Advances

in
Genetics, Volume 75

Serial Editors

Theodore Friedmann
University of California at San Diego, School of Medicine, USA

Jay C. Dunlap
Dartmouth Medical School, Hanover, NH, USA

Stephen F. Goodwin
University of Oxford, Oxford, UK

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Contributors
Numbers in parentheses indicate the pages on which the authors contributions begin.

Laura A. Baker (171) University of Southern California, Los Angeles,

California, USA
Patricia A. Brennan (1, 215) Department of Psychology, Emory University,
Atlanta, Georgia, USA
Ivan D. Chase (51) Department of Sociology, Stony Brook University, Stony
Brook, New York, USA
Emil F. Coccaro (151) Clinical Neuroscience Research Unit, Department of
Psychiatry, The University of Chicago Pritzker School of Medicine,
Chicago, Illinois, USA
Yu Gao (255) Department of Psychology, Brooklyn College, New York, USA
Andrea L. Glenn (255) Department of Child and Adolescent Psychiatry,
Institute of Mental Health, Singapore, Singapore
Kyle L. Gobrogge (121) Department of Psychology and Program in
Neuroscience, Florida State University, Tallahassee, Florida, USA
James L. Goodson (83) Department of Biology, Indiana University,
Bloomington, Indiana, USA
Roger T. Hanlon (23) Marine Resources Center, Marine Biological Laboratory,
Woods Hole, Massachusetts, USA
Robert Huber (1) JP Scott Center for Neuroscience, Mind & Behavior,
Biological Sciences, Bowling Green State University, Bowling Green,
Ohio, USA
Jamie L. LaPrairie (215) Department of Psychology, Emory University,
Atlanta, Georgia, USA
Patrik Lindenfors (7) Department of Zoology, and Centre for the Study of
Cultural Evolution, Stockholm University, Stockholm, Sweden
Donna L. Maney (83) Department of Psychology, Emory University, Atlanta,
Georgia, USA
Benjamin R. Nordstrom (255) Department of Psychiatry, University of
Pennsylvania, Philadelphia, USA
Melissa Peskin (255) Department of Psychology, University of Pennsylvania,
Philadelphia, USA
Adrian Raine (255) Departments of Psychiatry, Psychology and Criminology,
University of Pennsylvania, Philadelphia, USA
ix

Contributors

Brittany A. Robinson (215) Department of Psychology, Emory University,

Atlanta, Georgia, USA
Anna S. Rudo-Hutt (255) Department of Psychology, University of
Pennsylvania, Philadelphia, USA
Birgitta S. Tullberg (7) Department of Zoology, Stockholm University,
Stockholm, Sweden
Julia C. Schechter (215) Department of Psychology, Emory University,
Atlanta, Georgia, USA
Robert A. Schug (255) Department of Criminal Justice, California State
University, Long Branch, USA
William A. Searcy (23) Department of Biology, University of Miami, Coral
Gables, Florida, USA
Kristine Seitz (51) Department of Biology, Stony Brook University, Stony
Brook, New York, USA
Catherine Tuvblad (171) University of Southern California, Los Angeles,
California, USA
Moira J. van Staaden (23) Department of Biological Sciences and JP Scott
Center for Neuroscience, Mind & Behavior, Bowling Green State
University, Bowling Green, Ohio, USA
Zuoxin Wang (121) Department of Psychology and Program in Neuroscience,
Florida State University, Tallahassee, Florida, USA
Yaling Yang (255) Laboratory of Neuro Imaging, University of California,
Los Angeles, USA
Rachel Yanowitch (151) Clinical Neuroscience Research Unit, Department of
Psychiatry, The University of Chicago Pritzker School of Medicine,
Chicago, Illinois, USA

Aggression
Robert Huber* and Patricia A. Brennan
*JP Scott Center for Neuroscience, Mind & Behavior, Biological Sciences,
Bowling Green State University, Bowling Green, Ohio, USA

Department of Psychology, Emory University, Atlanta, Georgia, USA

Aggression ranks among the most misunderstood concepts in all the behavioral
sciences. It is commonly viewed by the general public as an aberrant form of
behavior, with situations of conflict pictured as unfavorable and stressful circumstances, brought about by amoral urges, in critical need of our cognitive control,
and with negative consequences for all involved. Such a view fundamentally
misunderstands the biological significance of the behaviors that occur during
conflict. Deeply rooted in the demands of the natural world, an individual must
fulfill its demands for self-preservation, defend its interests, or compete for
limited vital resources. Basic tendencies for aggression are virtually ubiquitous
throughout the animal kingdom, regardless of its bearers neural or cognitive
faculties, phylogenetic origins, or sociobiological circumstances. Just as widespread, however, are fundamental rules that govern physical conflict, such that
cases of unbridled hostility are surprisingly rare. In most species, visual
and elaborately ritualized displays effectively channel aggression, structure how
individuals interact, and govern the conflicts resolution.
As we witness animals engaged in situations of conflict, we cannot help
but be drawn in by the behaviors inherent relevance to our own biological roots.
The knowledge that human aggression arises from our genetic heritage makes
it all the more likely that it is of an adaptive nature. As we study the
individuals and environments where aggression is most commonly displayed,
we gain a better understanding of when aggression and violence may serve
an adaptive function and when it may not. Current research points to the
importance of delineating subtypes of aggression, focusing on such concepts as
proactive and reactive, direct and indirect, and adolescent limited versus life
course persistent. Each of these types of aggression has a distinct etiology and
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0065-2660/11 $35.00
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Huber and Brennan

utility, depending upon the social environment in which the individual must
function. For example, reactive aggression is aggression that occurs in response to
a threat in the external environment. It is easy to see how this type of aggression
may have its basis in our inherent survival instincts. Nevertheless, a propensity
for reactive aggression may be truly dysfunctional in environments that pose low
levels of threat, like many of those in which children in Western societies are
now raised. A more comprehensive understanding of how biology, behavior, and
environment intersect is paramount in the study of human violence and
aggression.
Studies of aggression, its motives, and its causes are of central interest to a
wide range of academic disciplinesbehavioral genetics, evolution, neuroscience, psychology, sociology, and criminology, to name just a few. Despite the
wealth of empirical and theoretical attention, it is remarkable that a comprehensive synthesis of aggression has stubbornly remained elusive. This partly stems
from the fact that the term aggression neither maps cleanly onto a monolithic
behavioral phenomenon nor lends itself to representation by a simple explanatory
concept. Another explanation for this paradox must reside in the absence of a
unified, operational definition of aggression across disciplines, or even of a general
agreement on what the term actually includes. For instance, most psychologists
define aggression as all behavior that is intended to cause bodily harm. Other
widely adopted classifications of aggression recognize subtypes, ranging from
competition between males, a mothers efforts to protect her offspring, or fighting
as a learned response to cope with a particular situation. Biologists regard a
definition focused solely on injury as insufficient as this excludes a wide range of
threat behaviors directed at rivals, for example, birds that challenge their adversaries with song, an impalas exaggerated strutting as a signal of strength, or a wolfs
territorial claims via scent markings. Moreover, there is little agreement on
whether a predators hunting behavior should be included. A lion chasing and
killing a gazelle undoubtedly inflicts injury, but is this more akin to a cow cropping
the top off a clump of grass, or to an elephant bull inflicting serious injury to a rival
in battle? Moreover, behavior in aggressive encounters always balances contrasting impulses for approach and attack with a tendency to fleerarely is either
present entirely alone. To acknowledge the difficulty of disentangling these
components, the term agonistic behavior has been introduced. The term specifically addresses the balance of forces for both attacking and fleeing and it accommodates all instances of attack and threat (i.e., offensive agonistic behavior) as
well as escape and submission (i.e., defensive agonistic behavior).
As with any other characteristic, natural selection is assumed to
enhance aggressions overall effectiveness. High ranking individuals are likely
to display a favorable combination of strength, along with an ability to titer
their levels of aggression, to pick fights that are winnable, and to only compete
in those that are worth it. Hyperaggressive phenotypes exist in most systems.

1. Aggression

These exhibit fighting that greatly exceeds the most effective norm, they
readily launch the initial attack even in situations where they ought not to,
are overly eager to escalate or retaliate, show a willingness to follow an
excessively physical trajectory even when an opponent has already withdrawn,
or fail to back down in situations where there is little prospect of winning.
Such behaviors rarely make for an effective strategy, as they coincide with
greater risk of injury or death, or in the best-case scenario, attaining a
low rank.
A thorough analysis of aggression minimally demands that we (1)
capture the essence of an inherently multifaceted phenotype, (2) address underlying elements of motivation that are not always readily observed or elicited,
(3) understand the various scenarios and contexts that influence its expression,
(4) decipher the neural, hormonal, and genetic causes that are at work, and (5)
explore how its components are shaped by evolution. The chapters in this
volume aim to provide a comprehensive overview of these topics as their authors
unravel the individual behavioral and neural strands constituting situations of
conflict.
Initial chapters of the volume characterize the elemental building
blocks of aggression; they assess, precisely delineate, and account for aggressions
different and unique components, and explain how intricate behavioral constructs often emerge from much simpler roots. The initial chapters review
aggression from a predominantly evolutionary perspective. Conflicts are energetically costly and carry inherent risks. Natural selection offers a powerful conceptual tool as it focuses on an individuals behavioral strategies and decision
making in ways that maximize its fitness. Evolution can only exert its influence
on characters that depend, at least partially, on genetic underpinnings. Lindenfors and Tullberg (Chapter 2) discuss the significance of sexual selection as a key
evolutionary structuring force in aggression. In most scenarios, ritualized displays
take the place of unchecked, aggressive interactions. Game theory offers a
powerful framework for why animals only tend to fight with great ferocity
when a resource of exceptional value is at stake. Resources are rarely worth the
risk of sustaining injury, and competing individuals will do best by resolving
conflicts with ritualized displays only. Skill in assessing the relative strength of an
opponent is key for navigating the demands, risks, and opportunities of social
living. The review by van Staaden and colleagues (Chapter 3) discusses a
prominent role for signaling aggressive behaviors, which permit individuals to
obtain valid estimates of an opponents true strength. Once an animal is bested
by an opponent, it is always better to adopt submissive behavior and accept
subordinate status, rather than risk something far worse. A wide range of attributes decides between victory and defeat. With prominent asymmetries in the
size of weapons, strength, or agility, fights are often quickly resolved. In many
instances, though, social success will depend also on an ability to form successful

Huber and Brennan

alliances, to harness cognitive skills, or to inherit status from high-ranking kin. A

paired dominance relationship is established when prior encounters produce a
lasting polarity in the outcome of future bouts. In its most common form, the past
loser will be less likely to initiate further bouts against the winner or will retreat
quickly if confronted. As individuals repeatedly meet and interact with others,
higher order social organization emerges through a series of sequential dyadic
interactions. Individuals of many species, including humans, tend to arrange
themselves in largely linear social hierarchies. Although individual characteristics such as size, strength, or agility are relatively fixed and may indeed
influence rank, Chase and Seitz (Chapter 4) illustrate that these qualities are
more often overshadowed by contextual factors and chance events.
The search for proximate mechanisms underlying aggression requires us
to view aggressions natural building blocks, to recognize the various factors that
control them, and to effectively label their behavioral expression in the form of
consistent and reliable phenotypes. Our understanding of the biological basis of
aggression in all vertebrates, including humans, has been built largely upon
discoveries first made in birds. An extensive literature indicates that hormonal
mechanisms are shared between humans and many avian species. This recent
development of hormonal, neuroendocrine, and genetic tools has established
songbirds as powerful models for understanding the neural basis and evolution of
vertebrate aggression. Maney and Goodson (Chapter 5) discuss the contributions
of field endocrinology toward a theoretical framework linking aggression with sex
steroids, explore evidence that the neural substrates of aggression are conserved
across vertebrate species, and describe a promising new songbird model for
studying the molecular genetic mechanisms underlying aggression. Voles have
recently emerged as a key model for a genetic dissection of social behavior and its
underlying neural mechanisms. Gobrogge and Wang (Chapter 6) discuss its
utility for the study of aggression and review recent findings that illustrate the
neurochemical mechanisms underlying pair bonding-induced aggression. Endogenous brain chemicals play a key role in the control of aggression in many taxa
including humans. Neurotransmitters effectively pattern and modulate the expression of basic behavioral components. Genetic abnormalities in a number of
neurotransmitter pathways have been implicated in aggression-related disorders.
Yanowitch and Coccaro (Chapter 7) review work that demonstrates that neurotransmitter function is intricately linked to aggressive state.
Subsequent chapters focus on human aggression, with an emphasis on
genetic and other biological factors. Human ingenuity for inflicting intentional
harm is without equal, although warring tendencies may already be rooted in a
deep, prehuman past. Instances of violence have been documented for a range of
nonhuman apes and may have arguably wired into our genes when our more
aggressive ancestors won against our less aggressive ancestors in terms of survival
and reproduction. Aside from an unprecedented potential for carnage and

1. Aggression

destruction, humans are at the same time also capable of the most remarkable
instances of compassion, understanding, and peaceful negotiation. The direction
depends on each individuals ethical codes and moral norms driven by the
societal expectations, good parenting, or social contexts. A clear vision has
emerged where natural tendencies for aggression appear to be ubiquitous, but
so too are a plethora of sophisticated mechanisms that keep conflicts in check,
channel aggression, negotiate fighting signals, resolve conflicts, and ultimately
govern social group structure.
Tuvblad and Baker (Chapter 8) demonstrate that genetic influences
serve as powerful predictors of human aggression and violence. The relative
influence of genetics depends upon developmental age, type of aggression, and
the environmental context faced by the individual. LaPrairie and colleagues
(Chapter 9) review research linking perinatal factors and aggression and conclude in a similar fashion that perinatal and neurodevelopmental factors
influence the expression of aggressive behaviors. Nordstrom and colleagues
(Chapter 10) further detail the importance of recognizing the role of brain
functioning deficits in the risk for aggressive outcomes. Recent advances in
imaging technology have enabled a far greater understanding of these influences
on human behavior and the risks of criminal outcomes. Importantly, the chapters
on human aggression also emphasize the fact that biology is not destiny and that,
in the case of human aggression and violence, there is much that can and should
be done in terms of early intervention and prevention.
The list of significant challenges in aggression research remains daunting and the need to harness the full power of interdisciplinary approaches now
appears more urgent than ever. Aside from our need to reconcile simple questions over terminology, a number of more serious impediments remain to be
acknowledged. Concepts seem so intimately connected that we are tempted to
view them as essentially overlapping, or to even use them synonymously (e.g.,
measures of an inherent tendency to fight, effectiveness in a contest, or the
ability to socially dominate others). A common fallacy views these simply as
separate perspectives onto the same, unitary phenomenon of aggression. For a
synthesis to emerge we must accept aggressions multidimensional nature and
recognize that the term aggression simply serves as an overarching label for an
entangled complex of multiple, distinct components, causes, and functions. This
volume comes at a critical juncture for defining a broader view of aggression and
with it we hope to help define the structural elements that comprise the behavior
in its full complexity.
The time is now right to bridge theoretical frameworks, combine
experimental approaches, and relate significant findings across the many individual disciplines that are instrumental in the analysis of aggression. Center
initiatives can serve as intellectual hubs for the comprehensive study of social
conflict, violence, and related phenomena. Bringing together individual

Huber and Brennan

researchers from a broad range of disciplines to foster integrative and overarching themes, such centers provide a forum for a rich exchange of ideas, the
development of human resources, a clearinghouse for notable discoveries, and
to publicize their societal relevance through public outreach. The development
of viewpoints spanning formerly separate disciplines, such as the one aimed for
in this book, is cause for optimism that the future is not quite as far off as we
had feared.

Evolutionary Aspects of
Aggression: The Importance of
Sexual Selection
Patrik Lindenfors*, and Birgitta S. Tullberg*
*Department of Zoology, Stockholm University, Stockholm, Sweden

Centre for the Study of Cultural Evolution, Stockholm University, Stockholm,

Sweden

I.
II.
III.
IV.
V.
VI.

Introduction
Sexual Selection
Mating Systems
When to Fight and When to Flee
Case Studies: Sexual Dimorphism
Humans and the Mammalian Pattern
Acknowledgment
References

ABSTRACT
Aggressive behaviors in animals, for example, threat, attack, and defense, are
commonly related to competition over resources, competition over mating
opportunities, or fights for survival. In this chapter, we focus on aggressive
competition over mating opportunities, since this competition explains much
of the distribution of weaponry and large body size, but also because this type of
competition sheds light on the sex skew in the use of violence in mammals,
including humans. Darwin (1871) termed this type of natural selection, where
differences in reproductive success are caused by competition over mates, sexual
selection. Not all species have a pronounced competition over mates, however.
Instead, this aspect of sociality is ultimately determined by ecological factors.
Advances in Genetics, Vol. 75
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0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00009-5

Lindenfors and Tullberg

In species where competition over mates is rampant, this has evolutionary effects
on weaponry and body size such that males commonly bear more vicious weapons
and are larger than females. A review of sexual selection in mammals reveals how
common aggressive competition over mating opportunities is in this group.
Nearly half of all mammal species exhibit male-biased sexual size dimorphism,
a pattern that is clearly linked to sexual selection. Sexual selection is also
common in primates, where it has left clear historical imprints in body mass
differences, in weaponry differences (canines), and also in brain structure differences. However, when comparing humans to our closest living primate relatives,
it is clear that the degree of male sexual competition has decreased in the
hominid lineage. Nevertheless, our species displays dimorphism, polygyny, and
sex-specific use of violence typical of a sexually selected mammal. Understanding
the biological background of aggressive behaviors is fundamental to understanding human aggression. 2011, Elsevier Inc.

I. INTRODUCTION
Why does aggression exist in nature? Darwin (1859, 1871) pointed out that the
ultimate explanation for any trait has to be found in the effect that it has on
survival and reproduction. From an evolutionary standpoint, individuals should
thus mainly be expected to fight over resources, for survival and for mating
opportunities, because these are what mainly affect how many genes that individual contributes to the gene pool of the coming generation. Another prediction is that the amount of aggression displayed in the encounters should increase
with increasing value of the fought-over resource. Aggressive behaviors are
associated with costs, and individuals are simply expected to take higher risks,
that is, pay potentially higher costs, with increasing potential gains. In this
chapter, we focus on aggression over mating opportunitiessexual selection
in mammals in general and in primates in particular. We focus on sexual selection
because evidence suggests that it is the primary reason why animals fight with
conspecifics and because it is the most likely explanation of some aspects of
human aggression, such as why males tend to be more aggressive than females.
An important point about evolutionary explanations is the philosophical distinction between proximate and ultimate explanations. Take sex, for
example. Do humans have sex because it feels good or in order to have children?
Most sexual intercourse in current society probably has very little to do with
actual procreation; on the contrary, there are many birth control methods
available to make it possible to have sex without this resulting in a pregnancy.
Despite the fact that protected sex happens because it feels good, the evolutionary explanation of sexual intercourse is because of procreation. This is
where the crucial distinction between proximate and ultimate explanations

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

comes into play. A proximate explanation is the explanation that is closest to the
event that is to be explained. The higher, ultimate explanation is instead the
deeper reason for why something happened.
In biology, the division in ultimate and proximate explanations has
been extended to what is usually termed Tinbergens four questions
(Tinbergen, 1963); the four potential explanations of any behavior: (1) survival
value or adaptive function, (2) phylogenetic history, (3) individual development, and (4) causal mechanisms such as hormonal mediation of behavior. The
first two of Tinbergens questions are ultimate whereas the latter two are proximate. To fully shed light on a biological phenomenon all four types of questions
are needed and the answers complement each other. However, in this chapter,
we focus entirely on ultimate, evolutionary answers to the question of why
aggression exists and takes the form it does.

II. SEXUAL SELECTION

Natural selection is all about who gets to reproduce and who does not (Darwin,
1859). A central aspect of getting to reproduce is to survive until the opportunity to
reproduce arises and to gain access to resources enabling you to do so, but another
important aspect concerns direct competition in connection with the reproductive
act itself. Darwin termed this second aspect sexual selection: differences in
reproductive success caused by competition over mates (Darwin, 1871).
Why did Darwin give a specific name to one part of natural selection:
why not just stick to the umbrella term natural selection? Darwin had noted
that there often seems to be a conflict of interest between traits that increase
survival and traits that increase reproduction; many traits that give an advantage
in reproduction have negative consequences for survival. A male peacocks large
tail feathers are a prime example of such a trait. How can such a long colorful tail
evolve when it makes the bearer simultaneously more visible and less adept at
escaping predators? When thinking about this problem before having formulated
the theory of sexual selection, Darwin wrote in a letter to his friend, the botanist
Asa Gray, the famous line: The sight of a feather in a peacocks tail, whenever
I gaze at it, makes me sick! (Darwin, 1860).
To clarify this second aspect of natural selectionselection that has to
do with competition over matesDarwin wrote a follow-up to On the Origin of
Species (1859), The Descent of Man and Selection in Relation to Sex (1871).
In this book, Darwin points out that there are two potential kinds of competition
over mates, two forms of sexual selection. Either individuals of one sex (usually
males) can fight with each other over mating opportunities (intrasexual selection) or, alternatively, individuals of one sex (usually females) can choose
individuals of the other sex on the basis of some trait (intersexual selection).

10

Lindenfors and Tullberg

This second form of sexual selection is the explanation of the peacocks tail:
peahens simply find it attractive and prefer to mate with the peacocks with the
most elaborate tail. Further, the tail provides information on the genetic quality
of the maleit is an honest signal (Petrie, 1994).
It is noteworthy that it was the idea of intersexual selection that caused
the most furious debate in Darwins time, foremost because it was judged utterly
questionable that female aesthetical judgment could be the ultimate explanation
for so many conspicuous characters in nature. However, partner choice is a more
peaceful process than direct competition within a sex. Thus, because it induces
so much aggression in nature, we focus in this chapter mainly on intrasexual
selection; physical competition over mating opportunities. It should be pointed
out that the two forms of sexual selection sometimes occur simultaneously, for
instance, in lekking species where females choose as mating partners the winning
males from physical competition (Andersson, 1994).
Sexual selection arises when one sex limits the reproductive success of
the other. Most often it is females who are the limiting resource for the reproductive success of males due to a fundamental asymmetry between males and
females in their defining characteristic, their gametes. Males are designated by
their smaller, mobile gametes, called sperm cells. Females are designated by their
larger, nutrition-carrying gametes, called eggs. Males can make more gametes
than females, simply because sperm are energetically cheaper to make than eggs;
thus, there is a fundamental reproductive difference between males and females.
This initial asymmetry has consequences. Making sperm is cheap and easy, so
this is not what limits the reproductive possibilities of males. Making eggs, on the
other hand, is much costlier. Thus, sexual selection commonlybut not exclusivelyaffects males, because given an equal sex ratio, male reproductive success
is limited by access to matings with females. Conversely, female reproductive
success is limited by the number of eggs she can produce (Andersson, 1994). This
sex specificity is so common that the reverse pattern, termed sex role reversal, is
subject to intense interest from evolutionary biologists when it occurs (e.g., Ralls,
1976; Vincent et al., 1992).
An important experimental verification of this theoretical insight was
made by the geneticist Bateman (1948), who experimented on fruit flies. Bateman noted a pattern demonstrating that the number of offspring a male fruit fly
can have is directly correlated with his number of matings. The same does not
hold true for females, who have roughly the same number of offspring no matter
how many times they mate (as long as it is at least once). This pattern is termed
Batemans principle. Later studies, however, have documented that a number of
exceptions to Batemans principle exist in nature (Birkhead, 2001). Individuals
are not only sperm and eggs; there are a number of additional factors that need to
be incorporated to understand what is going on in different species. In mammals,
especially, one needs to incorporate two unique adaptations. While the energy

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

11

investments in the mammal zygotes differ only marginally in relation to the body
mass of most mammals, the cost to mammal females greatly exceeds that to males
due to effects of pregnancy and lactation. This energy investment inequality has
existed since the origin of the class Mammalia, 125 million years ago.
There are some exceptions to the general mammalian pattern, however.
For instance, some mammal babies are so expensive to bring up to maturation that
both sexes have to partake in the upbringing for it to be possible. In these species,
where males and females work together to guard and rear the young, intrasexual
competition occurs just prior to pair formation. In these species, the two sexes are
usually morphologically alike. In other mammal species, however, competition
between males over mating opportunities is fierce. In some species this affects the
entire social life of the species, in that males physically exclude other males from
the group. The result is a social system akin to a harem structure, with immature
males roaming outside the social gathering or forming bachelor groups.
The importance of sexual selection in understanding aggression in
mammals is most clearly illustrated by the presence and absence of weaponry.
For example, male ungulates are commonly equipped with horns while females
are not. Horns would be a good weapon to fend off predators, especially when you
need to defend your young, or to fight off conspecific competitors. But most
young are cared for by single mothers; the fatherswho have the weaponsare
absent. Ungulate horns are commonly ready just in time for rutting season and
are then shed (e.g., deer). Instead of predator defense, male ungulates mainly use
their horns to fight each other (Caro et al., 2003; Stankowich and Caro, 2009).
A similar case can be made for the large, sharp canines of primates (Thoren et al.,
2006), and large body size in male mammals in general (Lindenfors et al., 2007a).
Such sex-skewed distribution of size and weaponry, in combination with observations of fierce aggression, is what enables us to assert that most serious conflict and
aggression in mammals is over mating opportunities.
Sexual selection acting primarily on one sex may have indirect but
pronounced consequences for the relationship between the sexes. Thus, direct
conflicts between males sometimes result in conflicts of interest between males
and females. Early thoughts on this issue (Parker, 1979, Trivers, 1972; Williams,
1966) have received much empirical support (Arnqvist and Rowe, 2005), and it
now almost seems the norm rather than an exception that there exists such a
conflict and that this becomes more severe under strong intrasexual competition.
This can lead to the interesting phenomena of sexually antagonistic coevolution
where males and females become involved in an arms race, as traits in one sex
entice the evolution of resistance in the other (Holland and Rice, 1998;
Gavrilets et al., 2001; and others). On the other hand, intrasexual competition
can lead to one sex dominating the other. With regard to aggression and physical
prowess, the common situation in mammals, including primates (Hrdy, 1981), is
that males are physically dominant over females.

12

Lindenfors and Tullberg

III. MATING SYSTEMS

Not all animals have clear sexual differences (Fairbairn et al., 2007). In birds, for
example, many species of gulls and penguins are so alike that it is impossible to
determine the sex except by closer inspections of the genitals. At the other
extreme are mallards, where the sexes are so different that Linnaeus classified
them as two different species (Andersson, 1994). In mammals, we find the same
variation even within a given mammalian order. Thus, within Pinnipedia we
have, on the one hand, elephant seals where males may weigh up to five times as
much as females and on the other hand, species such as Baikal seals where
females are of similar weight as males (Lindenfors et al., 2002). These differences
in dimorphism are due to differences in the degree of sexual selection. But why
are there differences in the degree of sexual selection between species to start
with?
Fundamentally, this question is about factors affecting male and female
social group size. These issues are commonly addressed by focusing on the
ecological variables that determine the spatiotemporal distribution of females,
based on the expectation that resources and predation account for variation in
female reproductive success. By comparison, access to females is generally assumed to be the major factor influencing male reproductive success (Emlen and
Oring, 1977; Trivers, 1972; Wilson, 1975). After risks and resources have
determined the spatiotemporal distribution of females, the distribution of
females is in turn expected to influence the degree of male intrasexual competition (Emlen and Oring, 1977). For instance, a group of concurrently fertile
females opens the field for male competition and monopolization. The general
framework is therefore that social evolution is driven by females.
The theoretical expectation that social evolution is ultimately driven by
female distribution is empirically supported by comparative studies on primates, a
group for which there is a significant correlation between evolution of male and
female sociality (e.g., Altmann, 1990; Mitani et al., 1996; Nunn, 1999). Further, a
phylogenetic investigation has shown that the evolution of female group size
precedes the evolution of male group size, that is, that evolutionary changes in
male group size lag changes in female group size (Lindenfors et al., 2004).
Ecological factors determine whether it is possible for a male to monopolize several mating opportunities. For example, elephant seal females give birth
on beaches. With a limited number of suitable beaches available in the elephant
seal range, females tend to crowd together when giving birth. Elephant seals
mate soon after they have given birth, so at the time of mating females are
gathered tightly on limited stretches of beach. Males can exclude other males
from a stretch of beach and thereby secure matings with a large number of
females. Successful males in this competition gain all matings, while the losers
get none. Fighting among elephant seals over mating opportunities is thus a

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

13

fierce and bloody affair, a scenario which has resulted in extreme size dimorphism. In other pinniped species, females give birth in isolated caves on the polar
ice pack; thus, no opportunity exists to monopolize matings. Without evolutionary pressure for male fighting ability, the sexes are more equal in size (Lindenfors
et al., 2002).
In conclusion, the ultimate cause for differences in mating systems can
be traced back to ecological circumstances. The differences in mating systems in
turn trigger differences in aggressive competition for mating opportunities which
is what drives the evolution of sex differences in size and weaponry. These
morphological sex differences are clear indicators of the severity of malemale
aggression.

IV. WHEN TO FIGHT AND WHEN TO FLEE

Given that fighting is most often about mating opportunities, how are they
predicted to pan out in terms of ferocity, number of behaviors involved, length
of time, and so on? There are two things that determine the ferocity of fighting:
the value of the object being fought over and the risks involved. The problem
can be reduced to a cost-benefit analysis. A male can not give up at first instance
to maximize his chances of survival, because that would result in total nonreproduction. Neither can he go all-in in just any aggressive encounter if there
exists only a minute chance of success. Instead, males in competitive situations
have to weigh the probabilities of success, injury, and survival against each other,
while considering other factors such as energy expenditures and probabilities of
success in future interactions with other competitors. It is important to note that
animals make calculations and decisions about how to act, but such processes do
not necessarily require the consciousness about the process usually ascribed to
human decision-making. Rather, animals are believed to use cues with regard
to the environment, as well as their own and the opponents current status, and
to use this information in an unconscious way when making decisions.
One consequence this accounting has had over evolutionary history is
that competitive interactions often take the form of a sequential assessment
game. Simply put, this prescribes that each competitor should attempt to assess
his opponents strength using as little energy as possible. Escalation should only
be initiated by the competitor that feels he has the upper hand, or by either
opponent if they cannot determine who is superior (Enquist and Leimar, 1983).
Thus, a meeting between two deer males often starts out with a stage of roaring,
which acts as a forcedly honest signal of body size. If this does not settle who is
the larger/stronger, it is followed by parallel walking, where each competitor
tries to judge the size and strength of the other by walking back and forth in
parallel. Only if it is still unclear who is the larger or stronger will the

14

Lindenfors and Tullberg

Fight (8)
Parallel
walk
(17)
Roar
contest
(33)

One stag
withdraws
(9)

One stag
withdraws
(16)

Approach
(50)

Fight (5)

No roar
contest
(17)

Parallel
walk
(7)

No
parallel
walk
(10)

One stag
withdraws
(2)
Fight (1)
One stag
withdraws
(9)

Figure 2.1. Sequential assessment in red deer (from Clutton-Brock and Albon, 1979).

competition escalate to actual fighting (Clutton-Brock and Albon, 1979;

Fig. 2.1). Thanks to this game, really fierce fights only happen between
opponents of equal sizeinferior competitors flee quickly to fight another day
(and another opponent).
There is a common interest among fighters in trying to expend as little
energy as possible while simultaneously minimizing the possibility of injury. For
example, wolves and other canids ritualistically greet each other several times
each day and display dominance or submission on a regular basisthey do not
determine their relationship at every encounter. Some cichlid fish have a system
akin to that of red deer, with different stages of escalation (Brick, 1999). Male
lions fight savagely only if they stand a good chance of winning a pride of females.
Research shows that they determine the quality of their rivals on cues from each
others manes (West and Packer, 2002). Lekking birds such as black grouse have
distinctive courtship rituals where they make calls and visual displays, an odd
mix of strength comparison and showing off, where females can pick winners
according to some criterion, sometimes just by copying other females choices
(Andersson, 1994; Dugatkin and Godin, 1993; Wade and Pruett-Jones, 1990).
Seldom do fights turn into vicious fighting, and when they do it is usually because
either the contestants are judged by each other to be of equal strength, or because

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

15

the benefit of winningthe value of the contested itemis much larger than the
cost of losing. If the choice is reproduction or death, fights become deadly. This is
why fights among elephant seals are so fierce and bloody. The chance to mate
occurs only once per year and most males never even get close. For the successful
males it is another storyin a study of Southern elephant seals, harem holders
accounted for 89.6% of the recorded paternities (Fabiani et al., 2004; Fig. 2.2).
The sequential assessment game is a variant of a game theoretical setup
termed the hawk-dove game (see also Chapter 3). In this game, there are two
possible strategies: always fight (hawk) and always yield (dove), where it is
assumed that the two competitors have equal fighting ability. An Evolutionarily

Number of males

12
RUB96

SF96

SF97

8
4
0

12

24

Number of males

12
SI296

SI196

SI297

8
4
0

24

21

32

Number of males

12
SM96
8

HH
NHH

4
0

0
2
12
Number of paternities

Figure 2.2. Number of paternities achieved by the harem holder (HH) and the other males (NHM)
associated with each harem in seven different populations of Southern elephant seals
(from Fabiani et al., 2004).

16

Lindenfors and Tullberg

Stable Strategy is a strategy which, if adopted by a population of players, cannot

be invaded by any alternative strategy. It has been shown that the ESS is a mix of
hawks and doves with proportions determined by the cost of fighting in relation
to the benefit of winning (Maynard Smith, 1982). This game provides theoretical information that in a population of nonfighters it is profitable to be a fighter,
and vice versa. If one extends the game to include a strategy called assessor that
determines whether it will act as a hawk or a dove based on some criterion
for example, depending on priority at the resourceone can arrive at the
sequential assessment game. The assessment strategy is also an ESS (Maynard
Smith, 1982).
The prediction from these game theoretical models is that populations
where individuals compete over resources or matings should consist of individuals utilizing different strategies depending on situation, where important
factors are the current size and physical state of self and opponents and the
value of resources (for instance, the number of females in the group being fought
over). In this context, it should be noted that some animal populations have
evolved alternatives to fighting strategies, usually known as sneaker strategies.
Such males are usually much smaller than fighting males and can covertly sneak
matings from females while the fighters are occupied with physical combat
(Gross, 1996).

V. CASE STUDIES: SEXUAL DIMORPHISM

As mentioned above, animal groups differ in both the way and the degree to
which they are exposed to sexual selection, and this will have great effects on the
evolution of sex differences (Fairbairn et al., 2007). Although mammals as a
group are characterized by a high degree of intrasexual selection (as compared
with, for instance, birds, where intersexual selection seems to be more common),
there is variation in the strength of sexual selection both within and among
mammalian orders. An example of this variation is the pinnipeds (seals, sea lions,
and walruses) where there exists a clear relationship between harem size and
sexual size dimorphism (Lindenfors et al., 2002; Fig. 2.3).
In this section, we bring up some studies that have compared different
mammalian groups with respect to the consequences of sexual selection on
behavioral and morphological evolution. There are 4629 extant or recently
extinct mammalian species, as listed by Wilson and Reeder (1993). In a survey
of 1370 of these, Lindenfors et al. (2007a) showed that sexual selection is a
prevalent selective force in mammals. With a cutoff point at a 10% size difference in either direction to count as sexual dimorphism, mammals were, on
average, male-biased size dimorphic (average male/female mass ratio 1.184;
paired t-test p0.001; Table 2.1) with males being larger than females in 45% of

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

17

log(male/female weight) contrasts

0.8

0.4

-1.5

-1.0

-0.5

0.0
0.0

0.5

1.0

1.5

-0.4

-0.8
log(harem size) contrasts
Figure 2.3. Regression line through the origin on harem size and body weight dimorphism. The data
points are from a phylogenetic independent contrasts analysis. There is a significant
relationship between harem size and sexual size dimorphism (b 0.376, p 0.000,
R2 0.577, n 36) (from Lindenfors et al., 2002).

extant species (Table 2.1). Systematists recognize 26 monophyletic mammalian

orders (Wilson and Reeder (1993)). When investigating each order separately,
the majority of orders also turned out to be significantly male-biased dimorphic
(average male/female mass ratio > 1.0 and p< 0.05). Some orders exhibited no
significant size dimorphism, and only one (Lagomorpha; hares, rabbits, and pikas)
was significantly female-biased dimorphic on average (average male/female mass
ratio < 1.0, p< 0.05; Table 2.1).
The mating system in a species describes the number of females a male
can monopolize and thus affects the potential strength of sexual selection males
are exposed to in that species. Using a phylogenetic tree for all mammals
(Bininda-Emonds et al., 2007) together with information about mating system
and sexual size dimorphism, Lindenfors et al. (2007a) tested whether sexual
selection could explain the variation in sexual size dimorphism among mammals.
Mating system was used as a three-state unordered categorical variable, an
independent variable used to test for differences in dimorphism between

18

Lindenfors and Tullberg

Table 2.1. Summary of the Patterns of Dimorphism Found in Mammals

Order

Number of
recognized
species

All mammals
Monotremata (Monotremes)
Didelphimorphia (American
marsupials)
Paucituberculata (Shrew oppossums)
Microbiotheria (Monito del monte)
Dasyuromorphia (Dasyuroids)
Peramelemorphia (Bandicoots
and bilbies)
Notoryctemorphia (Marsupial moles)
Diprotodontia (Kangaroos, etc.)
Insectivora (Insectivores)
Macroscelidea (Elephant shrews)
Scandentia (Tree shrews)
Dermoptera (Colugos)
Chiroptera (Bats)
Primates (Primates)
Xenarthra (sloths, armadillos,
and anteaters)
Pholidota (Pangolins)
Lagomorpha (Rabbits and pikas)
Rodentia (Rodents)
Cetacea (Whales, dolphins, and
porpoises)
Carnivora (Carnivores)
Tubulidentata (Aardwark)
Proboscidea (Elephants)
Hyracoidea (Hyraxes)
Sirenia (Dugongs and manatees)
Perissodactyla (Horses, rhinos,
and tapirs)
Artiodactyla (Antelopes,
camels, pigs, etc.)

Number of
species with
body mass data

Average
dimorphism

Sexual size
dimorphism

Mammalia
4629
1370

1.184

p  0.001

Subclass Prototheria
3
2

1.273

Subclass Metatheria
63
13

1.323

p 0.002

5
1
63
21

2
1
24
9

1.840
1.044
1.465
1.496

p  0.001
p 0.015

2
117

0
63

1.306

p  0.001

Subclass Eutheria
428
59
15
5
19
1
2
0
925
354
233
198
29
4

1.048
0.964

0.999
1.247
0.914

p 0.081
p 0.142

p 0.091
p  0.001
p 0.216

7
80
2015
78

3
21
295
10

1.767
0.930
1.092
1.414

p 0.001
p 0.012
p  0.001
p 0.082

271
1
2
6
5
18

180
0
2
1
0
8

1.476

1.900
1.111

1.164

p  0.001

p 0.156

220

115

1.340

p  0.001

Dimorphism is given as male mass/female mass. Mammals and the majority of mammalian orders
are on average male-biased dimorphic (average dimorphism > 1.0 and p < 0.05), even if there exist a
few orders with no significant dimorphism (p > 0.05) or female-biased dimorphism (Lagomorpha:
average dimorphism < 1.0 and p < 0.05). p-Values represent the significance of paired t-tests where
male body mass was paired with female body mass. Dashes indicate orders with too few data points for
statistical analysis (n < 3 for tests of the presence of dimorphism, from Lindenfors et al., 2007a).

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

19

more and less sexually selected (polygynous) sister taxa. These tests
revealed that a higher degree of sexual selection was associated with a higher
degree of male-biased dimorphism. More polygynous taxa not only had larger
males but also larger females than their less polygynous sister taxa. These results
indicate that sexual selection is a significant explanatory factor of both sexual
dimorphism as such, and of the general size increase in many mammalian
lineages.
In primates, the mammal order humans belong to, the pattern is similar.
Again using mating system as a three-state unordered categorical variable,
testing for differences in dimorphism between more and less sexually selected
sister taxa, a higher degree of sexual selection was associated with a higher degree
of male-biased dimorphism. Again, more polygynous taxa also had larger males
and females than their less polygynous sister taxa (Lindenfors, 2002; Lindenfors
and Tullberg, 1998). Here, however, a novel method investigating temporal
order of events revealed not only a correlation but also a causal link between
sexual selection and sexual size dimorphism where changes in mating systems
occurred before changes in the degree of sexual selection (Lindenfors and
Tullberg, 1998). Using similar methods, sexual selection has also been shown
to be an important determinant of sexual dimorphism in canine size in primates
(Thoren et al., 2006), although primate canines are also of importance in
predator defense (Harvey et al., 1978). Thus, both body size and canine size
bear witness to an evolutionary history of malemale aggression in primates.
This selection history has its grounds in a sexual difference in behavior.
While males compete more over matings than females, female reproduction is
instead limited by resource allocation (Emlen and Oring, 1977). These differing
demands should be expected to produce variation in the relative sizes of various
brain structures, just as they are expected to produce differences in other morphological structures. However, data on brain structures in primates are not
available for males and females separately. Instead, investigating species differences in brain structures and comparing them on basis of differences in the
species-typical degree of sexual selection, research has shown that the degree
of male intrasexual selection is positively correlated with several structures
involved in autonomic functions and sensory-motor skills, and in pathways
relating to aggression and aggression control (Lindenfors et al., 2007b).
The sizes of the mesencephalon, diencephalon (containing the hypothalamus), and amygdala, all involved in governing aggressive behaviors, are
positively correlated with the degree of sexual selection, whereas the size of the
septum, which has a role in facilitating aggression control, is negatively correlated with the degree of sexual selection. These correlations indicate that sexual
selection affects physical combat skills. Moreover, male group size was positively
correlated with the relative volume of the diencephalon and negatively
correlated with relative septum size, further strengthening the conclusion that

20

Lindenfors and Tullberg

aggression is an evolutionarily important component of malemale interactions

(Lindenfors et al., 2007b). Thus, primate brain organization also reflects a history
of malemale aggression.

VI. HUMANS AND THE MAMMALIAN PATTERN

So where do humans fit into this picture? Humans are one of the sexually sizedimorphic species in the primate order in Table 2.1. But compared to our closest
relatives (chimpanzees, bonobos, gorillas, and orangutans) humans have the
lowest degree of size dimorphism (Lindenfors, 2002), indicating a decreasing
degree of sexual selection over human evolution. Nevertheless, in all measurements of length that have ever been carried out in human populations, males
have been taller than females. The average dimorphism in humans from these
surveys is 1.07 (Gustafsson and Lindenfors, 2004). Does this mean that we
exhibit a tendency toward the polygyny that accompanies such size dimorphism?
According to the Ethnographic Atlas Codebook (Gray, 1999), a database of cultural characteristics for 1231 comparable cultures from around the
world, polygyny is common in 48% of human societies. In another 37% polygyny
is allowed, and in only 15% is monogamy the norm. Only four reported societies
are considered polyandrous. From these data and the degree of human size
dimorphism, one may draw the conclusion that humans are at least more
polygynous than monogamous (see also Low, 2000), and also that Western
cultures fall within the monogamous 15% of the world. Interestingly, intergroup
differences in size dimorphism are not correlated with differences in the degree of
polygyny (Gustafsson and Lindenfors, 2004), a clear indication that cultural
evolution proceeds faster than biological evolution.
There are more indications that humans have an evolutionary history of
sex differences as an explanatory factor in human aggression. For example, men
commit most of the worlds violent acts that are reported to the police. Men are
consequently overrepresented in the worlds prisons. Women typically make up
only 1015% of the prison population (Harrendorf et al., 2010). Further,
soldiering is most often an all-male vocation (personal observation). Humans
are, however, the products of both biological and cultural inheritance (Boyd and
Richerson, 2005). Here, we have presented only the biological side of the story,
but we agree with Archer (2009) that sexual selection probably is the best
explanation for the magnitude and nature of human sex differences in aggression.
Humans fit into the mammalian scheme of things very well.

