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.     

Facial width-to-height ratio predicts self-reported dominance and aggression in males and females,but a measure of masculinity does not

Recently, associations between facial structure and aggressive behaviour have been reported. Specifically, the facial width-to-height ratio (fWHR) is thought to link to aggression, although it is unclear whether this association is related to a specific dimension of aggression, or to a more generalized concept of dominance behaviour. Similarly, an association has been proposed between facial masculinity and dominant and aggressive behaviour, but, to date, this has not been formally tested. Because masculinity and fWHR are negatively correlated, it is unlikely that both signal similar behaviours. Here, we thus tested these associations and show that: (i) fWHR is related to both self-reported dominance and aggression; (ii) physical aggression, verbal aggression and anger, but not hostility are associated with fWHR; (iii) there is no evidence for a sex difference in associations between fWHR and aggression; and (iv) the facial masculinity index does not predict dominance or aggression. Taken together, these results indicate that fWHR, but not a measure of facial masculinity, cues dominance and specific types of aggression in both sexes.     

Neural mechanisms of aggression

Unchecked aggression and violence exact a significant toll on human societies. Aggression is an umbrella term for behaviours that are intended to inflict harm. These behaviours evolved as adaptations to deal with competition, but when expressed out of context, they can have destructive consequences. Uncontrolled aggression has several components, such as impaired recognition of social cues and enhanced impulsivity. Molecular approaches to the study of aggression have revealed biological signals that mediate the components of aggressive behaviour. These signals may provide targets for therapeutic intervention for individuals with extreme aggressive outbursts. This Review summarizes the complex interactions between genes, biological signals, neural circuits and the environment that influence the development and expression of aggressive behaviour.     

Rhythms,rhythmicity and aggression

The relationships between biological rhythms and human aggressive behavior are addressed and discussed in this article: First, circadian rhythms and aggression are considered. Studies of sleep/waking cycle disturbances in aggression are reported. Severe aggression is associated with profound changes in sleep architecture. Causal link is difficult to establish given that sleep disturbance and aggressive behavior could be the symptoms of the same disorder. Specific aggressive behavior developed during sleep is also described. In addition, hormonal circadian rhythm studies are reported. Thus, low cortisol levels, in particular low cortisol variability, are associated with aggressive behavior, suggesting an inhibitory role of cortisol. Testosterone has daily and seasonal fluctuations, but no link with aggression has been established. Neurophysiological underlying mechanisms are discussed in the last part of this article, with a focus on the relationship between brain rhythm and aggression. Increase of slow-wave EEG activities is observed in individuals with aggressive behavior. Epilepsy, as a disease of brain rhythm could be associated with aggressive behavior, in pre, post and inter ictal periodes. Incidence of aggression is not likely more prevalent in epileptic individuals compared to those with other neurological conditions. Ictal changes take the form of profound behavioral changes, including aggressive behavior which has been interpreted as the emergence of “archeical” or innate motor patterns. In this multidisciplinary approach, the main difficulty is the categorization of the differents types of aggression. Finally, taken together, these studies suggest that biological rhythms, especially circadian rhythms, could provide therapeutic benefits to human aggressive behavior. Biological rhythymicity seems to be a necessary permanent training offering interesting perspectives for the adaptation to changes in the field of aggression.     

Behavioural Phenotypes and the Structure of Human Cognition

Human cognitive uniqueness is often defined in terms of cognitive abilities such as introspection, imitation and cooperativeness. However, little is known about how those traits vary in populations or correlate across individuals. Here we test whether those three cognitive domains are correlated manifestations of an underlying factor, analogous to the psychometric ‘g’ factor, or independent ‘behavioural phenotypes’, analogous to the ‘Big-Five’ personality components. We selected eight variables measuring introspection and extraversion, verbal and physical imitation, cooperation and punishment, and evaluated their individual variability, domain-consistency and sub-structuring in a sample of 84 individuals. Results show high variation and limited clustering into three independent ‘behavioural phenotypes’ of introspection, imitation and cooperation. Only one significant correlation was identified (between two measures of extraversion), while other within-domain measures (introspection vs. extraversion, verbal vs. physical imitation, and cooperation vs. punishment) were not associated. Finally, no between-domain association was identified either through correlations or factor analysis. Overall, the results do not lend support to the hypothesis of a general ‘behavioural phenotype’ underlying individual behaviour. The independence of behaviours of introspection, imitation and cooperation may be the reason why individuals are able to adopt different behavioural strategies (combinations of behavioural phenotypes) and play distinct roles in the maintenance of human distinctive features such as hyper-cooperation and cumulative culture.     

