separately according to function or context (e.g. aggression towards a conspecific versus a predator). However, recent work on individual consistency in behavior predicts that different forms of aggression may be correlated across contexts, suggesting a lack of independence. For nesting birds, aggression towards both conspecifics and nest predators can affect reproductive success, yet the relationship between these behaviors, especially in females, is not known. Here we examine free-living female dark-eyed juncos (Junco hyemalis) and compare their aggressive responses towards three types of simulated intruders near the nest: a same-sex conspecific, an opposite-sex conspecific, and a nest predator. We also examine differences in the strength of response that might relate to the immediacy of the perceived threat the intruder poses for the female or her offspring. We found greater aggression directed towards a predator than a same-sex intruder, and towards a same-sex than an opposite-sex intruder, consistent with a predator being a more immediate threat than a same-sex intruder, followed by an opposite-sex intruder. We also found positive relationships across individuals between responses to a same-sex intruder and a simulated predator, and between responses to a same-sex and an opposite-sex intruder, indicating that individual females are consistent in their relative level of aggression across contexts. If correlated behaviors are mediated by related mechanisms, then different forms of aggression may be expressions of the same behavioral tendency and constrained from evolving independently.     

Prior residence and body size influence interactions between black sea urchins

Body size and prior residence can modulate agonistic interaction in several animal species, but scientists know little about these relationships in echinoderms. In this study, we tested the effects of these traits on interactions in the black sea urchin (Echinometra lucunter). After a sea urchin was isolated for 24-h in a glass tank to establish prior residence, we introduced an intruder animal adjacent to the resident in the tank and observed interactions for 30 min. The intruder animal was larger, smaller, or size-matched to the resident. We found body size and prior residence concomitantly modulated interactions among black sea urchins, with prior residence as the major determinant. Black sea urchins mainly exhibited opponent inspection and fleeing responses during interaction to avoid fights, especially when a fight could be seriously disadvantageous (small intruder vs. large resident).     

Chronic enhancement of brain oxytocin levels causes enduring anti-aggressive and pro-social explorative behavioral effects in male rats

Oxytocin (OXT) has been implicated in the regulation of social behaviors, including intermale offensive aggression. Recently, we showed that acute enhancement of brain OXT levels markedly suppressed offensive aggression and increased social exploration in resident rats confronted with an intruder in their home territory. Moreover, a different responsivity to the exogenous OXTergic manipulation was observed among individuals based on their baseline aggression. In this study we aimed at evaluating the behavioral response to chronically enhancing or attenuating central OXT levels, and at scrutinizing whether the trait-aggression moderates the treatment-induced behavioral changes. To this end, resident male wild-type Groningen rats were continuously (via osmotic minipumps) intracerebroventricularly infused with synthetic OXT or a selective OXT receptor (OXTR) antagonist for 7 days. Changes in behavior were assessed performing a resident–intruder test before and at the end of the treatment period, as well as after 7 days of withdrawal. Chronic infusion of OXT was found to selectively suppress aggression and enhance social exploration. Chronic blockage of OXTRs instead increased introductory aggressive behavior (i.e. lateral threat), yet without affecting the total duration of the aggression. The magnitude of the anti-aggressive changes correlated positively with the level of baseline aggression. Interestingly, OXT-induced behavioral changes persisted 7 days after cessation of the treatment. In conclusion, these findings provide further evidence that enhanced functional activity of the central OXTergic system decreases social offensive aggression while it increases social explorative behavior. The data also indicate that chronically enhancing brain OXT levels may cause enduring anti-aggressive and pro-social explorative behavioral effects.     

A quantitative trait locus on chromosome 1 modulates intermale aggression in mice

Aggression between male conspecifics is a complex social behavior that is likely modulated by multiple gene variants. In this study, the BXD recombinant inbred mouse strains (RIS) were used to map quantitative trait loci (QTLs) underlying behaviors associated with intermale aggression. Four hundred and fifty‐seven males from 55 strains (including the parentals) were observed at an age of 13 ± 1 week in a resident‐intruder test following 10 days of isolation. Attack latency was measured directly within a 10‐minute time period and the test was repeated 24 hours later. The variables we analyzed were the proportion of attacking males in a given strain as well as the attack latency (on days 1 and 2, and both days combined). On day 1, 29% of males attacked, and this increased to 37% on day 2. Large strain differences were obtained for all measures of aggression, indicating substantial heritability (intraclass correlations 0.10‐0.18). We identified a significant QTL on chromosome (Chr) 1 and suggestive QTLs on mouse Chrs 1 and 12 for both attack and latency variables. The significant Chr 1 locus maps to a gene‐sparse region between 82 and 88.5 Mb with the C57BL/6J allele increasing aggression and explaining about 18% of the variance. The most likely candidate gene modulating this trait is Htr2b which encodes the serotonin 2B receptor and has been implicated in aggressive and impulsive behavior in mice, humans and other species.     

Breeding Season Aggression of Female and Male Eastern Bluebirds (Sialia sialis) to Models of Potential Conspecific and Interspecific Egg Dumpers

Naturally occurring aggression between female eastern bluebirds (Sialia sialis) is dramatic, resulting in severe injuries and even death. Furthermore, aggression among bluebirds is usually sex specific: males attack males, females attack females. We hypothesized that the primary function of female-female aggression is to guard against the threat of intraspecific egg dumping and that, in this context, same sex aggression is related to the possibility of advantages for males of parasitism (egg dumping) of their nests. Our hypotheses to explain variation in naturally occurring aggression predict temporal variation in aggressive tendency within nest cycles and between the sexes depending on asymmetries in threats to the residents. We report the results of experimental trials in the field designed to determine temporal variation in the aggressive tendencies of resident females to models of intruder females of two species, eastern bluebirds and brown-headed cowbirds (Molothrus ater). Both species dump eggs in the nests of bluebirds. Female aggression to eastern bluebird models is greatest during early stages of nest cycles; the patterns are most consistent with protection against egg dumping and protection of nest sites from usurpation. Male residents seldom attack female eastern bluebird models, but often attack models of female brown-headed cowbirds, a result inconsistent with the hypothesis that patterns of differential parental care control aggression of female and male residents.     

When are neighbours ‘dear enemies’ and when are they not? The responses of territorial male variegated pupfish, Cyprinodon variegatus, to neighbours, strangers and heterospecifics

Dear enemy recognition reduces the costs of territorial defence in some species, but not others, when a neighbour is more threatening to a resident's fitness than an intruder. I asked whether dear enemy effects were fixed in a particular species, or if the reduced aggression between a resident and neighbour was disrupted by the presence of potential mating opportunities. Observing variegated pupfish, Cyprinodon variegatus, in the field and in the laboratory, I examined the effects of a female's presence in a male's territory on residents' aggressive responses to conspecific neighbours and strangers as well as heterospecific opponents. Although reduced aggression consistent with dear enemy recognition was seen between conspecific neighbours in the absence of females, the presence of a female in a male's territory instigated comparably greater aggression between the neighbours. No reduction in aggression was seen between pupfish males and heterospecific opponents. These findings suggest that dear enemy recognition may be a flexible, rather than a fixed, feature of the relationship of neighbouring conspecific males. Despite the disruption in dear enemy recognition caused by a female, residents in the laboratory faced with neighbours spent more time associating with the female than residents faced with strangers. This allowed the residents to secure as many spawns as did males who had been faced with no competitor. Residents faced with any other type of opponent had reduced reproductive success, suggesting that the dear enemy relationship between residents and neighbours is more complex than simply a reduction in aggression. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.