Acknowledgment
This research was supported through a generous research grant from the Swedish Research Council
(P. L.).

2. Evolutionary Aspects of Aggression: The Importance of Sexual Selection

21

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Signaling Aggression
Moira J. van Staaden,* William A. Searcy,
and Roger T. Hanlon
*Department of Biological Sciences and JP Scott Center for Neuroscience,
Mind & Behavior, Bowling Green State University, Bowling Green, Ohio,
USA

Department of Biology, University of Miami, Coral Gables, Florida, USA

Marine Resources Center, Marine Biological Laboratory, Woods Hole,

Massachusetts, USA

I. Introduction
A. An ethological approach to aggression
B. The classic game theory model
C. Signaling games
D. Threat displays and why they are part of aggression
E. Evolutionary issues
F. The challenge of incomplete honesty
G. Case studies in aggressive signaling
II. Bird Song Signals Aggressive Intentions: Speak Softly and
Carry a Big Stick
III. Visual Displays Signal Aggressive Intent in Cephalopods:
The Sweet Smell of Success
A. Cuttlefish agonistic bouts
B. Squid agonistic bouts
C. From molecules to aggression: Contact pheromone triggers
strong aggression in squid
D. Signaling aggression in humans
Acknowledgments
References

Advances in Genetics, Vol. 75

Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00008-3

24

van Staaden et al.

ABSTRACT
From psychological and sociological standpoints, aggression is regarded as intentional behavior aimed at inflicting pain and manifested by hostility and attacking
behaviors. In contrast, biologists define aggression as behavior associated with
attack or escalation toward attack, omitting any stipulation about intentions and
goals. Certain animal signals are strongly associated with escalation toward
attack and have the same function as physical attack in intimidating opponents
and winning contests, and ethologists therefore consider them an integral part of
aggressive behavior. Aggressive signals have been molded by evolution to make
them ever more effective in mediating interactions between the contestants.
Early theoretical analyses of aggressive signaling suggested that signals could
never be honest about fighting ability or aggressive intentions because weak
individuals would exaggerate such signals whenever they were effective in
influencing the behavior of opponents. More recent game theory models, however, demonstrate that given the right costs and constraints, aggressive signals
are both reliable about strength and intentions and effective in influencing
contest outcomes. Here, we review the role of signaling in lieu of physical
violence, considering threat displays from an ethological perspective as an
adaptive outcome of evolutionary selection pressures. Fighting prowess is conveyed by performance signals whose production is constrained by physical ability
and thus limited to just some individuals, whereas aggressive intent is encoded in
strategic signals that all signalers are able to produce. We illustrate recent
advances in the study of aggressive signaling with case studies of charismatic
taxa that employ a range of sensory modalities, viz. visual and chemical signaling
in cephalopod behavior, and indicators of aggressive intent in the territorial calls
of songbirds. 2011, Elsevier Inc.

I. INTRODUCTION
Although physical fighting, including the killing of conspecifics, is widespread in
nonhuman animals just as it is in humans, the majority of contests and disputes
in nonhuman animals are settled without physical fighting. Rather than resorting
to immediate physical combat, nonhuman animals often engage instead in
extended bouts of signaling, making prominent display of their weapons (e.g.,
antlers, claws, and teeth), or running through a repertoire of highly stereotyped
agonistic signals. With their high cognitive capacity, primates (humans
included) are particularly good at reducing social tensions and resolving conflicts
using agonistic signaling as opposed to sheer physical force (Cheney et al., 1986).

3. Signaling Aggression

25

Such aggressive signaling is found in virtually all of the multicellular

taxa and can involve all communication modalities. Orthoptera (Alexander,
1961; Simmonds and Bailey, 1993) and many other insects (Clark and Moore,
1995; Jonsson et al., 2011) use aggressive song to defend resources, and the use of
territorial song in birds is well known (Searcy and Yasukawa, 1990; Stoddard
et al., 1988). Calls are employed to similar effect in the dramatic displays of large
mammals or frog choruses (Bee et al., 1999; Reby et al., 2005; Wagner, 1992),
and more subtly by other vertebrate taxa such as fish (Raffinger and Ladich,
2009). In these scenarios, signaling can be just as effective as physical attack in
intimidating opponents and winning contested resources.
Chemical signals are widely used to signal resource defense and fighting
ability, deposited either as scent marks in fixed locales by terrestrial species (Page
and Jaeger, 2004) or contained in urine released during aggressive interactions in
some aquatic organisms (Breithaupt and Eger, 2002). Visual signals are perhaps
the most familiar and easily appreciated of aggressive displays, beginning with
Darwins (1871) graphic illustration of aggression and fear in the facial expression of the domestic dog. Visual signs of aggression include variable pigment
patterns of many fish and cephalopods (DiMarco and Hanlon, 1997; Moretz and
Morris, 2003), and the ritualized display of weapons (Huber and Kravitz, 1995;
Lundrigan, 1996) or inedible objects as props (Murphy, 2008).
Phylogenetic comparative analyses demonstrate that many of these
aggressive signals allowing opponents to resolve contests without physical
harm evolved from nonsignaling behaviors through the process of ritualization
(Scott et al., 2010; Turner et al., 2007). Whereas agonistic behavior runs the
gamut from passivity, defense, and escape to full conflict, here, we reserve the
terms aggressive/threatening behavior for that subset of agonistic behavior associated with the escalation toward physical fighting (Searcy and Beecher, 2009).

A. An ethological approach to aggression

The ethological approach to aggression derives historically from the traditional
instincts and drives articulated by Lorenz (1978). Although the simple psychohydraulic model of motivation underlying this view proved inadequate in the
long term, the idea that aggression is based on both internal state and external
stimuli, and the proposed value of a comparative evolutionary approach, were
both far-sighted and enduring. The classic On Aggression (Lorenz, 1963) which
was written for a popular audience, highlighted aggression as a natural, evolved
function, with a founding basis in other instincts, and a central role in animal
communication. A more nuanced view is found in his work known as the Russian
manuscript (Lorenz, 1995). In this, Lorenz discussed animals and humans separately, not because of any fundamental difference in their biology, but because
he believed it necessary for the reader to have an adequate frame of reference.

26

van Staaden et al.

Much current research on the biology of aggression focuses on identifying the physiological substrate to violence (i.e., on proximate cause and nonadaptive features). The ethological or sociobiological approach, in contrast,
focuses attention on the ultimate causes and adaptive forms of aggressive behavior
(e.g., Chen et al., 2002; Huber and Kravitz, 1995; Miczek, et al., 2007; Natarajan
et al., 2009): how and why has evolution molded complex agonistic interactions
built on reciprocal displays of threat or submission, affect or intent?

B. The classic game theory model

Evolutionary fitness is measured in terms of the number of offspring an individual
produces over the course of its lifetime. In the evolutionary race to transmit their
genes to the following generations at a higher frequency than that of their
conspecifics, these individuals must compete for access to all the resources
necessary to create and raise their progeny, including mates, dominance rights,
and desirable territory. Winners in this intraspecific competition thus stand to
gain both immediate personal advantages such as food, space, and safety, as well
as long-term evolutionary fitness, that is, more offspring and therefore copies of
their genes in subsequent generations. Simulation approaches from game theory
have long provided a theoretical framework for analyzing and predicting the
outcomes of competitive interactions. The classic Hawks and Doves game
(Maynard Smith and Price, 1973) considers symmetrical contests between pairs
of individuals who are equivalent in every respect (equal size, strength, fighting
ability, etc.), differing only in behavioral/fighting strategy in intraspecific
encounters. Hawk strategists are those who will always choose to fight when
they encounter a conspecific at a contested resource. Dove strategists, in contrast,
always retreat from an individual behaving as a Hawk, rather than engage them
in combat. Hawks always best Doves, but they incur costs when they compete
against other Hawks. The outcome between two Dove strategists is randomly
determined. Each conflict consists of a series of agonistic moves (incorporating
provocation, escalation, retaliation, etc.) with rewards or costs assigned to each
contestant according to a particular payoff matrix (Table 3.1).
Populations are expected to converge on an evolutionarily stable strategy (ESS), strategies that once they are predominant cannot be invaded by any
other strategy. The ESS depends critically on the ratio of what an individual
stands to gain over what it stands to lose in a fight. Thus, in the common
situation where the cost of injury exceeds the benefits of winning, populations
are expected to adjust to balanced proportions of the two strategies with the
majority of individuals behaving as Doves, while a smaller number of Hawk
strategists persists. Only in extreme situations where the value of a resource
greatly exceeds the cost of injury, will a Hawk strategy be superior and can
become so widespread as to completely replace the Dove strategy. For instance,

3. Signaling Aggression

27

Table 3.1. The Payoff Matrix for the HawkDove Game Shows the Consequences that Result When
a Player of a Given Strategy (Left Column) Encounters Another Players Strategy

Hawk
Dove

Hawk

Dove

Tie [(V
C)/2]

Lose [0]

Win [V]
Tie [V/2]

Choices are assumed to be rational where each individual would prefer to win, prefer to tie rather
than lose, and prefer to lose over receiving injury. In this payoff matrix, V (value of the contested
resource) and C (cost of an escalated fight) determines the net outcome when different strategies
meet. In encounters between Hawks, the winner gains control over the value of the resource while
the losing Hawk sustains an injury. In the common scenario, where the value of the resource is less
than the cost of injury (i.e., C > V), average payoff in a Hawk meeting a Hawk is negative and
less than that of a Dove meeting a Hawk. Only in rare situations, when the value of the resource
exceeds the cost of injury, will Hawk be unequivocally the superior strategy.

intense fighting among male elephant seals results in the victorious male both
monopolizing a section of the beach and gaining sole reproductive access to the
harem of females which resides there. In the vast majority of cases, however,
resources are rarely worth the risk of injury, and competing individuals would do
best to resolve conflicts via ritualized displays.

C. Signaling games
The earliest game theoretical analyses of aggressive signaling were pessimistic
about the evolutionary stability of such systems (Caryl, 1979; Maynard Smith,
1974, 1979). Their reasoning was that if we assume that signals can help in
winning contests by conveying high levels of aggression or fighting ability, then
it becomes advantageous for all individuals to give the highest levels of these
signals. If all individuals signal maximally, then there is no information in the
signal about either aggressive intentions or fighting ability. The first rigorous
game theoretical model to demonstrate that reliable aggressive signaling could be
evolutionarily stable was a mutual signaling game in which two interactants
chose between two cost-free signals to create a stable global strategy (Enquist,
1985). This model demonstrated how threat displays reveal information about
the strength or condition of the contestants via their choice of action in
aggressive encounters. The players in this game each have a hidden state
(strength or weakness) which determines their ability to win physical fights.
An honest weak individual gives a signal conveying weakness, and abandons the
contest if the other individual gives a signal conveying strength. A dishonest
weak individual can successfully bluff other weak individuals by giving the signal
of strength, but at a cost of sometimes being attacked by a better fighter if the

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van Staaden et al.

opponent turns out to be strong. If the cost of being attacked by a stronger

individual is high relative to the benefit of winning contests, then bluffing may
not be advantageous, and honest signaling can be evolutionarily stable.
There followed a slew of variant Hawk/Dove models which attempted to
accommodate the diversity of interactions between senders and receivers (e.g.,
Enquist and Leimar, 1983; Leimar and Enquist, 1984; Maynard Smith and
Harper, 1988; Skyrms, 2009). These models of communication may be classified
into five structures based on the relative timing of the (signal and/or response)
choices made by the two players during the game (reviewed in Hurd and Enquist,
2005). Mutual signaling games, which most closely resemble agonistic interactions between animals, are increasingly being used as models (e.g., Kim, 1995;
Szamado, 2000). In this structure, both players signal, and react to their opponents signal, in biologically realistic ways. Genetic algorithms are also being
used to examine non-ESS solutions to these games (Hamblin and Hurd, 2007).
Alternative approaches employ simulation methods and neural networks
(Noble, 2000; Wheeler and de Bourcier, 1995) to explore communication in
animal contests.

D. Threat displays and why they are part of aggression

Aggression is costly to participants not only in terms of energy expenditure and
the potential for injury but also because of opportunity costs. Time spent in
physical conflict is time that is not available for other vital activities such as
exploring, feeding, or mating. Thus, there are selective advantages to reducing
aggression. Threat displays are a critical component of aggression because they
modulate competitive social interactions among conspecifics. If signaling is
effectively delivered by a sender and appropriately interpreted by the intended
receiver it might be so subtle that the interaction is rendered virtually invisible
to an outside observer. Alternatively, if sender and receiver perceive the competitive difference between them to be slight, the social interaction is prolonged,
escalates in intensity, and may ultimately culminate in levels of overt conflict
that result in physical damage or death of one or both interactants.
In such aggressive signaling contests, two kinds of information are
important to receivers: information on the signalers willingness to escalate
(aggressiveness motivation) and on its fighting ability (resource-holding potential) (Searcy and Beecher, 2009). Classification schemes based on the type of
interaction in which communication takes place and the nature of the signals
used converge on the following signal categories (Hurd and Enquist, 2005;
Maynard Smith and Harper, 2003; Vehrencamp, 2000).
Performance signals are signals constrained to a subset of signalers either
by differences in the ability to perform them (Maynard Smith, 1982), or by
possessing the information needed to produce them (Hurd and Enquist, 2005).

3. Signaling Aggression

29

Performance displays (index signals of Maynard Smith and Harper, 2003) have
excellent empirical support, as do models of their use (e.g., Enquist and Leimar,
1983; Leimar and Enquist, 1984). Examples include the lateral displays of many
fish (Enquist and Jakobsson, 1986) or the pitch of calls in many frog and mammal
species (e.g., Bee et al., 1999; Reby et al., 2005), both unfakeable signals as they
are determined by the senders size and fighting ability.
Strategic signals are available to all signalers, and may be either classic
handicaps or conventional signals (Hurd and Enquist, 2005). Classic handicaps
have some inherent cost, independent of receiver response, and variation in the
level of cost experienced by different individuals produces different optimum
signaling levels (Grafen, 1990). Evidence for handicapped displays is theoretical
(Zahavi, 1987) rather than empirical, though threat displays have been shown to
advertise endurance in lizards (Brandt, 2002) and grasshoppers (Greenfield and
Minckley, 1993). Conventional signals are arbitrary with respect to signal design
and therefore dependent for meaning on an agreement between the signaler and
receiver. Honesty of conventional signals in agonistic interactions is maintained
by two forms of receiver-dependent stabilizing costs (Enquist, 1985; Guilford and
Dawkins, 1995); receiver retaliation (Enquist, 1985) has empirical support
(Molles and Vehrencamp, 2001) and vulnerability handicap (Zahavi, 1987) for
which empirical support is contradictory (Laidre and Vehrencamp, 2008; Searcy
et al., 2006). Most threat displays appear to be conventional signaling systems.
Examples include color patches and song-type sharing in birds (Molles and
Vehrencamp, 2001; Vehrencamp, 2000). Aggressiveness motivation (or willingness to escalate) is most likely to be encoded this way (Hurd and Enquist, 2005).

E. Evolutionary issues
Empirical analysis of aggressive signaling is more complex than the classic ESS
modeling approach would suggest. This is in large part attributable to the fact
that evolution is not necessarily equilibrial (Houston and McNamara, 1999).
An individuals success or failure in using signals depends upon how other
individuals use and interpret those signals, that is, it is a trait under frequencydependent selection (Maynard Smith, 1982). In addition to frequency
dependence of the signal phenotype itself, selection pressures acting on signaler
and receiver in a communicating dyad may be distinct if their genetic interests or
risk profiles (Searcy and Nowicki, 2006) are not identical, or if signals have dual
functions, affecting both aggression and mate choice (Wong and Candolin,
2005). Selection may also modify the responsiveness of other individuals to the
signals (Arak and Enquist, 1995). Thus, like other significant evolutionary
problems such as sexual selection and conflict, signaling strategies may lack
stable equilibria and remain in constant evolutionary flux. Understanding the

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van Staaden et al.

evolution of behavioral phenotypes under such nonequilibrial conditions

requires dynamic approaches which have yet to be adequately deployed in the
game-theoretical modeling of biological signaling (Hurd and Enquist, 2005).

F. The challenge of incomplete honesty

In animal contests, selection should favor displays providing reliable information
about the fighting ability or aggressive intent of competitors. However, considerable theoretical work predicts that low levels of deception may occur within
otherwise honest signaling systems (Adams and Mesterton-Gibbons, 1995;
Szamado 2000). Strategic signals (i.e., ones of intent) are particularly prone to
such corruption because they typically involve low production costs (Maynard
Smith, 1974, 1979, 1982). Testing for such incomplete honesty is challenging
because it is difficult to distinguish dishonest signals from natural variation in
signal size (Moore et al., 2009), and between a successful bluff and an honest
signal, especially when signaled information is continuous rather than discrete.
Hughes (2000) suggested that dishonesty could be detected by analysis of signal
residuals, the residuals from a measure of the regression of signal structure on
competitive ability. Whereas receivers take advantage of the strong relationship
between signal and fighting ability, for example, signalers take advantage of the
variation around this relationship. If individuals who exaggerate signals benefit
from doing so, they should perform more repetitions of the signaling activity than
those who do not exaggerate (Hughes, 2000). Empirical examples of incomplete
honesty, though still comparatively rare, suggest this is not a fixed behavioral
trait, and depends on context as well as signal residuals (Arnott and Elwood,
2010; Hughes, 2000; Lailvaux et al., 2009).

G. Case studies in aggressive signaling

Using animal models and invasive techniques (e.g., drugs, hormones, brain
lesions, and gene knockouts), we have made great strides in unraveling the
mechanisms and internal states underlying aggression in controlled lab situations. This is true also with respect to aggressive signaling (see Chapter 5).
Studies of nonmodel organisms are a necessary complement to this approach as
these can provide the telling exceptions in field situations where more complex
social/physical environments permit full expression of behaviors and analysis of
adaptive function (see Logue et al., 2010). Below, we present two case studies of
taxa employing multimodal signaling systems to artfully modulate aggressive
interactions in complex social systems.

3. Signaling Aggression

31

II. BIRD SONG SIGNALS AGGRESSIVE INTENTIONS: SPEAK SOFTLY

AND CARRY A BIG STICK
The use of song by songbirds provides an excellent illustration of how signals
function in aggression in nonhuman animals. The songbirds (suborder Passeres)
consist of over 4000 species of birds, which are distinguished in part by their
intricate vocal musculature. This musculature functions most importantly in the
production of the complex vocalizations from which the songbirds derive their
name. Most species in the group are territorial and monogamous, and their songs
are used in both territory defense and mate attraction (Catchpole and Slater,
2008; Searcy and Andersson, 1986). At least in temperate zone species, songs are
given mainly by males and mainly during the breeding season. Some attributes of
song and singing behavior have evolved to function in attracting females and
persuading them to mate, but others have evolved to function in aggressive
communication between males in the context of claiming and defending
a territory.
Many of the signals employed by songbirds in aggressive communication
can be illustrated using the signaling behavior of song sparrows (Melospiza melodia). Song sparrow songs (Fig. 3.1) are multipartedthat is, they contain multiple
phrases differing in structure (Mulligan, 1963). Individual males sing several
versions of the species song, each consisting of a distinct and largely nonoverlapping set of phrases. These distinct versions are called song types (Fig. 3.1), and the
collection of song types sung by one male is his song repertoire. Repertoire sizes vary
geographically in song sparrows, with averages in the range of 812 song types per
male (Peters et al., 2000). Male song sparrows produce their repertoires with
eventual variety, meaning that they sing several to many repetitions of
one song type before switching to another. The successive repetitions of a song
type are themselves typically not identical, but instead show differences that are
audible (Borror, 1965; Saunders, 1924) but of lower magnitude than differences
between song types (Nowicki et al., 1994). The minor variations of a song type are
termed song variants (Fig. 3.1). Song sparrows respond to differences between song
variants (Stoddard et al., 1988) but less strongly than to differences between song
types (Searcy et al., 1995).
In some species of songbirds, different song types have different functions; for example, in wood warblers (Parulidae) some song types may be
specialized for malefemale communication and others for malemale signaling
(Byers, 1996; Spector, 1992; Weary et al., 1994; but see Beebee, 2004). In song
sparrows, however, all song types are thought to be functionally equivalent, and
in that sense redundant. Even with redundant song types, however, certain
signals can be produced with a repertoire of song types that are not possible with
a single type. Some of these signals have been suggested to be aggressive.

32

van Staaden et al.

Figure 3.1. Spectrograms of two variants of each of three song types from a male song sparrow
recorded in northwestern Pennsylvania. Each row shows two variants of one song type.
Note that virtually every note differs between the different song types, whereas the two
variants of any one song type tend to differ only in their endings.

Singing behaviors associated with aggressive contexts in song sparrows

include:
1. Song-type switching. If a bird sings more than one song type, it can vary the
frequency with which it switches between song types, and switching frequency
becomes a possible signal. Song-type switching frequency has been suggested
to be a conventional signal of aggression (Vehrencamp, 2000)conventional
in the sense that the meaning of the signal is arbitrary with respect to its form.
In song sparrows, type-switching frequency increases in aggressive contexts,
for example, during counter singing between territorial males or when an
outside male intrudes on a territory (Kramer and Lemon, 1983; Kramer
et al., 1985; Searcy et al., 2000). In other species, the opposite pattern
holdstype-switching frequency decreases in aggressive contexts (Molles
and Vehrencamp, 1999; Searcy and Yasukawa, 1990). The fact that either
pattern can occur supports the arbitrariness of the signal (Vehrencamp, 2000).
2. Variant switching. In song sparrows, variant-switching frequency also
increases in aggressive contexts, and the increase is if anything more
consistent than the increase in type switching (Searcy et al., 2000). Given

3. Signaling Aggression

33

the evidence that male song sparrows attend to variant switching (Searcy
et al., 1995; Stoddard et al., 1988), variant-switching frequency is another
potential aggressive signal.
3. Song-type matching. Matching is a behavior in which one male replies to a
rival with the same song type that the rival has just sung. Matching can occur
by chance, but in song sparrows it has been shown that when wholly or
partially shared songs are played to males on or near their territories, those
males match the playback songs at levels significantly higher than chance
(Anderson et al., 2005; Burt et al., 2002; Stoddard et al., 1992). Song sparrows
match strangers more than neighbors (Stoddard et al., 1992), and are more
aggressive in general toward strangers (Stoddard et al., 1990), providing
further support for matching as an aggressive signal.
4. Song rate. The number of songs produced per unit time is a parameter that
birds can vary even if they sing only a single song type. In some species of
songbirds, territory owners consistently increase song rates in aggressive
contexts (Vehrencamp, 2000). Song sparrows have shown this pattern in
some experiments (Kramer et al., 1985) but not in others (Peters et al., 1980;
Searcy et al., 2000).
5. Soft song. In her classic monograph on song sparrow behavior, Nice (1943)
noted that during intense aggressive encounters, male song sparrows produce
songs of especially low amplitude. In some other songbirds, such soft songs are
produced during courtship as well as during aggression (Dabelsteen et al., 1998),
but in song sparrows they apparently are given only in aggressive contexts.
Anderson et al. (2008) found that the amplitude of soft songs was as much as
36 dB lower than the amplitude of the loudest normal or broadcast songs.
The five singing behaviors listed above are all associated with aggressive
contexts in song sparrows, but signals used in aggressive contexts can convey
submission or escape as well as attack, in which case they would be considered
agonistic but not aggressive. These alternative interpretations seem particularly likely a priori in the case of soft songs. To test whether a signal is aggressive
rather than submissive, it is necessary to determine whether the signal predicts
aggressive escalation (Searcy and Beecher, 2009). Aggressive escalation includes
outright physical attack of course, but also includes other behaviors that lead up
to attack, such as approach to a rival or giving signals that are higher in a
hierarchy of aggressive signaling.
A test of the predictive power of singing behaviors was carried out for
song sparrows by Searcy et al. (2006). In this study, a brief playback of song
sparrow song was used to elicit aggressive signaling from a territory owner. After a
5-min period during which displays were recorded, a taxidermic mount of a song
sparrow was revealed on the subjects territory, posed above the loudspeaker, in
conjunction with another brief playback. The subject was then given a set period

van Staaden et al.

34

of time (14 min) to attack or not attack the mount. Of 95 males that were tested,
20 attacked and 75 did not. The display behavior of attackers and nonattackers
was then compared, focusing on the five singing behaviors discussed above, plus
wing-waving, a display in which a male fans one or both wings while remaining
perched; this is the most prominent visual display given by song sparrows during
aggressive contests. For the initial recording period, none of the display measures
differed significantly between attackers and nonattackers, though the number of
soft songs approached significance. A second analysis focused on the 1-min period
directly before attack in the attacking subjects, using a matching time period in
nonattackers as the control. Here, number of soft songs was significantly higher in
attackers than nonattackers, whereas none of the other five measures differed
(Fig. 3.2). In single-variable discriminant function analyses, the number of soft
songs was the only display that discriminated between attackers and nonattackers;
this display correctly predicted presence/absence of attack in 74% of the tested
males. Soft song is thus a reliable signal of aggressive intentions in song sparrows.

B
Type switching frequency

P = 0.00015

2
1
0

0.05
0

No

NS

4
2

No

Yes
Attack

0.5
0.25
0

Yes

F
1.5

0.75
0.5

NS

0.25

NS
0.5

NS
0.75

No

Matching songs

Yes

E
8

Total songs

0.1

Yes

No

NS

0.15

Wing waves

Soft songs

C
0.2

Variant switching frequency

No

Yes
Attack

No

Yes
Attack

Figure 3.2. Display measures (mean  s.e.) for the 1 min just prior to attack for male song sparrows
that attacked compared to a matching 1-min period for nonattackers. The display
measures are (A) number of soft songs, (B) type-switching frequency, (C) variantswitching frequency, (D) total songs, (E) number of matching songs, and (F) number
of bouts of wing-waving. Only soft songs showed a significant difference between
attackers and nonattackers. Redrawn from data in Searcy et al. (2006).

3. Signaling Aggression

35

The use of soft, low-amplitude vocalizations as the most threatening of

signals is somewhat counterintuitive, but this result has since been replicated in
additional species. Ballentine et al. (2008) did a parallel study of aggressive
signaling in swamp sparrows (Melospiza georgiana), a close relative of song
sparrows, using methods similar to those of Searcy et al. (2006). Swamp sparrows
have simpler songs than song sparrows, but again have repertoires of apparently
redundant song types. In addition to songs, males give two types of calls in
aggressive contexts, buzzes and wheezes (Ballentine et al., 2008; Mowbray,
1997). In swamp sparrows as in song sparrows, wing-waving is the most prominent visual display given during aggressive encounters.
In 40 trials with swamp sparrows, 9 males attacked a taxidermic mount
of a conspecific male and 31 did not. For the initial recording period, five of seven
display measures did not differ between attackers and nonattackers; these were
switching frequency, number of matching songs, number of broadcast songs,
number of rasps, and number of wheezes. Two measures were significantly higher
in attackers: number of soft songs and number of wing waves. In a forward,
stepwise discriminant function analysis, soft songs entered first, followed by rasps,
and these together correctly classified 83% of males as attackers or nonattackers.
For the 1 min prior to attack, soft songs and wing waves were again the only two
display measures that differed between attackers and nonattackers. For this time
period, a discriminant function including soft songs and wing waves was the best
predictor of attack, classifying 85% of males correctly.
Hof and Hazlett (2010) have recently performed a similar experiment
with black-throated blue warblers (Dendroica caerulescens), which are also in the
songbird suborder but in another family (Parulidae). In 54 trials with blackthroated blue warblers, 19 males attacked the mount and 35 did not. Hof and
Hazlett (2010) compared attackers and nonattackers for four display measures:
type-switching frequency, total number of songs, number of soft songs, and
number of ctuk calls. For both an initial recording period and the 1 min prior
to attack, only the number of soft songs differed significantly between attackers
and nonattackers, with attackers giving substantially more. In logistic regressions
based on either time period, soft song was the only significant predictor of attack.
In a logistic regression that incorporated displays for the entire trial, soft song
correctly predicted attack behavior in a very impressive 93% of subjects.
In all three of the songbird species reviewed above, most of the displays
given in aggressive contexts are not predictive of attack. One theory about such
displays is that they were at one time predictors of attack, but that over evolutionary time their reliability was undermined by the spread of bluffing
(Andersson, 1980). If an aggressive display is beneficial in intimidating opponents, such that the benefit of giving it is greater than any costs, then selection
will favor its use in individuals that do not intend to attack as well as in those
that do. Use of the display will then increase in frequency among individuals not

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van Staaden et al.

intending attack, until at some point the signal ceases to be informative about
attack likelihood. Another hypothesis is that these agonistic displays have
evolved to convey messages other than imminent attack. Possible alternative
messages include at one extreme retreat or submission, but another possibility is
for a display to threaten a degree of aggressive escalation that falls short of attack.
Song-type matching in song sparrows, for example, has been suggested to be part
of a hierarchy of progressively more aggressive signals, which starts with singing a
shared song, precedes to type matching, then to staying on the match, soft song,
and finally attack (Beecher and Campbell, 2005; Searcy and Beecher, 2009).
Because matching is low in this hierarchy of escalation, with several steps
intervening between it and attack, matching would not be expected to be very
informative about attack likelihood; nevertheless, it might still be predictive of
the next level of escalation. Whether matching is predictive in this manner
requires further testing.
Among the small number of songbird species that have been studied in
this regard, soft song has emerged as an unusually reliable predictor of attack.
Why a display whose distinguishing characteristic is low amplitude should be
consistently favored for the highest level of aggressive signaling is not well
understood. One hypothesis is that by using soft song during an encounter with
an intruder, a territory owner lowers the chance of interference from other rival
males by preventing them from eavesdropping on the interaction (McGregor and
Dabelsteen, 1996), thereby concealing from them that an intrusion is taking
place. In contradiction to this idea, Searcy and Nowicki (2006) found that, in
song sparrows, more intrusions by third party males occurred during simulated
interactions between an owner giving soft songs and an intruder giving loud
songs than during interactions in which both owner and intruder gave loud
songs. In other words, use of soft songs if anything increased interference by
other rivals. A second hypothesis is that soft song is favored as an aggressive
signal because its low amplitude makes its target unambiguous: only the male
that is being confronted can discern the signal, so only he can be the target.
Another way of stating this is that soft song is a performance signal subject to an
informational constraint (Hurd and Enquist, 2005) that forces it to be honest at
least with respect to the identity of its target.
If a display is a reliable signal of aggressive intentions, as is soft song,
then theory predicts that it should be effective in changing the behavior of at
least some opponents to the signalers advantage (Enquist, 1985). In other words,
a believable threat should intimidate some opponents, presumably the weaker
ones, causing them to concede whatever resource is being contested. Effectiveness in this sense has not yet been demonstrated for soft song, in part because
arranging tests of the effectiveness of displays in territorial defense is quite
difficult (Searcy and Nowicki, 2000). Recent work with corn crakes (Crex
crex), which are not songbirds and do not sing, shows that low amplitude calls

3. Signaling Aggression

37

predict attack, and suggests that these soft calls cause some receivers to retreat
(Rek and Osiejuk, 2011). Effectiveness in intimidating opponents has been
demonstrated in some other aggressive signaling systems (Dingle, 1969; Fugle
et al., 1984; Wagner, 1992).

III. VISUAL DISPLAYS SIGNAL AGGRESSIVE INTENT IN

CEPHALOPODS: THE SWEET SMELL OF SUCCESS
Cephalopodssquid, octopus, and cuttlefishare marine molluscs with large
complex brains and highly diverse behavior (Hanlon and Messenger, 1996).
They are highly visual animals, exemplified partly by their huge optic lobes
that represent more than half of their central nervous system. These soft-bodied
cephalopods are renowned for their rapid adaptive coloration: individuals of each
species can instantly (< 1 s) switch between any of 1050 body patterns that are
used for a wide range of communication and camouflage. The appearance of the
animal can change so dramatically that they sometimes appear to be different
species. This capability has been termed rapid adaptive polyphenism because the
same genotype can produce multiple phenotypes.
Squids and cuttlefish have complex mating systems and their sexual
selection mechanisms have been studied in some detail. During spawning, the
operational sex ratio ranges from 24 M:F in some species to 411 M:F in others
(e.g., Hall and Hanlon, 2002; Hanlon et al., 1999, 2002; Jantzen and Havenhand,
2003). Thus, competition among males for mates is often intense and the
visual signaling involved with male rivalry is diverse and dramatic in some
cases. These agonistic visual displays are highly developed, and a few experimental studies have complemented field studies to determine the nature of aggression.
One of the most interesting aspects of agonistic behavior in cephalopods is its facultative nature. That is, small unpaired males seek extra-pair
copulations using various sneaking tactics, but these are usually nonaggressive
tactics that actively avoid confrontations with the paired males (for an unusual
case involving sexual mimicry, see Hanlon et al., 2005). However, if the large
consort male leaves or is displaced (experimentallyin the field or lab), the
small males immediately recognize the new behavioral context and become
paired consorts to the female and will use agonistic displays to ward off other
small males. This transition between sneaker/nonaggressive and consort/highly
aggressive is quite remarkable for its speed and fluidity, and testifies to the
cognitive abilities of these marine invertebrates. Many fishes and invertebrates
have obligatory (i.e., genetic) sneaker morphs (Gross, 1996), but cephalopods
accomplish this facultative switch with a large brain and extensive nervous
system.

38

van Staaden et al.

Early game theory models of agonistic behavior predicted that animals

should not signal their probability of attack to their opponents. As Maynard
Smith (1982) argued, if animals signaled their aggressive motivation during a
fight, there would be strong selective pressure for animals to bluff and to signal
the highest motivational state possible; such a system would likely be invaded by
cheaters and become unreliable. However, some animals do signal intent
(Hauser and Nelson, 1991), and below we provide an unusual example of this
in cuttlefish.
As in birds, cephalopods signal aggressive intent but they do so with
visual signals (chromatic skin patterns) as well as body postures (parallel positioning and arm postures). Two examples are given: one from cuttlefish (Order
Sepioidea) and one from squid (Order Teuthoidea). In addition, a new finding is
described in which a molecular trigger of aggression has been found in squid.

A. Cuttlefish agonistic bouts

In the Intense Zebra Display of the European cuttlefish, Sepia officinalis, the males
turn on high-contrast stripes and dark eye ring and extend their large 4th arm
toward the opponent (Fig. 3.3C). Such agonistic encounters between males can
lead to aggressive grappling and biting. The experiments of Adamo and Hanlon
(1996) showed that one visual component of the displaythe facial darkness
was by far the most highly variable in expression, and was a good predictor of
outcome in encounters in which one male withdrew. In non-escalated encounters, the male that ultimately withdrew always maintained a less dark face than
its opponent (Fig. 3.3A). When the face of a displaying cuttlefish became lighter,
the other male either remained in the Intense Zebra Display but did not
approach closely or lightened the intensity of its own display within 15 s.
When both males maintained a dark face, the agonistic encounters usually
escalated to physical pushing, and sometimes to grappling and biting (Fig. 3.3B).
Why would males show an agonistic display to a rival male but simultaneously signal their intent not to be aggressive? Adamo and Hanlon (1996)
pointed out that sexual recognition in cephalopods is poorly developed, and that
the Intense Zebra Display (with 4th arm extended) identifies the signaler as a
male. The authors suggest that male cuttlefish that are not prepared to attack an
opponent still give the modified (i.e., light-faced) Intense Zebra Display to
convey two messages: (1) that it is male, but (2) it is not prepared to escalate
to aggressive physical contact. As the authors point out, when agonistic displays
perform more than one function, signaling intent (i.e., signaling its likely
subsequent behavior) can be an ESS. Unless the fight escalated to grappling
and biting, there would be little cost to cheaters in this system since males that

39

3. Signaling Aggression

Darkness of face (pixel darkness)

Non-escalated encounter

210
200
190
180
170
160

10

12

14

16

Escalated encounter

D
100

Percentage of losing males

Darkness of face (pixel darkness)

220

220
210
200
190
180
170
160

80
60
40
20
0

10 12
Time (s)

Winners

14

Losers

16

Intense
Zebra

Extended
4th arm

First encounter
Second encounter (no copulation)
Second encounter (after copulation)

Figure 3.3. Cuttlefish signal intent to escalate a fight with a dark face component to their Intense
Zebra Display. (A, B) Differences in facial darkness during a non-escalated versus
escalated encounter. (C) Two males in Intense Zebra Display with different degrees of
facial darkness. (D) When males that lost a fight copulated with a female, they became
more aggressive in the successive fight. From Adamo and Hanlon (1996).

bluffed (i.e., gave a dark-faced Intense Zebra Display but had little fighting
motivation and/or ability) could withdraw at the next stage of agonistic behavior
with little penalty.
In the same study, the authors allowed losing males to copulate with a
female after a bout, and retested them with the male each had lost to. The former
losers increased facial darkness dramatically in those encounters, showed a longlasting Intense Zebra Display, and did not withdraw from an opponent
(Fig. 3.3D), thus supporting the contention that facial darkness signals the
animals motivational state (i.e., tendency to attack).

40

van Staaden et al.

B. Squid agonistic bouts

Malemale fights in Loligo plei are complex visual displays that include up to 21
behaviors. There is a hierarchy of agonistic signals that sometimes culminates in
an aggressive physical lateral display and fin beating (Fig. 3.4A and B), which are
then followed by chase or flee. DiMarco and Hanlon (1997) tested whether
dominance was based upon the duration or frequency of these behaviors, but it
was not. Instead, they found that certain visual features such as the lateral flame
markings (Fig. 3.4B, top squid) could be expressed with high contrast and that
this was a visual factor in escalation of the agonistic bout.
Two distinct tactics were exhibited by fighting males in this set of
laboratory experiments: (1) long bouts with slow escalation from visual signaling
to chasing and fleeing, or (2) short bouts with very rapid escalation from visual
signaling to lateral displaying, aggressive physical fin beating, followed by chasing and fleeing (Fig. 3.4C). It is noteworthy that the second tactic occurred when
a female was present (i.e., when a potential resource value was present). As shown
in Fig. 3.4D, the presence of a female in various combinations had a dramatic
effect on the nature and duration of the agonistic interactions. Longest bouts
(mean 14 min) occurred when only two males were present. Bouts became
progressively shorter when either two males and one female were assembled
simultaneously, or two males were interacting and a female was then added
(mean 9 and 3 min, respectively). But when a male and female were put in a
tank and allowed to pair, and then a nonpaired male was added, tactic 2 was used
and the highly aggressive interaction lasted only 30 s (a 28 difference over the
simple two male scenario). As a control, when females were added to male/
female pairs, there were no agonistic interactions (Fig. 3.4D).
In this squid species, the lateral display represents an escalation of
aggression because it involves parallel posturing and the simultaneous expression
of many high-contrast visual signals, which collectively give the impression of
making the squid look larger (e.g., the mid-ventral ridge of the mantle protrudes
vertically as in the dewlap extension of geckos). Fin beating is a physical, robust
contest of pushing that can transmit information about strength and size of the
competing individuals.

C. From molecules to aggression: Contact pheromone triggers strong

aggression in squid
In the squid Loligo pealei, which conducts visual agonistic bouts similar to L. plei
(above), it was found recently that females deposit a contact pheromone in the
outer tunic of egg capsules that they lay on the sea floor. When males see the egg
capsules (even in the absence of females), they are visually attracted to them and
then physically contact the eggs, which leads to extremely aggressive fighting

A
Escalation

Miscellaneous visual signaling

Visual signaling and

lateral display

First
parallel positioning

Lateral display and

fin beating

First
fin beating

Chase and flee

Last
fin beating

Contest duration

C
Misc. visual signaling
Chase and flee

20

10
8
6
4
2

Misc. visual signaling

Lateral display
Fin beating
Chase and flee

Average contest duration (min)

Mean contest duration (min)

12

18
16
14
12
10
8
6
4
2
0

Alternative fighting tactics

??

??/ ??+/ ?/+? ?/+/

?/

Combination
Figure 3.4. Male squid (Loligo plei) use complex lateral displays to conduct shorter fights with higher aggression when a resource value (i.e., a female mate) is
present. (A) Schema depicting the escalation pathway to a typical fully escalated agonistic contest. (B) Photograph of a fully deployed lateral
display and fin beating. The display comprises six visual components: arm spots, dorsal arm iridophores, stitchwork fins, mid-ventral ridge,
tentacular stripe, and lateral flame. (C) Short fights are more complex and involve lateral displays and physical fin beating. (D) The shortest, most
dramatic fights occur when a mating pair is already formed, and a rival male is introduced to the tank ( ).

van Staaden et al.

42

2. Physical
contact

3. Extreme
aggression

1. Visual
attraction

Aggressin
Human b-microseminoprotein

N
s

ss s

ss

ss s

ss

Figure 3.5. When male squids see egg capsules on the sea floor, then approach and touch them, this
leads to immediate and dramatic change from calm swimming to extreme fighting. The
contact pheromone (aggressin or Loligo b-MSP) is in the tunic of the egg capsules and
is similar in structure to that found in humans, mice, and other vertebrates.

within a minute or two (Fig. 3.5) (Cummins et al., 2011). Thus, there is a twostep sensory process: visual attraction to eggs followed by contact chemoreception that induces onset of aggression.
In controlled experiments, the 10 kDa protein pheromone (termed
Loligo b-microseminoprotein, b-MSP) was isolated and coated onto a clear
glass flask containing egg capsules, and males that touched the glass (but not
the eggs) began to signal, fight, and bite each other violently within seconds.
Glass flasks without the pheromone coating failed to elicit those aggressive
behaviors. Thus, direct contact with the protein molecules immediately led to
the full cascade of complex aggressive fighting in the absence of females. Given
that aggression is often considered to be a result of multiple interactions of
physiology, hormones, sensory stimuli, etc., this finding reminds us that perhaps
in some cases there are straightforward pathways to aggression. In fact, the
proximate mechanisms that trigger or strengthen aggression are not well
known for many taxa (Wingfield et al., 2005).
There is a noteworthy vertebrate/mammalian connection to this
finding. As shown in Fig. 3.6, the b-MSPs are highly conserved throughout the
animal kingdom. The greatest known concentration of b-MSPs is in human and
rodent seminal fluid, yet regrettably the functions of b-MSPs are unknown in any
taxa except cephalopods, as explained above (Cummins et al., 2011). As those
authors suggest, it would be worthwhile to look for an aggression function for

43

3. Signaling Aggression
Human (Homo sapien)
Other primate (consensus)
Pig (Sus scrofa)
Rat (Rattus norvegicus)
Mouse (Mus musculus)
Red jungle fowl (Gallus gallus)
Zebra finch (Taeniopygia guttata)

Ostrich (Struthio camelus)

Northern pike (Esox lucius)
Atlantic salmon (Salmo salar)
Zebrafish (Danio rerio)
Lancet (Branchiostoma belcheri)
California mussel (Mytilus californianus)

Pacific oyster (Crassostrea gigas)

Bay scallop (Argopecten irradians)
Limpet (Lottia gigantea)
Longfin squid (Loligo pealeii)
Abalone (Haliotis diversicolor)
Bobtail squid (Euprymna scolopes)

Rotifer (Adineta vaga)

Human (Homo sapien) CRISP
Mouse (Mus musculus) CRISP
Snake (Rhinoplocephalus nigrescens) CRISP
Frog (Xenopus laevis) CRISP

0.1

Phylum Chordata

Phylum Mollusca

Phylum Rotifera

Figure 3.6. Evolutionary origins and conservation of b-microseminoproteins. The tree shows
phylogenetic relationships among the protein sequences. The b-MSPs identified in
the Cummins et al. (2011) study are within the dotted lines.

b-MSPs in mammals and other vertebrates, given the molecular similarity and
unique structure of these proteins, all of which seem to be most concentrated in
exocrine glands in many taxa. Such findings remind us that multisensory cues are
often involved in stimulating behaviors and that a good deal more research is
needed before we understand subjects such as aggression.