Oestrogen regulates male aggression in the non-breeding season

Extensive research has focused on territorial aggression during the breeding season and the roles of circulating testosterone (T) and its conversion to 17beta-oestradiol (E2) in the brain. However, many species also defend territories in the non-breeding season, when circulating T-levels are low. The endocrine control of non-breeding territoriality is poorly understood. The male song sparrow of Washington State is highly territorial year-round, but plasma T is basal in the non-breeding season (autumn and winter). Castration has no effect on aggression in autumn, suggesting that autumnal territoriality is independent of gonadal hormones. However, non-gonadal sex steroids may regulate winter territoriality (e.g. oestrogen synthesis by brain aromatase). In this field experiment, we treated wild non-breeding male song sparrows with a specific aromatase inhibitor (fadrozole, FAD) using micro-osmotic pumps. FAD greatly reduced several aggressive behaviours. The effects of FAD were reversed by E2 replacement. Treatment did not affect body condition or plasma corticosterone, suggesting that all subjects were healthy These data indicate that E2 regulates male aggression in the non-breeding season and challenge the common belief that aggression in the non-breeding season is independent of sex steroids. More generally, these results raise fundamental questions about how sexual and/or aggressive behaviours are maintained in a variety of model vertebrate species despite low circulating levels of sex steroids or despite castration. Such non-classical endocrine mechanisms may be common among vertebrates and play an important role in the regulation of behaviour.     

The couple that sings together stays together: duetting,aggression and extra-pair paternity in a promiscuous bird species

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male–female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.     

The Relationships between Behavioural Categories and Social Influences in the Gregarious Big Brown Bat (Eptesicus fuscus)

Behavioural plasticity is a critical component of natural selection leading to evolution. However, a surge of studies in the last two decades has discovered a distinct limit to behavioural plasticity, commonly referred to as behaviour types and behavioural syndromes. We set out to understand the relationships across behavioural categories in wild‐caught adult, female big brown bats and how they compare between social and solitary behaviours. Using bats sampled from four different maternity colonies, we ran a series of behavioural assays to create a behavioural profile for each individual. The behavioural profile encompassed exploratory, learning, competitive and aggressive categories. We found that Big brown bats exhibit a mean profile relatively unique to other well‐documented species, where aggression was linked to increased competitive ability but not to boldness. Our results indicate that the solitary and socially directed behaviours of individuals are not necessarily related and that behaviours pertaining to social interactions are linked most closely to learning abilities. Furthermore, we found evidence that poor body condition may be a predictor of increased social interactions and that behaviours exhibited in the presence of conspecifics are unrelated to those exhibited in solitude. These findings indicate importance of social affiliations on individual behaviours in this species and their uniqueness relative to other well‐studied taxa.     

Brain size affects responsiveness in mating behaviour to variation in predation pressure and sex ratio

Despite ongoing advances in sexual selection theory, the evolution of mating decisions remains enigmatic. Cognitive processes often require simultaneous processing of multiple sources of information from environmental and social cues. However, little experimental data exist on how cognitive ability affects such fitness‐associated aspects of behaviour. Using advanced tracking techniques, we studied mating behaviours of guppies artificially selected for divergence in relative brain size, with known differences in cognitive ability, when predation threat and sex ratio was varied. In females, we found a general increase in copulation behaviour in when the sex ratio was female biased, but only large‐brained females responded with greater willingness to copulate under a low predation threat. In males, we found that small‐brained individuals courted more intensively and displayed more aggressive behaviours than large‐brained individuals. However, there were no differences in female response to males with different brain size. These results provide further evidence of a role for female brain size in optimal decision‐making in a mating context. In addition, our results indicate that brain size may affect mating display skill in male guppies. We suggest that it is important to consider the association between brain size, cognitive ability and sexual behaviour when studying how morphological and behavioural traits evolve in wild populations.     