D. Signaling aggression in humans

In humans, as in other species, signaler and receiver have both evolved to use
variation in aggressive signal structure to their own advantage. In the case of
human speech, fundamental vocal frequency is perceived to be associated with
social cues for dominance and submissiveness (Bolinger, 1978; Huron et al., 2009;
Ohala, 1994), with vocal pitch height used to signal aggression (low pitch), or

44

van Staaden et al.

appeasement (high pitch). Moreover, a strong correlation with eyebrow position

suggests an intermodal linkage between vocal and facial expressions (Huron et al.,
2009). Evidence implicates male dominance competition (Puts et al., 2006), rather
than intersexual selection (see Chapter 2), as the selective origin of this performance signal. Similarly, handgrip strength is correlated with level of aggression
and appears to be an honest signal for quality in males (Gallup et al., 2007).
Mathematical models show, however, that the tradeoff of deceptive efficacy and
dishonest signals of intent often favors signalers who produce imperfectly deceptive signals over perfectly honest or perfectly deceptive ones (Andrews, 2002).
Competition among coalition groups (a characteristic shared with chimpanzees)
initiated a social arms race, culminating in extraordinary human cognitive abilities
(Flinn et al., 2005), capable of parsing aggressive signals (Paul and Thelen, 1983),
and competitive displays (Hawkes and Bird, 2002). This great capacity for signaling is outstripped only by the uniquely human ability to extend our phenotype
with weaponrywith the unfortunate consequence that our potential to inflict
damage frequently exceeds our ability to control aggression.
Rather than maximizing its absolute amount, natural selection enhances
the overall effectiveness of aggression. In invertebrates, where individuals generally
pursue a solitary existence, physical superiority primarily determines the eventual
outcome of contests, and most fights are quickly resolved on the basis of prominent
asymmetries in body or weapon size. In vertebrates, which must navigate the
demands and opportunities of social living, aggressive success is largely contingent
on the development of social competence. In this case, natural selection favors
those with an ability to effectively anticipate their chances well in advance of a
contest, and to signal strength while hiding any intentions to eventually withdraw.
Generating and interpreting aggressive signals to form successful alliances and to
inherit status from high-ranking kin, is thus key to winning both short-term
contests and long-term evolutionary success.

Acknowledgments
Production of this chapter was partially supported by funding from NSF grant DUE-0757001 (to M. v. S.).
W. A. S. thanks his collaborators on the sparrow signaling research including Steve Nowicki, Rindy
Anderson, Barb Ballentine, Mike Beecher, and Susan Peters. R. T. H. is grateful for partial funding from
NSF grant IBN-0415519 and many wonderful colleagues who participated in these experiments and field
observations.

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Self-Structuring Properties of
Dominance Hierarchies: A New
Perspective
Ivan D. Chase* and Kristine Seitz
*Department of Sociology, Stony Brook University, Stony Brook,
New York, USA

Department of Biology, Stony Brook University, Stony Brook,

New York, USA

I. Introduction
II. Definitions
A. Dominance relationships
B. Dominance hierarchies
III. Animal Models
A. Chickens
B. Fish
C. Crustaceans
D. Primates
IV. Factors Affecting Dominance Relationships in Pairs of Animals
A. Physical differences
B. Physiology
C. Genetics
D. Behavioral states: Winner, loser and bystander effects
V. Formation of Dominance Relationships
and Dominance Hierarchies in Groups
A. Differences in individual attributes and hierarchy formation
B. Influence of social factors on linear hierarchy formation
VI. A New Approach to Explaining the Formation
of Linear Hierarchies: Behavioral Processes
A. Modifications of the jigsaw puzzle model
B. Experimental evidence concerning animal cognitive
abilities and processes of interaction
Advances in Genetics, Vol. 75
Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00001-0

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Chase and Seitz

VII. Conclusion
Acknowledgments
References

ABSTRACT
Using aggressive behavior, animals of many species establish dominance hierarchies in both nature and the laboratory. Rank in these hierarchies influences
many aspects of animals lives including their health, physiology, weight gain,
genetic expression, and ability to reproduce and raise viable offspring. In this
chapter, we define dominance relationships and dominance hierarchies, discuss
several model species used in dominance studies, and consider factors that
predict the outcomes of dominance encounters in dyads and small groups
of animals. Researchers have shown that individual differences in attributes, as
well as in states (recent behavioral experiences), influence the outcomes of
dominance encounters in dyads. Attributes include physical, physiological, and
genetic characteristics while states include recent experiences such as winning or
losing earlier contests. However, surprisingly, we marshal experimental and
theoretical evidence to demonstrate that these differences have significantly
less or no ability to predict the outcomes of dominance encounters for animals
in groups as small as three or four individuals. Given these results, we pose an
alternative research question: How do animals of so many species form hierarchies with characteristic linear structures despite the relatively low predictability
based upon individual differences? In answer to this question, we review the
evidence for an alternative approach suggesting that dominance hierarchies
are self-structuring. That is, we suggest that linear forms of organization in
hierarchies emerge from several kinds of behavioral processes, or sequences of
interaction, that are common across many different species of animals from ants
to chickens and fish and even some primates. This new approach inspires a
variety of further questions for research. 2011, Elsevier Inc.

I. INTRODUCTION
Both humans and animals use aggression in many contexts as discussed in this
volume. In this chapter, we talk about aggression as it is used in the social
context of establishing dominance relationships and dominance hierarchies.
A broad range of speciesfrom insects to humansform these types of relationships and hierarchies, and where they occur, hierarchy rank has wide-ranging
and serious consequences for individuals (Addison and Simmel, 1970; Barkan

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53

et al., 1986; Goessmann et al., 2000; Hausfater et al., 1982; Heinze, 1990;
Nelissen, 1985; Post, 1992; Savin-Williams, 1980; Vannini and Sardini, 1971;
Wilson, 1975). These consequences include variation in physiology, stress,
health, growth rate, access to sexual partners, ability to raise viable offspring,
and even in the thickness of nerves leading from the hypothalamus to the
pituitary gland (Clutton-Brock et al., 1984; Ellis, 1995; Francis et al., 1993;
Holekamp and Smale, 1993; Post, 1992; Sapolsky and Share, 1994).
Our discussion centers on dominance in less complex animals such as
chickens, fish, and nonprimate mammals. We begin with behavioral definitions
of dominance relationships and hierarchies. We then move on to the factors that
predict dominance in pairs of animals including differences in both traits and
behavioral states. Traits include genetic, physical, physiological, and personality
attributes; behavioral states include the influences of winning and losing contests, as well as observing the contests of other individuals. Next, we review the
research that demonstrates, very surprisingly, that factors affecting dyadic
encounters are poor predictors of outcome in dominance encounters within
groups of any size, even as small as three or four individuals. Consequently,
researchers should not expect that findings from dominance in pairs of animals
will easily generalize to small groups of animals.
Finally, we suggest that rather than trying to predict the ranks of
individuals in groups, a more appropriate research question is to ask how these
hierarchies often come to have a linear structure (defined below) across many
species. We discuss recent experimental findings that conclude that these linear
hierarchies are self-structuring or self-organizing. Self-structuring hierarchies are
common across a range of species. They emerge from the repeated use of several
characteristic, small-scale behavioral processes, or sequences of behavior. We
describe how these processes generate linear hierarchies and discuss some unresolved experimental questions suggested by these behavioral processes.

II. DEFINITIONS
A. Dominance relationships
While researchers have proposed a variety of definitions, in this chapter, we will
be using a strictly behavioral measure of dominance relationships. More specifically, we will define a dominance relationship as characterized by an asymmetry
of aggressive behaviors by one animal toward another. Typically, both noncontact and contact behaviors are involved. Common noncontact type behaviors
are chasing, displacement, or the threat of aggressive contact. Threat behaviors
vary by species and include gill flaring in fish; certain vocalizations and gestures
in primates; and short, rapid movements toward the threatened individual in a

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variety of species. Aggressive contact behaviors also vary by species and include
pecking in the case of chickens and other birds; biting in fish, rodents, and
primates; and grasping with claws in crayfish, lobsters, hermit crabs, and other
crustaceans.
There is no established standard that defines the number of acts in a row
that are recorded to determine dominance in different species. However, the
general rule is to use a sufficient number such that, when it is reached, a stable
relationship has been revealed with very little likelihood of the animal declared
subordinate beginning to attack the one declared dominant. For example,
in determining the presence of dominance relationships, Chase et al. (2002)
declared that one cichlid fish was dominant over another if it bit or chased
the other fish six times in a row without the other fish initiating an aggressive
action in return.
Other methods for determining dominance, such as recording which of
two animals obtains a desired piece of food, do not necessarily reflect the kind of
relatively stable social relationships that are indicated by asymmetries in aggressive behavior in pairs of animals. For example, when two monkeys are competing
for a peanut, the winner may be an otherwise subordinate animal that is quicker
and ready to withstand the chasing and harassing it will receive from the
normally dominant animal with which it lives in order to secure the peanut.
Researchers also sometimes determine dominance by observing which individual
delivers the majority, rather than an uninterrupted sequence, of aggressive acts
over a period of observation. A measure of dominance such as this may be
appropriate in some species, such as pigeons and young children, who do not
always form completely asymmetric relationships. Such measures, however, can
be misleading if used when animals meet for the first time. When animals meet
initially, there is often a trading back and forth of aggressive actions before one
individual begins to deliver all the actions and clearly becomes dominant over
the other. Figure 4.1 is a music notation graph showing the interactions of two

0:10

0:20
A

Figure 4.1. Graphic display of the record of interaction between two hens using music notation.
Horizontal lines represent individuals, ordered by eventual dominance rank. Each
aggressive act between individuals is indicated by a vertical arrow from the line
representing the initiator to the line representing the receiver. The time in minutes
since the assembly of the pair appears above the graph. Letters at the ends of the
horizontal lines identify the hens. See Chase (2006) for more information about the
uses of music notation in visualizing interactions in groups of animals and humans.

4. Self-Structuring Properties of Dominance Hierarchies

55

chickens setting up a relationship (Chase 2006). If only the first 10 min of

interactions are considered, then chicken B is dominant over A since B delivers
83% of the aggressive interactions and chicken A only 17%. However, as time
goes on, the back and forth actions stop, and chicken A is soon delivering
all aggressive acts. If a researcher had only considered which individual initiated
the majority of acts during the initial phases of the interaction, an incorrect
indication of dominance would have resulted.

B. Dominance hierarchies
A dominance hierarchy is the overall collection, or network, of dominance
relationships among the pairs of individuals in a group. In many small groups
of animals and human children of around eight or ten members or less, dominance hierarchies often take a classical linear form (Addison and Simmel, 1970;
Barkan et al., 1986; Goessmann et al., 2000; Hausfater et al., 1982; Heinze, 1990;
Nelissen, 1985; Post, 1992; Savin-Williams, 1980; Vannini and Sardini, 1971;
Wilson, 1975). In a linear hierarchy, there is one individual who dominates all
the other group members, a second who dominates all but the top individual, and
so on, down to the last individual who dominates no one. In larger groups, there
is often the skeleton of a linear structure, but even with extensive observations,
researchers do not see interactions between some pairs, especially those that
seem distant in rank. In hierarchies that are not linear, there are inconsistencies
in rank showing intransitive relationships (A dominates B, B dominates C, but
C dominates A). The hierarchies in some animals, especially those with more
complex social organization such as dolphins, chimpanzees, hyenas, baboons,
and macaques, are often too complex to be simply classified as linear (Holekamp
and Smale, 1993; Kummer, 1984; Moller et al., 2001, 2006; Surbeck et al., 2011;
Widdig et al., 2001, among many others). Our discussion here will concentrate
on those animals forming more linear hierarchies.

III. ANIMAL MODELS

Animal behaviorists have shown that a huge range of animals establish dominance
relationships and dominance hierarchies in the wild and in the laboratory. These
include insects such as fruit flies and some ants, wasps and cockroaches; crustaceans such as hermit crabs, crayfish, and lobsters; reptiles such as anoles; many
species of fish, birds, and mammals; and even human preschoolers and adolescents
(Addison and Simmel, 1970; Barkan et al., 1986; Clark, 1998; Goessmann et al.,
2000; Hausfater et al., 1982; Heinze, 1990; Nelissen, 1985; Post, 1992; Queller
et al., 2000; Savin-Williams, 1980; Vannini and Sardini, 1971; Wilson 1975).

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In biomedical research, an animal model is usually an animal species

used for research on a human disease or other condition. Dominance researchers
do not often use specific species in the strict sense of models for human conditions, but instead as models for dominance in animals more broadly. The partial
exception to this is that some researchers have studied dominance in primates to
discover information about how dominance processes may work in human groups
(see below). Below is a brief description of animals or animal groups used
frequently in dominance research and a representative, but by no means
comprehensive, sampling of work done with these animals.

A. Chickens
Chickens were among the first animals to be studied for their dominance
relationships. Schjelderup-Ebbe (1922) introduced dominance hierarchies into
the modern study of animal behavior and coined the term peck order (or
Hackordnung in the original German in which he wrote). Schjelderup-Ebbe
(1922) was among the first researchers to observe the highly linear structure of
pecking orders. He noted that a number of factors influenced rank in the flock,
including stress, prior experience, overall health, mating condition, and age. He
further concluded that dominance is based, not just on the size and strength of
the combatants but also on the perception of fellow flock members (SchjelderupEbbe, 1922).
Other early researchers used chickens to explore the relationship
between stress and dominance. Sactuary (1932), for example, showed that
hens that mysteriously molted out of season and went out of laying condition
had been relegated to the lower ranks of the flock. Thus Sactuary (1932) linked
rank to both fitness (ability to produce offspring) and stress levels.
Some more recent investigations in chickens have focused on the
relationship between dominance, aggression, and selective breeding. These
lines of inquiry began with the rise of the factory farms, in which aggression
leading to deaths and lowered egg production is of great concern (Craig and
Muir, 1996; Craig et al., 1965, 1969, 1975, among others).

B. Fish
Fish have recently become one of the most popular vertebrate models for
dominance research. The fish model system is comparable to chickens, in that
fish possess easily observed dominance behaviors (chases, bites, and threat
behaviors), recognize members of their group as individuals, and can maintain
their dominance hierarchies for extended periods of time. Fish, however, are
easier to maintain in the laboratory than chickens. They have been used for a
variety of studies relating to dominance which we can only briefly cover here.

4. Self-Structuring Properties of Dominance Hierarchies

57

One common type of study of fish explores how differences in behavioral states and individual attributes affect the outcome of dominance contests. For
example, researchers have used fish to investigate the so-called winner, loser, and
bystander effects (defined below) (Chase et al., 1994, 2002; Hsu and Wolf, 1999;
Hsu et al., 2006; Oliveira et al., 2009, among others); prior residency, a kind of
home field advantage assumed to confer benefits in social contexts (Beaugrand
and Beaugrand, 1991); and the effects of differences in size and prior social
experience (Beaugrand and Cotnoir, 1996).
Besides studying factors affecting the outcome of contests, researchers
have utilized fish in selection experiments studying the heritability of dominancerelated aggression (Bakker, 1985, 1986; Francis, 1984, 1987) and in investigations
into physiological and genetic components of dominance (see Sloman and
Armstrong 2002 for a review of physiological aspects).

C. Crustaceans
Crustaceans are a unique model system that allows researchers to study chemical
signaling behaviors, and the anatomy of their nervous systems enables researchers to
study the neural underpinnings of dominance relationship formation (Moore and
Bergman, 2005). One of the most commonly studied chemical signals in this group
of species is the release of urine during agonistic behaviors. In lobsters, this signal has
been implicated in the maintenance of dominance hierarchies (Breithaupt and
Atema, 2000; Karavanich and Atema, 1998), and in crayfish, it has been shown to
reduce aggression in opponents during dominance bouts (Breithaupt and Eger,
2002). Yeh et al. (1997) showed that changes in dominance status altered levels of
serotonin in the crayfish, Procambarus clarkii. These changes caused modifications in
the command neuron involved in escape behaviors in this species and were found to
be reversible and linked to changes in the population of serotonin receptors.

D. Primates
The dominance systems of primates are often more complex than the other
model systems just discussed. As a result, their dominance behavior can more
easily be generalized to humans. One of the most important lines of research in
primates has shown how stress affects the hormonal responses of animals of
different ranks. Sapolsky (1982) studied wild olive baboons (Papio anubis) and
found that high-ranking males showed a low initial level of cortisol, but in
response to stress, they had faster and larger spikes of cortisol than their less
successful counterparts. Sapolsky (1982) suggested that the high ranking members cortisol responses might be more adaptive to their social environments,
because their usual, lower cortisol levels conferred immunological and other
health benefits. A general review of the influence of hierarchies on primate
health can be found in Sapolsky (2005).

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IV. FACTORS AFFECTING DOMINANCE RELATIONSHIPS

IN PAIRS OF ANIMALS
In attempting to predict the outcomes of dominance contests in pairs of animals,
researchers have used two broad classes of variables: differences in attributes or
traits and differences in behavioral conditions or states. Attributes are relatively
long-lasting characteristics, while states are shorter-term conditions often influenced by behavioral events.

A. Physical differences
Differences in physical attributes often have a considerable impact on the
outcome of dominance encounters. One common characteristic used is differences in the sizes of the organisms, which can be broken down into two
categories: differences in weights and differences in lengths or heights. Researchers have found that larger, heavier animals usually dominate animals that are
smaller and lighter (Frey and Miller, 1972; Houpt et al., 1978; Nakano and
Furukawa-Tanaka, 1994; Knights, 1987; Lott and Galland, 1987). However,
when size differences are smaller, other factors can influence the outcomes of
contests. For example, in male green swordtail fish, a difference of 2030% in the
size of the lateral surface area of fish meeting in dyadic dominance contests
generally resulted in the larger fish becoming dominant over the smaller
(Beaugrand et al., 1996). Contests between fish with size differences of
1020%, however, showed that other factors such as prior social experiences
(winning or losing) and prior residency influence the outcome of contests.
Size differences below 10% do not influence dominance contests at all. Instead,
the social experience (discussed below) of the fish is usually the deciding factor in
dominance contests (Beaugrand et al., 1996). Similar to standard length, the
effects of weight on dominance success can be ameliorated by other factors such
as having won or lost a prior contest (Beacham, 1988; Schulte-Hostedde and
Millar, 2002).
Although size and weight are, perhaps, the physical attributes most
widely studied for their effect on dominance contests, other physical features
and conditions have also been implicated in dominance success. One example
that has been studied extensively is the dominance badge, an area of color on the
body of an animal that acts to indicate dominance to conspecifics (see Senar,
1999 for a review). Other examples include the state of molt and the size of
combs in chickens (Collias, 1943), the size of genital papilla in fish (Schwanck,
1980), and the bill size in birds (Shaw, 1986).

4. Self-Structuring Properties of Dominance Hierarchies

59

1. Behavioral profile or personality

Repeatable behavioral type or personality can be defined as suites of behaviors
that differ among individuals but are consistently repeatable in multiple contexts
over time (Bell et al., 2009; Boon et al., 2007; Groothius and Carere, 2005;
Martin and Reale, 2008; Sih et al., 2004; Sinn and Moltschaniwskyj, 2005;
Svartberg et al., 2005). Researchers have demonstrated that behavioral profiles
can predict the outcome of dyadic dominance encounters in a variety of species
with high accuracy. For example, in fish, brown trout that scored higher in
boldness were more likely to dominate those that scored lower (Sundstrom
et al., 2004), and rainbow trout that had shorter or more proactive responses to
stress were more likely to dominate those with longer or reactive responses
(verli et al., 2004; Schjolden et al., 2005). In birds, mountain chickadees
classified as high-exploring individuals (those that visited more sites within a
strange area) dominated low-exploring individuals, and in great tits, fast
explorers dominated slow explorers (Fox et al., 2009; Verbeek et al., 1996).
Interestingly, Verbeek et al. (1999) found that the same behavioral profiles in
great tits that predicted dominance in dyads gave opposite results in groups of five
to eight great tits. Here, the slow explorers had higher average dominance scores.

B. Physiology
Whether or not physiological differences can predict the outcome of dyadic
dominance encounters is an extremely vexed question. In the mid-twentieth
century, researchers thought that differences in testosterone, among other
hormones, were reliable determinants of dominance (For recent work see
Huber et al., 1997). However, subsequent research demonstrated that the causal
direction is often reversedin many species, the ranks of individuals in hierarchies has a strong influence on the levels of their hormones and other physiologically active chemicals rather than vice versa (see, e.g., Eaton and Resko,
1974; Sapolsky, 1982; Trainor and Hofmann, 2007). Further, Sloman and
Armstrong (2002), in a general review, suggest that at least for fish, the physiological effects of dominance encounters in simple laboratory settings may be
stronger than those observed in more complex laboratory or natural habitats.
These caveats notwithstanding, there is a considerable recent literature
on physiological predictors of dominance in the dyadic encounters of fish, chiefly
in trout and salmon. For example, Metcalfe et al. (1995), Cutts et al. (1999), and
McCarthy (2001) find that fish with higher relative metabolic rates dominate
those with lower relative rates. In tests of responses to stress, verli et al. (2004)
and Schjolden et al. (2005) report that trout with lower levels of cortisol defeat
those with higher levels. In experiments in which Arctic charr are dosed with

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Chase and Seitz

L-dopa, the immediate precursor of the neurotransmitter dopamine, and trout are
dosed with growth hormone, treated fish dominated control fish at significant
rates (Johnsson and Bjornsson, 1994; Winberg and Nilsson, 1992).
We obviously need further research to untangle the complicated chains
of cause and effect among various physiological variables and outcomes in
dominance relationships.

C. Genetics
The inheritance of dominance and aggressiveness has been a topic of interest
since the fields inception. In artificial selection experiments, Craig et al. (1965)
were able to produce hens with diverging dominance abilities. In dyadic contests,
hens of high dominance ability usually defeated those of low dominance ability.
Even based on these early findings, however, Craig et al. (1965) concluded that
variations caused by interactions between genes (nonadditive genetic variation)
and environmental factors were likely to be important in the inheritance of
dominance. Similar studies of paradise fish (Francis, 1984, 1987), cockroaches
(Moore, 1990), and deer mice (Dewsbury, 1990) confirmed that dominance
could be artificially selected in a variety of species. Artificial selection, however,
can only imply a genetic basis for dominance and cannot identify which genes
are responsible for dominance or subordination. An alternative explanation for
at least some of these results is that the social environment of mothers (including
their levels of aggression and dominance ranks) can expose prenatal young to
androgens that can influence their offsprings behavior. Such maternal influences
operate independently of genotype and have been implicated in the inheritance
of rank-related behavior. For example, the level of female aggression affects the
amount of maternally derived testosterone in tree swallow eggs, which, in turn,
influences the growth and dominance of the hatchlings (Whittingham and
Schwabl, 2002). In mammals, higher ranking female hyenas (Crocuta crocuta)
have higher levels of in utero androgens causing their cubs to more aggressive
than those of lower ranking females (Dloniak et al., 2006).
To begin to tease apart these and other influences on rank order, the
newest technological advances in molecular biology are being employed to
investigate which genes influence social behavior. Sociogenomics, the study of
social systems at a molecular level, can offer us insights and information never
before available to behavioral scientists. A variety of unique insights have arisen
from this new way of studying social dominance and are revealing two major
themes: one theme is that genes involved in nonsocial behaviors are often also
implicated in social behaviors; the second is that genes are highly sensitive to
social influences, and regulation of gene expression by social factors heavily
influences behavior (Robinson et al., 2005).

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61

An outstanding example of the interplay between genetic expression

and social factors occurs in the cichlid fish Astatolapia burtoni. In this fish,
dominant males are brightly colored and actively defend territories for mating.
Subordinate males are nonreproductive, move about in schools and mimic
females cryptic coloration. Subordinate males, however, grow faster than dominant males, giving subordinates the opportunity to depose dominant males from
their territories. These phenotypes are plastic and males may switch back and
forth between phenotypes several times in a life span, depending on the availability of suitable territories to defend (Burmeister et al., 2005; Renn et al., 2008).
Burmeister et al. (2005) investigated the neural mechanisms linking
social environment to physiological changes associated with dominance. They
found that when a subordinate male perceives an opportunity to move to a
territory and become dominant, he begins to produce dominant coloration and
some initial behavioral changes in as little as a day (Burmeister et al., 2005).
It takes about 7 days, however, for males ascending to dominance to produce the
same amount of gonadotropin-releasing hormone (GnRH1) as a dominant male,
during which time the size of testes and GnRH1 neurons increase to sizes
comparable to dominants (Burmeister et al., 2005). In A. burtoni, GnRH1 is
produced by neurons in the anterior parvocellular preoptic nucleus (aPPn), the
most anterior part of the preoptic area in teleosts. To study the behavioral and the
genomic response to social opportunity, researchers chose to focus on the gene
egr-1, which codes for a transcription factor involved in neuronal plasticity and
links membrane depolarization to late-response target genes. Expression of this
gene was compared in socially ascending males and dominant and subordinate
males in stable hierarchies (Burmeister et al., 2005). Their results show that
socially ascending males had a twofold induction of egr-1 in the aPPn, compared
to the both dominant and subordinate males in stable positions. Expression levels
in other parts of the brain did not differ with social status or opportunity
(Burmeister et al., 2005). Stable dominant males do not show this spike in
egr-1, suggesting that this change is a response to social opportunity rather
than a response to dominance itself. Although socially ascending males also
show a difference in physical activity (e.g., more threat displays), it is not clear
whether there is a simple relationship between egr-1 expression and increased
motor activity. Instead, Burmeister et al. (2005) conclude that the relationship of
social context, expression of egr-1, and activity differences have a complex
relationship that cannot be adequately explained by the simple functional
motor and sensory aspects of the experience (Burmeister et al., 2005).
Renn et al. (2008) studied how social context affects physiology, but in
this case, a microarray was used to investigate coregulated gene sets that might
differentiate dominant males, subordinate males, and brooding females. The
results show that there are, indeed, gene sets that are common to each of these
phenotypes, with males (both dominant and subordinate) and females having

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Chase and Seitz

the largest (16%) difference in gene expression (Renn et al., 2008). Twenty-one
genes were found to be upregulated in the subordinate male phenotype, and it
was hypothesized that downregulation of these genes would lead to the dominant
phenotype. Additionally, subordinate males and brooding females were found to
have a similar expression pattern for 16 genes, possibly suggesting a type of
subordination module (Renn et al., 2008). Interestingly, although gene sets for
phenotypic traits were found, results also showed that there was as much variation in gene expression between individuals of the same phenotype as there was
between the phenotypes themselves. This suggests that widely variant gene
expression in individuals can still yield reliable, easily identifiable phenotypes
(Renn et al., 2008).
Trainor and Hofmann (2007) investigated the neuropeptide hormone
somatostatin, and its receptors, for possible involvement in social behavior. This
hormone and its numerous receptor subtypes have been shown to play a role in
the inhibition of growth hormone secretion, among other more diverse effects.
The relationship between somatostatin gene expression and body size differed
between dominant and subordinate individuals. In dominant males, the gene
expression of one subgroup of receptors in the hypothalamus was negatively
associated with body size. In subordinate fish, however, gene expression was
positively correlated with body size. This suggests that growth in this animal
may be socially mediated at the genetic level (Trainor and Hofmann, 2007).

D. Behavioral states: Winner, loser and bystander effects

In addition to differences in attributes or traits, considerable research also
demonstrates that differences in states can influence the outcomes of dominance
encounters in pairs of animals. Most of this research has examined what are
known as winner, loser, and bystander effects. In a winner effect, an animal that
has won an earlier contest with one individual has an increased probability of
winning a second contest with another individual. In a loser effect, an animal
that has lost a dominance encounter with one individual has an increased
probability of losing a subsequent contest with another individual. In a bystander
effect, an animal that has observed a dominance contest between two others
alters its behavior, compared to a nonobserver, when it meets either of the
animals that it observed interacting.
Researchers have discovered loser effects in a broad range of species,
and there is some evidence that these effects may last for several days (see, e.g.,
Chase et al., 1994; Hsu et al., 2006). Winner effects seem to be less common
across species and not as strong as loser effects. Further, some species seem not to
have them at all (Chase et al., 1994; Rutte et al., 2006). In particular, Fuxjagera
and Marlera (2010) show that winner effects can be documented in some species

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63

but can be nonexistent in other, closely related species. Where winner effects
occur, there is some evidence that they are of much shorter duration than loser
effects, lasting perhaps less than an hour or so after an individuals initial winning
experience (Bergman et al., 2003; Chase et al., 1994). Oliveira et al. (2009) have
shown that winner effects can be ameliorated with antiandrogen drugs, but loser
effects are unchanged. Clearly, additional work is needed in this area to elucidate
the role these effects have on the formation of dominance relationships in pairs
of animals.
Research indicates that animals in many species are attentive observers
of other individuals and that they use the information gained in their observations in shaping their future behavior with those observed. For example, a
bystander fish may be less aggressive when it meets another fish it has observed
winning a contest. Bystander effects have been observed in a broad range of
species (see, e.g., Oliveira et al., 1998; Oliveira et al., 2001; Danchin et al., 2004;
Peake and McGregor, 2004).

V. FORMATION OF DOMINANCE RELATIONSHIPS

AND DOMINANCE HIERARCHIES IN GROUPS
Given the research that we have just reviewed, it would seem natural to assume
that the same factors that strongly predict the outcomes of dominance encounters in pairs of animals by themselves should also work for dominance encounters
between pairs of animals in groups. That is, the factors that predict dominance
in isolated pairs should also predict dominance for socially embedded pairs.
Predicting the outcome of dominance encounters for all the embedded pairs in
a group would allow us to rank individuals within the dominance hierarchy and
reveal the hierarchical structure. Surprisingly, while individual differences
in attributes and states do have some influence on rank in hierarchies, that
influence is significantly less in groups than it is in dyadic pairs. Consequently,
other factors must be at work in determining individual ranks within hierarchies
and in generating hierarchical structure. Unraveling that paradoxhow individuals can be clearly differentiated by rank, but with that differentiation not
strongly based upon individual differencesis a great challenge in the study of
dominance hierarchies.
In the next section, we present evidence demonstrating that individual
differences can neither adequately predict the places of individuals within
hierarchies nor explain their overall linear structure. Following that, we describe
a new approach that we believe can account for the common formation of linear
hierarchies across a variety of species.

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Chase and Seitz

A. Differences in individual attributes and hierarchy formation

The prior attributes hypothesis proposes that differences in the characteristics
that animals possess before forming a hierarchy predetermine their resulting
hierarchy ranks. Figure 4.2 illustrates this hypothesis in graphical form. In the
hypothesis, the individual ranking highest on attributes takes the top position
when the hierarchy forms; the individual ranking second-highest takes the
next-to-the-top position; and so on. Rank based on prior attributes could be
determined by any set of characteristics: physical ones such as weight, personality
ones such as aggressiveness or boldness, genetic ones such as overall genotype or
specific genetic markers, social ones such as the conditions of rearing or family
background, physiological ones such as various hormone levels, and so on.
Prior
attribute
score

Hierarchy
rank

Figure 4.2. Graphical illustration of the prior attributes hypothesis. Size indicates relative prior
attribute value; larger size indicates higher rank on prior attributes. Figure adapted from
Figure 24.1, p. 570 in Dominance hierarchies by Ivan D. Chase and W. Brent
Lindquist from Oxford Handbook of Analytical Sociology ed. by Hedstrom, P. and Bearman, P. (2009), by permission of Oxford University Press.

4. Self-Structuring Properties of Dominance Hierarchies

65

The problem in testing the prior attributes hypothesis is that although

an experimenter might know some of the traits that influence dominance, he or
she might not know all those involved or the size of the contribution of a specific
trait to dominance outcomes. In order to get around this problem, Chase et al.
(2002) designed an experiment to test the prior attributes hypothesis without
knowing which attributes or the sizes of their contributions that might be
involved in hierarchy formation.
In their experiment, they brought together groups of four cichlid fish
and let them form hierarchies, separated the fish for two weeks, which was
sufficient time for them to forget one another as individuals, and then reassembled them to form second hierarchies. The plan was to let the fish form a
hierarchy and then, to the extent possible, rewind their tape, removing all
memory of recent social experience before letting them form a second hierarchy.
If prior attributes, whatever they might have been, determined the ranks of the
fish in the first hierarchy, the attributes, provided they were reasonably stable,
should also have determined the ranks of the fish in the second hierarchies.
Consequently, by the prior attributes hypothesis, the positions of the fish in the
first and second hierarchies should have been the same for all, or at least most, of
the groups.
The results of this experiment are shown in Fig. 4.3 and Table 4.1.
Instead of a high proportion of groups having identical first and second hierarchies, the experimenters found that only about a quarter (26%) of the groups did
so. In nearly three-quarters of the groups, two, three, or even all four fish had
different ranks in the two hierarchies. Prior attributes did, however, have a
moderate influence on the ranks of the fish within the hierarchymore groups
formed identical first and second hierarchies than expected by chance alone, and
there was, on average, moderate rank order correlations between the ranks of
individuals in the two hierarchies. However, the lack of a high proportion of
groups with identical first and second hierarchies indicated that some other
factor played a substantial part in the formation of linear hierarchies and the
ranks of individuals within them.
One question that can be raised about the interpretation of these results
is, what if the fish changed after the first hierarchy so that their attribute ranks
were different before they formed their second hierarchy? For example, for
simplicity consider just one attribute called dominance ability. What if the
rank on dominance ability before the first hierarchy had been A, B, C, D, but
before they formed the second hierarchy their order had changed to give a new
ranking D, C, A, B? The difference in dominance ability could still have
accounted for the linear hierarchies but the fish would have different ranks in
the second hierarchy than the first. This question is discussed in some detail in
Chase et al., (2002), which argues against this counter-explanation. In addition
to that discussion, some more recent experimental work also suggests a lack of

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Chase and Seitz

1st
Hierarchy

2nd
Hierarchy

1st
Hierarchy

2nd
Hierarchy

C
D

(6)

(1)
B

(4)

(1)

A
C2

C
D

(1)

C1

C2

C3

C1

(1)
A

(1)

(2)
B

B
C

C3

D
B

D
(1)

(2)

C
(1)

C2
C3

C1

C2

C3

A
C1
(1)

Figure 4.3. Transition pattern between the ranks of the fish in their first and second hierarchies.
The total number of groups in the experiment was 22; the number of groups showing a
particular transition pattern is indicated in parentheses below each pattern. Fish that
have an intransitive dominance relationship (A dominates B, B dominates C, and
C dominates A) share the same rank. Intransitive relationships are discussed below.

4. Self-Structuring Properties of Dominance Hierarchies

67

Table 4.1. Percentage of Groups with Different Numbers of Fish

Changing Ranks Between their First and Second Hierarchies (n 22)
No. of fish changing ranks

Percentage of groups

0
2
3
4

27.3
36.4
18.2
18.2

support for this counter-explanation. When isolated pairs of fish are tested under
the same experimental conditions as the groups forming and reforming hierarchies, they have an extremely high rate (94%) of forming the same dominance
relationship each time. If A dominated B when they met the first time,
A virtually always dominated B the second time they met. However, at 76%,
the replication rate for socially embedded pairs in the hierarchy groups was
significantly less than that of isolated pairs. If the rank of the fish on attributes
changed between meetings so that they did not always dominate the same fish
when their hierarchies formed the second time, then likewise there should have
been a similarly low rate of replication in relationships when the isolated pairs
met for the second time. But this did not occur, so the changes in the relationships and ranks of the fish must be accounted for by other factors rather than
changes in ranks on attributes.

B. Influence of social factors on linear hierarchy formation

In order to discover what factors were necessary for the formation of linear
hierarchies, Chase et al. (2002) carried out a second experiment with cichlid
fish. In this experiment, they set out to test that social processes, behavioral
processes that could only take place in a group context, were crucial for linear
hierarchy formation and that they contributed more to linearity than prior
attributes. In this experiment, they allowed groups of four and five fish to form
hierarchies by two means: round-robin competition and group assembly. In roundrobin competition, the fish in a group met only as isolated pairs, out of sight of the
other members of their group. The sequence of meeting was as follows: first, A and
B met, then C and D, A and C, D and B, and so on. In this way, differences in
individual attributes could determine which one of a pair would dominate. If, say,
A was superior in dominance attributes to B, A could dominate when they met as a
pair. However, social processes such as C getting information by observing the
outcome of a contest between A and B and then using that information in

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Chase and Seitz

interacting with either A or B was not possible, since each pair formed a relationship in isolation from other group members. In group assembly, all the members of
a group met in an aquarium at the same time. This allowed fish to use whatever
social process they were capable of in forming their hierarchies.
Table 4.2 shows the results of this experiment. When groups of fish
established their hierarchies using round-robin competition, only about half of
them formed linear hierarchies (but see McGhee and Travis 2010 for contrasting
results). When they established their hierarchies using group assembly, nearly all
of the hierarchies were linear. Behavior that only occurred in a group context
ensured the development of linear hierarchies, while differences in individual
attributes did not. However, differences in individual attributes still had some
influence on the production of linear hierarchies: the proportion of linear
hierarchies with round-robin competition was higher in groups of five fish than
would be expected by chance alone.
Although the experiments just described demonstrated that differences
in the attributes of individuals were of some importance in generating linear
hierarchy structures, social processes of some sort were necessary to ensure the
formation of the structures. Another way to look at these findings is that, given
the attributes of individuals, there was still considerable randomness in their
positions in the hierarchies. It was far from total randomness, but the amount of
chance in dominance rank was still substantial. In spite of this degree of
randomness, the hierarchy structures themselves were almost always linear.
What social processes could ensure the common formation of these linear
forms of social organization in spite of the lack of predictability concerning the
individuals in the structure?
Chase (1982) proposed that winner, loser, and bystander effects together
might be the social processes largely accounting for the formation of linear hierarchies across a variety of species. The basic idea was that even if you started with a
group of animals of equal prior attributes, they could eventually be differentiated in
terms of dominance through feedback during the course of their interactions. For
example, assume that there are both winner and loser effects for some species and
that A and B have the first interaction when a group is assembled. If A defeats B, A
Table 4.2. Percentage of Linear Structures Expected in Random Hierarchies and Observed in
Round-Robin Competition and Group Assembly in Groups of Four and Five Fish
Method of forming hierarchy
Size of group

Random (%)

Round robin (%)

Group assembly (%)

4
5

37.5
11.7

56.2 (n 16)
50.0 (n 12)

92.0 (n 25)
90.9 (n 11)

4. Self-Structuring Properties of Dominance Hierarchies

69

increases her probability of winning her next encounter and B decreases hers. A next
meets C, defeats her, and again increases her probability of winning, while B
encounters D, loses, and decreases her probability further.
A number of researchers have developed mathematical models and
computer simulations to show that feedback from winner and loser effects, either
working by themselves or together, can, at least in theory, produce highly linear
hierarchies (e.g., Bonabeau et al., 1999; Dugatkin, 1997; Hemelrijk, 1999; Hock
and Huber, 2006; 2007; 2009; Skvoretz and Fararo, 1996; Skvoretz et al., 1996).
However, these models were not tested against actual interaction records of real
animals forming dominance hierarchies. When Lindquist and Chase (2009) did
evaluate three (Bonabeau et al., 1999; Dugatkin, 1997; Hemelrijk, 1999) of the
most prominent of these models and simulations using detailed data records for
hens establishing hierarchies (Chase 1982), they found little support for the idea
that winner and loser effects were responsible for the formation of linear dominance structures. In addition, when Lindquist and Chase (2009) examined the
background assumptions on which these models and simulations were based,
they found little support for these assumptions in the experimental literature.
Assumptions in the models and simulations include animals not remembering
one another as individuals, outcomes of earlier dominance contests during
hierarchy formation not influencing the outcomes of later contests, and most
important, winner and loser effects actually occurring in groups forming hierarchies. In fact, the literature indicated that the actual experimental findings
were in virtually all cases directly opposite to the assumptions of the models and
simulations. For example, animals setting up hierarchies do remember one
another as individualseven in the case of fruit flies (Yurkovic et al., 2006).
The outcome of earlier contests do influence the later ones, and perhaps most
striking of all, winner and loser effects do not seem to occur in groups forming
hierarchies (Brown and Colgan, 1986; Chase et al., 2003; Cheney and Seyfarth,
1990; DEath and Keeling, 2003; DEttore and Heinze, 2005; Gherardi and
Atema, 2005; Karavanich and Atema, 1998; Lai et al., 2005; McLeman et al.,
2005; Tibbetts, 2002; Todd et al., 1967; Yurkovic et al., 2006).
In particular, Chase et al. (2003) investigated several basic aspects of
dominance relationships in isolated versus socially embedded pairs in groups of
three and four fish. These aspects of relationships included winner and loser
effects, stability of relationships over time, and the ability of pairs to replicate a
relationship after a separation of two weeks (as described above). Specifically,
while there was a strong loser effect in isolated pairs of fish, this effect was not
above chance for socially embedded pairs. There was no winner effect in either
isolated or socially embedded pairs. In addition, dominance relationships were
much less stable over time for pairs within groups (a significant proportion of
these relationships reversed over 24 h) compared to no relationships reversing
in isolated pairs, and a significantly smaller proportion of pairs within groups

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Chase and Seitz

did not form the same relationships when they met a second time after a
separation of two weeks as compared to isolated pairs. In summary, all the
aspects of relationships the researchers tested either disappeared or were significantly reduced for socially embedded pairs as compared to pairs by themselves.
This experiment provides a strong warning of the danger of simply assuming that experimental results for isolated pairs can be automatically generalized
to animals that are part of groupseven those as small as three or four
individuals.
Given the lack of fit between these three prominent winner/loser
models and actual data on the formation of hierarchies in real animals, and the
almost total absence of experimental support for the basic assumptions of the
models, it seems reasonable to suggest that winner and loser effects cannot
account for the common occurrence of linear hierarchies in animal groups. But
could some other models, based upon states, still satisfactorily explain linear
structures? For example, what about bystander states? These states have also been
used in models, both for animals and humans, as a way to account for linear
hierarchies (e.g., see Dugatkin and Earley, 2003; Skvoretz and Fararo, 1996;
Skvoretz et al., 1996). Although Lindquist and Chase (2009) did not look at
bystander effects per se, they did point out that a bystander effect can often be
decomposed into winner and loser effects; for example, a bystander increases its
probability of winning over an individual that it has observed losing a contest
and decreases its probability of defeating an individual that it has observed
winning a contest. In cases of this sort, Lindquist and Chases (2009) results
also indicate the difficulty of bystander effects in explaining the common presence of linear structures.
While it is impossible to prove categorically that no differences in states
for individuals could ever account for the forms of hierarchy structures, winner,
loser, and bystander effects are the best candidates that have been proposed so
far. Given the lack of support for them, it appears doubtful, at least to us, that
differences in the states of animals can be adequate explanations for the social
organization of hierarchies.

VI. A NEW APPROACH TO EXPLAINING THE FORMATION

OF LINEAR HIERARCHIES: BEHAVIORAL PROCESSES
Given the apparent absence of support for differences in individual attributes and
states as satisfactory explanations for linear hierarchies, we now review an
alternative view: that the social organization of hierarchies can be explained
by characteristic behavioral processes that commonly occur across many species
during hierarchy formation.

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4. Self-Structuring Properties of Dominance Hierarchies

Chases (1982) jigsaw puzzle model presented the original version of

this idea. The jigsaw puzzle model suggested that like the picture in a real jigsaw
puzzle, a linear hierarchy forms when the right small pieces, in this case of
social interaction, are put together in the correct manner. In this way, the model
sees the dominance hierarchy as self-organizing or self-structuring. More specifically, the model indicates four possible sequences for the formation of the first
two dominance relationships in subgroups of three animals making up a larger
group. These four sequences, shown in Fig. 4.4, have different implications for
the formation of linear hierarchies. The two patterns on the left, Double Dominance and Double Subordinance, guarantee transitive dominance relationships,
regardless of the direction that the missing third relationship in those sequences
takes when it fills in later. In a transitive relationship, individual X dominates
individual Y, individual Y dominates individual Z, and individual X also dominates individual Z. For example, in Double Dominance, if B later comes
to dominate C, the transitive relationship is A dominates B, B dominates C,
and A dominates C. If C later comes to dominate B, the transitive relationship is
A dominates C, C dominates B, and A dominates B. The fact that Double
Dominance and Double Subordinance guarantee transitive relationships is very
important because transitive relationships are the building blocks of linear
hierarchies. By mathematical definition, if all the subgroups of three individuals
in a larger group have transitive relationships, the hierarchy is necessarily linear.
Thus the presence of only Double Dominance and Double Subordinance
sequences in the subgroups of three animals (component triads) making up a
larger group guarantees that a hierarchy will be linear, even before the missing
third relationships in the component triads have formed.
A
1

A
2

1
C

Double
dominance

2
Double
subordinance

1
C

A
2

1
C

Bystander
dominates
initial dominant

2
Initial
subordinate
dominates
bystander

Figure 4.4. The four possible sequences for the first two dominance relationships in a component
triad. Arrows show the direction of dominance relationships between the members of a
triad. The number 1 indicates the first relationship to form in a triad and 2 indicates the
second relationship. In all triads, A is the initial dominant, B is the initial subordinate,
and C is the bystander. Figure adapted from Figure 24.2, p. 574, in Dominance
hierarchies by Ivan D. Chase and W. Brent Lindquist from Oxford Handbook of
Analytical Sociology ed. by Hedstrom, P. and Bearman, P. (2009), by permission of
Oxford University Press.

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Chase and Seitz

On the other hand, if a hierarchy is nonlinear, it contains at least one

component triad with an intransitive dominance relationship; the more intransitive triads, the further the hierarchy is from linearity. In an intransitive
relationship, X dominates Y, Y dominates Z, but Z dominates X. The two
sequences on the right of the figure, Bystander Dominates Initial Dominant
and Initial Subordinate Dominates Bystander, can lead to either transitive or
intransitive relationships depending upon how the third dominance relationship
eventually fills in. For example, in Bystander Dominates Initial Dominant, the
relationship is transitive if C later dominates B (C dominates A, A dominates B,
and C dominates B), but intransitive if B later dominates C (A dominates B,
B dominates C, C dominates A). If a group had one or more Bystander Dominates Initial Dominant and Initial Subordinate Dominates Bystander sequences,
the chance for a nonlinear hierarchy would be increased when the third relationships in the triads eventually formed.
In a study of groups of three hens forming hierarchies, Chase (1982)
found that almost all relationships were established using Double Dominance
and Double Subordinance sequences. In 23 groups of three hens, 91% of the
groups used Double Dominance and Double Subordinance together, while only
8% used the sequences not ensuring transitivity. In a second study of 14 groups of
four hens (Chase, 1982), approximately 87% of the component triads in the
groups (each group of four had four subgroups of three for 56 triads altogether)
used Double Subordinance and Double Dominance, while approximately 13%
had sequences not guaranteeing transitivity. These results are in contrast to those
expected by chance, in which each sequence would have occurred about 25% of
the time (or 50% combined for the two ensuring transitivity and 50% for the two
not doing so).
Thus, the jigsaw puzzle model indicated that the hens established
dominance relationships largely through behavioral sequences that guaranteed
transitivity in their triads, and transitivity in their triads in turn guaranteed
overall linear hierarchy structures. After Chases (1982) application of the model
to hens, other researchers used the original model and some modifications of it to
examine dominance interactions in a broad range of species including rhesus
monkeys, Japanese macaques, Harris sparrows, crayfish, and ants (Barchas and
Mendoza, 1984; Chase and Rohwer, 1987; Eaton, 1984; Goessmann et al., 2000;
Heinze, personal communication; Mendoza and Barchas, 1983). In spite of the
great differences among these species in phylogenetics, intelligence, and ways of
making a living, all showed highly significant use of sequences ensuring transitivity, although this was somewhat lower in crayfish and large groups of Harris
sparrows (Chase and Rohwer, 1987; Goessmann et al., 2000). These results
suggest that behavioral sequences ensuring transitive dominance relationships
may be common for many species that form dominance hierarchies. Further
research to confirm this possibility would be helpful.

4. Self-Structuring Properties of Dominance Hierarchies

73

A. Modifications of the jigsaw puzzle model

In recent work, Lindquist and Chase (2009) reanalyzed Chases (1982) original
data for groups of four hens forming dominance hierarchies and discovered two
additional behavioral processes promoting the efficient formation of linear hierarchies in addition to those described above under the jigsaw puzzle model. The
first additional process is the relative lack of back and forth fighting in pairs of
animals within a group establishing a dominance hierarchy. Lindquist and Chase
(2009) referred to back and forth fighting as pair flipsfirst A attacks B, then B
attacks A, and so forth. Consider two groups forming a dominance hierarchy: in
one group, there are many pair flips before they eventually form a stable linear
hierarchy. In the second group, there are no counterattacks, and the group forms a
stable linear hierarchy without pair flips. The formation of dominance relationships and their linear hierarchy is much more efficient in the second group.
In their analysis, Lindquist and Chase (2009) found that the hens
formed their relationships with a high level of efficiencyone approaching
that of the hypothetical second group just mentioned. Of the 7257 aggressive
acts recorded over the 12 h of observation for each of the 14 groups of four hens
(168 h of observation, total), only 138 interactions (1.9%) involved pair flips.
The second additional behavioral process was the rapid conversion of
intransitive dominance relationships to transitive ones. As indicated above, the
original application of the jigsaw puzzle model to the hen data showed that the
great majority (87%) of the behavioral sequences in the component triads for the
groups of four hens were those ensuring transitivity. However, a more detailed
reanalysis of the data indicated that a few triads did initially form intransitive
relationships and that several others that initially had transitive relationships
later developed intransitive ones. For example, if the triad ABC initially had a
transitive relationship A > B, B > C, and A > C, it would become intransitive if
C reversed its relationship with A to give A > B, B > C, and C > A.
In their analysis, Chase and Linquist, (2009) found that, in virtually all
cases, intransitive relationships were unstable and quickly converted to transitive ones, returning hierarchies to linearity after brief episodes of nonlinearity.
The average number of dominance interactions (pecks, feather pulls, etc.) that
occurred among group members before an intransitive triad was converted back
to a transitive one was approximately 5.2. In contrast, the average number of
interactions occurring before a transitive triad was converted into an intransitive
one or into a different transitive one was approximately 54.3 interactions or over
10 times as many. Research by Chase and Rohwer (1987) on Harris sparrows
supports these findings: they also found a strong tendency for intransitive dominance relationships to be unstable and to convert to transitive ones. Further
experimental work is needed to determine whether the instability of intransitive
relationships and their reformation as transitive ones are found in other species.

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B. Experimental evidence concerning animal cognitive abilities

and processes of interaction
In order for animals to carry out the kinds of behavioral processes that we have
just discussed, they must possess an array of quite complex cognitive abilities.
These include the abilities to remember one another as individuals, to make
inferences about their own interactions and the interactions of others, and to use
those inferences in adjusting their future dominance behavior. We have already
discussed the extensive experimental evidence concerning the ability of animals
to identify and remember one another as individuals, and to make inferences
about certain kinds of interactions. In particular, we know that a broad range of
species can infer transitivity (Bond et al., 2003; Davis, 1992; Gillian, 1981;
Grosenick et al., 2007; Lazareva, 2004; Paz-y-Mino et al., 2004; Roberts and
Phelps, 1994; Steirn et al., 1995; von Fersen et al., 1991). For example, if B has
dominated C, and C observes A dominating B, C will act less aggressively toward
A when they meet than C will toward an animal that it has simply seen dominate
another individual.
As far as we are aware, however, there have been no experimental
studies to show that animals can infer or act upon intransitivity. Such studies
could confirm the findings of Lindquist and Chase (2009) and Chase and Rohwer
(1987) mentioned above and extend our knowledge of the behavioral processes
leading to the formation of linear hierarchies.

VII. CONCLUSION
We have pointed out that there are two types of approaches that researchers can
use to explain the formation of dominance relationships and dominance hierarchies in small groups of animals. The first approach uses individuals as the unit
of analysiseither concentrating on differences in their traits before hierarchy
formation or differences in the states that they develop during group formation.
The theoretical and experimental evidence that we have reviewed indicates that
explanations based upon differences in the attributes and states of individuals
often work quite well to predict the outcome of dominance encounters in
isolated pairs of animals. But that evidence also demonstrates, surprisingly,
that these same differences in individuals are less able to predict the outcomes
of relationships in socially embedded pairs or the overall ranks of individuals in
their groups.
In order to resolve this problem, we have suggested that we need to ask a
new research questionnot what determines the ranks of individuals in hierarchies, but how linear hierarchies themselves develop. As the beginning of an
answer to this question, we have discussed the support for a new approach that

4. Self-Structuring Properties of Dominance Hierarchies

75

uses behavioral processes to account for hierarchy structures. For some, such an
approach may seem to be a kind of cheating, an avoidance of discovering
things about individuals that really do explain their successes and failures in
winning dominance contests within hierarchies. However, because the greater
complexities of groups introduce an unavoidable chance element into the predictions about individuals within hierarchies, then perforce we need an approach
that does not depend upon those individuals as units of analysis. A rough analogy
is the way we look at the organization of tosses of a coin. Because of randomness,
we do not try to predict the outcomes of individual coin tosses. Instead we move
to a higher level of the phenomenon: we say something about the organization,
or form of the distribution, of a great many coin flips. The behavioral process
explanation of hierarchy structure is our attempt to get around the chance
elements in what individuals do in hierarchies, and to say something about the
organization of hierarchies in spite of that randomness.
Recognizing when individual-based and process-based approaches are
best applied in studies of dominance has fundamental importance in choosing
the kinds of data we collect, how we analyze those data, the explanations that we
develop for hierarchies, and for the cognitive capacities, for both humans and
animals, that we envision as underlying dominance behavior.

Acknowledgments
We thank Hronn Axelsdottir and Paul St. Denis for their help with the graphics in this chapter and
Robert Huber for inviting us to participate in this volume.

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Neurogenomic Mechanisms of
Aggression in Songbirds
Donna L. Maney* and James L. Goodson
*Department of Psychology, Emory University, Atlanta, Georgia, USA

Department of Biology, Indiana University, Bloomington, Indiana, USA

I. Aggression in Context
II. Hormonal Mechanisms of Aggression
A. Territoriality in the breeding season
B. Hormones and territoriality
C. Aggression outside the breeding season
D. Evolution of aggression and life history strategies
III. Transcriptional Activity and Neural Mechanisms
of Aggression in Birds
A. Transcriptional traces of aggression reveal ubiquitous
vertebrate themes
B. Neurochemistry and major modulators
IV. A Natural Model Uniting Social Behavior, Hormones, and
Genetics
A. The white-throated sparrow
B. Endocrine and neuroendocrine correlates of
behavioral polymorphism
C. Causality and phenotypic engineering
D. Mapping the ZAL2m
V. Future Directions
Acknowledgments
References

Advances in Genetics, Vol. 75

Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00002-2

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ABSTRACT
Our understanding of the biological basis of aggression in all vertebrates, including humans, has been built largely upon discoveries first made in birds.
A voluminous literature now indicates that hormonal mechanisms are shared
between humans and a number of avian species. Research on genetics mechanisms in birds has lagged behind the more typical laboratory species because the
necessary tools have been lacking until recently. Over the past 30 years, three
major technical advances have propelled forward our understanding of the
hormonal, neural, and genetic bases of aggression in birds: (1) the development
of assays to measure plasma levels of hormones in free-living individuals, or field
endocrinology; (2) the immunohistochemical labeling of immediate early gene
products to map neural responses to social stimuli; and (3) the sequencing of the
zebra finch genome, which makes available a tremendous set of genomic tools for
studying gene sequences, expression, and chromosomal structure in species for
which we already have large datasets on aggressive behavior. This combination
of hormonal, neuroendocrine, and genetic tools has established songbirds as
powerful models for understanding the neural basis and evolution of aggression
in vertebrates. In this chapter, we discuss the contributions of field endocrinology
toward a theoretical framework linking aggression with sex steroids, explore
evidence that the neural substrates of aggression are conserved across vertebrate
species, and describe a promising new songbird model for studying the molecular
genetic mechanisms underlying aggression. 2011, Elsevier Inc.

I. AGGRESSION IN CONTEXT
Biomedical studies of aggression and its genetic basis are most often focused on
pathology, yet aggressive behaviors and related agonistic displays are essential,
adaptive components of social behavior that enable animals to secure and defend
food, mates, and territories. For many species, aggression is also required to
protect offspring from would-be predators. Thus, given that effective aggression
is often essential for gene propagation, we can expect that it will be under strong
selection to meet species-typical and population-specific demands. Further, for
any given species, aggression will be adaptive in some contexts but not others,
and it may therefore be the case that the neural and neurogenomic mechanisms
of aggression vary in relation to the functional goals of the behavior. Numerous
findings support this view, including evidence that parental aggression and male
male aggression are regulated by different suites of neuroendocrine mechanisms
in rodents (Gammie, 2005; Trainor et al., 2008; Veenema et al., 2007) and that
neuropeptides differentially influence territorial aggression and aggressive competition for mates in songbirds (Goodson and Kabelik, 2009). Indeed, the idea

5. Neurogenomic Mechanisms of Aggression in Songbirds

85

that aggression is differentially regulated across distinct functional contexts, and

distinct motivational states, has been around for more than 40 years (Moyer,
1968). This functional perspective suggests that ethological approaches will be
particularly useful for identifying integrated suites of neurogenomic mechanisms
that regulate aggression in any given context and will provide a powerful
framework for distinguishing pathology from normal, adaptive variation
(Blanchard and Blanchard, 2003, 2005).
In this review, we focus on aggression in the context of competition for
resources, for example, defending a breeding territory or a position in a dominance hierarchy within a social group. This type of aggression, particularly in a
reproductive context, is part of a suite of related behaviors that characterize a
life history strategy maximizing short-term gains as opposed to longer term
investments (Maynard-Smith, 1977; Trivers, 1972). Short-term relationships
with mates, high aggression among same-sex individuals, and low parental care
typify this strategy. At the other end of this continuum is a strategy characterized
by commitment to one mate, avoidance of injury, and a high level of parental
care. The two strategies are difficult to employ simultaneously, resulting in a
trade-off between time spent on territorial aggression versus parenting. This
trade-off has become a classic principle in ethology and is universal among
vertebrates, including humans (Trivers, 1972).
Disruptive selection that drives the sequestration of territorial and
parental behavior into alternative strategies is most likely to act on genes with
widespread effectsparticularly those with multiple functions. Genes encoding
the action or regulation of hormones are obvious examples of such genes (Finch
and Rose, 1995; Hau, 2007; Ketterson and Nolan, 1992; McGlothlin and
Ketterson, 2007; Miles et al., 2007; Moore, 1991; Nijhout, 2003; Rhen and
Crews, 2002; Sinervo and Svensson, 2002). A growing literature suggests that
trade-offs between parenting and territorial aggression are associated with gonadal steroids; in many species of fish, birds, rodents, and primates, including humans,
high levels of circulating androgens are associated with increased intrasexual
competition manifested as aggression or mating effort, whereas low levels are
associated with increased parenting effort (e.g., Ketterson and Nolan, 1994;
McGlothlin et al., 2007). In humans, paternal care and fatherhood have been
repeatedly shown to correspond to low levels of testosterone (T) (Fleming et al.,
2002; Gray, 2003; Gray et al., 2002; Storey et al., 2000; Wynne-Edwards, 2001),
whereas high T levels are associated with malemale aggression and competition
(Bernhardt et al., 1998; Book et al., 2001; Booth et al., 1989). These opposing
strategies can be generalized as a tendency to prioritize shorter term goals (mating) versus longer term goals (parental investment); at the former end of this
continuum in humans, associations have been reported between T and antisocial
activities such as alcoholism, drug use, reckless driving, failure to plan ahead, risktaking, and assaults (Aromaki et al., 1999; Dabbs and Morris, 1990; Udry, 1990).

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Strategies to balance effort toward short-term versus long-term goals may therefore involve a limited number of hormones and genes. In this review, we attempt
to bring together behavior, reproductive endocrinology, and genetics by focusing
on species in which all three have been characterized in some detail.
Since the scientific study of behavior began, birds have been the most
commonly studied animals in relation to territoriality, dominance, and agonistic
communication. Their popularity primarily reflects their unique accessibility
including location and use of vocal and visual communication channelsand
the fact that territorial birds are readily captured using mist nets and playback of
song. For the biomedical researcher attempting to model social behavior in
humans, birds may seem to represent a rather distant taxonomic group. But in
fact, birds have provided the test bed for some of the most influential theories in
the history of aggression research, and it is no exaggeration to say that our
understanding of the hormonal mechanisms of aggression in all vertebrates,
including humans, has been built in large part upon discoveries that were
first made in birds (Archer, 2006; Goodson et al., 2005a,b,c; Konishi et al.,
1989). For example, pioneering studies in birds established the theoretical
framework currently used by researchers to understand how hormones mediate
a trade-off between aggression and parenting in mammals (Wingfield et al.,
1990). This theoretical framework, which has been called the challenge
hypothesis, is based on the idea that the role of gonadal steroids in aggression
is modulated by social context. It predicts that when males are challenged in a
reproductive context, T levels rise to facilitate territorial aggression and suppress
parental behavior. Since it was first proposed by Wingfield et al. (1990), the
challenge hypothesis has found support in a wide variety of nonavian vertebrate
taxa including fish, reptiles, and primates, including humans (reviewed by
Archer, 2006). The parallels between songbirds (particularly New World sparrows) and humans with regard to the social modulation of gonadal steroids and
their effects on aggressive and parental behavior are voluminous and are summarized in Table 5.1. The underlying neuroendocrine mechanisms are nearly
identical in birds and humans and are based on the function of the hypothalamopituitary-gonadal (HPG) axis, which is universally recognized as being highly
conserved across all vertebrates (reviewed by Adkins-Regan, 2005).
Despite the contributions of avian research to our understanding of
human behavior, genomic resources in birds have lagged well behind those in
mammalsalthough this situation is now rapidly changing. In the sections that
follow, we first explore the neural and endocrine literature on songbird aggression,
and then describe a relatively new research program that is focused on the neurogenomics of territorial aggression in white-throated sparrows (Zonotrichia albicollis),
a species that exhibits morphological and behavioral polymorphisms associated
with a chromosomal inversion (Thomas et al., 2008; Thorneycroft, 1975). Importantly, the morphs differ not only in their territorial aggression, but also in parental

5. Neurogenomic Mechanisms of Aggression in Songbirds

87

Table 5.1. Evidence of Shared Mechanisms of Competitive Aggression in Birds and Humans
Prediction

Evidence in New World sparrows

Evidence in humans

Males respond to competition

with increased plasma T

Wingfield (1985), Wingfield and

Hahn (1994), Wingfield and
Wada (1989), Wingfield et al.
(1990)
Archawaranon et al. (1991),
Wingfield (1984b, 1994b)

Meta-analysis of 23 studies in
Archer (2006)

Wingfield (1984a), Wingfield

and Farner (1978), Wingfield
and Goldsmith (1990),
Wingfield et al. (1990)
Archawaranon and Wiley
(1988), Schlinger (1987),
Wiley et al. (1993)
Hau (2007), Ketterson and
Nolan (1992), McGlothlin
et al. (2007), Schoech et al.
(1998), Spinney et al. (2006),
Wingfield (1984a,b,c)

Berg and Wynne-Edwards

(2001), Fleming et al.
(2002), Gray et al. (2002),
Storey et al. (2000)
Meta-analysis of 13 studies in
Archer (2006)

The plasma T response to

challenge increases
aggression
Plasma T levels are lower
among paternal males

Aggressive dominance is
correlated with plasma
T levels
Plasma T is associated with
alternative life history
strategies regarding
territoriality versus
parenting

Meta-analysis of 11 studies in
Archer (2006)

Dabbs and Morris (1990),

Dabbs et al. (1997),
Daitzman and Zuckerman
(1980), Gray et al. (2002),
Julian and McHenry (1989)

The endocrine underpinnings of competitive aggression are broadly similar in New World
sparrows (here limited to the Zonotrichia, Melospiza, and Junco genera) and humans (based primarily
on Archer, 2006). Only a fraction of the relevant literature is cited here.

behavior, and thus this species offers an extraordinary opportunity to examine

neurogenomic mechanisms that integrate aggression with other aspects of social
phenotype and context-specific behavior.

II. HORMONAL MECHANISMS OF AGGRESSION

A. Territoriality in the breeding season
There are about 10,000 species of birds, almost half of which are songbirds.
Territoriality runs the gamut, with members of some species nesting colonially or
cooperatively, others defending territories of several hectares. Perhaps the beststudied territorial species are the seasonally breeding New World sparrows,
which include song sparrows (Melospiza melodia), field sparrows (Spizella pusilla),
white-crowned sparrows (Zonotrichia leucophrys), and dark-eyed juncos (Junco
hyemalis; see Arcese et al., 2002; Chilton et al., 1995; Carey et al., 2008; Nolan
et al., 2002 for reviews). In migratory populations, the males arrive at the

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breeding grounds a week or so before the females and stake out territories
containing food sources and nest sites. The females then arrive, basing their
mate choices on the quality of the males as well as their territories. It is therefore
important, in fact critical, for males to establish high-quality territories early in
the breeding season. Once a male has attracted a mate, she will help defend the
territory.
The most ubiquitous and frequent behavior used for territory defense by
songbirds is, not surprisingly, song. Each species song is distinct, and within a
species there is enough variation that individuals can recognize each others
songs (Krebs, 1971). Some species sing different types of song in different
contexts; for example, the complex song of the field sparrow is considered
more aggressive than the simple song (Carey et al., 2008; Nelson and Croner,
1991), and the chestnut-sided warbler (Dendroica pensylvanica) sings a different
song to an intruder than he does to a potential mate (Kroodsma et al., 1989; Lein,
1978). Although most of the singing is done by males, females of some species do
sing during agonistic encounters (e.g., Baptista et al., 1993; Falls and Kopachena,
2010). Males typically choose a centrally located perch and sing loudly at regular
intervals, making their presence known to would-be mates and intruders. In a
now-classic study, Krebs (1976) showed that experimental removal of territorial
male great tits (Parus major) resulted in rapid takeover of the vacated territories
by other males; however, broadcasting a former residents song from a loudspeaker
in his territory significantly delayed that takeover (see also Falls, 1988).
Although most song is typically sung from a prominent perch in the center, it
is also commonly used near territory boundaries, particularly directed at neighbors, as the territory is established. Males learn to recognize their neighbors
songs and will tolerate them at a distance; however, hearing an unfamiliar song
will generally trigger an investigation and aggressive response (Falls, 1969;
Goldman, 1973, Krebs, 1971; Kroodsma, 1976).
In addition to song, territorial sparrows are likely to exhibit a number of
other displays during territory establishment and maintenance. Birds of both
sexes may puff out their feathers, in particular raising those on the head to form a
crest, or quiver their wings while pointing a closed bill at the intruder
(Elekonich, 2000; Nice, 1943). They may peck furiously at nearby objects. If
the intruder is unfazed, the resident then resorts to more direct physical threats,
flying directly over the intruder, chasing him, and eventually attacking him.
Opponents may fly at each other with feet stretched forward and may even fall to
the ground as they engage and struggle. Physical fights are rare, however, and
generally limited to the early breeding season before territory boundaries are
firmly established.
Territorial responses can be studied in the field by observing naturally
occurring behavior or by staging a simulated territorial intrusion (STI). In this
procedure, experimenters place a decoy intruder, often accompanied by song

5. Neurogenomic Mechanisms of Aggression in Songbirds

89

played through a loudspeaker, onto a residents territory; the residents behavioral

response is then quantified. Taxidermic or painted models may be used as decoys,
or a live, unfamiliar male in cage may be presented. The most robust responses are
obtained by presenting both decoy and recorded song so that the resident receives
both visual and auditory cues (Wingfield and Wada, 1989). The behavioral data
that are collected typically include latency to respond, songs, flights directed at
the decoy threat displays (e.g., wing quivers), distance from the decoy at the
closest approach, and the time spent within a certain distance, for example 5 m,
of the decoy (Wingfield, 1984b, 1985; Wingfield and Hahn, 1994).

B. Hormones and territoriality

In the 1970s and 1980s, John Wingfield and Donald Farner revolutionized the
study of behavior in songbirds by developing methods to measure gonadal
hormones in small plasma samples collected from free-living individuals
(Wingfield and Farner, 1976). The ensuing research in field endocrinology
(Wingfield et al., 1990; Walker et al., 2005) elucidated patterns of gonadal
hormone secretion over the reproductive cycle in a wide variety of avian species.
In general, the stages of breeding associated with high levels of aggression
coincide with high plasma levels of T. In song sparrows, for example T peaks
during territory establishment when agonistic encounters are most frequent
(reviewed by Wingfield et al., 2001), rises again during egg-laying, and slowly
declines until the incubation phase when territory disputes are rare (Fig. 5.1A).
In some multiple-brooded species, for example house sparrows (Passer domesticus), competition for nest holes appears to drive an increase in plasma T during
each egg-laying period (Hegner and Wingfield, 1986; Fig. 5.1B).
The temporal correlation between high plasma T and territorial behavior suggests that the two are related, and experimental manipulation of either T
or the competitive environment shows that the relationship is bidirectional.
Male song sparrows implanted subcutaneously with T-filled silastic capsules
during territory establishment showed a more aggressive response to STI than
males given empty capsules, and won territories that were twice the size
(Wingfield, 1984b,c). Perhaps more interesting, however, was the effect on
these males neighbors. The residents occupying territories adjacent to the
treated males also showed increases in plasma T, suggesting that having to
defend their territories against their more aggressive, T-treated neighbors stimulated HPG activity. In a separate study, male song sparrows were removed from
their territories, allowing new residents to take over. In this case, both the new
residents and their neighbors experienced high T levels compared with unmanipulated controls (Wingfield et al., 1987). Together, these studies show not only
that T increases aggression, but also that engaging in agonistic encounters
increases plasma T. The HPG response is rapid; plasma T rises significantly

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Plasma level of testosterone

Prebreeding

Song sparrow
monogamous

Sexual

Parental

ta
ren
Pa
al
xu
Se

ta
ren
Pa
al
xu
Se

ta
ren
Pa
al
xu
Se

Prebreeding

House sparrow
monogamous

C
Red-winged blackbird
polygynous

Prebreeding

Breeding

Figure 5.1. Plasma testosterone (T) profiles over the breeding season in males of three passerine
species. (A) In song sparrows, T peaks during territory establishment (prebreeding) and
again during laying of the first clutch when females are receptive (sexual), and then falls
during incubation and feeding (parental). (B) In house sparrows, T peaks during periods
of intense competition for nest sites, prior to each of multiple broods. (C) In red-winged
blackbirds (Agelaius phoeniceus), males provide little parental care and spend more time
on territorial defense; T remains relatively high until the end of the breeding season.
Redrawn from data in Wingfield (1984a) and Hegner and Wingfield (1986).

within 10 min of STI onset in male song sparrows (Wingfield et al., 1987) and
can remain high for several days. This prolonged hormonal response probably
heightens vigilance in anticipation of a sustained challenge (Wingfield, 1994a).

5. Neurogenomic Mechanisms of Aggression in Songbirds

91

C. Aggression outside the breeding season

In seasonally breeding birds, the gonads regress and become quiescent during the
nonbreeding season. A testis that measures more than 10 mm across during
breeding may shrink to less than 1 mm in the fall. Ovaries likewise regress such
that follicles are barely visible. As a result, plasma levels of gonadal steroids fall
to low or even nondetectable levels (Wingfield and Farner, 1993). The gonads
remain in this state until the long days of spring stimulate photoreceptors in
the mediobasal hypothalamus, triggering HPG hormone secretion and gonadal
recrudescence (reviewed by Dawson et al., 2001).
For many species, the fall in plasma gonadal steroid levels at the end of
the breeding season coincides with abandonment of breeding territories and the
onset of flocking behavior. For others, quiescence of the HPG axis does not seem
to affect territorial behavior at all. Both of these scenarios are considered below.

1. Aggression in flocks
In species that do not defend territories year-round, the conclusion of territoriality each year may give rise to flocking behavior. In flocks, birds maximize foodfinding while minimizing predation risk (Hamilton, 1971). Competition for food,
roosting sites, and other resources within flocks creates many opportunities for
agonistic interactions, and some of the same behaviors used to defend territories,
for example, song and threat displays, are also seen in this context. Other
common aggressive displays in flocks include displacements, wherein one individual approaches another and causes it to move away, and hold-offs, wherein an
individual refuses to be displaced. Each of these behaviors is easily observed in
free-living groups, for example, in the vicinity of a popular food source (e.g.,
Ficken et al., 1978; Harrington, 1973; Rohwer and Rohwer, 1978), or in captivity
(e.g., Schlinger, 1987; Watt, et al., 1984).
In some species, winter flocks adopt a highly organized social structure.
Many of us are familiar, for example, with the dominance hierarchies, or pecking order, established by chickens (Gallus gallus domesticus; Allee, 1936, 1942).
Similar social arrangements have been observed in wild and captive groups of
sparrows, for example, dark-eyed juncos (Junco hyemalis; Sabine, 1959), whitethroated sparrows (Schneider, 1984; Watt et al., 1984), Harris sparrows (Zonotrichia querula; Rohwer, 1975) and to a lesser extent, song sparrows (Nice, 1943).
Within a group, each pair of individuals has a stable relationship such that one is
dominant to the other. The subordinate will allow the dominant to displace it,
deferring access to resources, and the dominant is unlikely to tolerate the close
proximity of the subordinate. When all members of the group are considered
together, there is in most cases a linear order of dominance; in other words, there
is an alpha bird that dominates all others, a beta that dominates all but the alpha,
and so on down to a bird that is subordinate to all. Exceptions, such as triangular

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Maney and Goodson

relationships, are fairly common. Reversals, in which the hierarchy is challenged

and altered, do occur, but overall the arrangement is fixed and stable (Sabine,
1959). In abiding by this social structure, the members of the group avoid the
potential injuries and high energy expenditure that would result from constant
aggressive encounters; when the hierarchy is stable, actual fighting is extremely
rare. Only newcomers are subject to aggressive behavior, which subsides as they
are assimilated into the group and assume a fixed rank (Tompkins, 1933).
Whereas physical contact and escalated fights are not normally required
for the maintenance of a stable hierarchy, its initial establishment is associated
with frequent aggressive interactions. When unfamiliar birds are forming a
group, or when newcomers arrive, rank is settled by the outcome of agonistic
encounters. Age and sex can predict rank in some cases. For example in whitecrowned sparrows and related species, males tend to dominate females and older
birds dominate younger ones such that the hierarchy within a group follows the
general rule: adult males > adult females > immature males > immature females
(Keys and Rothstein, 1991). In some species, such as house sparrows and Harris
sparrows, plumage characteristics can predict rank; dominant individuals have
dark bibs that appear to serve as status signals (Mller, 1987; Rohwer, 1975).
Manipulation of bib coloration does not, however, alter status; rather, it results in
heightened aggression toward the altered individuals, whose new plumage coloration is inconsistent with their behavior (Rohwer and Rohwer, 1978).
The relationships between dominance rank and HPG function have
been explored in many species of birds. This body of work, which spans almost 75
years, collectively shows that dominance rank is predicted by plasma T levels
only in groups that are newly forming. In other words, when unfamiliar birds
come together to form a social group, their T levels during the establishment of
the hierarchy contribute toward their eventual rank. Later, after the hierarchy is
settled and stable, rank is unrelated to plasma T (Baptista et al., 1987; Buchanan
et al., 2010; Chase, 1982; Ramenofsky, 1984; Schlinger, 1987; Wiley et al., 1999).
Given that engaging in aggressive behavior causes T to rise (Wingfield
et al., 1987), we must ask whether high T leads to the acquisition of a high rank,
or vice versa. Some authors have reported that short-term treatment with
exogenous T can alter stable hierarchies; the newly acquired ranks were maintained in white-crowned sparrows (Baptista et al., 1987) and domestic hens
(Allee et al., 1939) but not Japanese quail (Coturnix coturnix japonica; Selinger
and Bermant, 1967). In the majority of such studies, T treatment affects eventual
rank when it is done early during hierarchy establishment. After rank is stable,
however, rank is usually unaffected by T administration (Buchanan et al., 2010;
Crook and Butterfield, 1968; Lumia, 1972; Mathewson, 1961; Rohwer and
Rohwer, 1978; Wiley et al., 1999). The lack of an effect of T treatment on
established, stable ranks has been attributed to learning, or social inertia
(Guhl, 1968; Wiley et al., 1999), in groups of individuals that are familiar with

5. Neurogenomic Mechanisms of Aggression in Songbirds

93

each other. In house sparrows, which do not defend large breeding territories,
dominance rank during the nonbreeding season is determined largely by rank at
the end of the breeding season when plasma T level is falling (Buchanan et al.,
2010). In other words, winners stay winners and losers stay losers (Chase, 1982).
HPG activity during the breeding season may therefore contribute toward rank
during the nonbreeding season. During both times of year, actual physical aggression is limited to periods of instability during which high-ranking positions up for
grabs or otherwise in dispute. After the establishment of social relationships and
boundaries, physical aggression is rare and plasma levels of T are much lower.

2. Territoriality in the nonbreeding season

Song sparrows in resident populations, despite being seasonal breeders that
undergo gonadal regression in the fall, can maintain essentially the same
territories year-round. Whereas the song sparrows studied by Wingfield in
New York State (e.g., Wingfield, 1984a,b,c, 1985) abandon their territories
and migrate at the conclusion of the breeding season, populations in Western
Washington remain on the same territories, molt their feathers, and then,
despite having completely regressed gonads and nondetectable levels of T,
resume territorial defense (Wingfield and Hahn, 1994). Furthermore, young
males just hatched the previous spring can establish new territories in the fall
without an increase in T. STI during the fall induces the same behavioral
responses as in spring, but without an accompanying HPG response (Soma and
Wingfield, 2001; Wingfield and Hahn, 1994), and castration does not interfere
with the ability to maintain a territory (Wingfield, 1994b). These results led to
the hypothesis that territorial aggression and gonadal steroid secretion can
become uncoupled in this and other species that defend territories outside
the breeding season.
To address this question, Soma et al. (1999, 2000a,b) tested whether T
action is necessary for autumnal aggression in a population of song sparrows in
Western Washington. To block the effects of T, they administered androgen
receptor antagonists and, because T can also act via conversion to estradiol (E2),
blockers of that conversion. They found that blocking the action of aromatase,
an enzyme that converts T to E2, reduced territorial aggression even in the fall
when plasma levels of gonadal steroids are naturally very low. This result
suggested that autumnal aggression is not in fact independent of steroid hormones. This reduction was reversed by treatment with E2 (Soma et al., 2000a).
Because gonads are not required for autumnal territorial defense
(Wingfield, 1994b), the E2 that drives this behavior must come from a nongonadal source. One such source may be the brain itself, which contains high
levels of aromatase. In song sparrows, aromatase mRNA is expressed in the brain
at all times of year (Soma et al., 2003; Wacker et al., 2010) suggesting a possible

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source of E2 available to brain tissue year-round. Aromatase activity in the

ventral telencephalon, which contains the putative avian homologue of the
amygdala, is reduced during molt, at which time aggression is also low (Soma
et al., 2003). Brain-generated E2 may thus be an important regulator of territorial
aggression in this species. To synthesize E2, the brain may make use of androgen
precursors from regressed gonads or the adrenals (see Soma, 2006; Soma et al.,
2008 for reviews). Alternatively, some regions of the brain contain all of the
enzymes necessary to synthesize E2 de novo from cholesterol substrate (reviewed
by Soma et al., 2008; Remage-Healey et al., 2010), obviating the need for a
peripheral steroid synthesis altogether. The regions of the brain important for
aggressive behaviors, for example the nuclei that control singing behavior, are
rich in these enzymes (Remage-Healey et al., 2010). Aromatase expression is
high in the ventromedial nucleus of the hypothalamus (VMH) during all times of
year except during molt, when aggression is virtually absent (Wacker et al.,
2010). In mice, distinct populations of VMH neurons contribute to fighting
and mating behavior (Lin et al., 2011). In Section III, we will explore further
the role of this region in aggression in songbirds.
Like androgen release from the gonad, E2 synthesis by the brain appears to
be behaviorally regulated. Remage-Healey et al. (2008) recently showed that in
zebra finches (Taeniopygia guttata), hearing conspecific song increases E2 concentrations in the auditory forebrain within minutes. Pradhan et al. (2010) showed
subsequently that in nonbreeding, territorial song sparrows, exposure to STI rapidly
increases activity of 3b-hydroxysteroid dehydrogenase, an enzyme necessary to
synthesize E2 from androgen precursors. These findings demonstrate that the steroid
environment within the brain is dynamic, sensitive to the social environment, and
more independent of the gonad than previously thought. These discoveries of
socially regulated, brain-generated steroid synthesis challenge the traditional view
of hormone-mediated aggression and highlight the importance of songbird models
to our understanding of how steroids regulate gene activity in the brain.
Forty years of research on free-living sparrows has shown that aggression
depends on steroid hormones. Even when at first glance it appears that aggression
and steroid hormones have come uncoupled, for example, when resident song
sparrows vigorously defend territories despite low plasma T, the evidence shows
that low levels are necessary for the expression of territoriality and that the brain
itself may produce sufficient amounts. The role of steroid hormones, particularly
E2, in aggression seems very similar to their role in sexual receptivity (reviewed
by Maney, 2010): plasma levels need not be high, and in fact seasonal peaks in
plasma levels need not be associated in time with the behavior. A low level,
however, is required for the behavior to be expressed. Because the frequency of
aggressive behavior is clearly not always correlated directly with plasma levels of
steroid hormones, it is possible that the hormones play a priming, or permissive,
role and that other hormones or neurotransmitters are also important.

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95

D. Evolution of aggression and life history strategies

Research on wild songbirds has demonstrated a robust, two-way relationship between
aggression and HPG activity. What does that finding tell us about the evolution and
genetic control of these behaviors? Because steroid hormones affect suites of behaviors, not just aggression, it is helpful to think about this issue in terms of behavioral
strategies. As discussed in Section I above, investment in territory defense and matefinding defines a strategy at one end of a behavioral continuum, with investment in
survival and parenting at the other (Trivers, 1972). This trade-off appears to be
mediated, at least in part, by HPG activity (Ketterson and Nolan, 1994; McGlothlin
et al., 2007; Wingfield et al., 1990). In species with male parental care, T is high during
territory establishment but falls during the parental phase (Fig. 5.1A, B). Exogenous
administration of T during the parental phase inhibits parental behavior and
increases territorial behavior (Hegner and Wingfield, 1987; Schoech et al., 1998;
Silverin, 1980). In species without male parental care, for example polygynous
species in which females do the bulk of the care, T remains high in males for the
duration of the season (Fig. 5.1C). In a study by Wingfield (1984c), T treatment of
male song sparrows not only reduced parental care but also induced polygyny in this
normally monogamous species. These males spent much of their time singing and
acquired huge territories, attracting multiple females. Their failure to provision the
young, however, likely reduced their overall reproductive success (Hegner and
Wingfield, 1987; Silverin, 1980). Alterations in HPG function could therefore result
in large, cascading effects and make an important contribution to variation in social
behavior and social strategies (Ketterson and Nolan, 1992; Sinervo and Svensson,
2002). When the effects of a hormone are antagonistic with respect to behavior, for
example, in the case of T and parenting versus aggression, antagonistic pleiotropy
can give rise to behavioral trade-offs (Finch and Rose, 1995). We hypothesize that
suites of related genes, the expression of which is tightly governed by social cues, may
act hierarchically to organize and regulate the hormonal and neural systems that
promote territorial aggression and reduce parental behavior. In the next section, we
explore the neural circuits that are involved and consider how evolution has shaped
them in species with different behavioral strategies.

III. TRANSCRIPTIONAL ACTIVITY AND NEURAL MECHANISMS

OF AGGRESSION IN BIRDS
A. Transcriptional traces of aggression reveal ubiquitous
vertebrate themes
Although it has long been known that all vertebrates share some basic features in
the organization of the amygdala, hypothalamic nuclei, and associated (limbic)
areas of the basal forebrain and midbrain, the extent of these similarities has

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Maney and Goodson

become much more clear in the past 10 years as investigators have combined
genomic data with conventional neuroanatomical and functional approaches
(e.g., using lesions and pharmacological manipulations). We now know that
birds and rodents exhibit extraordinary similarities in the organization of limbic
brain areas (Goodson, 2005; Newman, 1999), including distinct homologies at
the subnuclear level (e.g., Goodson et al., 2004a; Kingsbury et al., 2011) and very
specific similarities in the topographical patterns of transcriptional response to
aggressive interactions (and other social interactions, as well), as established
through the experimental induction of immediate early gene (IEG) transcripts
and their protein products (Ball and Balthazart, 2001; Goodson, 2005). The IEGs
most commonly used for such functional studies are c-fos and a gene variably
known as zif-268, egr-1, NGFI-A, krox-24, or Zenk (the latter being a name often
used in birds as an acronym for the other four names; Mello et al., 1992).
Experimentally induced increases in IEG mRNA can be detected by
in situ hybridization (ISH) within 1530 min. For detection of IEG proteins
by immunocytochemistry (ICC), most investigators harvest brain tissue
6090 min after the experimental manipulation, such as an aggressive interaction. Because the induced IEG proteins are still elevated at 90 min and two halflives of the protein have passed (Herdegen and Leah, 1998), it is possible to
determine whether the experimental manipulation may have decreased IEG
activity from control levels (e.g., Bharati and Goodson, 2006; Goodson and
Wang, 2006). Most behavioral neuroscientists are primarily interested in IEGs
not because of what they do inside the cell, but rather because they provide a
proxy marker to indicate that a cell has responded in some way to a stimulus.
That response may or may not be associated with action potentials and release of
neurochemicals (Herdegen and Leah, 1998), but by labeling for IEG transcripts
and proteins, investigators can gain a good idea about the functional properties of
different brain areas or cell groups. The actual molecular functions of IEGs are
varied, but typically include the regulation of other genes involved in experience-dependent neuroplasticity (Herdegen and Leah, 1998; Mello and Ribeiro,
1998), and thus IEGs probably have the ultimate effect of changing the way that
cells function and behave during subsequent behavioral interactions.
In rodents, residentintruder encounters induce IEG activity in a characteristic pattern that includes the medial amygdala (MeA), medial bed nucleus
of the stria terminalis (BSTm, a component of the medial extended amygdala
that shares many anatomical and functional properties with the MeA), anterior
hypothalamus (AH), ventrolateral lateral septum (LS), ventrolateral subdivision
of the ventromedial nucleus of the hypothalamus (VMHvl; or lateral VMH in
hamsters), dorsal premammillary nucleus, and the dorsal midbrain periaqueductal gray (Kollack-Walker et al., 1997; Motta et al., 2009). Notably, along with the
medial preoptic area, these same brain areas are central to the regulation of most
other social behaviors, including communication behaviors, parental care, pair

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97

bonding, appetitive and consummatory sexual behavior, juvenile play, social

recognition, and both same-sex and opposite-sex affiliation (Goodson, 2005;
Newman, 1999). Despite the similarities, the relative amount of IEG activity
across the different nodes of this social behavior network is distinctive for each
social context, suggesting that functional relationships across the network nodes
are dynamic and context-specific. Distinct patterns of correlated activity between network nodes in different social contexts have now been demonstrated in
multiple vertebrate classes (Crews et al., 2006; Hoke et al., 2005; Yang and
Wilczynski, 2007).
The areas comprising the social behavior network are readily identified
in birds and are anatomically and functionally conserved across amniote vertebrates, and in fact, the basic features of this network are present even in fish
(Goodson, 2005; Goodson and Bass, 2002). Consistent with this conservation,
territorial songbirds housed in captivity exhibit a pattern of IEG activity after
STI that is virtually identical to the pattern described for rodents after a
residentintruder encounter (Goodson and Evans, 2004; Goodson et al.,
2005b). This work has been conducted in animals housed in their natural
habitat, and data for catecholaminergic midbrain areas are even available from
animals occupying natural territories (Maney and Ball, 2003). In addition,
following exposure to same-sex conspecifics through a wire barrier in a quiet
room (which elicits very little overt behavior), territorial finches exhibit relatively greater Fos and/or egr-1 responses than do gregarious species in a pattern
similar to aggressive encounters (Goodson et al., 2005a). Hence, at least to an
extent, the IEG activity of these brain areas reflects perceptual or motivational
processes, not simply activation of aggression.
Although it is intuitive to interpret IEG induction as reflecting a
positive relationship between a brain area and behavior, negative correlations
between IEG cell counts and aggressive behavior are observed for multiple brain
areas. These include the AH, both pallial and subpallial subdivisions of the LS,
and the paraventricular nucleus of the hypothalamus (PVN; Fig. 5.2; Goodson
et al., 2005b). This pattern of results suggests that aggression is under inhibitory
control, at least by some areas. Consistent with this idea, lesions of the LS
increase residentintruder aggression in male field sparrows and pigeons
(Columba livia; Goodson et al., 1999; Ramirez et al., 1988). Note, however, that
such effects are not observed in some contexts, such as aggressive competition for
mates in male zebra finches, a highly gregarious species (Goodson et al., 1999).
The PVN is heavily interconnected with the social behavior network
and plays an important role in the regulation of autonomic and pituitary activity
in relation to behavioral state. A subset of cells in the PVN produce arginine
vasotocin (VT; homologue and evolutionary precursor of mammalian arginine
vasopressin, VP), and the percentage of those cells that express Fos is also
negatively correlated with aggressive response to an STI in male song sparrows

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LSc.v

In contacts

r = -0.571
P = 0.020

r = -0.688
P = 0.003

-1

-1

-1

10 15 20 25 30

10

15 20

r = -0.632
P = 0.008

r = -0.478
P = 0.060

-1

-1

-1

10

15 20

25 30

Fos-ir nuclei/100 mm

10

15 20

LSc.vl

r = -0.693
P = 0.002

LSc.l

r = -0.551
P = 0.026

-1

-1

-1

10

30

10

Zenk-ir nuclei/100 mm2

r = -0.530
P = 0.034

PVN

10

r = -0.573
P = 0.020

Zenk-ir nuclei/100 mm2

25

Zenk-ir nuclei/100 mm2

G
5

LSr

25 30

Fos-ir nuclei/100 mm

15 20

10

AH

Fos-ir nuclei/100 mm2

PVN

25 30

Fos-ir nuclei/100 mm2

r = -0.534
P = 0.033

Fos-ir nuclei/100 mm2

LSc.d

In contacts

LSc.vl

In contacts

10

Zenk-ir nuclei/100 mm2

Figure 5.2. (AE) Correlations between aggressive behavior and Fos-immunoreactive (-ir) cell
counts in the subpallial (ventral, ventrolateral) and pallial (dorsal) zones of the caudal
lateral septum (LSc.v, LSc.vl, and LSc.d; AC, respectively), paraventricular hypothalamus (PVN; D), and anterior hypothalamus (AH; E) of male song sparrows exposed to
STI (n 16). The intruders cage and a speaker broadcasting song were placed adjacent
to the subjects cage. Subjects showed selective flights to the cage wall adjoining the
intruder, providing a good measure of aggressive response. Data are shown as the natural
log (ln) of the number of contacts with the wire barrier during a 10-min test. (FI)
Correlations between barrier contacts and Zenk-ir cell counts in the rostral LS (LSr; F),
LS.vl (G), lateral zone of the LSc (LSc.l; H), and PVN (I). Cell counts are shown as the
number of immunoreactive nuclei per 100 mm2. Modified from Goodson et al. (2005b).