Male aggression,limited female choice and the ontogeny of mating behaviour in the flesh fly Sarcophaga crassipalpis

Previous work has shown that male flesh flies (Sarcophaga crassipalpis Macquart) exhibit an ontogeny of behaviour from eclosion through sexual maturity that includes extensive changes in the expression of aggressive, non‐aggressive interactive and non‐interactive behaviours. To determine how the presence of a female flesh fly influences the manifestation of these behaviours, male flesh flies of different ages post‐eclosion are paired with same‐age females and their behaviours are monitored in a simple arena during a 50‐min observation period. All flies are socially isolated until pairing. Although the levels of expression of aggressive and non‐aggressive interactive behaviours are depressed relative to previous findings in male‐opponent pairs, the ontogeny of aggression still occurs as indicated by a significant increase, with age, in the agonistic behaviour ‘hold’. Similar to male‐opponent pairs and individual males, the performance by males of the non‐interactive behaviours ‘walking’ and ‘standing’ diminishes, whereas ‘upside‐down’ increases with age. By contrast, ‘grooming’ shows a significant age‐related decline. No courtship behaviours are observed in the males, although the aggressive behaviour ‘hold’ is a significant transition to mating. Females show no obvious courtship or rejection behaviours, although the significant increase in ‘upside‐down’ with age could possibly be a behavioural gateway to mating. The results of this study indicate that extensive age‐related changes encompassing the entire behavioural repertoire are intrinsic to male flesh flies and persist under a variety of different social contexts.     

Optimal reproductive-skew models fail to predict aggression in wasps

Optimal-skew models (OSMs) predict that cooperative breeding occurs as a result of dominants conceding reproductive benefits to subordinates, and that division of reproduction within groups reflects each cooperator's willingness and ability to contest aggressively for dominance. Polistine paper wasps are a leading model system for testing OSMs, and data on reproduction and aggression appear to support OSMs. These studies, however, measure aggression as a single rate rather than by the activity patterns of individuals. This leads to a potential error: if individuals are more likely to receive aggression when active than when inactive, differences in aggression across samples can reflect changes in activity rather than hostility. This study replicates a field manipulation cited as strongly supporting OSMs. We show that fundamentally different conclusions arise when controlling for individual activity states. Our analyses strongly suggest that behaviours classified as 'aggression' in paper wasps are unlikely to function in establishing, maintaining or responding to changes in reproductive skew. This illustrates that OSM tests using aggression or other non-reproductive behaviour as a metric for reproductive partitioning must demonstrate those links rather than assume them.     

Heritability of interpack aggression in a wild pedigreed population of North American grey wolves

Aggression is a quantitative trait deeply entwined with individual fitness. Mapping the genomic architecture underlying such traits is complicated by complex inheritance patterns, social structure, pedigree information and gene pleiotropy. Here, we leveraged the pedigree of a reintroduced population of grey wolves (Canis lupus) in Yellowstone National Park, Wyoming, USA, to examine the heritability of and the genetic variation associated with aggression. Since their reintroduction, many ecological and behavioural aspects have been documented, providing unmatched records of aggressive behaviour across multiple generations of a wild population of wolves. Using a linear mixed model, a robust genetic relationship matrix, 12,288 single nucleotide polymorphisms (SNPs) and 111 wolves, we estimated the SNP‐based heritability of aggression to be 37% and an additional 14% of the phenotypic variation explained by shared environmental exposures. We identified 598 SNP genotypes from 425 grey wolves to resolve a consensus pedigree that was included in a heritability analysis of 141 individuals with SNP genotype, metadata and aggression data. The pedigree‐based heritability estimate for aggression is 14%, and an additional 16% of the phenotypic variation was explained by shared environmental exposures. We find strong effects of breeding status and relative pack size on aggression. Through an integrative approach, these results provide a framework for understanding the genetic architecture of a complex trait that influences individual fitness, with linkages to reproduction, in a social carnivore. Along with a few other studies, we show here the incredible utility of a pedigreed natural population for dissecting a complex, fitness‐related behavioural trait.     