5. Neurogenomic Mechanisms of Aggression in Songbirds

r 2 = 0.305
p = 0.026

5
In contacts

99

4
3
2
1
0
-1
0

10
15 20 25 30
%VT-ir neurons Fos-ir+

35

Figure 5.3. The percentage of arginine vasotocin (VT) neurons in the PVN that express Fos after a
10-min STI is negatively correlated with aggression (ln, the number of contacts with the
cage wall adjoining the intruders cage; see Fig. 5.2 caption; n 16) in song sparrows.
Modified from Goodson and Kabelik (2009).

(Fig. 5.3; Goodson and Kabelik, 2009). VT and VP are secretagogues for adrenocorticotropic hormone, and thus the lower IEG activity of the PVN VT cells
in more aggressive males likely reflects a lower stress response to the encounter.
Virtually identical results for VPFos colocalization are obtained in lab mice (Ho
et al., 2010). As addressed in Section III.B below, this negative relationship
between aggression and VTFos colocalization in the PVN accurately predicts
pharmacological effects that vary in relation to the subjects dominance status
(Goodson et al., 2009b).

B. Neurochemistry and major modulators

Although territorial aggression in birds has been the focus of hundreds of studies,
including many that address proximate endocrine mechanisms (Goodson et al.,
2005c; Konishi et al., 1989), a surprisingly small number of experiments have been
conducted with the goal of delineating relevant neurochemical circuits in the
brain. An early study of whole-brain neurochemistry shows that dopamine, norepinephrine, and acetylcholine are all associated with aggressive behavior in male
Japanese quail (Edens, 1987), and catecholaminergic midbrain nuclei show
increased IEG activity in response to STI in song sparrows (Maney and Ball, 2003).
Following aggressive competition for a potential mate, male zebra
finches exhibit significant increases in the percentages of tyrosine hydroxylase-ir
(TH-ir) cells expressing Fos within the retrorubral area (A8), substantial nigra
(A9), ventral tegmental area (VTA; A10), and midbrain central gray (A11), but
show a significant decrease in THFos colocalization within the A12 neurons of
the tuberal hypothalamus (Bharati and Goodson, 2006). TH is the rate-limiting

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enzyme for catecholamine synthesis, and all of the cell groups just listed are
known to be dopaminergic. Despite these results, treatments with quinpirole, a
dopamine D2 receptor agonist, significantly decrease aggression during mate
competition. D1 and D4 agonists are without effect, although a modest inhibition is observed with the D3 agonist 7-OH-DPAT, which may reflect weak
binding to the D2 receptor (Kabelik et al., 2010). These seemingly contradictory
results likely reflect the fact that courtship is displayed at a high rate during the
competition tests, and given that THFos colocalization in the central gray and
caudal VTA correlates positively with courtship singing (Goodson et al., 2009a),
the increased colocalization of TH and Fos following mate competition is likely
attributable to directed singing and not the display of aggression. The number of
TH-ir cells in the central gray also correlates positively with the average number
of songs that male zebra finches sing to females during courtship tests. Notably,
territorial finch species exhibit fewer TH-ir cells in the caudal VTA than do
gregarious species such as the zebra finch, although this may reflect a lower level
of affiliation rather than a negative relationship between this cell group and
aggression (Goodson et al., 2009a).
Dopaminergic mechanisms of song have also been examined in European starlings (Sturnus vulgaris), which sing in the context of breeding both to
attract females and to repel other males. Antagonism of D1 receptors decreases
song in breeding-condition males, whereas a dopamine reuptake inhibitor facilitates it (Schroeder and Riters, 2006), and aggressive song correlates negatively
with D1 receptor density in numerous areas, including the LS, BSTm, medial
preoptic area, and central gray (Heimovics et al., 2009).
The handful of other neurochemical manipulations that have been
conducted in studies of avian aggression have focused on neuromodulators
such as VT, vasoactive intestinal polypeptide (VIP), and endogenous opioids.
Of these, the endogenous opioids have received the least attention, but are
known to inhibit aggression in Japanese quail, at least partially via the delta
receptor subtype (Kotegawa et al., 1997). These neuropeptides are each produced
in multiple brain areas, and as suggested for VT, it may be the case that the
different cell groups have divergent effects on behavior (a possibility that should
also be considered in relation to the major neurotransmitters just discussed;
Goodson and Kabelik, 2009).
Both VIP and VT exert complex effects on aggression that likely reflect
the modulation of stress- and anxiety-related processes. For instance, in territorial male field sparrows housed in aviaries placed in their natural habitat,
intraseptal infusions of VT decrease aggression in residentintruder tests, but
selectively facilitate the spontaneous use of an agonistic song type during the
dawn song period (Goodson, 1998a). No effects are observed for the multipurpose song type that is used to attract females, and VIP tends to exert an opposite
pattern of effects (Goodson, 1998a,b). Interestingly, the VT and VIP systems in

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101

the LS are both sensitive to sex steroids. Castration causes down- and upregulation of VT and VIP immunoreactivity, respectively, and T or E2 replacement
reverses these effects (Aste et al., 1997; Panzica et al., 2001; Voorhuis et al., 1988;
but see Wacker et al., 2008). The VT/VIP systems therefore represent a possible
mechanism whereby gonadal steroids may modulate aggression.
In order to determine whether VT modulates stress-related processes,
and whether it does so in a manner that is integrated with its effects on agonistic
behavior, Goodson and Evans (2004) examined Zenk responses to nonsocial
stress alone (capture in an outdoor flight cage and restraint for intraventricular
infusions), or the same nonsocial stressors followed by STI. These manipulations
were conducted in male song sparrows housed in flight cages placed in their
natural habitat. Subjects were infused with either vehicle or a VT V1a receptor
antagonist and were sacrificed at the completion of testing for immunolabeling of
Zenk and VT. In some brain areas, nonsocial and social stimuli induced Zenk
within the same subset of cells, which was discernable because (1) in vehicletreated animals, the nonsocial stressor induced a significant increase in Zenk-ir
cell numbers, and subsequent exposure to the social challenge produced no
further increase, but (2) blocking the Zenk response to handling with the V1a
antagonist revealed a sensitivity to the social challenge (i.e., by eliminating the
ceiling effect). This integrated pattern of Zenk response was observed for
numerous areas, including the AH, POA, lateral VMH, lateral BST, and most
zones of the LS. Notably, in all of these cases, the antagonist exerted more
pronounced effects in the subjects that were exposed to the nonsocial stress
alone. However, in the BSTm and ventrolateral LS, Zenk responses to the social
challenge were significantly greater than to the nonsocial stressor, even in
vehicle-treated subjects, indicating that at least some cells in these areas are
more selectively activated by social challenge. The BSTm showed particularly
selective responses to the social challenge, which were completely blocked by
the V1a antagonist (Goodson and Evans, 2004).
Unfortunately, VT-ir cells of the BSTm were not detectable in this study
(these neurons are weakly immunoreactive in most vertebrates and may store
little peptide relative to the amount being released), but the VT-immunoreactive
neurons of the PVN showed significant responses to social challenge and, most
interestingly, the VTZenk colocalization was reduced by the V1a antagonist only
in the animals exposed to the STI (Goodson and Evans, 2004). As assessed in a
later study with more robust immunolabeling of VT, VTFos colocalization in the
BSTm of male song sparrows is not increased by social challenge, whereas
colocalization in the PVN is negatively correlated with aggression (Fig. 5.2;
Goodson and Kabelik, 2009).
In territorial estrildid finches, exposure to a same-sex conspecific
through a wire barrier actually decreases VTFos colocalization in the BSTm,
but the same manipulation increases VTFos colocalization in gregarious finch

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Maney and Goodson

species, and the territorial birds do show large increases in VTFos colocalization
if they are reunited with their pair-bond partner. Conversely, socially induced
VTFos colocalization in the BSTm is blocked in the gregarious zebra finch if the
subjects are intensely subjugated by a dominant bird (Goodson and Wang,
2006). Thus, the VT neurons of the BSTm exhibit an exquisite sensitivity to
the valence of social stimuli, and more recent findings suggest that this valence
sensitivity is not extended to nonsocial stimuli (Goodson et al., 2009c).
The differential response profiles of the VT neurons in the BSTm and
PVN may account for at least a portion of the context-specificity that is observed
following central infusions of VT or V1 receptor antagonists. For instance, in
zebra finches, VT promotes aggression in the context of mate competition and a
V1a antagonist inhibits aggression (Goodson et al., 2004b). These effects are
consistent with the observation that VTFos colocalization is increased in the
BSTm during mate competition, but not in the PVN. Conversely, resident
intruder aggression is inhibited by VT infusions in territorial species, consistent
with the negative correlation between aggression and VTFos colocalization in
the PVN (Goodson and Kabelik, 2009; Goodson and Wang, 2006). The different
effects on mate competition and residentintruder aggression (or nest defense in
zebra finches) can be observed in the same species (Goodson et al., 2009b;
Kabelik et al., 2009), as shown for the territorial violet-eared waxbill (Uraeginthus
granatina) in Fig. 5.4AB. However, in the violet-eared waxbill, males that are
typically dominant do not show a behavioral response to the V1a antagonist in
standard residentintruder tests whereas aggression is facilitated in subordinates
(Fig. 5.4C; Goodson et al., 2009b). Thus, perhaps only the subordinate males
activate the PVN VT neurons during aggressive encounters and this activation
inhibits aggression.

Figure 5.4. (A) Peripheral injections of a novel V1a antagonist that crosses the bloodbrain barrier
have no effect on residentintruder aggression in male violet-eared waxbills that are
aggressive and typically dominant, but aggression in the context of mate competition is
significantly reduced by the antagonist in the same males (B). (C) In males that are
typically subordinate, residentintruder aggression is disinhibited by the same treatments. Modified from Goodson et al. (2009b).

5. Neurogenomic Mechanisms of Aggression in Songbirds

103

The ability to label IEG products has provided immeasurable insight

into the neural basis of aggression, allowing the identification and mapping of
specific circuits that respond rapidly to social stimuli. Lacking until recently were
powerful genomic methods necessary for a more complete understanding of the
complex protein interactions involved in social responses. The sequencing of the
zebra finch genome (Warren et al., 2010) has provided unprecedented insight
into what happens inside the songbird brain during agonistic encounters. Using
tools such as high throughput sequencing and microarray analysis, investigators
can now look at the regulation of many hundreds of genes simultaneously. In a
recent gene profiling study, Mukai et al. (2009) compared the expression of more
than 11,500 different gene transcripts in free-living song sparrows responding
either to STI or a control intrusion by a heterospecific. For behavioral manipulations conducted during the breeding season, 67 gene transcripts were differentially expressed in the hypothalamus following exposure to an STI compared to
control. During the fall, when territorial aggression seems to be independent of
gonadal steroid production (reviewed by Soma, 2006; Soma et al., 2008; see also
Section II), 173 transcripts were affected (Mukai et al., 2009). There were
significant interactions between season and STI for 88 transcripts (Mukai et al.,
2009), which may in part reflect the differential regulation of the pituitary
gonadal axis across seasons. The expression of many of the gene transcripts was
not, however, affected by season and therefore may be important for the regulation of aggressive behavior itself rather than endocrine responses to aggressive
encounters. This study represents the early days of genomic analysis of social
behavior in free-living, natural populations and sets the standard for many more
sure to follow. In the next section, we consider a songbird species that because of
a natural genetic anomaly is becoming a popular model for studying the genetic
mechanisms underlying aggression.

IV. A NATURAL MODEL UNITING SOCIAL BEHAVIOR, HORMONES,

AND GENETICS
A. The white-throated sparrow
The underlying genetic basis of variation in social behavior is of intense interest,
yet only a handful of genes have been linked to specific social behaviors in
vertebrates (reviewed by Robinson et al., 2005). Thus, there is an obvious need to
identify populations, human or otherwise, in which there is clear linkage between genes and social behavior. A common wild songbird, the white-throated
sparrow, offers such an opportunity. This species, in which socially monogamous
pairs defend breeding territories, provision the young with food, and form flocks
with stable dominance hierarchies in the winter, is a typical New World sparrow

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Maney and Goodson

in nearly all respects. What sets it apart from other songbirds is that it exhibits
alternative phenotypes, defined by a plumage polymorphism, that differ in their
social behavior. Both males and females can be categorized into one of two
plumage morphs that differ primarily in the color of the crown stripes (Lowther,
1961; Piper and Wiley, 1989; Watt, 1986; see Fig. 5.5). Behavioral studies
conducted in the animals natural habitat have established that individuals
with a white medial stripe (WS) on the crown engage in a more aggressive
strategy, whereas birds with a tan medial stripe (TS) are more parental.
The species represents a promising model in which to study the genetic
basis of aggression because the plumage pattern segregates with the presence or
absence of a structural rearrangement of chromosome 2. WS individuals are
heterozygous for the rearranged chromosome (ZAL2m), whereas those of the TS
morph are homozygous for the wild-type chromosome (ZAL2; Thorneycroft,
1975). Once they molt into adult plumage the phenotype is fixed for the lifetime
of the individual. Within a population, approximately half of the birds are WS
(ZAL2/2m), whereas the other half are TS (ZAL2/2; Lowther, 1961;
Thorneycroft, 1975). This balanced polymorphism is maintained in the population by disassortative matingWS and TS birds nearly always mate with individuals of the opposite morph (Knapton and Falls, 1983; Lowther, 1961;
Thorneycroft, 1975; Tuttle, 1993). This mating pattern results in a virtual
absence of birds homozygous for ZAL2m, a genotype that Thorneycroft (1975)
hypothesized may be less viable due to recessive deleterious mutations. Of more
than 1000 individuals genotyped, only one was found to be homozygous for
ZAL2m (Maney et al. unpublished data; Romanov et al., 2009; Thorneycroft,
1975).

Figure 5.5. Plumage polymorphism in white-throated sparrows. (A) Individuals of the white-stripe
(WS) morph have alternating black and white stripes on the crown, bright yellow lores,
and a clear white throat patch. (B) Individuals of the tan-stripe (TS) morph have
alternating brown and tan stripes on the crown, duller yellow lores, and dark bars within
the white throat patch. Photos by Allison Reid. Reprinted from Maney (2008).

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105

The behavioral differences that segregate with the ZAL2m chromosome

have been well documented in field studies. Males and females of the WS morph
are more aggressive, both in territorial defense and in mate-seeking, than their
TS counterparts. WS males sing more in response to STI than TS males (Collins
and Houtman, 1999; Kopachena and Falls, 1993a; Horton and Maney, unpublished observations) and are more likely to trespass onto the territories of other
males (Tuttle, 2003). Whereas WS females sing and engage in active territorial
defense independently of their mates, TS females do so only rarely (Kopachena
and Falls, 1993a; Horton and Maney, unpublished observations). TS birds of
both sexes feed young more often during the parental phase of the breeding
season than do WS birds (Knapton and Falls, 1983; Kopachena and Falls,
1993b). The relative strategies employed by the different morphs of this species
therefore fall onto different ends of the behavioral continuum between territoriality and parenting (Trivers, 1972).

B. Endocrine and neuroendocrine correlates of

behavioral polymorphism
Because the behavioral trade-off between territorial defense and parenting is
clearly mediated at least in part by HPG activity in songbirds (Ketterson and
Nolan, 1994; McGlothlin et al., 2007; Wingfield et al., 1990), we should immediately suspect that, in white-throated sparrows, HPG function may vary according to morph. Spinney et al. (2006) found that in free-living birds in breeding
condition, WS males do have larger testes and higher levels of circulating T than
TS males. This phenomenon has also been demonstrated in captive populations
(Maney, 2008; Swett and Breuner, 2009). In both the field and the lab, however,
the difference in plasma T disappears when birds are not in breeding condition
(Maney, 2008; Spinney et al., 2006). Interestingly, morph differences in aggression appear only during the breeding season, mirroring the morph difference in
circulating T. In winter flocks and in laboratory-housed birds held on short days,
morph is not related to dominance rank or to aggression (Dearborn and Wiley,
1993; Harrington, 1973; Piper and Wiley, 1989; Schlinger, 1987; Schwabl et al.,
1988; Watt et al., 1984; Wiley et al., 1999). In contrast, when birds are held on
long days and undergo gonadal recrudescence, WS birds engage in significantly
more aggression than their TS cage-mates and tend to outrank them (Fig. 5.6; see
also Watt et al., 1984). Morph differences in dominance and aggression may
therefore depend on season and thus perhaps on differences in HPG function.
Because levels of gonadal steroids differ between the morphs, the
behavioral polymorphism may be driven by the effects of these steroids on the
brain. To evaluate this hypothesis, Maney et al. (2005) compared the morphs
with respect to the VT and VIP neuropeptide systems, which are highly steroid
dependent (Aste et al., 1997; Panzica et al., 2001; Voorhuis et al., 1988). WS birds

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Figure 5.6. Medians, IQR, and ranges for (A) aggression scores (number of aggressive acts initiated
per hour) and (B) individual ranks (as percent opponents dominated) within social
groups. Males were introduced in single-sex groups of six birds (three WS and three TS
per group) in indoor aviaries. Aggression scores and ranks were determined 1014 days
later by observing interactions and constructing dominance matrices. During spring-like
day lengths (16L:8D), WS males were (A) more aggressive and (B) outranked TS males.
Rank was unrelated to morph on short days (8L:16D). The long- and short-day experiments were conducted on different individuals. Data from Horton and Maney,
unpublished.

had higher levels of VT-immunoreactivity in the BSTm and ventrolateral LS

than TS birds. Since T is higher in WS males, this result is consistent with the
idea that T may be engaging the VT system in the LS. Central administration of
VT in the closely related white-throated sparrow induces agonistic song (Maney
et al., 1997), suggesting that engagement of this system may be directly related to
aggressive behaviors. Central administration of VIP, in contrast, reduces agonistic song in field sparrows (Goodson, 1998a); immunoreactivity for this peptide
was higher in the ventrolateral LS of the TS (less aggressive) morph. VIP
immunoreactivity in this region is inversely proportional to T levels (Aste
et al., 1997) again supporting a possible role for gonadal sex steroids in the
control of aggression in this species.

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107

C. Causality and phenotypic engineering

Looking for morph differences in endocrine variables in unmanipulated individuals
is an important endeavor, in that significant correlations can help illuminate
possible physiological causes of aggression. Such correlations alone, however, can
provide only limited information on causal mechanisms. The morph difference in
plasma T, for example, could be a consequence, rather than a cause, of polymorphic
behavior. Either scenario would explain the observed correlations between T and
social behavior (Spinney et al., 2006). As discussed in Section II above, experiments
involving manipulation of T or of social contexts in songbirds have revealed causal
effects in both directions. Recall that in other songbird species, free-living males
treated with T defend larger territories, engage in more aggression, acquire more
mates, and provide less parental care than untreated males (Hegner and Wingfield,
1987; Schoech et al., 1998; Silverin, 1980; Wingfield, 1984b,c). Territorial intrusion or the presence of receptive females, however, cause release of endogenous T
(Dufty and Wingfield, 1986; Moore, 1983; Wingfield and Hahn, 1994; Wingfield
and Monk, 1994). A one-way causal effect of T on aggression and parenting may
not completely explain polymorphic behavior in white-throated sparrows.
Some authors have suggested that the role of hormones in alternative
phenotypes is best studied by performing hormonal manipulations, or phenotypic
engineering (Ketterson and Nolan, 1992; Miles et al., 2007; Zera and Harshman,
2001). To test whether morph-dependent variation in territorial behavior in male
white-throated sparrows is attributable entirely to variation in T, Maney et al.
(2009) eliminated morph differences in T and then compared WS and TS
responses to STI in the lab. Males in nonbreeding condition received silastic
implants containing T, so that plasma levels in the WS and TS groups were
high and equal. When presented with audio playback of conspecific male song,
WS males sang significantly more often than TS males. This result suggests that
WS males respond more aggressively to a territorial challenge than TS males, even
when T levels are experimentally equalized between the morphs.
If morph differences in social behavior are not caused simply by differences
in plasma T, then our search for causal factors should turn to other aspects of HPG
function, for example, steroid binding or metabolism. The list of such factors is long
and includes a large number of receptors, enzymes, and binding globulins. Comparative genomic approaches are required to conduct large-scale comparisons of gene
expression as well as detailed analysis of the genetic differences between the morphs.

D. Mapping the ZAL2m

The early genetic work in the white-throated sparrow, done more than 35 years
ago (Thorneycroft, 1975), showed definitively that morph differences are associated with a clear, tractable chromosomal rearrangement. The ZAL2m

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Maney and Goodson

chromosome thus offers a powerful starting point for understanding the mechanisms underlying aggressive behavior in birds and other vertebrates. In essence,
nature has created a genetic manipulation that allows us to identify genes that
are affected by the rearrangement and therefore potentially causal for heightened
aggression in the WS individuals.
The identification of such genes first requires mapping of the ZAL2m
rearrangement; genes that map within it can then be evaluated as likely candidates. Using a comparative genomic approach, Thomas et al. (2008) (see also
Davis et al., 2011; Huynh et al., 2010a,b) began the initial modern genomic
characterization of the ZAL2m rearrangement. By taking advantage of the
genomic resources available for two other avian species, the chicken and the
zebra finch, they established a comparative map of ZAL2m and found that the
chromosome contains a complex rearrangement involving not one but at least
two inversions around the centromere (Fig. 5.7). The two inversions may have
occurred in succession, with the second completely contained within the first.
Alternatively, ZAL2 and ZAL2m may each represent rearranged versions of an
ancestral chromosome 2, having undergone rearrangement at different times.
The rearrangement now spans the majority of the chromosome and could
contain as many as 1000 protein-coding genes (Davis et al., 2011; Thomas
et al., 2008). Thus, although the region containing the rearrangement is large,
this work has delineated a finite set of genes linked to the behavioral and
plumage polymorphisms in this species.

Presumed
ancestral/intermediate

2m
Figure 5.7. Model for the ZAL2m rearrangement. A minimum of two pericentric inversions,
represented by the pairs of dashed lines, are hypothesized to have led to the ZAL2/2m
polymorphism. ZAL2 (top) and ZAL2m (bottom) are shown along with a hypothetical
chromosomal arrangement (middle) that could be either ancestral to both the ZAL2
and ZAL2m or an intermediate arrangement. Centromeres are represented by filled
circles. Dark and light boxes represent segments originating on the short and long arms
of the presumed ancestral chromosome, respectively. Free recombination between the
ZAL2 and ZAL2m is limited to the tip of the short arm (hatched boxes).

5. Neurogenomic Mechanisms of Aggression in Songbirds

109

Exactly how does the architecture of ZAL2m affect the expression of the
genes inside the rearrangement and the proteins they encode? Inversions are
hypothesized to affect gene and protein function in two main ways. First, genes at
or near the breakpoints may be physically disrupted or otherwise directly affected
by the breakage and subsequent change in position. So far, sequencing efforts
have identified no genes physically disrupted by the ZAL2m breakpoints (Davis
et al., 2011); however, position effects may have led to functionally distinct
alleles for those nearby. For example, a cluster of genes encoding bitter taste
receptors has been separated by one of the breakpoints and now maps to different
arms of the chromosome (Davis et al., 2010). This separation, which appears to
have led to nonsynonymous variants detected between the ZAL2 and ZAL2m,
may have implications for diet and habitat selection but is unlikely to explain
morph differences in aggression and parenting.
The behavioral polymorphisms in social behavior in this species are more
likely related to a second important consequence of pericentric inversions, which
is the suppression of recombination and subsequent genetic differentiation of the
inverted region. Thorneycroft (1975) observed that pairing in the ZAL2/2m
bivalent during meiosis was limited to one arm of each chromosome. Cytogenetic
mapping efforts (Davis et al., 2011; Thomas et al., 2008) suggest that single
recombination events elsewhere in the chromosome would give rise to gametes
with large duplications and deletions, thereby effectively preventing the inheritance of the recombined chromosomes. ZAL2m may therefore be largely isolated
from ZAL2. Population genetics studies have confirmed differentiation between
the ZAL2 and ZAL2m over the entire rearranged region as a result of suppression of
recombination (Huynh et al., 2010a; Thomas et al., 2008). Alleles are shared
between the haplotypes only at the tip of the short arm of ZAL2/2m, which is
outside the rearrangement (Fig. 5.7). The rearrangement itself contains a unique
set of alleles that are not shared with ZAL2an estimated 3000 fixed differences
(Davis et al., 2011), and this set is inherited together. Thus, the lack of gene flow
between the ZAL2 and ZAL2m has provided opportunity for the evolution of
functionally distinct alleles that are restricted to one arrangement or the other. In
the continuing analysis of the rearrangement, we should expect to find a series of
genes, inherited together as a unit in WS birds, that are functionally distinct from
the ZAL2 alleles with regard to either their protein products or patterns of
expression. Given the important role of the HPG axis in aggression in this and
other species, the strongest candidates will be closely related to HPG function.

V. FUTURE DIRECTIONS
Genetic research with comparative models will ultimately show how key genes,
the molecular functions of which are conserved across evolutionary divergence,
relate to complex and highly derived social behaviors such as aggression.

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The mechanisms that underlie social behaviors in less accessible species, such as
humans, are best studied in species that live in societies, particularly those that
can be studied in their natural habitats or under naturalistic conditions (Insel
and Fernald, 2004). The existing database on avian social behavior is unparalleledfor example, for over 4000 species, we know whether they are territorial
or colonial, socially monogamous or polygynous, migratory, or sedentary. We
have high-quality recordings of their vocalizations. No other group of animals,
invertebrate or vertebrate, has been studied with such passion and intensity.
This collective database, although it could provide profound insight into the
neuroendocrine basis of diverse social behaviors, is underutilized by neuroscientists because the availability of genomic tools has, until recently, been limited.
The recent sequencing of the zebra finch genome (Warren et al., 2010) now
makes possible unprecedented advances in our understanding of social behavior
because the resulting tools are applicable to all songbirds.
Advances in genomic technology, together with conservation of underlying mechanisms, will make it more and more feasible to bridge from wellcharacterized data-rich lab organisms, such as mice, to phenomena-rich wild
species. These species, which include fish, lizards, songbirds, and voles, are
proving to be rich resources for the analysis of social behavior and for the
development of general principles (Robinson et al., 2005). Studies with these
model organisms have demonstrated the power of a comparative approach
looking for neural or genetic differences among individuals with known behavioral differences (Bullock, 1984; Robinson, et al., 2005). The songbird model is
preferable to more typical laboratory species in the study of social behavior
because of the greater parallels with humans regarding societal structures and
hormonal bases of behavioral strategies, as well as the potential to study freeliving populations under natural conditions. Our work and that of others is
making these natural and powerful models of vertebrate behavior feasible for
genomic and neuroendocrine analysis.

Acknowledgments
The authors thank Jim Thomas for his contributions to the work described in Section IV. The
research from the authors labs was supported by NIH MH062656 to J. L. G., by NIH
1R01MH082833-01, NIH 5R21MH082046-02, and NSF IOS-0723805 to D. L. M. and the Center
for Behavioral Neuroscience.

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Genetics of Aggression in Voles

Kyle L. Gobrogge1 and Zuoxin Wang
Department of Psychology and Program in Neuroscience, Florida State
University, Tallahassee, Florida, USA

I.
II.
III.
IV.
V.

Introduction
The Prairie Vole Model
Neural Correlates
Neural Circuitry
Neurochemical Regulation of Selective Aggression
A. Neuropeptides
B. Dopamine
C. Steroid hormones
D. Classical neurotransmitters
VI. Molecular Genetics of Selective Aggression
VII. Drug-induced Aggression
VIII. Conclusions and Future Directions
Acknowledgments
References

ABSTRACT
Prairie voles (Microtus ochrogaster) are socially monogamous rodents that form
pair bondsa behavior composed of several social interactions including attachment with a familiar mate and aggression toward conspecific strangers.
1
Present address: Department of Neurobiology, Harvard Medical School, Boston,
Massachusetts, USA

Advances in Genetics, Vol. 75

Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00003-4

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Therefore, this species has provided an excellent opportunity for the study of pair
bonding behavior and its underlying neural mechanisms. In this chapter, we
discuss the utility of this unique animal model in the study of aggression and
review recent findings illustrating the neurochemical mechanisms underlying
pair bonding-induced aggression. Implications of this research for our understanding of the neurobiology of human violence are also discussed. 2011, Elsevier Inc.

I. INTRODUCTION
Mating induces aggression in several organisms throughout the animal kingdom.
Within species, patterns of inter- and intrasexual aggression vary as a function of
monogamy, parental investment, and group structure. In the wild, the appropriate coordination of social behavior is necessary for survival and reproductive
success. How organisms make decisions about which behavior to display in the
natural environment remains an important area of biological investigation. To
address these questions, previous work has relied on using traditional laboratory
rodents. However, these animals do not readily display certain types of social
behaviors and thus are not appropriate for some investigations. For example,
laboratory rats and mice do not exhibit strong social bonds between mates, and
males typically do not display paternal behavior or female-directed aggression.
Because mating naturally induces pair bonding, aggression, and biparental behavior in the socially monogamous prairie vole (Microtus ochrogaster), this
species represents a unique animal model to study the underlying neural mechanisms regulating social behavior associated with a monogamous life strategy.
In this chapter, we begin by describing the prairie vole model and
reviewing the neural correlates of pair bonding behavior. We focus on the
neuropeptides arginine vasopressin (AVP) and oxytocin; neurotransmitters dopamine (DA), gamma-aminobutyric acid (GABA), and glutamate; and steroid
hormones testosterone and estrogen in the regulation of aggression. We highlight the molecular genetics underlying courtship and aggression associated with
monogamous pair bonding in voles and humans. Finally, we speculate on the
potential for translation, of aggression studies in prairie voles, for research
examining the etiology of violence in human populationswith a particular
emphasis on the interactions between drug abuse and social behavior.

II. THE PRAIRIE VOLE MODEL

Voles are microtine (Microtus) rodents that are taxonomically and genetically
similar, yet show remarkable differences in their social behavior (Young and
Wang, 2004; Young et al., 2008, 2011a). These animals have provided an

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123

excellent opportunity for comparative studies examining social behaviors associated with different life strategies. For example, prairie (M. ochrogaster) and pine
(M. pinetorum) voles are highly social and monogamous, whereas meadow
(M. pennsylvanicus) and montane (M. montanus) voles are asocial and promiscuous (Dewsbury, 1987; Insel and Hulihan, 1995; Jannett, 1982). In the laboratory,
prairie and pine voles are biparental, with both parents equally caring for their
young, while meadow and montane voles are primarily maternal and males do
not stay in the natal nest after female parturition (McGuire and Novak, 1984,
1986; Oliveras and Novak, 1986). Following mating, prairie voles develop pair
bonds between mates (Fig. 6.1A; Young and Wang, 2004) and males even display
aggression selectively toward conspecific strangers but not toward their familiar
partner (Fig. 6.1B; Aragona et al., 2006; Gobrogge et al., 2007, 2009; Winslow
et al., 1993)behaviors that are not exhibited by promiscuous meadow or
montane voles (Insel et al., 1995; Lim et al., 2004). Interestingly, these vole
species do not differ in their nonsocial behavior (Tamarin, 1985), further
indicating associations between species-specific social behavior and life strategy
(Carter et al., 1995; Insel et al., 1998; Wang and Aragona, 2004; Young and
Wang, 2004; Young et al., 1998). Therefore, prairie voles represent a unique
model system to dissect the neural mechanisms underlying ethologically relevant
social behavior.
One behavioral index of pair bonding is selective aggression, which is
more prominent in male than in female prairie voles. It has been suggested that
selective aggression is a behavioral trait associated with mate guarding that is
important for pair bonding (Carter et al., 1995). Selective aggression is studied
using a residentintruder test (RIT) (Fig. 6.1C; Gobrogge et al., 2007, 2009;
Winslow et al., 1993; Wang et al., 1997a). A conspecific intruder is introduced
into the male resident cage and their behavioral interactions are videotaped for
510 min (Aragona et al., 2006; Gobrogge et al., 2007, 2009; Wang et al., 1997a;
Winslow et al., 1993). Subjects behavioral interactions with the intruder are
recorded and the frequency of aggressive behaviors including attacks, bites,
chases, defensive/offensive upright postures, offensive sniffs, threats, and retaliatory attacks are calculated as a composite score (Gobrogge et al., 2007, 2009) as
well as the duration of affiliative side-by-side physical contact (Gobrogge et al.,
2007, 2009; Winslow et al., 1993). It is important to note that both offensive and
defensive types of aggression are critical components of selective aggression in
male prairie voles (Wang et al., 1997a; Winslow et al., 1993).
Selective aggression is associated with mating, as cohabitation in the
absence of mating does not induce this behavior in male prairie voles (Insel et al.,
1995; Wang et al., 1997a; Winslow et al., 1993). Selective aggression is also
enduring (Aragona et al., 2006; Gobrogge et al., 2007, 2009; Insel et al., 1995)
and lasts for at least 2 weeks after partner preference formation (Aragona et al.,
2006; Gobrogge et al., 2007, 2009), even in the absence of continuous exposure

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B
100
80

Partner
Stranger

60
40
20
0

6 h Cohab

24 h Mating

Aggression (# attacks/10 min)

Contact time (min/3 h)

C
120

Naive

80

40
a

0
Stranger Partner Stranger Stranger
female
male

E
Partner

2000
Density Fos-ir (#/mm3)

Paired

Stranger

AH

Partner
Stranger

1600

OT

1200

800

OT
MeA

400
AcA

AH

MeA

Figure 6.1. Neural correlates of selective aggression. (A) After 24 h, but not 6 h, of mating, male
and female prairie voles display significantly more time in side-by-side physical contact
with an opposite sex familiar partner than with a stranger. (B) Sexually nave male
prairie voles (Nave) do not display aggression toward a stranger female, whereas 2 weeks
of sexual and social experience (Paired) induces selective aggression toward both male
and female strangers but not toward familiar female partners. (C) Photo depicts a pair
bonded male prairie vole (left) preparing to attack asexually receptivestranger
female prairie vole (right). (D) Stereological estimates reveal a significantly higher
density of Fos-ir cells in the anterior hypothalamus (AH) and medial amygdala
(MeA) of pair bonded males displaying aggression toward a stranger female (Stranger)
compared to males displaying affiliation toward their familiar female partner (Partner).
(E) Photomicrographs showing Fos-ir (dark nuclear staining) in the AH and MeA from
pair bonded males re-exposed to their familiar female partner (Partner) or to a stranger
female (Stranger). F: fornix; OT: optic tract. Bars indicate means
standard error of the
mean. Bars with different Greek letters differ significantly from each other. *p < 0.05.
Scale bar 100 mm. Adapted from Aragona and Wang (2009), Gobrogge and Wang
(2009), Gobrogge et al. (2007), Wang et al. (1997a), Winslow et al. (1993), and Young
et al. (2011a).

to a partner (Insel et al., 1995). Importantly, males display aggression not only
toward conspecific males (Fig. 6.1B; Aragona et al., 2006; Gobrogge et al., 2007,
2009; Insel et al., 1995; Wang et al., 1997a; Winslow et al., 1993) but also toward
sexually receptive females (Fig. 6.1B and C; Gobrogge et al., 2007, 2009). This
selective aggression functions to maintain monogamous pair bonds as males
reject potential female mates (Fig. 6.1B and C; Aragona et al., 2006; Gobrogge

125

6. Genetics of Aggression in Voles

et al., 2007, 2009; Wang et al., 1997a). Together, these reliably expressed and
measurable agonistic behaviors make the prairie vole an excellent model for
investigation of the neural mechanisms underlying naturally occurring aggression associated with monogamy. It should be mentioned that although female
aggression has been less studied in voles, female prairie voles exhibit similar
aggressive behavior as males and this behavior is influenced by a females social
and sexual experience (Bowler et al., 2002).

III. NEURAL CORRELATES

With considerable overlap of brain areas involved in several forms of social
(Newman, 1999) and agonistic (Table 6.1) behaviors, there is a significant
amount of ambiguity regarding which brain areas may be involved in the
regulation of selective aggression. Using a neuronal activation marker of an
immediate early gene, c-fos, previous studies in voles have examined neuronal
Table 6.1. Summary of Brain Areas Implicated in Aggression
Brain area
Anterior hypothalamus (AH)

Species
Human
Prairie vole
Rat

Syrian hamster

Lateral septum (LS)

Medial amygdala (MeA)

Nucleus accumbens (NAcc)

Ventromedial hypothalamus
(VMH)

Rat
Human
Prairie vole
Rat
Prairie vole
Mouse

References
Sano et al. (1966), Ramamurthi (1988)
Gobrogge et al. (2007, 2009), Gobrogge and
Wang (2009)
Veening et al. (2005), Kruk (1991), Bermond
et al. (1982), Kruk et al. (1984), Adams et al.
(1993), Roeling et al. (1993), Haller et al.
(1998), Veenema et al. (2006), Motta et al.
(2009)
Delville et al. (2000), Ferris and Potegal (1988),
Caldwell and Albers (2004), Ferris et al. (1997,
1989), Albers et al. (2006), Harrison et al.
(2000b), Jackson et al. (2005), Grimes et al.
(2007), Ricci et al. (2009), Schwartzer et al.
(2009), Schwartzer and Melloni (2010a,b)
Veenema et al. (2010)
Ramamurthi (1988)
Wang et al. (1997a), Gobrogge and Wang (2009)
Koolhaas et al. (1990)
Aragona et al. (2006)
Choi et al. (2005), Lin et al. (2011)

Brain structures involved in aggression, across species, with corresponding references to ground
brain area acronyms used throughout the chapter.

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Gobrogge and Wang

activity associated with aggression (Wang et al., 1997a), maternal (Katz et al.,
1999) and paternal behavior (Kirkpatrick et al., 1994), mating (Curtis and
Wang, 2003; Lim and Young, 2004), anxiety (Stowe et al., 2005), spatial learning
(Kuptsov et al., 2005), chemosensory processing (Hairston et al., 2003; Tubbiola
and Wysocki, 1997), social experience (Cushing et al., 2003a; Kramer et al.,
2006), or pharmacological challenges (Curtis and Wang, 2005b; Cushing et al.,
2003b; Gingrich et al., 1997). Within these studies, however, typically only one
type of behavior was investigated. Little focus was aimed at examining other
forms of social behavior, including affiliation or general social olfactory processing. Consequently, there is considerable overlap in brainbehavior relationships
among these studies leading to ambiguity as to which brain areas regulate
selective aggression. Nevertheless, in an early study, male prairie voles displayed
aggression toward a male intruder following 24 h of mating, but not following
24 h of cohabitation with a female without mating (Wang et al., 1997a).
However, despite their differences in sociosexual experience and in aggressive
behavior, both types of male exposure led to equal levels of Fos-ir (immunoreactivity) expression in some brain areas, such as the bed nucleus of the stria
terminalis (BNST). Males that mated for 24 h and displayed high levels of
aggression toward either a male or a female intruder showed increased levels of
Fos-ir expression in the medial amygdala (MeA; Wang et al., 1997a), compared
to males that cohabitated with a female without mating, implicating the MeA as
a brain area associated with the display of mating-induced selective aggression
(Fig. 6.1D and E).
In a more recent study, several brain areas including the BNST, medial
preoptic area (MPOA), paraventricular nucleus (PVN), and lateral septum (LS)
showed higher levels of Fos expression in pair bonded males that had experienced an RIT compared to pair bonded males not exposed to a social intruder
(Gobrogge et al., 2007). However, no group differences in Fos expression across
these brain areas were found among males that were exposed to different social
stimuli or displaying different patterns of social behavior, including aggression or
affiliation toward intruders. These data suggest that the increased neuronal
activation in these brain regions is probably due to olfactory stimulation or
general arousal associated with exposure to a conspecific, but such a response is
nonselective. A unique pattern of Fos expression was found in the anterior
hypothalamus (AH), in which exposure to a conspecific stranger, either male
or female, induced a significant increase in AH-Fos over those reexposed to their
familiar partner (Fig. 6.1D and E; Gobrogge et al., 2007). This increase in Fos
staining may indicate a stimulus-specific response. The AH appears to be more
responsive to chemosensory, tactile, and/or visual cues associated with conspecific strangers, but not familiar partners (Gobrogge et al., 2007). These data
indicate that the increased neuronal activation in the AH may be involved in
aggressive behavior displayed by pair bonded male prairie voles (Gobrogge et al.,

6. Genetics of Aggression in Voles

127

2007). This notion is corroborated by previous research documenting a critical

role of the hypothalamus in regulating aggression across several mammalian
species. For example, the ventromedial hypothalamus (VMH) in mice (Choi
et al., 2005; Lin et al., 2011) and AH in rats (Veening et al., 2005) is responsive
to conspecific chemosensory cues, which elicit aggressive behavior. Electrical
stimulation applied directly to the AH induces attack toward conspecifics in rats
(Kruk, 1991) and other animals (Albert and Walsh, 1984; Siegel et al., 1999).
Interestingly, in humans, surgical lesioning of the AH reduces physical violence
(Ramamurthi, 1988; Sano et al., 1966). In summary, data from vole studies
demonstrate that activation of the MeA and AH is associated with the display
of selective aggression (Gobrogge et al., 2007; Wang et al., 1997a).