Corticosterone,Avoidance of Novelty,Risk‐Taking and Aggression in a Wild Bird: No Evidence for Pleiotropic Effects

Certain inherent characteristics of individuals can determine both physiological and behavioural responses to environmental challenges, which could drive a correlation between levels of corticosterone (CORT), the most important stress hormone and behavioural profiles. Therefore, CORT level may mediate consistent behaviours along the shy/bold continuum, and thus, it could serve as a pleiotropic basis for behavioural syndromes. Moreover, behavioural responses to environmental challenges may have consequences for CORT concentrations, which would also result in a correlation between physiology and behaviours even without requiring pleiotropic mechanisms. Accordingly, we investigated the relationship between CORT and behaviour in free‐living male collared flycatchers, Ficedula albicollis, using recently developed field assays. More specifically, we characterised novel object avoidance, intraspecific aggression and risk‐taking in males and related these correlated behaviours to the concentration of CORT metabolites in droppings measured by enzyme immunoassay. Individuals with higher levels of excreted CORT metabolites had no consistently higher or lower behavioural scores along the shy/bold spectrum, as avoidance of novelty, aggression and risk‐taking were not systematically related to CORT metabolite concentrations in the same direction. Moreover, environmental challenges owing to the presence of a novel object, territorial intruder and a potential predator caused no elevation in the level of CORT metabolites. Therefore, we did not find correlative evidence for CORT driving correlated behaviours through pleiotropic effects or for particular behaviours during courtship causing elevation in CORT levels.     

Behavioural syndromes differ predictably between 12 populations of three-spined stickleback

Animals often differ in suites of correlated behaviours, comparable with how humans differ in personality. Constraints on the architecture of behaviour have been invoked to explain why such 'behavioural syndromes' exist. From an adaptationist viewpoint, however, behavioural syndromes should evolve only in those populations where natural selection has favoured such trait covariance, and they should therefore exist only in particular types of population. A comparative approach was used to examine this prediction of the adaptive hypothesis. We measured behavioural correlations in 12 different populations of three-spined stickleback (Gasterosteus aculeatus) and assessed whether they indeed varied consistently according to the selective environment, where population was unit of analysis. For a sample of fry from each population, we measured five different behaviours within the categories of (i) aggression (towards conspecifics); (ii) general activity; and (iii) exploration-avoidance (of novel foods, novel environments and altered environments). We show that behavioural syndromes are not always the same in different types of stickleback population: the often-documented syndrome between aggressiveness, activity and exploratory behaviour existed only in large ponds where piscivorous predators were present. In small ponds where predators were absent, these behaviours were not (or only weakly) associated. Our findings imply that population variation in behavioural syndromes does not result from stochastic evolutionary processes, but may result instead from adaptive evolution of behaviour favouring what should prove to be optimal trait combinations.     

Individual differences in behaviour explain variation in survival: a meta‐analysis

Research focusing on among‐individual differences in behaviour (‘animal personality’) has been blooming for over a decade. Central theories explaining the maintenance of such behavioural variation posits that individuals expressing greater “risky” behaviours should suffer higher mortality. Here, for the first time, we synthesize the existing empirical evidence for this key prediction. Our results did not support this prediction as there was no directional relationship between riskier behaviour and greater mortality; however there was a significant absolute relationship between behaviour and survival. In total, behaviour explained a significant, but small, portion (5.8%) of the variance in survival. We also found that risky (vs. “shy”) behavioural types live significantly longer in the wild, but not in the laboratory. This suggests that individuals expressing risky behaviours might be of overall higher quality but the lack of predation pressure and resource restrictions mask this effect in laboratory environments. Our work demonstrates that individual differences in behaviour explain important differences in survival but not in the direction predicted by theory. Importantly, this suggests that models predicting behaviour to be a mediator of reproduction‐survival trade‐offs may need revision and/or empiricists may need to reconsider their proxies of risky behaviours when testing such theory.     