IV. NEURAL CIRCUITRY

To directly evaluate the neural circuitry programming selective aggression, we
performed a series of tract tracing experiments focusing on the AH and MeA.
Intra-AH injections of an anterograde tracer, biotinylated dextran amine
(BDA), resulted in BDA-ir staining in several brain regions. The AH projected
to areas involved in processing chemosensory cues including the MeA; areas
important for regulating social behavior including the LS, BNST, MPOA, VMH,
and dorsal raphe (DR); and areas coordinating motor output, such as the
periaqueductal gray (Gobrogge and Wang, 2009). The AH also projected to
brain areas implicated in evaluating incentive salience including the medial
prefrontal cortex (mPFC), nucleus accumbens (NAcc), and ventral pallidum
(VP), as well as areas involved in memory formation and consolidation including
hippocampal regions CA3 and the dentate gyrus (Gobrogge and Wang, 2009).
Further, site-specific injections of a retrograde tracer, fluorogold (FG), into the
LS, NAcc, or MeA resulted in FG-ir staining in the AH, indicating reciprocal
connections between the AH and regions involved in motivation and chemosensory communication (Gobrogge and Wang, 2009).
Fos-ir staining was also used to assess neuronal activation, in this circuit,
associated with the display of pair bonding behavior. Males displaying aggression
toward an unfamiliar female showed a significantly higher density of Fos-ir in the
AH and MeA relative to males displaying affiliation toward their female partner
(Fig. 6.1D and E), replicating our previous findings (Gobrogge et al., 2007; Wang
et al., 1997a). Interestingly, we identified a MeA-AH-LS circuit that was activated when males were displaying aggression and a DR-AH circuit that was
recruited when males were displaying affiliation (Gobrogge and Wang, 2009).
The identification of these two neural circuits indicates a specific neuronal
framework associated with the choice between affiliation (DR-AH circuit) and
aggression (MeA-AH-LS circuit) in pair bonded male prairie voles.

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V. NEUROCHEMICAL REGULATION OF SELECTIVE AGGRESSION

Previous work has primarily focused on partner preference formation and documented a growing list of neurochemicals, including oxytocin (OT), AVP, corticotropin releasing hormone, DA, GABA, and glutamate, as well as their
interactions in the regulation of pair bonding behavior (Aragona et al., 2003;
Curtis and Wang, 2005a,b; Carter et al., 1995; DeVries et al., 1995; Gingrich
et al., 2000; Lim and Young, 2004; Liu and Wang, 2003; Lim et al., 2004; Liu
et al., 2001; Smeltzer et al., 2006; Wang et al., 1998, 1999; Williams et al., 1992,
1994; Winslow et al., 1993). Importantly, data from several studies indicate a
select subset of neurochemicals in the regulation of selective aggression.

A. Neuropeptides
Comparative approaches have been utilized in studies examining neuroendocrine mechanisms regulating social behavior in voles (Insel, 2010). Studies have
focused on examining the central AVP system, a nine amino acid neuropeptide
with diverse forebrain projections, across monogamous and promiscuous vole
species. AVP is an antidiuretic hormone and has been shown to stimulate three
structurally distinct receptors V1a, V1b, and V2, each activating very specific
second messenger systems (Michell et al., 1979). Classically, AVP was first
described as a primary homeostatic factor controlling kidney water reabsorption,
blood volume/pressure, and vasodilatation in the peripheral nervous system.
AVP and its receptors have been shown to be widely expressed in the central
nervous system (Thibonnier, 1992), within specific brain regions (Johnson et al.,
1993).
The V1a AVP receptor subtype (V1aR), in particular, has been extensively studied in the regulation of social behavior (Insel et al., 1994) including
aggression (Albers et al., 2006; Cooper et al., 2005; Ferris et al., 2006; Winslow
et al., 1993). V1aRs are directly coupled to stimulatory (s) Gq-11 proteins
(Thibonnier et al., 1993). Stimulation of these G-proteins leads to activation
of adenylate cyclase, cAMP, protein kinase C, and phospholipases C, A2, and D
(Raggenbass et al., 1991; Thibonnier, 1992; Thibonnier et al., 1992, 1994)
enhancing calcium influx through L-type calcium channels (Son and Brinton,
2001). Such activation enhances learning and memory in the aging brain (Deyo
et al., 1989; Yamada et al., 1996) via direct effects on gene expression (Murphy
et al., 1991).
Because AVP regulates species-specific social behaviors such as aggression (Ferris et al., 1984; Ryding et al., 2008), it was hypothesized that the
organization of central AVP systems may differ between monogamous and
promiscuous vole species (Bamshad et al., 1993b; Insel and Shapiro, 1992). To
test this hypothesis, the distribution pattern of AVP cells, fibers, and receptors

6. Genetics of Aggression in Voles

129

were mapped in the vole brain. In all vole species examined, AVP-ir neurons
were found in several brain regions, including the PVN and SON (supraoptic
nucleus) of the hypothalamus, the BNST, MeA, AH, and MPOA (Bamshad
et al., 1993b; Gobrogge et al., 2007; Wang, 1995; Wang et al., 1996). AVP-ir
fibers were localized in the LS, lateral habenular nucleus, diagonal band, BNST,
MPOA, and MeA (Bamshad et al., 1993b; Wang et al., 1996). Overall, AVP
distribution patterns were highly conserved between monogamous and promiscuous vole species (Wang, 1995; Wang et al., 1996). Dramatic species differences
in the distribution patterns and regional densities of V1aRs, however, were
observed between vole species exhibiting different life strategies (Hammock
and Young, 2002). For example, prairie voles have higher densities of V1aRs in
the BNST, VP, central and basolateral nuclei of the amygdala, and accessory
olfactory bulb, whereas montane voles exhibit a higher density of V1aRs in the
LS and mPFC (Insel et al., 1994; Lim et al., 2004; Smeltzer et al., 2006; Wang
et al., 1997c; Young et al., 1997). Further, prairie and pine voles exhibit similar
patterns of V1aR binding, which differ from that of promiscuous meadow and
montane voles (Insel et al., 1994; Lim et al., 2004). Species differences in V1aR
distribution are stable across the lifespan (Wang et al., 1997b,c) and are receptorspecific, as no species differences are found in either the benzodiazepine or opiate
receptor systems (Insel and Shapiro, 1992). In addition, monogamous prairie and
promiscuous meadow voles differ in central AVP activity during mating and
reproduction (Bamshad et al., 1993a; Wang et al., 1994). Because of these
anatomical and functional differences, central AVP was thought to underlie
selective aggression in male prairie voles (Winslow et al., 1993).
Among the neuropeptides underlying aggression (Miczek et al., 2007;
Siever, 2008), AVP, and its homolog vasotocin, have been found to regulate
several forms of aggression across species (Caldwell et al., 2008; Riters and
Panksepp, 1997) and diverse taxa (Backstrom and Winberg, 2009; Goodson,
2008). In humans, central AVP correlates with aggressive behavior (Coccaro
et al., 1998) and mediates anger (Thompson et al., 2004). Thus, the central AVP
system may have evolved to be primed by a wide variety of experiences to induce
aggression, when appropriate, in social animals (Donaldson and Young, 2008).
Because central AVP underlies territorial aggression in other rodents (Ferris
et al., 1984), AVP was proposed to regulate mating-induced aggression in prairie
voles. In a pharmacological study, injections of a V1aR antagonist (V1aR Ant)
into the lateral ventricle of male prairie voles blocked selective aggression
induced by mating whereas injections of AVP-induced aggression toward an
intruder in the absence of mating (Winslow et al., 1993). These effects were
neuropeptide specific, as intracerebroventricular (ICV) infusion of an OT receptor antagonist had no effect on mating-induced aggression (Winslow et al.,
1993). Importantly, developmental exposure to either AVP in male prairie
voles (Stribley and Carter, 1999) or OT in female prairie voles (Bales and

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Gobrogge and Wang

Carter, 2003) facilitates aggression in adulthood. Together, these data highlight

a critical role of neuropeptide regulation of prairie vole aggression. However, the
action site and release dynamics of neuropeptides in the regulation of selective
aggression were unclear.
In a more recent study, it was found that the display of selective aggression was associated with increased neuronal activation in the AH, specifically in
neurons expressing AVP (Fig. 6.2A and B; Gobrogge et al., 2007). In a previous
study in Syrian hamsters (Mesocricetus auratus), aggression has also been shown to
be associated with an increase in AVP-ir/Fos-ir double-labeled cells in the nucleus
circularis (NC), medial SON (mSON), and surrounding areas ventral to the fornix
in the AH (Delville et al., 2000). Our data, combined with previous results from
other species, suggest that the AH may be a brain area in which AVP regulates
selective aggression. Indeed, AH-AVP has been implicated in various forms of
aggressive behavior. In Syrian hamsters, for example, blockade of V1aRs in the
AH diminished offensive aggression (Caldwell and Albers, 2004; Ferris and
Potegal, 1988) whereas intra-AH administration of a V1aR agonist enhanced
aggressive behavior (Caldwell and Albers, 2004; Ferris et al., 1997). More recently,
the density of V1aRs in the AH has been found to increase significantly in Syrian
hamsters after their display of offensive aggression (Albers et al., 2006).
Because selective aggression was associated with neuronal activation in
the AH, specifically in AVP-containing neurons (Fig. 6.2A and B; Gobrogge et al.,
2007), we tested the hypothesis that selective aggression is associated with AHAVP release. In vivo brain microdialysis, with ELISA, was performed on male
prairie voles that were pair bonded for 2 weeks. Pair bonded males displayed
significantly higher levels of aggression toward novel females but more side-byside affiliation with their familiar female partner (Gobrogge et al., 2009). ELISA
analysis indicated that exposure to a stranger female, compared to a familiar
partner, increased AH-AVP release (Fig. 6.2C), which is further confirmed by
correlation analyses indicating that AH-AVP release was coupled positively with
aggression and negatively with affiliation (Gobrogge et al., 2009). Moreover, intraAH administration of AVP at a high (500 ng/side), but not a low (5 ng/side), dose
in sexually nave males induced aggression toward a novel female, and this effect
was mediated by V1aR as concurrent administration of a 10-fold higher dose of a
V1aR Ant blocked AVP-induced aggression (Fig. 6.2D; Gobrogge et al., 2009).
Further, intra-AH infusions of a V1aR Ant (5 mg/side), in pair bonded males,
blocked aggression and facilitated social affiliation toward novel females
(Fig. 6.2D; Gobrogge et al., 2009). Thus, AH-AVP is both necessary and sufficient
to regulate mating-induced selective aggression in male prairie voles.
Prior research has shown that the social environment has a significant
impact on signaling and structural components of AVP systems in the brain. In
marmoset monkeys, for example, prefrontal V1aR increases during fatherhood
(Kozorovitskiy et al., 2006). In hamsters, several social and drug paradigms have

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6. Genetics of Aggression in Voles

B
F

AH

6
4
a

2
0

Partner

Paired

30

Naive

20

AH
a
a
CSF

AVP

AVP+
V1aR Ant

CSF V1aR Ant

100
50

Partner Stranger
female

10

*
150

Stranger Stranger
female
male

E
40 Naive

200

OT

Control

D
Aggression (# attacks/10 min)

Paired

Aggression (# attacks/10 min)

AVP-ir/Fos-ir cells (density)

10

AVP release (% baseline)

80

60

40

20

Control AAV-V1aR

Figure 6.2. Vasopressin (AVP) regulation of selective aggression. (A) Pair bonded male prairie voles
that display aggression toward female or male strangers exhibit a significantly higher
density of AVP-ir/Fos-ir double-labeled cells in the AH relative to pair bonded males
re-exposed to their female partner or to males not exposed to any social stimulus
(Control). (B) Photomicrograph of AVP-ir cell bodies and fibers (brown cytoplasmic
staining), Fos-ir (dark nuclear staining), or AVP-ir/Fos-ir double labeled cells (insert) in
the anterior hypothalamus (AH). (C) In vivo brain microdialysis reveals a significant
increase in AH-AVP release in pair bonded male prairie voles displaying aggression
toward a stranger female compared to males reexposed to their female partner. (D) IntraAH AVP microinfusion, in sexually nave males (Nave), is sufficient to induce aggression toward a stranger female compared to control males infused with cerebral spinal
fluid (CSF). AH-AVP-induced aggression is blocked with concurrent administration of
AVP with a V1aR Ant. Pair bonded males (Paired) display aggression toward stranger
females, which is blocked by intra-AH infusion of a V1aR Ant. (E) Pair bonded males
(Paired) exhibit a significantly higher density of AVP-V1a receptor (V1aR) binding in
the AH relative to sexually nave males (Nave). (F) Sexually nave males infused with
an adeno-associated virus expressing the V1aR gene (AAV-V1aR) in the AH exhibit
enhanced aggression toward stranger females relative to males infused with the
LacZ-gene (Control). F, fornix; OT, optic tract. Bars indicate means
standard error
of the mean. Bars with different Greek letters differ significantly from each other.
*p < 0.05. Scale bars 100 mm, insert scale bars 10 mm. Adapted from Aragona et al.
(2006), Gobrogge et al. (2007, 2009), and Young et al. (2011a).

been shown to directly alter the AH-AVP system to regulate offensive aggression
(Ferris et al., 1989; Grimes et al., 2007; Harrison et al., 2000b; Jackson et al.,
2005). In a previous study in male prairie voles, cohabitation with a female

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significantly increased the number of AVP mRNA labeled cells in the BNST
(Wang et al., 1994). Because social isolation increases the density of V1aRs in
the AH to regulate offensive aggression in golden hamsters (Albers et al., 2006),
we tested the hypothesis that the density of AH-V1aR changes with pair bonding
experience to engage selective aggression. Pair bonded males showed higher
densities of V1aR binding, site specifically, in the AH (Fig. 6.2E), with no
change in OT receptor binding, demonstrating that pair bonding experience
induces a neural plastic reorganization of V1aRs in a region- and receptorspecific manner (Gobrogge et al., 2009). To determine whether this increase in
V1aR density in the AH, following pair bonding, was directly related to the
emergence of aggression toward novel females, we used viral vector mediated
gene transfer to artificially elevate V1aR density in the AH. Males that received
intra-AH infusions of the AAV-V1aR displayed higher levels of aggression
toward a novel female compared to control males that received infusions of the
LacZ-gene (Fig. 6.2F; Gobrogge et al., 2009). Similar viral vector mediated
increases in V1aR expression in the VP in voles (Lim et al., 2004; Pitkow
et al., 2001) and LS in mice (Bielsky et al., 2005) enhanced affiliation. In male
rats, intermale aggression correlates with AVP release in the LS while AVP
release in the BNST is inversely related to aggression levels (Veenema et al.,
2010). Together, these data support the notion that region-specific AVP functioning regulates specific types of social behaviors, and multiple brain regions
serve as a circuit in which AVP coordinates a range of adaptive behaviors
important for reproductive success.

B. Dopamine
Anatomically, central DA is divided into three distinct pathways: nigrostriatal,
incertohypothalamic, and mesocorticolimbic. DA cell bodies projecting from
the substantia nigra synapse in the dorsal striatum and comprise the nigrostriatal
path (Swanson, 1982). Incertohypothalamic paths extend from DA cell bodies of
the A1214 cell groups and project to the MPOA and PVN (Cheung et al.,
1998). The mesocorticolimbic path represents DA cell bodies originating in the
ventral tegmental area (VTA; Fig. 6.3C) projecting to the mPFC and NAcc
(Fig. 6.3C; Carr and Sesack, 2000; Swanson, 1982). In addition, DA cells in the
AH (Fig. 6.3B) project to forebrain areas including the striatum, LS, NAcc, and
mPFC (Alcaro et al., 2007; Lindvall and Stenevi, 1978; Maeda and Mogenson,
1980).
DA preferentially binds to two families of receptors: D1-like and D2like. Both types of DA receptors are found in the mPFC, NAcc, LS, and MeA
(Boyson et al., 1986). D1-like receptors are directly coupled to both stimulatory
(s) Ga and Gaolf proteins (Neve et al., 2004). Stimulation of these G-proteins
leads to activation of adenylate cyclase, cAMP, and protein phosphatase-1

133

6. Genetics of Aggression in Voles

20

AH

15

a
Control

OT
Partner

Stranger Stranger
female
male

D
DAR binding (optical density)

TH-VTA

10

TH-NAcc

E
200

*
160

Naive
Naive
Paired

120
80

NAcc

40
0
D1R

D2R

Paired

Aggression (# attacks /10 min)

TH-ir/Fos-ir cells (density)

40
30

20
a

10
a
0

CSF
CSF D2R Ant D1R Ant
partner stranger stranger stranger

Figure 6.3. Dopamine (DA) regulation of selective aggression. (A) Pair bonded male prairie voles
that display aggression toward female or male strangers exhibit a significantly higher
density of TH-ir/Fos-ir double-labeled cells in the AH relative to pair bonded males reexposed to their female partner or to males not exposed to any social stimulus (Control).
(B) Photomicrograph of TH-ir cell bodies and fibers (brown cytoplasmic staining), Fos-ir
(dark nuclear staining), or TH-ir/Fos-ir double labeled cells (insert) in the anterior
hypothalamus (AH). (C) Photomicrograph of TH-ir fibers in the nucleus accumbens
(NAcc) and neurons in the ventral tegmental area (VTA). (D, E) Pair bonded males
(Paired) exhibit a significantly higher density of DA D1-like (D1R), but not D2-like
(D2R), receptor binding in the NAcc compared to sexually nave males (Nave). (F)
Pair bonded males, infused with CSF in the NAcc, display aggression toward a stranger
female but not toward their female partner. Concurrent infusion of CSF with a DA D1R
antagonist (D1R Ant), but not D2R antagonist (D2R Ant), in the NAcc is sufficient to
attenuate pair bonding-induced aggression toward a stranger female. F, fornix; OT, optic
tract. Bars indicate means
standard error of the mean. Bars with different Greek letters
differ significantly from each other. *p < 0.05. Scale bars 100 mm, insert scale
bars 10 mm. Adapted from Aragona et al. (2006), Gobrogge et al. (2007, 2009), and
Young et al. (2011a).

inhibitor DARP-32 (Neve et al., 2004). Conversely, D2-like receptors couple to

inhibitory (i) Ga proteins and, when activated, downregulate adenylate cyclase,
cAMP, and protein phosphatase-1 inhibitor DARP-32 (Neve et al., 2004). D1receptor stimulation plays a critical role in calcium influx, via L-type calcium
channels, which is important for cellular long-term potentiation facilitating
learning and memory in the aging brain (Deyo et al., 1989; Yamada et al.,
1996) through direct influences on gene expression (Murphy et al., 1991).

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Because mesocorticolimbic DA underlies partner preference formation

(Aragona and Wang, 2009; Aragona et al., 2003; Gingrich et al., 2000; Gobrogge
et al., 2008; Wang et al., 1999), studies focused on examining the potential role
of central DA regulating selective aggression (Gobrogge et al., 2008). Pair
bonded male prairie voles have significantly higher levels of DA D1-type receptors (D1Rs), but not D2-type receptors (D2Rs), in the NAcc (Fig. 6.3D and E;
Aragona et al., 2006). Males that cohabitated with a female for 24 h, with or
without mating, did not exhibit an increase in D1Rs in the NAcc, supporting the
idea that upregulation of NAcc D1Rs, after pair bonding, may directly regulate
selective aggression. To test this notion, pair bonded male prairie voles were
injected with a D1R antagonist (D1R Ant) into the NAcc. NAcc-D1R, not D2R
(D2R Ant), antagonism was sufficient to block selective aggression in pair
bonded male prairie voles (Fig. 6.3F; Aragona et al., 2006). In other work,
both brief and extended cohabitation with unfamiliar conspecifics in female
prairie voles significantly increased the number of DA-ergic cells in the BNST
and MeA (Cavanaugh and Lonstein, 2010) and blocking D2Rs, during development, decreased aggression-related behavior including infanticide in adult
female, but not male, prairie voles (Hostetler et al., 2010). Further, pair bonded
male prairie volesdisplaying aggression toward either male or female intruders,
had a significantly higher density of cells in the AH that were double-labeled for
tyrosine hydroxylase-ir (THrate-limiting enzyme in DA biosynthesis) and Fosir than males not exposed to a social stimulus or males that were re-exposed to
their familiar female partner (Fig. 6.3A and B), implicating AH-DA involvement in selective aggression (Gobrogge et al., 2007).

C. Steroid hormones
Physical aggression is significantly more common in males than females and
these behavioral sex differences have been observed across many species
(Gatewood et al., 2006). Research describing biological contributions underlying
these sex differences has focused primarily on steroid hormones (Gatewood et al.,
2006). Several studies have examined the role of androgens in the development
of aggressive behavior, both organizationally (e.g., treatment with prenatal
testosterone) and activationally (e.g., treatment with postnatal testosterone).
Previous research has found that prenatal androgen exposure increases the
behavioral expression of adult aggression (Michard-Vanhee, 1988; Vale et al.,
1972). Although organizational and activational influences of androgen on
aggression have been noted, some inconsistent results have been reported. For
example, castration in male rats (Koolhaas et al., 1990) and male prairie voles
(Demas et al., 1999) has no affect on aggression. Thus, circulating testosterone,
alone, cannot solely contribute to the expression of aggressive behavior in all
rodent species. However, these findings do not rule out the possible effects of

6. Genetics of Aggression in Voles

135

testosterone having organizational influences on other neurochemical systems in

the brainwhich, together, may regulate aggression in adulthood. Thus,
neurochemicalsteroid hormone interactionsunderlying aggressionhave
also been examined. For example, AVP administered directly into the MeA
facilitates territorial aggression in male rats and is sufficient to block the effects of
castration on reducing aggression (Koolhaas et al., 1990). Further, castration
(Bermond et al., 1982), but not ovariectomy (Kruk et al., 1984), decreases the
excitability of neurons in the AHblocking electrically induced aggression,
which in castrates can be reversed by testosterone treatment (Bermond et al.,
1982). Therefore, circulating testosterone may be acting as a potent neuromodulatorinteracting with neurochemicals, like AVP, to regulate aggression.
Additional evidence demonstrating steroid hormoneneurotransmitter
interactions exists in research investigating central DA. For example, 75% of
TH-ir expressing cells in the hamster posterior MeA contain androgen receptors,
are DA-ergic (i.e., they do not co-label with DA beta hydroxylase), and are
highly influenced by gonadal hormones compared to TH-ir cells found in the
anterior MeA (Asmus and Newman, 1993; Asmus et al., 1992). Interestingly,
this same group of TH-ir cells is found in the posterior MeA and BNST in male
prairie voles, which appears to be influenced by testosterone (Northcutt et al.,
2007) and activated after mating and social experience (Northcutt and Lonstein,
2009). Together, these data suggest interactions between steroid hormones and
central DA, in areas such as the MeA, in processing chemosensory cues related to
social communication.

D. Classical neurotransmitters
In addition to the effects of neurotransmitters and hormones on aggression,
neuromodulators such as GABA and glutamate have also been shown to be
involved in the display of agonistic behavior. For example, microinjection of a
GABA antagonist (Adams et al., 1993; Roeling et al., 1993) with concurrent
treatment of a glutamate agonist (Haller et al., 1998) in the AH facilitates attack
behavior in rodentswith higher doses having greater behavioral effects. Further, reverse microdialysis infusion with a glutamate agonist and a GABA-A
antagonist into the AH of rats, recently having experienced an agonistic
encounter, also facilitates aggression (Haller et al., 1998). Finally, it is worth
mentioning that neuromodulators in the VTA, which provides the major
source of DA projections to the NAcc (Fig. 6.3C) and mPFC, are also involved in pair bonding behavior. Glutamate and GABA receptor blockade in
the VTA, which alters DA activity in the NAcc, induces partner preference
formation in the absence of mating in male prairie voles (Curtis and Wang,
2005b).

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VI. MOLECULAR GENETICS OF SELECTIVE AGGRESSION

Monogamous male prairie voles carry several repetitive microsatellite DNA
sequences in the promoter region of the V1aR gene that are not found in
promiscuous male voles (Hammock and Young, 2002, 2004; Young, 1999).
These genetic differences directly contribute to species differences in social
organization (Landgraf et al., 2003; Lim et al., 2004; Pitkow et al., 2001). Further,
mice carrying a transgene coding for the prairie vole V1aR exhibit central V1aR
patterns similar to prairie voles and, when injected with AVP, display enhanced
social affiliation (Young et al., 1999). Male voles injected in the VP, with a virus
expressing V1aR, display enhanced partner preference in the absence of mating
(Lim et al., 2004; Pitkow et al., 2001). Interestingly, individual variability in the
genetic sequences coding V1aRs has revealed remarkable within species differences in the strength of monogamous pair bonds in prairie voles (Hammock and
Young, 2005; Ophir et al., 2008).
Because prairie voles carry varying lengths of DNA to code V1aRs
(Hammock and Young, 2005), this genomic predisposition enables their brain
to dynamically express V1aRs after sociosexual experience. This genetic loading
distinguishes prairie voles from traditional laboratory rodents that lack this
genetic makeup. Future work would benefit from comparing aggression levels
between male prairie voles carrying long versus short versions of the promoter
region encoding the V1aR gene. In humans, polymorphisms in the promoter
region encoding V1aR are associated with differences in sociosexual bonding
behaviors (Prichard et al., 2007; Walum et al., 2008) including altruism (Israel
et al., 2008) and deficits in social communication observed in individuals with
autistic spectrum disorders (Israel et al., 2008; Kim et al., 2002; MeyerLindenberg et al., 2008). To date, no study has examined potential associations
between the V1aR gene and patterns of aggression in humans. Thus, it would be
interesting to examine polymorphisms in the V1aR gene in patients with a
lifetime history of pathological violence, as the V1aR system may harbor susceptibility genes underlying extreme forms of aggression, increasing the prevalence
of homicide and suicide in human populations.

VII. DRUG-INDUCED AGGRESSION

The prairie vole has been established as an animal model for depression related to
social separation (Bosch et al., 2009; Grippo et al., 2007). Further, chronic metal
ingestiona potential model for autismproduces social avoidance in male, but
not female, prairie voles exposed to unfamiliar same-sex conspecific strangers
(Curtis et al., 2010), suggesting a developmental mechanism underlying the social

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137

deficits associated with autistic spectrum disorders in humans. Recently, prairie

voles have also been utilized to examine the effects of drugs of abuse on pair
bonding behavior (Gobrogge et al., 2009; Liu et al., 2010; Young et al., 2011b).
Drug addiction is a significant problem for many humans because drug
abuse has such a powerful control over social behavior essential for survival
(Kelley and Berridge, 2002; Nesse and Berridge, 1997; Panksepp et al., 2002). In
humans, substance abuse has been associated with weapon-related violence and
homicide (Hagelstam and Hakkanen, 2006; Madan et al., 2001; Spunt et al.,
1998), intimate partner aggression, including partner-directed physical and
psychological aggression (Chermack et al., 2008; OFarrell and Fals-Stewart,
2000), sexual (El-Bassel et al., 2001), and child abuse (Haapasalo and
Hamalainen, 1996; Mokuau, 2002; Walsh et al., 2003). Collectively, drugrelated violence leads to family system dysfunction and incarceration (Krug
et al., 2002), creating significant societal concerns. While aggression research
in humans has provided valuable information regarding relationships between
drug abuse and violence, animal models have been used to examine neural
mechanisms underlying drug-induced aggression.
Drug use can override neurobiological programs to activate maladaptive
forms of agonistic behavior, engaging inappropriate types of physical aggression
(Swartz et al., 1998) such as domestic violence (Moore et al., 2008) and intimate
partner homicide (Farooque et al., 2005). As a result, chronic drug abuse can
cause permanent neural reorganization (Nestler and Aghajanian, 1997; White
and Kalivas, 1998), impairing the adaptivesocial brain (Panksepp et al., 2002),
leading to the display of maladaptive social behavior (Wise, 2002). Multiple
studies have demonstrated that aggression may be altered shortly after drug
exposure and that the directionality of these effects depends on drug, dose, and
individual differences between subjects.
Repeated exposure to several drugs of abuse, during adolescence or
adulthood, persistently enhances agonistic behaviors, specifically those associated with offensive aggression. For example, Syrian hamsters treated during
adolescence with cocaine (DeLeon et al., 2002a; Harrison et al., 2000a; Jackson
et al., 2005; Knyshevski et al., 2005a,b; Melloni et al., 2001) or anabolic-androgenic steroids (AASs) (DeLeon et al., 2002b; Harrison et al., 2000b; Melloni and
Ferris, 1996; Melloni et al., 1997) display enhanced offensive aggression in
adulthood. Interestingly, these drug experiences reorganize AVP (Grimes et al.,
2007; Harrison et al., 2000b; Jackson et al., 2005), DA (Ricci et al., 2009;
Schwartzer et al., 2009), and GABA (Schwartzer et al., 2009) signaling in
the AH.
For example, when compared with nonaggressive sesame oil-treated
control males, aggressive AAS-treated males exhibit significant neuroplastic
changes in the AH including increased AVP-ir fiber density and AVP content
(Harrison et al., 2000b), an increase in TH-ir cell and fiber density (Ricci et al.,

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Gobrogge and Wang

2009), enhanced DA-D2R expression (Schwartzer et al., 2009), a higher number

of GAD67-ir cells (Schwartzer et al., 2009), and decreased GABAA receptor
expression (Schwartzer et al., 2009). Further, pharmacological blockade of D2
(Schwartzer and Melloni, 2010a,b), but not D5 (Schwartzer and Melloni,
2010b), DA receptors in the AH abolishes these effects. Together, results from
this work suggests that AVP and DA signaling facilitates aggression by GABA
inhibition in the AH of AAS-treated male Syrian hamsters.
As noted above, previous work has shown that exposure to drugs of
abuse, such as cocaine, enhances malemale aggression by reorganizing the AHAVP system in hamsters (Jackson et al., 2005). Therefore, we tested the hypothesis that amphetamine (AMPH), another commonly abused psychostimulant,
would act in a similar fashion in affecting male-to-female aggression in prairie
voles. Because our recent data revealed that repeated AMPH treatment(1 mg/
kg) for 3 consecutive daysinduces a conditioned place preference (Aragona
et al., 2007) and blocks mating-induced partner preference (Fig. 6.4A; Liu et al.,
2010), this treatment regimen was used. To examine the selectivity of AMPHinduced aggression, males treated with saline or AMPH were tested for aggression toward an unfamiliar female or a familiar female (that cohabitated with a
male across a wire mesh screen for 24 h without mating). Compared with salinetreated controls, AMPH-treated males displayed significantly higher levels of
aggression toward either familiar or unfamiliar females (Fig. 6.4B), indicating
that AMPH exposure induces generalized aggression, rather than being selective
to novel females. This AMPH treatment also induced an increase in the density
of AVP-V1aR binding in the AH, but not MPOA, relative to saline control
males (Fig. 6.4C). Further, intra-AH infusions of CSF containing the V1aR Ant,
but not CSF alone, diminished AMPH-induced aggression toward novel females
(Fig. 6.4D). These data suggest that repeated exposure to AMPH can induce
female-directed aggression and that this behavior is mediated by AH-AVP.
Interestingly, these behavioral effects coincide with upregulation of D1Rs in
the NAcc (Liu et al., 2010) and V1aRs in the AH (Gobrogge et al., 2009)
which both facilitate aggression toward novel females (Aragona et al., 2006;
Gobrogge et al., 2009); indicating that drugs of abuse can hijack neuroplasticity
evolved to maintain monogamous pair bonds.

VIII. CONCLUSIONS AND FUTURE DIRECTIONS

Prairie voles have provided an excellent model system to study the neurobiology
of ethologically meaningful aggression associated with monogamous pair bonds.
Aggression can be easily manipulated under laboratory conditions and reliably
expressed following mating and social cohabitation. Several brain areas: MeA,
AH, and NAcc, work in a neural circuit to regulate selective aggression via AVP

139

6. Genetics of Aggression in Voles

80

40

**

Partner
Stranger

**

60
40
20
0

Intact

Frequency of aggression

Side-by-Side contact (min/3 h)

100

1.0

Unfamiliar

30

20

10

0
0.0

Familiar

5.0

Saline

AMPH

AMPH (mg/kg)

D
30
25

30

Saline

*
Frequency of aggression

V1aR binding (optical density)

AMPH

20
15
10
5
0

25
20
15
10
5
0

MPOA

AH

CSF

V1aR Ant

Figure 6.4. Drug experience impairs pair bonding behavior. (A) Pair bonded (Intact) and saline
treated (0.0) male prairie voles, receiving 3-dayonce daily; repeated injections, spend
significantly more time in physical side-by-side contact with their familiar female
partner than with an unfamiliar stranger female. Pair bonded males injected (i.p.,
intraperitoneal) with 1.0 or 5.0 mg/kg amphetamine (AMPH) spent equal amounts of
time in physical side-by-side contact with their female partner as with a stranger female.
(B, C) Repeated AMPH exposure, in sexually nave males, increases aggression toward
both familiar and unfamiliar females and enhances the density of vasopressin (AVP)
receptor (V1aR) expression in the anterior hypothalamus (AH) but not in the medial
preoptic area (MPOA). (D) Site-specific microinfusion of an AVP-V1aR antagonist
(V1aR Ant) into the AH, of males receiving 3-day repeated AMPH exposure (i.p.),
significantly decreases AMPH-induced aggression toward novel females relative to
males receiving intra-AH infusions of cerebral spinal fluid (CSF). Bars indicate means
standard error of the mean. Bars with different Greek letters differ significantly from
each other. *p < 0.05; **p < 0.01. Adapted from Gobrogge et al. (2009), Liu et al.
(2010), and Young et al. (2011a).

and DA. Commonly abused drugs, like AMPH, can usurp these neurochemical
circuits to engage maladaptive social behavior impairing monogamous pair
bonds.

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Although male-to-male aggression has been studied in a variety of

mammals, we know surprisingly little about male-to-female aggression and its
underlying neuromechanisms. Interestingly, pair bonded male prairie voles naturally display aggression toward conspecific females but not toward their female
partner and, therefore, selective aggression allows for investigation of the neurobiology of male-to-female aggression. Data have demonstrated that this form of
selective aggression is mediated by elevated AVP release and increased V1aR
expression in the AHpriming male prairie voles to respond aggressively to
novel females. In addition, data have also shown that the same AH-AVP system
mediates generalized, female-directed aggression induced by AMPH. Together
with previous research from other animals (Ferris et al., 1989, 1997; Grimes et al.,
2007; Harrison et al., 2000b; Jackson et al., 2005; Veenema et al., 2006), these
data demonstrate a unique point of convergence in the mammalian brain (Choi
et al., 2005; Motta et al., 2009). The AH-AVP system is highly conserved and
functions to control different forms of aggression to maintain a wide range of
resources important for reproductive success. These highly evolved neuropeptide
systems appear to be extremely vulnerable to drugs of abuse, as our data show that
hypothalamic AVP controls both naturally occurring as well as drug-facilitated
female-directed aggression, suggesting that psychostimulant drugs, like AMPH,
are capable of switching adaptive (functional) forms of aggression (e.g., mate
guarding) to aberrant (dysfunctional) forms of violent behavior (e.g., partnerdirected aggression). Together, these data demonstrate the utility of the prairie
vole model for evaluation of the effects of drug abuse on neural systems
controlling adaptive forms of aggressionsuch as mate guarding.
Finally, because other neurochemicals, such as DA (Aragona et al.,
2006) and serotonin (Villalba et al., 1997), also regulate selective aggression in
prairie voles, offensive aggression related to drug experience (Tidey and Miczek,
1992) and AVP/5-HT interactions mediate aggression in other rodents (Ferris
et al., 1997; Veenema et al., 2006), future studies should examine potential
neurochemical interactions in the regulation of selective aggression. By understanding the basic neuroendocrinology of pair bonding in prairie voles, we may
eventually be able to better clarify the neural chemistry of mental health deficits
associated with aberrations in social behavior in patients suffering from drug
addiction or pathological violence.

Acknowledgments
The authors would like to thank Benjamin William Tyson for critically reading this manuscript.
The work reviewed in this chapter was supported by National Institutes of Health grants MHF3179600 to K. L. G., MHR01-58616, MHR01-89852, DAR01-19627, and DAK02-23048 to Z. X. W.,
and NIH Program Training Grant T32 NS-07437.

6. Genetics of Aggression in Voles

141

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498515.

The Neurochemistry of Human

Aggression
Rachel Yanowitch and Emil F. Coccaro
Clinical Neuroscience Research Unit, Department of Psychiatry, The University
of Chicago Pritzker School of Medicine, Chicago, Illinois, USA

I.
II.
III.
IV.
V.
VI.
VII.

Introduction
Serotonin
Dopamine
Norepinephrine (Noradrenaline)
GABA
Peptides
Conclusion
References

ABSTRACT
Various data from scientific research studies conducted over the past three decades
suggest that central neurotransmitters play a key role in the modulation of
aggression in all mammalian species, including humans. Specific neurotransmitter
systems involved in mammalian aggression include serotonin, dopamine, norepinephrine, GABA, and neuropeptides such as vasopressin and oxytocin. Neurotransmitters not only help to execute basic behavioral components but also serve
to modulate these preexisting behavioral states by amplifying or reducing their
effects. This chapter reviews the currently available data to present a contemporary view of how central neurotransmitters influence the vulnerability for aggressive behavior and/or initiation of aggressive behavior in social situations. Data
reviewed in this chapter include emoiric information from neurochemical,
pharmaco-challenge, molecular genetic and neuroimaging studies. 2011, Elsevier Inc.
Advances in Genetics, Vol. 75
Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00005-8

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I. INTRODUCTION
Since the late 1970s, data from scientific research studies have suggested that
endogenous brain chemicals called neurotransmitters play a key role in the
modulation of aggression. Human aggression is a multidimensional behavior
that is determined by an amalgamation of biological, genetic, environmental,
and psychological factors. Neurotransmitters not only help to execute these basic
behavioral components but also serve to modulate these preexisting behavioral
states by amplifying or reducing their effects. Genetic abnormalities in a number
of neurotransmitter pathways have been implicated in aggression-related disorders. Current and future research aims to understand how these neurotransmitters function both normally and abnormally to mediate aggression and other
human behaviors. With the evolution of genetic testing and continued development of neuroimaging technologies such as functional magnetic resonance
imaging (fMRI) and positron emission tomography (PET) scanning, the ability
of the scientific researcher to investigate the brains constellation of synapses and
neurotransmitters is growing ever more proficient. While it is clear from these
studies that neurotransmitters contribute significantly to the predisposition of an
individual toward aggressiveness, whether neurotransmitter dysfunction alone is
sufficient to cause violent aggression remains unclear.
Aggression may be impulsive or premeditated in nature. In the former
case, impulsivity defines, or describes, the aggression. That is, it is the aggression
that is impulsive not that the person is aggressive and at other times impulsive,
though that may be true as well. Diagnoses associated with impulsive aggression
include Intermittent Explosive Disorder (IED) characterized by frequent and
problematic impulsive aggressive outbursts, and Borderline Personality Disorder
(BPD) characterized by instability in self-image, in interpersonal relationships as
well as impulsivity and affect (including anger and aggression). In the latter case,
the aggression is planned and carried out in order to achieve some tangible goal.
Diagnoses associated with this type of aggression include Antisocial Personality
Disorder (AsPD) which is characterized by a pattern of disregard for, and violation of, the rights of others. These types of aggression are not mutually exclusive,
however, and some individuals display both types of aggression at different times.

II. SEROTONIN
Serotonin or 5-hydroxytryptamine (5-HT) is a multipurpose monoamine neurotransmitter derived from the amino acid, L-tryptophan, and has been implicated
as an important regulator of mood (Kumar et al., 2010; Kunisato et al., 2010;
Ruhe et al., 2007), appetite (Curzon, 1991; Dourish, 1995; Lam et al., 2010),
gastrointestinal muscle contractility (Gershon, 2004; Xu et al., 2007), self-

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153

injurious behavior (Peddeer, 1992), and sleep (Monti, 2010; Monti and Jantos,
2008; Monti and Monti, 2000). With respect to aggression and other behavioral
disorders, serotonin action is highly complex and varies depending upon which
receptor it is bound to, how much 5-HT is available in the synapse, how much
enzymatic activity is present, and whether other agonists or antagonists are
available for competitive binding. Both the clinical and molecular data on
central 5-HT function in the mammalian brain overwhelmingly suggests that a
reduction in 5-HT activity in emotion-modulating brain regions such as the
prefrontal cortex and the anterior cingulate cortex leads to a predisposition for
impulsive aggressiveness (New et al., 2002; Parsey et al., 2002; Seo et al., 2008;
Siever et al., 1999). Research suggests that 5-HT significantly contributes to the
genetically determined differences seen in individuals and that its primary
mechanism of action is via the genes encoding major components of 5-HT
viability in the brain such as the enzymes tryptophan hydroxylase-1 and monoamine oxidase A (MAOA) (Popova, 2008). Most of the literature discussing 5HT regulation of aggression focuses on 5-HT metabolite levels and the functional state of 5-HT receptors.
The first literature written on serotonin and impulsive aggressive behavior in human subjects came from two independent research groups (Asberg
et al., 1976; Sheard et al., 1976) in 1976. Sheard et al. reported that administration of the putative 5-HT-enhancing agent, lithium carbonate, significantly
reduced impulsive aggressive behavior in a prison inmate population. Asberg
et al. found that lower concentrations of lumbar CSF 5-hydroxyindoleactic acid
(5-HIAA), the most stable 5-HT metabolite in the brain, were correlated with
violent and suicidal behavior. In 1979, Brown et al. studied 26 males with
significant personality disorder traits (Brown et al., 1979). CSF amine metabolite
levels of serotonin (5-HIAA), norepinephrine (3-methoxy-4-hydroxy-phenylglycol, MHPG), and dopamine (homovanillic acid, HVA), respectively, were
studied. CSF 5-HIAA was significantly negatively correlated with aggression
(r  0.78), and MHPG was significantly positively correlated with aggression
(r 0.64). Brown et al. replicated this finding for CSF 5-HIAA and extended
these findings to include other measures of aggression such as psychopathic
deviance (i.e., defiance of authority and impulsivity) (Brown et al., 1982;
Coccaro and Siever, 2002). Despite the fact that a number of subsequent studies
supported the findings of an inverse relationship between aggression and CSF
5-HIAA levels (Kruesi et al., 1990; Lidberg et al., 1985; Limson et al., 1991;
Linnoila et al., 1983), additional reports also suggest a direct (Castellanos et al.,
1994; Moller et al., 1996; Prochazka and Agren, 2003) or no relationship
(Coccaro et al., 1997c; Gardner et al., 1990) between the two. In a recent
paper by Coccaro et al., the authors were able to reconcile the disputed data by
reconsidering the CSF 5-HIAA levels in the context of (1) the severity of the
aggression of the individual and (2) the CSF HVA levels present concomitantly

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(Coccaro and Lee, 2010). Under this new paradigm, the results emerged against
Browns preliminary findings: CSF 5-HIAA concentrations varied directly with
aggression and CSF HVA concentrations varied inversely. In this model, a
deficiency hypothesis of 5-HT for aggressiveness is only fulfilled if presynaptic
release of 5-HT is being reduced and there is compensation of postsynaptic 5-HT
receptor function (Coccaro, 1998).
Evidence for a model in which postsynaptic 5-HT receptor function is
altered by presynaptic reduction begins with Stanley et al.s (1982) report
demonstrating a reduced number of presynaptic 5-HT transporter sites in aggressive suicide victims as compared with accident victims (Stanley et al., 1982). The
following year, Stanley and Mann published additional results showing increased
postsynaptic 5-HT2A receptor sites in suicide subjects (Stanley and Mann,
1983), suggesting that, in addition to modified responsiveness, there may be a
change in receptor number as well. In response to these data, researchers
designed psychopharmacologic challenge studies in order to further assess preand postsynaptic function in premortem subjects (Coccaro, 1998). These pharmacochallenge studies involve the activation of a specific neurotransmitter
system through the administration and consequent ligandreceptor interaction
of a pharmacologic agent. Subsequent signaling cascades result in physiological
events that trigger homeostatic, behavioral, and hormonal alterations that can
be measured as an index of the responsiveness of the neurotransmitter system in
question (Coccaro and Kavoussi, 1994).
The first report of a correlation between aggression and pharmacochallenge studies were published by Coccaro et al., 1989. In this study, prolactin
responses to 60 mg of oral D,L-fenfluramine of 45 males with major affective
(n 25) and/or personality (n 20) disorder were compared to those of 18 healthy
male controls. D,L-fenfluramine was chosen as a challenge probe because of its
properties as a serotonin-releasing agent. Its mechanism of action is the release of
serotonin by disrupting vesicular storage of the neurotransmitter and reversing
serotonin transporter function (Welch and Lim, 2007). Since prolactin secretion
is directly dependent upon 5-HT transmission, recording prolactin levels can
provide an indirect but effective measurement of 5-HT activity (Coccaro et al.,
1998a). Both groups of subjects demonstrated reduced prolactin responses to D,Lfenfluramine compared to controls. However, significant correlations appeared
between reduced prolactin responses to D,L-fenfluramine and history of suicide
attempts in all experimental subjects and impulsive aggression in males with
personality disorder (Coccaro et al., 1989). These results suggest that altered 5-HT
activity, specifically reduced receptor function, is apparent in subjects with aggression-related disorders. In a later study by Coccaro et al., the relationship between life
history of aggression and prolactin response to D-fenfluramine and to CSF 5-HIAA
concentration was evaluated (Coccaro et al., 1997a). The results were consistent
with the altered postsynaptic 5-HT receptor function hypothesis: aggression was

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155

significantly and inversely correlated with prolactin responses to D-fenfluramine but

not with CSF 5-HIAA levels. Notably, prolactin response to fenfluramine appears
to reflect activation of 5-HT2 receptors, likely of the 5-HT2c subtype (Coccaro
et al., 2010a). Additional research has revealed that prolactin responses to fenfluramine are also positively correlated with prolactin responses to m-CPP challenge,
which assesses 5-HT postsynaptic receptor activation (Coccaro et al., 1997b).
Thus far, seven subtypes of 5-HT receptors have been identified, ranging from 5-HTR1 to 5-HTR7. These receptors have been found to mediate both
excitatory and inhibitory inputs in a number of brain regions associated with
aggression (Siever, 2008), emotion regulation, and cognition. Inhibition of
offensive aggression via agonists of 5-HT1a attenuates various forms of aggression in animals (Ferris et al., 1999; Joppa et al., 1996; Miczek et al., 2004;
Olivier et al., 1995; Ricci et al., 2006; White et al., 1991). According to one
study by Popova et al., less aggressive rats had higher 5-HT1a receptor expression
in the midbrain (Popova et al., 2005), whereas in the frontal cortex, lower
aggression was associated with a decrease in 5-HT1a receptor mRNA (Popova
et al., 2007). In support of this hypothesis, a recent study showed that high 5HT1a receptor density corresponded to increased aggressiveness in male Golden
hamsters (Cervantes and Delville, 2009). Additional confirmation came from a
study in which PET imaging of healthy subjects revealed that aggression is
positively correlated to 5-HT1a receptor distribution in the dorsolateral and
ventromedial prefrontal cortex, in the orbitofrontal cortex, and in the anterior
cingulate cortex (Witte et al., 2009). Support of 5-HT1as involvement in
aggression also comes from animal studies showing that offensive aggression in
hamsters is inhibited by 5-HT1a receptors and facilitated by 5-HT3 receptor
activation (Cervantes et al., 2010). Agonists of the 5-HT1a and 5-HT1b (5HT1d in the human) receptors in the medial prefrontal cortex or septal area can
increase aggressive behavior under specific conditions (Takahashi et al., 2011).
Activation of these two receptors, as well as the 5-HT2a and 5-HT2c receptors
in mesocorticolimbic areas, reduces species-typical and other aggressive behaviors. Pathological aggression is reportedly reduced by activation of 5-HT transporters, whereas dysfunction of genes that affect the 5-HT system directly such as
MAOA cause an escalation in pathological aggression (Alia-Klein et al., 2008).
With respect to 5-HT2a distribution, PET imaging demonstrates that
individuals with IED and current physical aggression have increased receptor
density in the orbitofrontal cortex when compared to individuals with IED but
no current physical aggression or when compared to individuals who served as
healthy controls (Rosell et al., 2010). This is similar to 5-HT1a distribution in
the orbitofrontal cortex with the respect to aggression, as noted above (Witte
et al., 2009). In a separate study, 5-HT2a receptor-binding activity was investigated in a nearby brain region, the dorsolateral prefrontal cortex, and a pattern
different to that seen in the orbitofrontal cortex emerged. The results found that

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5-HT2a receptor-binding potentials were lower in the dorsolateral prefrontal

cortex in individuals with more severe impulsivity and aggression than in healthy
subjects (Meyer et al., 2008). Lower 5-HT2a binding potentials occur at younger
ages, when violent behavior is more frequent and is more prominent when
impulsivity and aggression are more severe. However, this has not been causally
linked; a low binding potential indicates low ligand-receptor-binding interaction
and therefore the cause of these reduced binding potentials require further
investigation. In a novel study led by Soloff et al., gender differences were
identified in 5-HT2a availability with respect to aggression, negativism, and
suspiciousness, highlighting a potential for gender biases and a need to control
for them when conducting research (Soloff et al., 2010).
Advances in molecular biology and neuroimaging have allowed for
experimental studies in which 5-HT activity can be altered by tryptophan
manipulation and subsequent brain activity and behavior monitored.
These studies have long noted that 5-HT in the central nervous system (CNS),
as well as in the periphery (e.g., through assessment of 5-HT transporter binding
sites on the blood platelet) is reduced in aggressive behavior (Coccaro et al.,
2010a). Platelet 5-HTT sites are structurally identical to corresponding sites on
central 5-HT neurons (Lesch et al., 1993) and are therefore appropriate for further
hypothesis testing. Preliminary studies by Stoff et al. found that lowered tryptophan levels and ingestion of alcohol were associated with increased aggression
and lower 5-HTT binding (B) by H3-imipramine in normal adult males, suggesting
that low 5-HT levels may be involved in the etiology of aggression and particularly,
alcohol-induced violence (Pihl et al., 1995). Similarly, Birmaher et al., reported
that a reduction in platelet H3-imipramine (Bmax) was associated with aggression in
children and adolescents (Birmaher et al., 1990). Two studies by Coccaro et al. have
also demonstrated that the number of 5-HTT binding sites assessed by platelet H3paroxetine is inversely related to aggression (Coccaro et al., 1996, 2010b). Individuals with IED also had fewer 5-HT transporter platelet binding sites than comparable personality disordered subjects without IED; measures of impulsivity did not
correlate with 5-HTT binding in these studies.
Animal and clinical studies have highlighted that impulsive aggression
and its comorbid psychiatric disorders may result from a failure of the 5-HT
system to communicate properly with other neurotransmitter systems, particularly that of dopamine (De Simoni et al., 1987). Specifically, failure of the
dopamine and serotonin systems to successfully interact in the prefrontal cortex
may underlie impulsive aggression (Seo et al., 2008). Van Erp and Miczek
recently reported that increased aggressive behavior in male Long-Evans rats
was related to both increased dopamine in the nucleus accumbens and reduced
5-HT levels in the frontal cortex (Van Erp and Miczek, 2000). Previous studies
have illustrated that serotonergic and dopaminergic systems are tightly linked
(Daw et al., 2002; Kapur and Remington, 1996; Wong et al., 1995), and it is

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157

thought that subnormal serotonergic function may lead to dopaminergic hyperactivity, which in turn leads to impulsive and aggressive behavior (Seo et al.,
2008).

III. DOPAMINE
Dopamine (DA) is a catecholamine neurotransmitter that acts both on the central
and the sympathetic branch of the peripheral nervous systems. DA in the CNS has
been linked to cognition (Browman et al., 2005; Heijtz et al., 2007), movement
(Devos et al., 2003), sleep (Dzirasa et al., 2006; Lima et al., 2008), mood (Brown
and Gershon, 1993; Diehl and Gershon, 1992), attention (Nieoullon, 2002), and
learning and memory (Arias-Carrion and Poppel, 2007; Denenberg et al., 2004).
Additionally, DA has developed a well-established and essential role as the
neurotransmitter responsible for reward pathways involved in drug use (Pettit
and Justice, 1991; Ranaldi et al., 1999; Weiss et al., 1992), eating (Hernandez
and Hoebel, 1988), and sexual behavior (Hull et al., 1993; Pfaus et al., 1990). In
patients with frontotemporal dementia, increased dopaminergic neurotransmission and serotonergic modulation of dopaminergic activity is, respectively, associated with agitated and aggressive behavior (Engelborghs et al., 2008), suggesting
DA function contributes to the aggressive behavioral state. While much of what
we know about dopamine and its biological effects remains to be determined, it is
clear from the literature and data so far that dopamine is a neurotransmitter with a
multitude of behavioral, physiological, and psychological capabilities.
From a molecular perspective, research into DA function in aggressive
individuals has revealed a spectrum of genetic variability that is linked to a
number of polymorphisms in DA-specific genes. Led by Elena L. Grigorenko of
Yale Universitys Child Study Center, a coalition of scientists in 2010 found
positive correlates between genetic polymorphisms in four genes involved in DA
turnover and behavior pathology (Grigorenko et al., 2010). The four genes
investigated included catechol-O-methyl-transferase (COMT), involved in catecholamine metabolism; dopamine beta hydroxylase (DbH), responsible for
dopamine conversion; and MAOA and MAOB, both involved in the degradation of DA and/or other neurotransmitters. In this study, blood samples from 179
adolescent offender males sentenced to a juvenile detention center in a large
capital city in Northern Russia were compared for genetic analysis to those of
two control groups of Russian male adolescents (n 182; n 60). While no
single dopaminergic polymorphism revealed a definitive causal link to conduct
disorder, criminality, aggression, or delinquency, combination of variants across
two (COMT and DbH), three (COMT, DbH, and MAOB), or all four (COMT,
DbH, MAOA, and MAOB) of the DA-specific genes investigated showed
positive correlations with the behavioral traits in question. Nemoda et al.

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found similar results among patients with borderline personality disorder in a

separate study done in 2010 using young adults from low-to-moderate income
households (n 99) and major depressive or bipolar patients (n 136) (Nemoda
et al., 2010). The results of this study found that a promoter variant in the
dopamine D4 receptor may be involved in the development of BPD traits,
including aggression. The DA D4 receptor has been postulated as a candidate
nexus for BPD because of its preferential expression in the prefrontal cortex (Oak
et al., 2000), and its noted role in novelty-seeking and impulsivity (Munafo` et al.,
2008). Data from both experimental groups showed polymorphisms in COMT
and the DA transporter (DAT1) of the dopamine D2 receptor were directly
related to self-injurious and impulsive behavior, both BPD traits. Other reports
have confirmed genetic abnormalities with COMT in the presence of BPD,
including a recent study citing an over-representation of the low activity Met/
Met genotype of the gene in BPD patients (n 161) (Tadic et al., 2009).
Interestingly, COMT and DAT1 are similarly implicated in bipolar and major
depressive disorder (Joyce et al., 2006), suggesting DA dysfunction may encompass a much larger behavioral and physiological state.
In 2008, Couppis and Kennedy published novel findings that found
dopamine to be a reward for aggressive behavior in mice (Couppis and
Kennedy, 2008). The authors had hypothesized that aggression could be linked
to the dopaminergic receptors of the nucleus accumbens (NAc), citing their
reputation as the most strongly implicated neurotransmitter in positive reinforcement (Wise, 2004) and reward behavior. The results of their studies showed
that administration of a D1-like (D1 and D5) receptor antagonist (SCH-23390),
or a D2-like (D2, D3, and D4) receptor antagonist (sulperide) into the NAc
significantly reduced aggression responses when compared to administration
outside of the NAc. In addition to the reductions in aggression, concomitant
reductions in mobility were seen in these first studies. These results showing a
simultaneous reduction in aggression and DA levels were consistent with previous reports that had suggested increased DA in the NAc led to increased
aggression (Van Erp and Miczek, 2000). After Couppis and Kennedys initial
publication, Schwartzer and Melloni reported similar findings that dopamine
activity primarily mediated by D2 receptors was involved in modulating anabolic/androgenic steroid-induced offensive aggression in Syrian hamsters
(Schwartzer and Melloni, 2010b). Interestingly, administration of the D2-like
DA antagonist into the anterior hypothalamus (AH) rather than the NAc
produced no side effects of reduced mobility: in a follow-up experiment, the
authors reported that treatment of male Syrian hamsters with the D2-like
receptor antagonist eticlopride in the AH results in dose-dependent suppression
of aggression behaviors without causing mobility changes (Schwartzer and
Melloni, 2010a). Conversely, injection of SCH-23390 into the AH reduced
aggressiveness but showed simultaneous changes in sociability and mobility.

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Postmortem studies revealed sparse population of GAD67 (a GABA production

marker) neurons distributed within the D5 receptors of the lateral AH. Based on
these findings, the authors conclude that D5 receptors in the lateral AH modulate non-GABAergic pathways that may indirectly influence aggression behavior. Future aggression studies should aim to better understand the role of
dopaminergic activity in the hypothalamus and other limbic structures that are
in part physiologically responsible for emotion and behavior regulation.

IV. NOREPINEPHRINE (NORADRENALINE)

Synthesized from tyrosine-derived dopamine via dopamine decarboxylase and
b-hydroxylase (Sofuoglu and Sewell, 2009), norepinephrine (NE) is both a
catecholamine neurotransmitter and a stimulant stress hormone. As a stress
hormone, NE primarily targets brain regions responsible for attention such as
the amygdala and works in conjunction with epinephrine (adrenaline) to produce the fight-or-flight response (Tanaka et al., 2000). During times of high
stress, this response increases heart rate, releases glucose from energy stores, and
increases blood flow to skeletal muscle in an attempt to increase the oxygen
supply to the brain. When released from the locus ceruleus, NE also works to
actively suppress neuroinflammation that may potentially cause damage to the
brain (Heneka et al., 2010).
One of the earliest reports relating aggression to norepinephrine emerged
in a 1972 publication by Thoa and colleagues in Science magazine (Thoa et al.,
1972). In this study, rats that received an intraventricular injection of 90 mg of
6-hydroxydopamine (a neurotoxic agent used to selectively target dopaminergic or
noradrenergic neurons) showed increased shock-induced aggression and reduced
brain norepinephrine while dopamine levels remained unaltered. This inverse
relationship between norepinephrine availability and shock-induced aggression
suggests that the behavioral trait is partially modulated by noradrenergic function.
In the mid-1980s, Pucilowski and colleagues launched a series of studies that
confirmed NE was intimately related to aggression. The first paper, dating from
1985, demonstrated that chemically induced muricide could be in part suppressed
by norepinephrine (Pucilowski and Valzelli, 1985). A second study, published
shortly thereafter, showed that bilateral microinjections of hydroxydopamine into
the nuclei loci coerulei of male Wistar rats resulted in decreased mesencephalic
and striatal norepinephrine levels as well as marked increased aggression
(Pucilowski et al., 1986). In 1987, a similar study by the same group gave microinjections of the NE-depleting toxin N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine (DSP-4) with or without apomorphine into the amygdala. Here, the results

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clearly showed that NE was able to markedly reduce apomorphine-induced aggression (Pucilowski et al., 1987). The data also showed that norepinephrine significantly reduced locomotor activity and to a lesser degree, sensitivity to pain.
In 1998, a novel research experiment authored by Spivak et al. reported
that neuroleptic-resistant chronic schizophrenic patients maintained on clozapine
for 1 year had significantly less aggression (p < 0.01), higher plasma NE levels
(p < 0.0001), and higher serum triglycerides (p < 0.01) than patients treated with
classical antipsychotic agents for the same period of time (Spivak et al., 1998).
Clozapine is a dibenzodiazepine antipsychotic used for the treatment of schizophrenia, and its mechanism of action is primarily anchored by binding to dopamine and serotonin receptors (Naheed and Green, 2001). Based on these findings,
the authors conclude that the antiaggressive/antisuicidal activity of clozapine may
be a direct result of elevated plasma NE levels (Spivak et al., 1998). Further, this
inverse relationship between increased NE levels and decreased aggression confirms what was first seen by Thoa and colleagues in the 1972 Science reports and
substantiates a role for NE in modulating behavioral aggression.
Although it is clear that alterations in NE levels affect aggressiveness
directly, there is also evidence to suggest that norepinephrine plays an indirect
role in modulating serotonergic-mediated impulsive aggression. In 1991, Siever
and Davis published findings that suggested decreased NE activity leads to
depression, suicide, and self-directed aggression whereas increases in NE activity
can lead to irritability and violent aggression (Siever and Davis, 1991). In the
same year, Coccaro et al., published additional findings that demonstrated that
greater growth hormone responses to the NE agonist clonidine were positively
correlated with behavioral irritability (Coccaro et al., 1991). This finding was not
replicated in a subsequent study by the same author (Coccaro and Kavoussi,
2010), but another study from this group reported an inverse relationship between plasma MHPG and life history of aggression in personality disordered
subjects (Coccaro et al., 2003). In this case, presynaptic NE (reflected by plasma
MHPG) could be associated with higher postsynaptic NE receptor sensitivity,
and thus, increased fight or flight responses when presented with an aversive
stimulus.

V. GABA
While gamma-aminobutyric acid (GABA) has a critical and well-defined function in vertebrate neurological systems, its role in behavioral aggression is not as
prominent as 5-HT, DA, and NE. GABA is a primary neurotransmitter in the
CNS, and is known as chief inhibitory neurotransmitter (de Almeida et al.,
2005). GABA-related activity and dysfunction has been associated with

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161

schizophrenia (Kantrowitz et al., 2009; Wassef et al., 1999), epilepsy (Snodgrass,

1992; Treiman, 2001), and pain and nociception (Enna and McCarson, 2006;
Sawynok, 1984).
In 2007, researchers at the Model Organism Research Center of the
Shanghai Institutes for Biological Sciences found that GABA transporter subtype
1-deficient (or GAT1/) mice exhibit lower behavioral aggressiveness compared
to wild-type mice (Coccaro et al., 1998b). Deficiency in GABA transporter function, analogous to inhibition of GABA transporters, leads to an increase in synaptic
GABA. Later, Takahashi et al. found that pharmacological activation of GABA
(B), but not GABA(A), receptors in the dorsal raphe nucleus significantly increased
aggression (Takahashi et al., 2010). The authors theorized that since the majority of
forebrain 5-HT originates from the raphe nucleus, GABAergic control of this region
could provide an indirect mechanism for escalations in behavioral aggression. A
similar study by the same group showed that male CFW mice, treated with the
GABA(A) receptor agonist muscimol, had increased aggressive tendencies following alcohol consumption compared to mice given water. These results demonstrate
that GABA(A), but not GABA(B), receptors in the dorsal raphe nucleus are one of
the neurobiological targets of alcohol-induced aggression (Coid et al., 1983), and
illustrate a functional role for GABA in modulating aggressive behavior.
In addition to its affiliations with serotonin, it has also been demonstrated that GABA is associated with the dopaminergic systems as well and that
this relationship may influence displays of aggression. GABAergic interneurons
in various brain regions including the AH are commonly found to express
dopamine D2 receptors (Gerfen et al., 1990; Santana et al., 2009). Based on
this observation and the known presence of DA D2 receptors in the AH (Ricci
et al., 2009), Schwartzer et al. postulated that DA D2 receptor activity may be
modulating behavioral aggression through direct inhibition of GABA in the AH
(Schwartzer et al., 2009). The authors found that adolescent male Syrian hamsters exposed to anabolic-androgenic steroids had DA-stimulated increased aggression marked by the removal of GABAergic inhibition in the lateral AH.
Human studies of GABA and aggression are limited but include two
studies in personality disordered subjects from the laboratory of Coccaro et al. In
the first study, Lee et al. demonstrated a direct relationship between CSF GABA
and measures of impulsivity and history of suicide attempt (but not aggression) in
personality disordered subjects (Lee et al., 2008). In the second study, the growth
hormone (GH) response to the GABA(B) receptor agonist, baclofen, was found
to be inversely correlated with measures of impulsivity (but not aggression) (Lee
et al., in press). Taken together, these studies suggest that elevated central
GABA may lead to, or be associated with, a reduction of GABA(B) receptors
and that this reduction in downstream GABA(B) mediated activity is associated
with increased liability to impulsive behavior. As such, these data are consistent
with the work of Takahashi et al. (2010).

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VI. PEPTIDES
Limited published data suggest relationships between human aggression and
central vasopressin, oxytocin, and opiates. (Coccaro et al., 1998b) first reported
a positive correlation between CSF vasopressin concentration and life history of
aggression in male and female subjects with personality disorders. This relationship was confined to males and remained even after the inverse correlation
between CSF vasopressin and a collateral assessment of serotonin function
(i.e., PRL response to FEN) was accounted for. Later, Lee et al. (2009) reported
an inverse relationship between CSF oxytocin and life history of aggression in an
overlapping group of subjects. CSF vasopressin and CSF oxytocin were inversely
correlated, but CSF oxytocin continued to be related to aggression even after the
influence of CSF vasopressin on aggression was controlled for. This lab has also
noted a positive correlation between CSF Neuropeptide Y and CSF Substance P
in these same subjects. In addition, circulating levels of metenkephalins have
been associated with self-injurious behaviors in one study (Coid et al., 1983).
Postmortem studies of violent suicide victims have found greater number of mu
receptors in the brain. In healthy volunteers, administration of codeine (Spiga
et al., 1990) or morphine (Berman et al., 1993) heightened aggression on
laboratory measures. These studies suggest that increased opioid activity may
increase the likelihood of aggressive behavior. In fact, naltrexone, an opioid
antagonist, attenuates self-injurious behavior in autistic and retarded patients
(Sandman et al., 1990, 2000).

VII. CONCLUSION
The neurobiology of aggression is clearly complex. However, we now know more
about the biological underpinnings of this behavior than ever before and this
knowledge points the way to possible strategies for treatment. Many agents appear
to have therapeutic efficacy but many only work on the brain 5-HT system. In the
upcoming years, we look to the development of agents that work on non-5-HT
systems (e.g., vasopressin, oxytocin, etc.) so that we may have a more varied
toolbox with which to treat individuals with problematic aggressive behavior.

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Human Aggression Across the

Lifespan: Genetic Propensities
and Environmental Moderators
Catherine Tuvblad and Laura A. Baker
University of Southern California, Los Angeles, California, USA

I. Heritability of Aggression: Twin and Adoption Studies

A. Does heritability vary depending on sex?
B. Does heritability change across age?
C. Do heritabilities vary across methods of assessment?
D. Do heritabilities vary across forms of aggression?
E. Does heritability vary depending on study design (twins vs.
adopted siblings)?
F. Criticisms of twin and adoption studies: Assumptions and
generalizability
II. G
E Interaction in Aggressive Behavior
A. Potential moderators of genetic influence found in adoption
and twin studies
III. Specific Genes for Aggressive Behavior: Findings from Molecular
Genetic Studies
A. G
E interaction involving specific genes for aggressive
behavior
IV. Conclusions
References

ABSTRACT
This chapter reviews the recent evidence of genetic and environmental influences
on human aggression. Findings from a large selection of the twin and adoption
studies that have investigated the genetic and environmental architecture of
Advances in Genetics, Vol. 75
Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00007-1

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Tuvblad and Baker

aggressive behavior are summarized. These studies together show that about half
(50%) of the variance in aggressive behavior is explained by genetic influences in
both males and females, with the remaining 50% of the variance being explained
by environmental factors not shared by family members. Form of aggression
(reactive, proactive, direct/physical, indirect/relational), method of assessment
(laboratory observation, self-report, ratings by parents and teachers), and age of
the subjectsall seem to be significant moderators of the magnitude of genetic
and environmental influences on aggressive behavior. Neither study design (twin
vs. sibling adoption design) nor sex (male vs. female) seems to impact the magnitude of the genetic and environmental influences on aggression. There is also some
evidence of gene-environment interaction (G
E) from both twin/adoption
studies and molecular genetic studies. Various measures of family adversity and
social disadvantage have been found to moderate genetic influences on aggressive
behavior. Findings from these G
E studies suggest that not all individuals will be
affected to the same degree by experiences and exposures, and that genetic predispositions may have different effects depending on the environment. 2011, Elsevier Inc.
Are all humans innately and equally capable of inflicting harm on others? Do we
learn by our various experiences to manipulate and even harm others for our own
personal gain; or conversely, to be kind and benevolent, offering help even at
costs to ourselves? Although these fundamental questions pertaining to the
nature of human aggression have plagued scientists and laypersons for centuries,
some answers can be found in research spanning the last few decades.
The early experiments of Milgram (1963) made it clear that, under
certain circumstances, individuals can be coaxed into aggression and violence.
The presence of a strict authority and removal of personal responsibility for ones
actions can result in aggressive behaviors that inflict harm on others. The
infamous Stanford prison experiment (Haney et al., 1973) also demonstrated
that the propensity toward violence and aggression can be elicitedextremely
and unexpectedlyin situations, where a legitimized ideology and a powerful
authority can lead to impressionability and obedience.
Yet, while these powerful studies revealed the importance of social
factors in inducing aggressive behaviors, not all individuals responded in an
equally aggressive manner. In Milgrams (1963) first set of experiments, while
65% (26 of 40) of participants complied with the instruction to administer what
they believed to be a final, massive 450-volt shock, the remaining 35% did not
comply. Many of those who engaged in the aggressive behavior stated they were
very uncomfortable doing so, and every participant reportedly questioned the
experiment at some point or refused money promised for their study participation
(Milgram, 1963). Although the studies by Milgram and Zimbardo provide clear
evidence for the role of environment and social situations in affecting aggressive
behavior, there are, nonetheless, large individual differences in the propensity for
violence and aggression, even under these extreme circumstances.

8. Human Aggression Across the Lifespan

173

What factors contribute to individual differences in aggression? Behavioral genetic studies of family members resemblance for aggressive behavior help
shed light on the matter. Twin and adoption studies agree with the experimental
literature on aggression, which shows that a large effect of environmental factors
is evident, particularly of the nonshared variety. Yet, there is also plenty of
evidence, based on a variety of definitions of aggressive behavior from children
to adults, for genetic propensity toward aggression (see reviews by Burt, 2009;
Miles and Carey, 1997; Rhee and Waldman, 2002). Although few behavioral
genetic studies have explicitly examined the question of gene by environment
(G
E) interactions, we contend that such interactions are likely to exist and
that the genetic propensity for aggression should exert its effects more strongly in
some situations than others. Consistent with the early findings of Milgram and
Zimbardo, individual genetic predispositions should moderate the extent to
which aggression can be elicited, even in extreme situations such as these
infamous studies. Our view is that while many, if not most, humans may have
the potential for aggression and violence under the right circumstances, not all
individuals will succumb to these behaviors under the same circumstances.
This chapter will review recent evidence of genetic and environmental
influences on human aggression, with particular attention to several key
questions and issues. We first consider how estimates of the relative importance
of genetic effects (i.e., heritability) may vary across forms of aggression and
the way in which it is measured. As detailed in other chapters of this volume,
there are numerous definitions of aggression. Some definitions distinguish between reactive and proactive forms (Dodge et al., 1997; Raine et al., 2006), and
others consider direct and indirect forms of aggression (e.g., physical vs. relational; Lahey et al., 2004; Tackett et al., 2009). Some definitions may include
extreme criminal violence, such as assault, rape, and murder, although these
extreme behaviors are relatively rare and have not been studied extensively in
genetically informative designs. Measures of aggression can include self-reporting, teacher and parent reports (particularly for young children), and official
records from schools or the justice system. This review focuses on twin and
sibling adoption studies of aggressive behavior measured as a trait within the
wider population. We compare effect sizes (heritability) across these various
definitions and ways of measuring aggression. We also consider how heritability
estimates may vary across both age and gender. Given higher levels of aggression
in males across the lifespan, one obvious question concerns whether genetic
propensities are of greater importance in one sex and how these differences might
vary across age. We consider a variety of measurable environmental factors that
might moderate these genetic influences and which may thus lead to G
E
interactions for aggressive behavior. Although direct tests of G
E interactions
have been relatively rare in the behavioral genetic literature on human aggression,
it is likely that such interactions exist, given their robust effects in other forms of
antisocial behavior (e.g., property criminal offending; Cloninger et al., 1982).

174

Tuvblad and Baker

Finally, we briefly review evidence for specific genetic influences in aggression by

summarizing some of the more recent findings from molecular genetic studies.
These effects are reviewed in detail elsewhere in this volume, so our focus here is on
how a few specific genes may be involved in G
E interactions.

I. HERITABILITY OF AGGRESSION: TWIN AND ADOPTION STUDIES

Behavioral genetic research relies on the different levels of genetic relatedness
between family members in order to estimate the relative contribution of heritable
and environmental factors to individual differences in a phenotype of interest.
Major research designs include: (a) studies of twins raised together and (b) studies of
adopted individuals and their biological and adoptive family members. Although
designs combining both approaches are the most powerful for separating genetic
and environmental effects in human behavior, such studies of twins separated at
birth and raised apart are rare and have not studied aggressive behavior extensively.
Nonetheless, there are a handful of adoption studies and over two dozen studies of
twins raised together which have specifically examined the genetic and environmental influence in aggression in nonselected samples from Northern America and
Europe that are reasonably representative of the general population.
In the classical twin design, monozygotic (identical) twins share their
common environment and they are assumed to share 100% of their genes.
Dizygotic (fraternal) twins also share their common environment and they are
assumed to share on average 50% of their genes. By comparing the resemblance
for aggressive behavior between monozygotic and dizygotic twins, the total
phenotypic variance of aggression can be divided into additive genetic factors
(or heritability, h2), shared environmental factors (c2), and nonshared environmental factors (e2). Shared environmental factors refer to nongenetic influences
that contribute to similarity within pairs of twins. Nonshared environmental
factors are those individual experiences that cause siblings to differ in their levels
of aggressive behavior. Heritability is the proportion of total phenotypic variance
due to genetic variation (Neale and Cardon, 1992). Genetic influences may also
be divided into those that are additive (i.e., allelic effects add up across loci) and
those that are nonadditive (i.e., due to dominance or epistasis). In twin studies,
however, it is not possible to estimate both additive and nonadditive genetic
effects (d2) simultaneously with shared twin environment effects. The twin
correlations summarized in Table 8.2 can be used to estimate the genetic and
environmental influences to aggressive behavior. Twice the difference between
the MZ and DZ correlations provides an estimate of the relative contribution of
additive genetic influences to aggressive behavior [h2 2(rMZ  rDZ)]. The
contribution of the nonadditive genetic effects due to dominance or epistasis
(d2) is obtained by subtracting four times the DZ correlation from twice the MZ

8. Human Aggression Across the Lifespan

175

correlation (d2 2rMZ  4rDZ). The proportion of the variance that is due to
shared environmental influence is given by subtracting the MZ correlation from
twice the DZ correlation (c2 2rDZ  rMZ). Finally, the contribution of the nonshared environmental influences can be obtained by subtracting the MZ correlation from unit correlation (e2 1  rMZ) (Posthuma et al., 2003). Many twin
studies do not specifically examine or test for nonadditive genetic effects and
instead report heritability estimates based on additive effects only. However,
some twin studies compare models with additive effects and nonadditive effects
versus models with additive genetic effects and shared environment.
In sibling adoption studies, the correlation between adoptive siblings is
compared with the correlation between biological siblings to estimate the influence of genetic and environmental factors on aggressive behavior (Plomin et al.,
2001). Resemblance between adoptive siblings for measures of aggression is
indicative of shared (or common) family environment, while the extent to
which biological sibling resemblance exceeds that of adoptive siblings is taken
as evidence of heritable genetic influences for aggressive behavior.
There have been a few meta-analyses of twin and adoption studies of
aggressive behavior and the wider construct of antisocial behavior. In one early
meta-analysis of 24 twin and adoption studies, heritable influences explained
about half of the total variance in aggressive behavior and the nonshared environment explained the remaining 50% (Miles and Carey, 1997). Rhee and Waldman
(2002) also summarized the results from 51 twin and adoption studies on criminal
behavior, delinquency, psychopathy, conduct disorder, and antisocial personality
disorder, as well as aggressive behavior, in children, adolescents, and adults.
Genetic factors explained 41% of the variance in antisocial behavior, 16% was
explained by shared environmental influences, and the remaining 43% of variance
was explained by nonshared environmental factors. A more recent review focused
on 19 twin and adoption studies using child and adolescent samples; studies
including adult subjects were excluded. Heritability was found to explain 65%,
shared environment explained 5%, and the nonshared environment explained the
remaining 30% of the variance in aggressive behavior (Burt, 2009). Both Burt
(2009) and Rhee and Waldman (2002) examined nonadditive genetic effects, but
only Rhee and Waldman (2002) found significant nonadditive genetic effects for
antisocial behavior. It is noteworthy that genetic influences are consistently found
across these reviews, while shared environmental influences are comparatively
small or nonexistent. Family similarity in aggressive and antisocial behavior,
therefore, is primarily the result of shared genes, not environment.
Tables 8.1 and 8.2, respectively, summarize a large selection of twin and
sibling adoption studies which have specifically examined the genetic and
environmental influences on aggressive behavior in child, adolescent, and
adult samples. Several studies use prospective, longitudinal designs, and large
samples, and three of the twin studies were designed, in particular, to study

Table 8.1. Effect Sizes for Aggressive Behavior from Adoption Studies

Study
(author, year)

Aggression
measure

Informant

Age in years

Dutch adoptees
(van den Oord et al., 1994)

Aggression
(CBCL)

Parent ratings

1015
Mean 12.4

Dutch adoptees
(van der Valk et al., 1998)

Aggression
(CBCL)

Parent ratings

1015

Colorado adoptees
(Deater-Deckard and
Plomin, 1999)

Aggression
(CBCL)

Parent ratings

1318
7, 9, 10, 11, 12
Mean 9.5

Aggression
(TRF)
Aggression
(as reported in Rhee
and Waldman,
2002; Burt, 2009)

Teacher ratings

Unknown
(Parker, 1989)a

Parent ratings

47

Sex

Biological
siblings
r(N)

Adoptive
siblings
r(N)

M
F
MF
MF

0.40 (30)
0.45 (35)
0.38 (46)
0.42 (111)

0.02 (44)
0.21 (48)
0.05 (129)
0.13 (221)

MF
MF

0.36 (152)
0.39 (94)

MF
MF

h2

c2

0.52
0.32

0.00
0.25

0.61

0.13

0.26 (156)
0.26 (78)

0.52
0.24

0.12
0.27

0.25 (188)

0.06 (156)

0.49

0.00

0.44 (66)

0.47 (45)

M, Male; F, Female; h2, heritability; c2, shared environment; CBCL, Child Behavior Checklist (Achenbach, 1991b); TRF, Teacher Report Form
(Achenbach, 1991a).
a
Genetic and shared environmental estimates were not reported by the authors.

Table 8.2. Effect Sizes (Correlations) for Aggressive Behavior from Twin Studies
Study sample
(author, year)
Boston twins
(Scarr, 1966)
Missouri twins
(Owen and Sines,
1970)
California twins
(Rahe et al., 1978)
Colorado twins
(OConnor et al., 1980)
London twins, UK
(Rushton et al., 1986)
California preschool
twins
Ghodesian-Carpey and
Baker, 1987
Philadelphia twins
(Meininger et al.,
1988)
Minnesota twins
(McGue et al., 1993)c

Midwest twins
(Cates et al., 1993)

Colorado twins
(Schmitz et al., 1995)

Aggression measure

Assessment
method

Age in years

Sex

MZ
r(N)

DZ
r(N)

h2

c2

Sex limitation effects

Aggression
(ACL)
Aggressive reaction
(MCPS)

Parent ratings

610

0.35 (24)

 0.08 (28)

0.40

Lab observation

614

M
F

0.09 (10)
0.58 (8)

 0.24 (11)
0.22 (13)

0.44a

Not tested

Aggression
(ACL)
Aggression/bullying
(PSR)
Aggression
(IBS)
Aggression
(CBCL)
Aggression
(MOCL)
Impatience/aggression
Competitive achievement striving
Aggression
(MPQ)
Aggression
(MPQ)
BDHIassault
BDHIindirect
hostility
BDHIverbal
hostility
Aggression
(CBCL)

Self-report

4256
Mean 48
Mean 7.6

0.31 (93)

0.21 (97)

0.56a

N/A

MF

0.72 (52)

0.42 (32)

Not tested

1960
Mean 30
Mean 5.2

MF

0.40 (296)

0.04 (179)

0.72a

MF

0.78 (21)

0.31 (17)

0.94a

Parent ratings
Self-report
Parent ratings

N/A

Not tested
Not tested

Mothers
observations
Teacher rating

Mean 5.2

MF

0.65 (21)

0.35 (17)

0.60a

611

MF

0.67 (71)
0.63 (71)

0.11 (34)
0.13 (34)

1.12a
1.00a

Self-report

Mean 19.8

MF

0.61 (79)

 0.09 (48)

Not tested

Self-report

Mean 29.6

MF

0.58 (79)

 0.14 (48)

Not tested

Self-report
Self-report

Mean 42.5
Mean 42.5

F
F

0.07 (77)
0.40 (77)

0.41 (21)
0.01 (21)

0.00
0.78

N/A
N/A

Self-report

Mean 42.5

0.41 (77)

0.06 (21)

0.70

N/A

Parent rating

23
411

MF

0.68 (77)
0.79 (66)

0.40 (183)
0.41 (137)

0.52
0.55

0.16
0.19

Not tested

Not tested

(Continues)

Table 8.2. (Continued)

Study sample
(author, year)
Ohio twins, Western
Reserve Twin Project
(Edelbrock et al., 1995)
Dutch twins
(van den Oord et al.,
1996)
Minnesota twins
(Finkel and McGue,
1997)
VET twins
(Coccaro et al., 1997)

Aggression measure

Assessment
method

Age in years

Sex

MZ
r(N)

DZ
r(N)

h2

c2

Sex limitation effects

Aggression
(CBCL)

Parent rating

715
Mean 11.0

MF

0.75 (99)

0.45 (82)

0.60

0.15

Not tested

Aggression
(CBCL)

Parent rating

0.81 (210)
0.83 (265)

0.12

Not tested

Self-report

2764
Mean 37.8

0.35
0.39

0.00
0.00

NS quantitative sex
differences

Self-report
Self-report

Mean 44.1

0.50 (182)
0.42 (182)

0.49 (236)
0.49 (238)
0.45 (409)
0.12 (165)
0.14 (352)
0.12 (114)
0.19 (118)
0.02 (118)

0.69

Aggression
(MPQ)

M
F
MF
M
F
MF
M
M

0.47
0.40

0.00
0.00

N/A
N/A

0.28 (182)

0.07 (118)

0.28

0.00

N/A

BDHIassault
BDHIindirect
hostility
BDHIverbal
hostility
Swedish twins (TCHAD; Aggression
Eley et al., 1999)
(CBCL)

UK twins (sample
Aggression
obtained from Register
(CBCL)
of Child Twins; Eley
et al., 1999)
Virginia twins
Aggression
(Simonoff et al., 1998)
(physical)

Self-report

0.37 (220)
0.39 (406)

Parent rating

89

M
F
MF

0.72 (176)
0.82 (160)

0.41 (182)
0.45 (194)
0.41 (310)

0.70

0.07

Parent rating

12

M
F
MF

0.68 (99)
0.77 (124)

0.45 (93)
0.44 (80)
0.27 (95)

0.69

0.04

Parent rating

816

MF

0.76 (268)

0.46 (166)

0.58

0.18

NS quantitative sex
differences,
NS qualitative sex
differences
NS quantitative sex
differences,
NS qualitative sex
differences
Not tested

Self-report

816

MF

0.31 (268)

0.22 (166)

0.21

0.11

Not tested

Missouri twins
(Hudziak et al., 2000)
Dutch twins
(Hudziak et al., 2003)

Aggression
(CBCL)
Aggression
(TRF)

Parent rating

812

Parent rating

1.5

M
F
M
F
MF
M
F
MF
M
F
MF
M
F
MF
M
F
MF
M
F
MF
MF

Teacher rating

Parent rating

MF

0.73 (602)

0.24 (514)

0.72

0.00

Not tested

Self-report

1118
Mean 13.8
12

MF

0.64 (115)

0.40 (143)

0.68

0.00

Not tested

M
F
MF

0.72 (260)
0.78 (300)

0.59 (292)
0.53 (278)
0.58 (517)

0.14
0.54

0.75
0.25

Significant quantitative
sex differences

10

Dutch twins
(van Beijsterveldt
et al., 2003)c

Aggression
(CBCL)

Parent rating

10

12

Canadian twins
(Dionne et al., 2003)
UK (E-risk) twins
(Taylor, 2004)
South Wales twins
(Button et al., 2004)
Finnish twins
(Vierikko et al., 2004)

Aggression
(physical)
Aggression
(CBCL)
Aggression
(IAB)
Aggression
(MPNI)

Parent rating

0.77 (129)
0.73 (91)
0.72 (181)
0.71 (214)

0.59 (107)

0.50 (156)
0.40 (115)
0.33 (160)
0.33 (151)
0.26 (330)
0.41 (140)
0.25 (125)
0.17 (283)
0.55 (1066)
0.53 (997)
0.48 (2144)
0.48 (1069)
0.53 (858)
0.51 (1723)
0.50 (621)
0.55 (458)
0.47 (907)
0.45 (317)
0.55 (233)
0.57 (433)
0.28 (174)

0.58

0.00

Not tested

0.73 (153)
0.73 (202)
0.81 (1055)
0.82 (1226)
0.83 (927)
0.84 (898)
0.84 (526)
0.79 (471)
0.86 (289)
0.83 (237)

0.77
0.70
0.69

0.00

Not tested

0.00

NS quantitative sex
differences

0.72
0.21

0.00
0.49

Significant quantitative
sex differences
Significant quantitative
sex differences
Significant quantitative
sex differences
Significant quantitative
sex differences
Significant quantitative
sex differences

(Continues)

Table 8.2. (Continued)

Study sample
(author, year)

Aggression measure

Dutch twins
(Polderman et al.,
2006)

Aggression
(TRF)

Colorado twins
(Haberstick et al.,
2006a)

Aggression
(CBCL)

Assessment
method
Teacher rating
(same teacher)
Teacher rating
(different
teachers)
Parent rating

Age in years

DZ
r(N)

MF

0.84 (67)

0.43 (59)

MF

0.40 (45)

0.21 (44)

7b

M
F

0.74 (69)
0.79 (91)

M
F
M
F
M
F
M
F
M
F
M
F
M
F
M
F
M
F
M
F

0.57 (73)
0.76 (75)
0.77 (58)
0.70 (67)
0.64 (58)
0.86 (56)
0.68 (69)
0.83 (78)
0.63 (71)
0.56 (79)
0.58 (66)
0.70 (70)
0.54 (63)
0.67 (74)
0.39 (63)
0.49 (64)
0.56 (68)
0.50 (70)
0.35 (55)
0.48 (60)

11
12
Teacher rating

MZ
r(N)

10

Aggression
(TRF)

Sex

7
8
9
10
11
12

h2

c2

Sex limitation effects

0.49

0.00

Not tested

0.56 (76)
0.44 (62)