Psychophysiological correlates of aggression and violence: an integrative review

This paper reviews existing psychophysiological studies of aggression and violent behaviour including research employing autonomic, electrocortical and neuroimaging measures. Robust physiological correlates of persistent aggressive behaviour evident in this literature include low baseline heart rate, enhanced autonomic reactivity to stressful or aversive stimuli, enhanced EEG slow wave activity, reduced P300 brain potential response and indications from structural and functional neuroimaging studies of dysfunction in frontocortical and limbic brain regions that mediate emotional processing and regulation. The findings are interpreted within a conceptual framework that draws on two integrative models in the literature. The first is a recently developed hierarchical model of impulse control (externalizing) problems, in which various disinhibitory syndromes including aggressive and addictive behaviours of different kinds are seen as arising from common as well as distinctive aetiologic factors. This model represents an approach to organizing these various interrelated phenotypes and investigating their common and distinctive aetiologic substrates. The other is a neurobiological model that posits impairments in affective regulatory circuits in the brain as a key mechanism for impulsive aggressive behaviour. This model provides a perspective for integrating findings from studies employing different measures that have implicated varying brain structures and physiological systems in violent and aggressive behaviour.     

Diverse societies are more productive: a lesson from ants

The fitness consequences of animal personalities (also known as behavioural syndromes) have recently been studied in several solitary species. However, the adaptive significance of collective personalities in social insects and especially of behavioural variation among group members remains largely unexplored. Although intracolonial behavioural variation is an important component of division of labour, and as such a key feature for the success of societies, empirical links between behavioural variation and fitness are scarce. We investigated aggression, exploration and brood care behaviour in Temnothorax longispinosus ant colonies. We focused on two distinct aspects: intercolonial variability and its consistency across time and contexts, and intracolonial variability and its influence on productivity. Aggressiveness was consistent over four to five months with a new generation of workers emerging in between trial series. Other behaviours were not consistent over time. Exploration of novel environments responded to the sequence of assays: colonies were faster in discovering when workers previously encountered opponents in aggression experiments. Suites of correlated behaviours (e.g. aggression-exploration syndrome) present in the first series did not persist over time. Finally, colonies with more intracolonial behavioural variation in brood care and exploration of novel objects were more productive under standardized conditions than colonies with less variation.     

Law, evolution and the brain: applications and open questions

This paper discusses several issues at the intersection of law and brain science. It focuses principally on ways in which an improved understanding of how evolutionary processes affect brain function and human behaviour may improve law's ability to regulate behaviour. It explores sample uses of such 'evolutionary analysis in law' and also raises questions about how that analysis might be improved in the future. Among the discussed uses are: (i) clarifying cost-benefit analyses; (ii) providing theoretical foundation and potential predictive power; (iii) assessing comparative effectiveness of legal strategies; and (iv) revealing deep patterns in legal architecture. Throughout, the paper emphasizes the extent to which effective law requires: (i) building effective behavioural models; (ii) integrating life-science perspectives with social-science perspectives; (iii) considering the effects of brain biology on behaviours that law seeks to regulate; and (iv) examining the effects of evolutionary processes on brain design.     

Sex differences in indirect aggression: Psychological evidence from young adults

Many studies have found differences in the types of aggression used by males and females, at least in children and adolescents. Boys tend to use direct physical or verbal aggression, whereas girls tend to use more indirect forms of aggression that prominently feature gossip. Evolutionary theories of sex differences in indirect aggression propose selection pressures that would have acted on older teenagers and adults. Evidence for sex differences in indirect aggression in adults, however, is equivocal. Virtually all studies of adults have found a sex difference in physical aggression, but most have failed to find sex differences in the use of the more indirect forms of aggression. Almost all of these studies have measured indirect aggression using self-reports of aggressive behavior. We investigated sex differences in the psychology of indirect aggression by exposing young adult women and men to the same aggression-evoking stimulus. As evolutionary models predict, we found that women had a stronger desire than men to aggress indirectly, even after controlling for perceptions of social norms and approval. Future work on both evolutionary and social norm models of indirect aggression is warranted.