0.79

0.00

NS quantitative sex
differences

0.50 (63)
0.55 (60)
0.47 (52)
0.56 (57)
0.41 (55)
0.59 (49)
0.45 (61)
0.45 (65)
0.39 (70)
0.34 (62)
0.46 (62)
0.41 (60)
0.29 (59)
0.37 (53)
0.44 (56)
0.18 (54)
0.12 (54)
0.45 (54)
0.32 (39)
0.24 (49)

0.76

0.00

0.76

0.00

0.84

0.00

0.79

0.00

0.58

0.00

0.61

0.00

0.59

0.00

0.43

0.00

0.52

0.00

0.42

0.00

NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences
NS quantitative sex
differences

Ad-Health
(Cho et al., 2006)

Aggression

Self-report

1219

Colorado twins
(Gelhorn et al., 2006)
Finnish twins
(von der Pahlen et al.,
2008)

Aggression
(DISC items)
Aggression
(BPAQ)

Self-report

1118
Mean 14.5
1833

Norwegian twins
(Czajkowski et al.,
2008)

Passive
aggression
(DSM-IV)

Self-report

1936
Mean 28.2

M
F
MF

0.35 (221)
0.30 (448)

Tennessee twins
(Tackett et al., 2009)

Relational aggression
(CAPS)

Self- report

918

0.54 (356)
0.41 (376)

Parent rating

918

Parent rating

910

Self-report

910

Teacher rating

910

M
F
MF
M
F
MF
M
F
MF
M
F
MF
M
F
MF

California twinsRFAB
cohort (Baker et al.,
2008)

Reactive aggression
(RPQ)

Self-report

M
F
MF
MF
MF
M
F
MF

0.47 (141)
0.47 (141)
0.47 (531)
0.45 (190)
0.52 (608)

0.66 (356)
0.65 (376)
0.48 (141)
0.60 (142)
0.38 (138)
0.37 (139)
0.59 (67)
0.70 (68)

0.29 (131)
0.27 (114)
0.21 (197)
0.27 (569)
0.28 (212)
0.22 (167
321 sibs)
0.18 (387
1838 sibs)
0.20 (508
1559 sibs)
0.45 (116)
0.19 (261)
0.21 (340)
0.39 (328)
0.36 (332)
0.16 (589)
0.61 (328)
0.35 (332)
0.48 (589)
0.35 (87)
0.46 (98)
0.50 (151)
0.28 (83)
0.38 (96)
0.08 (146)
0.49 (45)
0.43 (45)
0.60 (62)

0.50
0.30

0.00
0.00

Not tested

0.49

0.00

Not tested

0.70
0.69

0.00
0.00

Not tested

0.14

0.18

0.49

0.00

NS quantitative sex
differences,
NS qualitative sex
differences
NS quantitative sex
differences

0.21
0.42

0.46
0.22

Significant quantitative
sex differences

0.26

0.27

NS quantitative sex
differences

0.38
0.00

0.00
0.36

Significant quantitative
sex differences

0.20

0.43

NS quantitative sex
differences
(Continues)

Table 8.2. (Continued)

Study sample
(author, year)

Aggression measure
Proactive aggression
(RPQ)

California twinsRFAB
cohort (follow-up)
(Tuvblad et al., 2009)

Weighted average

Assessment
method

Age in years

Parent rating

910

Self-report

910

Teacher rating

910

Reactive aggression
(RPQ)

Parent rating

1114

Proactive aggression
(RPQ)

Parent rating

1114

Sex
M
F
MF
M
F
MF
M
F
MF
M
F
MF
M
F
MF
M
F
MF
MF

MZ
r(N)
0.61 (141)
0.57 (142)
0.60 (138)
0.12 (139)
0.56 (67)
0.74 (68)
0.49 (102)
0.58 (98)
0.55 (102)
0.46 (98)
0.66
0.63
0.59

DZ
r(N)
0.34 (87)
0.48 (98)
0.55 (151)
0.34 (83)
0.28 (96)
0.14 (146)
0.42 (45)
0.38 (45)
0.35 (62)
0.33 (55)
0.38 (77)
0.42 (103)
0.35 (55)
0.27 (77)
0.40 (103)
0.42
0.35
0.38
0.28

h2

c2

Sex limitation effects

0.32

0.21

NS quantitative sex
differences

0.50
0.00

0.00
0.14

Significant quantitative
sex differences

0.45

0.14

NS quantitative sex
differences

0.43

0.15

NS quantitative sex
differences

0.48

0.08

NS quantitative sex
differences

MZ, monozygotic; DZ, dizygotic; M, male twin pairs; F, female twin pairs; MF, malefemale twin pairs; M F, male and female pairs combined; h2, heritability; c2, shared
environment; CBCL, Child Behavior Checklist (Achenbach, 1991b) [20 items scored as 0 (not true), 1 (somewhat true), and 2 (very true), e.g., bragging and boasting, argues a
lot, cruelty or meanness to other, disobedience (home and school)]; MOCL, Mothers Observational Checklist, including the following behaviors: rejection, destructiveness,
negativism, noncompliance, teasing, physical negative, insult, verbal threat, yelling; ACL, Adjective Checklist (Gough, 1960) [consists of 300 adjectives that yields 26 scales];
MCPS, Missouri Childrens Picture Series (Sines et al., 1966) [consists of 238 line drawings, each portrays the figure of a child engaged in some activity or situation, the subject is
required to sort the cards into two groups, those that look like fun and those that do not look like fun]; PSR, Parent Symptom Ratings (Conners, 1970) [includes six aggression
items: bullying, hits or kicks other children, mean, sassy to grown-ups, fights constantly, picks on other children]; IBS, Interpersonal Behavior Survey (Mauger, 1980) [includes

items such as: some people think I have a violent temper or I try not to give people a hard time]; The Mathews Youth Test for Health (MYTH; Mathew and Angulo, 1980)
[developed to measure Type A behavior in school-aged children. The instrument consists of 17 items characterized by overt type A behavior and yields two subscales: impatience/
aggression and competitive achievement striving]; BDHI, Buss-Durkee Hostility Inventory (Buss and Durkee, 1957) [contains of three subscales: the assault scale (10 items on
physical aggression), the verbal hostility scale (13 items on verbal aggression), and the indirect hostility scale (nine items on indirect or undirected or displaced aggression)];
MPQ, Minnesota Personality Questionnaire (Tellegen, unpublished) [physically aggressive, vindictive, likes violent scenes, higher order factor, negative emotionality]; Physical
Aggression scale, (Simonoff et al., 1998) [items on physical aggression, extortion, public fight, use of weapon in a fight, cruelty to animal, thrown objects at people, carried a
weapon, sworn at teacher, based on Olweus, 1989]; Physical Aggression scale (Dionne et al., 2003) is a 37 item check list on which parents reported whether the child engaged,
sometimes engaged, often engaged in a behavior. Based on factor analysis, 10 of the 37 behaviors were determined as direct physical aggression, for example, is cruel toward others,
bullies other children, bites others, kicks, fights, takes things away from others, pushes, threatens to hit; IAB, instrument of aggressive behavior (Olweus, 1989) [contains two
subscales: aggressive and nonaggressive antisocial behavior. The aggression scale contains 11 items of direct verbal and physical aggression, e.g., swearing at a teacher, bullying];
MPNI, Multidimensional Peer Nomination Inventory (Pulikkined et al., 1999) [contains of 38 items and the aggression subscale contains of six items, e.g., calls people names,
may hurt other kids, bullying, goes around telling peoples secrets to others]; Ad-Health [aggression is based on four items, got into a serious physical fight, hurt someone badly
enough they needed medical care, used to threaten to use a weapon to get something from someone, took part in a gang fight]; DISC, Diagnostic Interview Schedule for Children
(Shaffer et al., 2000) [Gelhorn et al. (2006) only included aggression to people or animals, items 17]; BPAQ, Buss and Perry Aggression Questionnaire (Buss and Perry, 1992)
[nine items on physical aggression and five items on verbal aggression, e.g., I cannot help getting into arguments when people disagree with me, I have threatened people I know, I
get into fights a little bit more often than average people]; DSM-IV, the Norwegian version of the Structured Interview for DSM-IV personality (Pfohl et al., 1997) [the
instrument is a semi-structured diagnostic interview for the assessment of all DSM axis II disorders, including passive-aggressive personality disorder]; CAPS, Child and
Adolescent Psychopathology Scale (Lahey et al., 2004) [relational aggression was assessed via the CAPS, a structured interview assessing DSM-IV symptoms of common
childhood disorders. Seven items measured relational aggression, for example, tried to keep kids he/she does not like outside his/her friend group, spread rumors to make others
stop liking someone, stopped talking to people because he/she was mad at them, teased other people in a mean way]; RPQ, Reactive and Proactive Questionnaire (Raine et al.,
2006). [The RPQ is a validated 23-item questionnaire designed to measure reactive and proactive aggression in children and adolescents from the age of 8. The RPQ includes 11
reactive items (e.g., he/she damages things when he/she is mad; he/she gets mad or hits others when they tease him/her) and 12 proactive items (e.g., he/she threatens and
bullies other kids; he/she damages or breaks things for fun). The items in the RPQ have a three-point response format: 0 never, 1 sometimes, 2 often.]; RFAB, USC twin
study of Risk Factors for Antisocial Behavior; TCHAD: Twin Study of Child and Adolescent Development.
a
Heritability estimate is based on either Holzingers H or Falconer equation and did not report shared environmental influences.
b
Parent reported CBCL ratings were not collected at age 8.
c
Genetic and shared environmental estimates were not reported by the authors.

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Tuvblad and Baker

aggressive and antisocial outcomes. All three of these studies are ongoing. One of
these is the University of Southern California Twin Study of Risk Factors for
Antisocial Behavior (RFAB), which is a prospective study of the interplay of
genetic, environmental, social, and biological (psychophysiological) factors on
the development of antisocial and aggressive behavior from childhood to emerging
adulthood. The project includes more than 750 twin pairs studied on several
occasions, at ages 910, 1113, 1416, and 1718 years (Baker et al., 2006). A
second major twin study is the Environmental Risk Longitudinal Twin Study (Erisk study) in the United Kingdom. The E-risk study involves data on more than
1000 twin pairs at ages 5, 7, and 12 with the special focus on what factors in the
home, family, school, and neighborhood (i.e., environmental risks) promote childrens aggression (Moffitt, 2002). The Minnesota Study of Twins and Families
(MFTS) is a third major longitudinal twin study that specifically investigates
antisocial behavior and substance use across development. MTFS was established
in 1989 using same-sexed twin pairs aged 11 or 17. Five hundred additional 11-yearold twin pairs were added in 2000. All twins of those ages, who were born in
Minnesota, as identified by birth registry data, were invited to participate. Participants are asked about academic ability, personality, and interests; family and social
relationships; mental and physical health; and physiological measurements. Of
particular interest are prevalence of psychopathology, substance abuse, divorce,
leadership, and other traits and behaviors related to mental and physical health,
relationships, and religiosity (Iacono et al., 2006; Keyes et al., 2009).
Before reviewing the twin and sibling adoption studies on aggressive
behavior presented in Tables 8.1 and 8.2, it is important to consider the ways in
which the phenotype of aggressive behavior is defined and measured. The various
instruments utilized in the studies reviewed in this chapter are summarized in
Tables 8.1 and 8.2, to provide a clear idea of the nature of the aggressive behavior
phenotype being investigated. By and large, the Child Behavior Checklist
(CBCL; Achenbach, 1991b) has been used more often than any other single
instrument in behavioral genetic studies of aggression. Although self-report
version of the CBCL is available for older adolescents and young adults (Youth
Self Report (YSR); Achenbach, 1991c), studies more commonly rely on parent
or teacher (Teachers Report Form (TRF); Achenbach, 1991a) rating versions.
The aggressive behavior subscale of the CBCL includes 20 items on which the
child is rated. These include defiance, argumentativeness, physical aggression,
and cruelty toward others. Although there are a handful of other instruments
that also yield single aggressive behavior scores, two instruments provide multiple scales: the Reactive and Proactive Aggression Questionnaire (RPQ; Raine
et al., 2006), which provides separate scales for aggressive reactions to provocation and more planned or proactive forms of aggression; and the Buss-Durkee
Hostility Inventory (BDHI; Buss and Durkee, 1957), which yields several subscales of aggression, including assault, verbal, and indirect hostility.

8. Human Aggression Across the Lifespan

185

The studies summarized in Tables 8.1 and 8.2 vary on how aggressive
behavior was defined (i.e., physical, verbal, relational, reactive, proactive, indirect,
bullying) and measured (observation, self-report, parent/caregiver, teacher). A
wide range of ages were included, from preschool children to adults; however,
the vast majority of studies have used childhood samples (i.e., 12 years of age or
younger) which explains why the CBCL is so frequently used to assess aggressive
behavior. Correlations for biological and adoptive siblings (Table 8.1), and MZ
and DZ twins (Table 8.2) are shown for each study. Most studies reported correlations separately for same-sex pairs of males (M), females (F), and opposite-sex pairs
(MF); however, a few studies involve correlations for samples of male and female
pairs combined. We review the key questions concerning the genetic influence
(heritability) of human aggression based on the effect sizes reported for these
studies. We also examine various potential moderators of these effects, including
sex, age, method of assessment, form of aggression, study design (twin vs. sibling
adoption design), and various social factors and circumstances that may exacerbate
or ameliorate the genetic risk for aggression from one person to the next.

A. Does heritability vary depending on sex?

Since it is well documented that males are much more likely than females to
engage in most forms of aggressive behavior (Moffitt et al., 2001; Rutter et al.,
2003), it is also of interest to examine whether the same genetic and environmental influences are important in both sexes and whether the magnitude of
these effects differs between males and females.
In the classical twin design, genetic and environmental variance components for aggressive behavior can be estimated using data from same-sex MZ
and DZ twins. Apart from estimating genetic and environmental effects on
aggression, it is also possible to investigate whether sex-specific genetic or
environmental influences are important. Such effects are referred to as sexlimitation or sex-limited effects. There are two primary questions about sex
limitation in genetic research, one being whether there are qualitative differences
between males and females, such that different genes and/or environmental
influences operate in the two sexes, and whether quantitative differences exist
in the relative magnitude of influences across sexes. To assess whether the
magnitude of genetic and environmental effects in aggressive behavior differ
between males and females (i.e., quantitative sex differences), only data from
same-sex twin pairs are required. However, to determine whether or not it is the
same set of genes or shared environmental experiences that influences aggressive
behavior in males and females (i.e., qualitative sex differences), data from
opposite-sex twin pairs are also needed. If qualitatively different genetic influences are important for aggressive behavior in males and females, then the
opposite-sex twins will be less genetically similar for the trait than DZ twins.

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Tuvblad and Baker

Not all twin studies have examined sex-limited effects, either qualitative or quantitative, and several studies combined males and females when
computing twin correlations, making it impossible to evaluate these effects
based on published results shown in Table 8.2. Nonetheless, quantitative sex
differences can be easily evaluated across at least 18 studies in Table 8.2, which
present separate twin or sibling correlations by sex. Among these, there are a
dozen studies that also include MF, which allow investigation of qualitative sex
differences. The average twin correlations across these 18 studies, weighted by
their respective sample sizes, shows quite similar twin correlations for both
identical (rMZMales 0.66; rMZFemales 0.63) and nonidentical same-sex pairs
(rDZMales 0.42; rDZFemales 0.35), indicating that there are no appreciable
quantitative sex differences in aggressive behavior. This is consistent with the
individual results across studies which formally tested for quantitative sex differences (e.g., Baker et al., 2008; Czajkowski et al., 2008; Eley et al., 1999; Finkel
and McGue, 1997; Tackett et al., 2009; Tuvblad et al., 2009). As indicated in
Table 8.2, only a small handful of studies have reported significant differences in
heritability of aggression for males and females (and these are primarily for
younger samples; e.g., Hudziak et al., 2003; van Beijsterveldt et al., 2003;
Vierikko et al., 2004). The lack of quantitative sex differences is also well in
line with what was reported in a recent meta-analysis summarizing 19 twin and
family/adoption studies, whereby genetic influences were found to explain 54%
of the variance in aggressive behavior in boys and 57% of the variance in girls
(Burt, 2009).
There is no evidence of qualitative sex differences either, given that the
weighted twin correlation for MF (DZMaleFemale) is 0.38, which is quite similar
to the same-sex DZ twin correlations (0.42 in males and 0.35 in females).
In spite of the consistent sex difference in mean levels of aggression, the
underlying etiologies of aggressive behavior appear to be remarkably similar for
both sexes. There may still be biological and social differences between the sexes
that might account for the greater mean levels of aggression observed in males,
yet the same genes and the same environmental factors appear to explain
individual differences in aggression within each sex to the same degree. One
interesting question that has not been addressed, however, is to what extent
there may be sex differences in moderators of genetic factors. In other words,
there may be different circumstances or experiences in males and females that
lead to greater expression of genetic predispositions for aggression. For example,
sexual jealousy might trigger genetic propensity for aggression to a greater extent
in males than females, while threats to resources might be a more important
moderator of genetic influences in females compared to males, as discussed
in Chapter 9. Other moderators are discussed later in II.A, although more
research is clearly warranted to explore the degree to which they may be sex
specific.

187

8. Human Aggression Across the Lifespan

B. Does heritability change across age?

Although genetic studies of aggression have spanned from childhood to adulthood, most studies included in Tables 8.1 and 8.2 involved children 12 years of
age or younger. This suggests that more studies examining the heritability of
aggressive behavior in adolescents and adults are needed. Keeping this in mind, it
is useful to examine the magnitude of twin correlations across age groups, which
span from early childhood to middle-age adults. These correlations are summarized in Fig. 8.1, according to five age groups (early childhood, age 1.56 years;
middle childhood, age 710; adolescence 1115; late adolescence/young adulthood, age 1626; and adulthood, age 2748; Fig. 8.1). These results show that
aggressive behavior is clearly influenced by genetic factors across the lifespan,
given the fact that the MZ correlations exceed those for DZ pairs at all ages. (The
Twin correlations across age groups (all studies)

Mean twin correlation

0.80

0.60

0.40

0.20

0.00
Early
childhood
(1.56)

Middle
childhood
(710)

Adolescence
Late
(1115)
adolescence/
young adult
(1626)

Adult
(2748)

Age group
Zygosity
MZ

DZ samesex

DZ malefemale

Figure 8.1. Twin correlations across age groups (all studies).

188

Tuvblad and Baker

lack of qualitative sex differences is also evident across the life span, in that the
DZ correlation is comparable for same-sex and MF pairs across ages.) However,
both MZ and DZ correlations decline steadily across development, suggesting the
waning importance of shared environmental effects from childhood to adolescence and then adulthood. The DZ correlation exceeds half the value of the MZ
correlation (taken as evidence for shared environment) only in early childhood,
but not in later age groups. The pattern shown in Fig. 8.1 is evident in individual
studies as well. Aggressive behavior in childhood is influenced by genetic factors
in all studies, and most of these studies also report shared environmental influences (Table 8.2; e.g., Baker et al., 2008; Eley et al., 1999; Hudziak et al., 2003;
Schmitz et al., 1995; Simonoff et al., 1998; Tuvblad et al., 2009; van den Oord
et al., 1996; Vierikko et al., 2004; but for an exception see Dionne et al., 2003;
Taylor, 2004). Studies including adolescent twins ( younger than 19 years of
age) do not in most cases report finding any shared environmental influences
(Table 8.2; e.g., Button et al., 2004; Cho et al., 2006; Gelhorn et al., 2006;
Tackett et al., 2009). Similarly, studies including adult twins do not report
finding any shared environmental influences (Table 8.2; e.g., Coccaro et al.,
1997; Finkel and McGue, 1997; von der Pahlen et al., 2008; but for an exception
see Czajkowski et al., 2008). The overall pattern across the studies presented in
Table 8.2 and Fig. 8.1 indicates that genetic influences for aggressive behavior
become increasingly more important, while shared environmental effects become less so as children develop from childhood, through adolescence, and into
adulthood. Similarly, findings from a recent meta-analysis reported that genetic
influences increased from 55.2% at ages 15 years to 62.7% at ages 610 years
and 62.9% at ages 1118 years. At the same time, shared environmental influences were decreasing from 18.7% at ages 15 years to 13.9% at ages 610 years
and 2.7% at ages 1118 years (Burt, 2009). This pattern of decrease in shared
environment, and a concomitant increase in heritability during development, is
relatively common for personality traits and cognitive abilities (Bartels et al.,
2002; Loehlin, 1992; Plomin et al., 2001; Scarr and McCartney, 1983), and has
also been found for other phenotypes including prosocial behavior (Knafo and
Plomin, 2006).
It should also be kept in mind, however, that methods of assessing
aggression vary across age, such that studies of children tend to rely on ratings
by teachers and parents, while studies of adults (and some older adolescents) rely
more heavily on self-report methods. The confound between method of assessment and age of the subjects has made it difficult in prior studies and metaanalyses to disentangle age effects on heritability from differences that arise from
different methods of assessment. Increasing heritability estimates from child to
adulthood could therefore also be explained by different methods of assessment
as well (e.g., parental bias may lead to overestimation of shared environmental
effects and thus attenuate heritability estimates in childhood).

189

8. Human Aggression Across the Lifespan

C. Do heritabilities vary across methods of assessment?

It is important to examine the magnitude of twin correlations across methods of
assessment, as heritability estimates may vary depending on who is rating the
subject. This is especially important given the age trends found for heritable
influences in Fig. 8.1, since different methods of assessment tend to be employed
for different age groups. As previously discussed, studies of younger subjects rely
on parent or teacher ratings, while self-report methods are typically used in studies
of adults and often adolescents. The twin correlations are summarized in Fig. 8.2,
according to laboratory observation, self-reports, teacher ratings, and parent/
caregiver ratings. Indeed, twin correlationsand thus the estimates of genetic
and environmental influences on aggressive behaviordo appear to vary across
method of assessment. According to the twin correlations summarized in Fig. 8.2,
the heritability of aggressive behavior based on laboratory observation is approximately 32% [h2: 2(rMZ  rDZ) 2(0.27  0.11)], dominant genetic effect accounts
for approximately 10% [d2: 2(rMZ  rDZ) 2(0.27) 4(0.11)], and the nonshared
Twin correlations across method of assessment (all studies)
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Observation

Self-report
MZ

DZ same-sex

Teacher

Parent

DZ male-female

Figure 8.2. Twin correlations across method of assessment (all studies).

190

Tuvblad and Baker

environment accounts for the remaining 58% of the variance. The heritability of
aggressive behavior based on self-reports is 40% and the nonshared environment
accounts for the remaining 60% of the variance. There is no evidence of shared
environmental contribution, as the DZ correlation is approximately half the MZ
correlation. The heritability of aggressive behavior based on teacher ratings is
54%, shared environmental influences account for 6% [c2: 2rDZ  rMZ 2(0.33 
0.60)], and the nonshared environment accounts for the remaining 40% of the
variance. The heritability of aggressive behavior based on parent/caregiver ratings
is 54%, shared environmental influences account for 17%, and the nonshared
environment accounts for the remaining 29% of the variance. Thus, parent/
caregiver ratings have the largest familial influence, explaining 71% of the
variance (h2 c2 0.54% 17%) in individual differences in aggressive behavior. It should be kept in mind that this is a descriptive approach and that formal
modeling is required to determine how well these estimates describe the observed
data. Also, this approach does not allow for actual testing of different hypotheses,
for example, to test whether it is possible to set any of these effects to zero. It is
difficult to discern whether the parent/caregiver rating patterns reflect true shared
environment or are instead an artifact of rater bias whereby raters are less able to
discriminate between the two twins aggressive behavior and thus inflate the
similarities between them, regardless of zygosity. In fact, when the two co-twins
are rated by different teachers (e.g., they are in different classrooms), twin
correlations are lower for both MZ and DZ pairs for the wider construct of
antisocial behavior (Baker et al., 2007).
A few specific twin studies in Table 8.2, which utilize multiple raters in
their design, also illustrate that genetic and environmental influences on aggressive behavior vary depending on method of assessment. For example, twin
similarity for relational aggression was influenced only by genetic factors when
using self-reported data, explaining 49% of the total variance. When using parent
ratings (only biological mothers were used as raters) of relational aggression both
genetic and shared environmental influences were important (boys: h2 21%,
c2 46%, e2 33%; girls: h2 42%, c2 22%, e2 36%). However, when using
youth self-reports, only genetic and nonshared environmental influences were
significant (h2 49%, e2 51%; Tackett et al., 2009). A similar pattern was found
for reactive and proactive aggression in 910-year-old boys, whereby only genetic
influences were important for self-reports, but both genes and shared environment
were important for teacher and parent ratings (Baker et al., 2008). Aggressive
behavior in another sample of twins aged 712 years was found to be largely
influenced by genetic (or familial) factors (76%84%), as reported by parents.
Data were collected from one or both parents; however, only mother-reported
ratings were included in the analyses, as they accounted for the majority of the
ratings collected (85.3%90.1%). In contrast, when teacher ratings were used,
aggressive behavior was found to be slightly less influenced by genetic (or familial)

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factors (42%61%; Haberstick et al., 2006a). Significant shared environmental

effects were not found for either parent or teacher ratings, and were therefore
dropped from the models, suggesting that any shared environmental influences
are likely to be included in the genetic component. Apart from rater bias, which
may result in inflated twin similarity across the board when using single raters for
multiple children, the varying patterns of genetic and environmental influence
across methods of assessment could be the result of different raters reporting
different aspects of the childs aggressive behavior. This could arise in part because
individuals behave differently in different situations (e.g., school vs. home) or
because some types of aggressive behaviors are more likely to be noticed (e.g.,
overt forms such as physical aggression) than other types of aggressive behaviors
which may be more subtle or covert (e.g., relational aggression). Different raters
provide important and unique pieces of information regarding behaviors. Selfreporters are aware of their own motives and behaviors, which may go undetected
by their caregivers, teachers, or peers. On the other hand, caregivers or teachers
may be able to understand difficult and complex constructs better than children.
A teacher is also more likely to compare a childs behavior to his or her peers,
whereas a parent is likely to compare a childs behavior to his or her siblings
(Bartels et al., 2003). Regardless of the source of these discrepant results across
methods of assessment, it is important to keep in mind that when it comes to
studies of aggression, it matters who is doing the rating.

D. Do heritabilities vary across forms of aggression?

Different types of aggressive behavior have been investigated across twin and
adoption studies, with notable distinctions between reactive and proactive forms
of aggression, as well as direct/physical and indirect/relational aggression
(Table 8.3). It is likely that there are different etiologies for different forms of
aggression; for example, defensive reactions to threatening stimuli may be more
environmentally influenced, while more planned, proactive forms may be more
genetically influenced (Tuvblad et al., 2009). Comparing heritability estimates
collectively across the various measures employed is a reasonable way to address
Table 8.3. Forms of Aggression
Form of aggression
Reactive/hostile/affective
Proactive/instrumental
Direct/physical
Indirect/relational

Description
Angry or frustrated responses to a real or perceived threat
Planning, the motive of the act extends beyond harming the victim
Intentionally causing pain or harm to the victim
Relational social manipulation such as gossip and peer exclusion

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this question about whether some kinds of aggression are more heritable than
others. When multiple forms of aggressive behavior are measured within the
same study, it is also possible to investigate the extent to which the same genes
and/or environmental factors are important to different manifestations of aggressive tendencies.
Reactive aggression refers to angry or frustrated responses to a real or
perceived threat. This specific type of aggression has been characterized to
involve both high emotional arousal, impulsivity, and an inability to regulate
or control affect. In contrast, proactive aggression is conceptualized as a more
regulated, instrumental form of aggression, with more positive expectancies
about the outcomes of aggression (Dodge, 1991; Dodge and Coie, 1987;
Schwartz et al., 1998). Although reactive and proactive aggression have each
been found to be mainly influenced by genetic and nonshared environmental
factors, their genetic correlation is significantly less than 1.0, indicating some
genetic specificity for the two forms of aggression. Reactive and proactive aggression
each exhibit different developmental patterns in these influences (see Table 8.2;
Baker et al., 2008; Tuvblad et al., 2009), that is, the genetic and environmental
stability in reactive and proactive aggression has been found to differ. In one of the
few longitudinal analyses of these constructs, the stability in reactive aggression
from childhood to adolescence could be explained by genetic (48%), shared (11%),
and nonshared (41%) environmental influences, whereas the continuity in proactive aggression was primarily genetically (85%) mediated (Tuvblad et al., 2009).
Relational forms of aggression, which involve social manipulation such
as gossip and peer exclusion, are often more indirect compared to other forms of
aggression (Crick and Grotpeter, 1996). Like reactive and proactive forms,
relational aggression appears to be influenced by genetic factors, both in
self-report (49%) as well as parental reports (boys, 42%; girls, 21%). However,
unlike the other more direct forms of aggression, relational aggression is also
influenced by shared environmental influences, but only in parental reports
(boys, 22%; girls, 46%) and not in self-report measures (Tackett et al., 2009).
Together these findingsthat is, the less than perfect genetic correlation between reactive and proactive forms, their different developmental etiologies,
and the significant shared environmental effects in relational aggression only
provide support for at least some genetic and environmental etiological distinction among different forms of aggression. It should be noted, however, that no
study to date has examined the genetic and environmental overlap between
relational aggression and other forms such as proactive and reactive aggression.
Other studies based on multifactorial measures of aggression, such as the
BDHI, suggest some variability in the heritability estimates across subscales,
although the patterns are not entirely consistent across studies. For example,
indirect hostility showed the lowest heritability (28%) in one study of adult
twins (Coccaro et al., 1997), compared to modest heritability for verbal

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hostility (47%) and assault (40%). Yet, Cates et al. (1993) found no genetic
influences for assault, but strong heritability for both verbal hostility (78%) and
indirect hostility (70%). In multivariate genetic analyses, both studies found
some support for genetic specificity for the various subscales, similar to what has
been found for reactive and proactive aggression, in that genetic correlations
(rG) among the BDHI subscales were less than unity: rG 0.39 between indirect
hostility and assault, rG 0.60 between indirect hostility and verbal hostility,
rG 0.17 between verbal hostility and assault (Coccaro et al., 1997), rG 0.35
between indirect hostility and assault, rG 0.39 between indirect hostility and
verbal hostility, and rG 0.49 between verbal hostility and assault (Cates et al.,
1993). Overall, genetic influences are generally found for most, if not all forms of
aggression, although somewhat different genetic factors may be operating across
these different forms. The mechanisms that underlie more direct, planned,
confrontational, and often physical forms of aggression may to some extent be
different than those for reactive or indirect aggressive behaviors.

E. Does heritability vary depending on study design (twins vs.

adopted siblings)?
There were only a handful of studies identified examining the heritability of
aggressive behavior using the sibling adoption design. Visual inspection of the
results from these sibling adoption studies (see Table 8.1) compared to the results
from studies including twin samples (Table 8.2) indicate that heritability estimates
(i.e., h2) and the shared environmental estimates (i.e., c2) for aggressive behavior are
very similar. This is also well in line with the results of a meta-analysis on antisocial
and aggressive behavior that found no differences between twin and sibling adoption
studies (h2 48%; c2 13%, e2 0.39%) (Rhee and Waldman, 2002). Thus, the
heritability of aggressive behavior does not seem to vary depending on study design.

F. Criticisms of twin and adoption studies: Assumptions and

generalizability
There are several assumptions in both twin and adoption studies that are important
to consider when reviewing their findings. In adoption studies, the most important
factors are (1) random placement of the adoptees into homes and (2) generalizability. Selective placement or matching (i.e., similarities between adoptive and
biological parents) for certain characteristics can lead to inflated correlations
between adoptive siblings (and thus overestimated effects of shared environment).
Although such matching may occur for physical characteristics (including race),
direct selective placement is unlikely to be made for aggressive behavior, per se.
(Children with more aggressive or antisocial biological parents would not be placed
into homes with more aggressive adoptive parents.) Thus, it is unlikely that the

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genetic and environmental effects summarized in Table 8.1 are biased in any way as
a result of selective placement. In terms of generalizability, it is often the case that
adoptive parents tend to be in good health and from higher socioeconomic levels;
thus, findings from adoption studies may not always be unquestionably generalized
to the entire population (Rutter, 2006). Adopted children may also be at greater
risk for aggression compared to nonadoptees, since birth parents giving up their
children may have increased rates of disordered behaviors, including substance use,
criminal offending, and aggression (Cloninger et al., 1985; Lewis et al., 2001). In the
Deater-Deckard and Plomin (1999) study, the adopted children did in fact have
higher aggression scores compared to the nonadopted children, consistent with the
notion that adoptees may be at higher genetic risk for aggression compared to
nonadopted individuals. The elevated levels of aggression in adoptees occurred in
spite of the fact that background characteristics of the adoptive families were found
to be representative of families with children in the larger Denver area, and that the
demographic characteristics of the adoptive grandparents and the adopted childrens biological grandparents were similar, with regard to educational and occupational level. Similarly, van der Valk et al. (1998) reported mean differences
between adoptees and nonadoptees, with adoptees showing higher mean levels in
aggressive behavior. About 75% of the adoptees were adopted from Korea, India,
Columbia, Indonesia, Bangladesh, or Lebanon and the remaining 25% were
adopted from European or other non-European countries in both the van der
Valk et al. (1998) and the van den Oord et al. (1994) studies, and the majority of
the adoptive parents had a higher level of occupation. Given the higher aggression
scores among adoptees compared to nonadoptees, as well as the somewhat greater
affluence and ethnic heterogeneity in at least some of the adoption samples, the
generalizability of adoption study results to the wider population could be
questioned.
To what extent are the twin study results generalizable to the wider
population? Twins and singletons have been found to experience similar rates of
psychiatric disorders (e.g., attention-deficit hyperactivity disorder (ADHD),
oppositional defiant disorder, conduct disorder) and behavioral and emotional
problems (Gjone and Novik, 1995; Moilanen et al., 1999; Simonoff et al., 1997;
van den Oord et al., 1995). Findings from the RFAB study show no differences in
mean levels between MZ and DZ twins in reactive or proactive aggression (Baker
et al., 2008; Tuvblad et al., 2009). It can, therefore, be assumed that twins and
singletons display equal rates of aggressive behavior.
There are, however, two ways in which twins differ from singletons:
(i) lower birth weight, due to shorter length of gestation (Plomin et al., 2001) and
(ii) delayed language development (Rutter and Redshaw, 1991). Birth weight has
been found to have a minimal effect on academic performance; for twins this effect
was judged relative to what is a normal birth weight for twins and not for singletons
(Christensen et al., 2006). However, studies have shown that children with birth

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complications are more likely to later develop antisocial and aggressive behavior
(Raine, 2002), but birth complications may not by themselves predispose antisocial
and aggressive behaviors, but will require the presence of an environmental risk
factor (e.g., poor parenting, maternal rejection). In other words, the relationship
between birth complications and antisocial and aggressive behavior is confounded
by environmental risk factors (Hodgins et al., 2001; Raine et al., 1997).
In addition to generalizability, there are several key assumptions of the
classical twin design that need to be kept in mind when reviewing findings from
these studies. These include (1) the equal environments assumption, (2) random
mating, and (3) lack of correlation or interaction between genetic and environmental influences. We briefly review each of these assumptions hereboth in
general and as they pertain to aggressive behavior in particularand consider
their possible effects on the results summarized across studies.
Perhaps the most important and commonly criticized assumption is the
equal environment assumption (EEA). In the classical twin design, MZ twins,
who are assumed to share 100% of their genes, are compared to DZ twins, who
are assumed to on average share 50% of their genes. If MZ twins are more similar
than DZ twins, it may be inferred that the difference is caused by genetic effects.
To make this inference, however, it is necessary to rely on the EEA. It is assumed
that environmentally caused similarity is roughly equal for both MZ and DZ
twins. If this assumption is violated, higher correlations among MZ twins may be
due to environmental factors, rather than genetic factors, and heritability estimate will be overestimated (Plomin et al., 2001).
Several twin studies of various phenotypes have examined the EEA.
One way to test the validity of the EEA is to examine whether a trait of interest is
influenced by perceived versus assigned zygosity. The effect of perceived zygosity
can be added as a specified familial environment in a univariate ACE twin
model (Kendler et al., 1993) and if this parameter can be omitted without any
significant loss in data fit, it can be assumed that the EEA holds for the
phenotype under study. These studies generally report that the EEA assumption
holds for numerous phenotypes such as physical activity, eating behavior, psychiatric disorders (e.g., major depression, generalized anxiety disorder, phobia,
alcohol, and drug abuse; Eriksson et al., 2006; Hettema et al., 1995; Kendler et al.,
1993; Klump et al., 2000; Xian et al., 2000), including child and adolescent
psychopathology such as anxiety disorder, ADHD, oppositional defiant disorder,
conduct disorder, antisocial behavior (Cronk et al., 2002; Jacobson et al., 2002;
Tuvblad et al., 2011) as well as aggressive behavior (Derks et al., 2006).
The assumption of random mating for aggression in the parents of the
twins is also important to consider, since nonrandom mating can lead to
increased resemblance for DZ but not MZ twin pairs. Assortative mating in the
parent generation acts to increase the resemblance between dizygotic twins and
thereby bias shared environmental estimates upward and additive genetic effects

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downward. A significant correlation between spouses for a particular trait is often

interpreted as assortative mating (Maes et al., 1998). This assumption is probably
violated when it comes to antisocial and aggressive behavior, as significant
spouse correlations have been found suggesting that assortative mating exists
in this behavioral domain (Krueger et al., 1998; Maes et al., 2007; Taylor et al.,
2000). Taylor et al. (2000) found that parents of twins were correlated for
retrospectively reported delinquency (r 0.23 in families of boys and r 0.35
in families of girls) and concluded that assortative mating is modest in degree.
Another study using data from the Dunedin sample in New Zealand (Silva and
Stanton, 1996) when the participants were 21-years-old found a correlation
(r 0.54) between couple members reports of antisocial behavior in their
peers (i.e., participants were asked how many of their friends had aggression,
personal, alcohol, or drug problems, or did things against the law), which was
identical to the correlation for couple members reports of their own antisocial
behavior as measured by a variety of offenses (e.g., theft, force, fraud, vice). They
concluded that assortative mating for antisocial behavior is substantial and that
antisocial individuals tend to cluster in peer groups with similar antisocial peers.
As such, assortative mating should to be taken into account when modeling
antisocial behavior (Krueger et al., 1998). It is interesting, however, that the
shared environmental effects are fairly negligible in twin studies of aggressive
behavior, both in the prior meta-analyses as well as in our summary in Table 8.2.
Thus, any assortative mating for aggression does not appear to have resulted in
severe overestimates of shared environment when considering these studies
en masse. It is possible, on the other hand, that genetic influences themselves
have been underestimated and could be larger than the 50% or so than these
meta-analyses and our summary suggest.
It is also assumed in the classical twin design that genetic and environmental influences combine additively (i.e., do not interact) and are uncorrelated.
It is possible, however, that some genetic predispositions may be associated with
certain kinds of social environments or experiences, leading to a correlation
between genes and environments. (G
E interactions are also discussed at
length in a later section of this chapter.) Such G
E correlations (rGE) can
arise in three different ways (Scarr and McCartney, 1983): (i) Passive rGE occurs
when genes overlap between parents and their offspring. For example, a child
with aggressive parents inherits genetic susceptibility for aggression as well as
experiences an adverse rearing environment. An example of passive rGE was
reported in a study comparing genetic and environmental influences on mothering. Passive rGE correlations were suggested for mothers positivity and monitoring. For mothers negativity and control, primarily nonpassive rGE correlations
were suggested (Neiderhiser et al., 2004). (ii) Evocative/reactive rGE can arise
when a specific child characteristic elicits a particular response from the environment. For example, aggressive children tend to elicit more negative affect and

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harsh discipline from their parents (Ge et al., 1996; OConnor et al., 1998). In a
more recent study, using the classical twin design the association between
parental criticism and adolescent antisocial behavior was found to be entirely
genetically influenced. Approximately half of the genetic contribution to this
association was explained by early adolescent aggression. Thus, child aggression
seemed to elicit negative parenting followed by adolescent antisocial behavior,
indicating an evocative rGE (Narusyte et al., 2006). (iii) Active rGE is defined as
the process whereby an individual actively seeks out environmental situations
that are more closely matched to the persons genotype. Active rGE has been
suggested in adolescent drinking behavior, specifically among girls (Loehlin,
2010). If the assumption of no G
E correlation is violated, heritability estimates
for aggressive behavior in twin studies could include both additive genetic effects
and the effects of G
E correlation (i.e., heritability estimates are inflated).
Apart from these specific examples cited here, few studies have examined the
effects of rGE in aggressive behavior, making it difficult to know the extent of
their effect on heritability estimates in twin studies.
In conclusion, findings from adoption studies should probably be
generalized cautiously to other populations as adoptees tend to show higher
scores on aggressive behavior compared to controls. On the other hand, most
of the assumptions of the classical twin design seem to hold for aggressive
behavior. The EEA has been tested and found to hold for various phenotypes
including aggressive behavior, and twins and singletons have been found to
display similar scores on aggressive behavior, suggesting that findings from twin
studies can be generalized to other populations. Most twin studies report finding
little or no shared environmental influences on aggressive behavior, suggesting
that random mating is of little importance for aggressive behavior. Only a few
studies have examined the influence of G
E correlation on aggressive behavior,
suggesting that more research is needed on this topic before we can draw any firm
conclusions. Last, in the classical twin design, it is assumed that genetic and
environmental influences combine additively and do not interact. This assumption is probably violated to some extent when it comes to aggressive behavior,
as several studies have reported finding significant interaction effects. G
E
interaction is discussed in detail in the next section of this chapter.

II. G
E INTERACTION IN AGGRESSIVE BEHAVIOR

There is a general recognition that genes and environment work togetheroften
in complex waysto produce wide variations in behavior and psychological
function. G
E interaction, by definition, is a statistical term indicating that
genetic effects on a given phenotype depend upon environmental factors or vice
versa. Gene expression, for example, can be moderated by an individuals

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experiences or exposure to certain environments. Likewise, various individuals

may respond differently to the same environmental exposure because they have
different genotypes. Such genetic sensitivity to the environment has been
demonstrated extensively in plant and animal species for a variety of traits. But
even though the importance of G
E interactions in human behavior has long
been considered (Eaves, 1984; Mather and Jinks, 1982), G
E interactions have
been rarely reported in human traits until relatively recently. The failure to find
G
E interactions in studies of human characteristics may be due to a number of
factors. One likely explanation is related to statistical power. In general, it is
difficult to detect G
E effects due to their low statistical power (Rowe, 2003).
For example, behavioral genetic studies rely on genetic relatedness for groups of
individuals, rather than on sharing of specific alleles between pairs of relatives.
Studies relying on variance partitioning often do not find significant G
E
effects, or find that they explain a very small portion of the total variance, and
are thus dropped from further analysis. When G
E is not taken into account in
behavioral genetic studies, heritability estimates will tend to be biased, although
the direction of the bias depends on whether the moderating environmental
influences are of the shared or nonshared variety.
G
E interactions can be tested or modeled in behavioral genetic studies
using several different study designs (e.g., twin or adoption). The two most
frequently used methods testing for G
E interactions in twin and adoption studies
include: (1) a mean levels approach, testing whether mean values of a phenotype
differ across different combinations of genetic risk and environmental settings and
(2) a moderated variance components approach, examining whether genetic and
environmental variance for a trait varies across different measured environmental
settings. These two different methods stem from the same conceptual idea, namely,
that genetic effects vary across environments or vice versa. Their interpretations
and meanings can be rather different, since one is based on means and the other is
based on variances. The mean levels G
E is perhaps a more traditional approach,
is typically presented as a statistical interaction in an ANOVA, and indicates
whether particular experiences, exposures, or other conditions may (on average)
ameliorate or exacerbate specific genetic effects in groups of individuals with
similar genetic and environmental risks. In comparison, the moderated effects
approach does not address mean levels of risk, but instead evaluates whether
variance in genes or environment differs across various measured conditions.
Moderation can occur in either raw variances (VA, VC, and VE) or in relative
effects (i.e., h2, c2, and e2), and may not necessarily coincide with G
E interactions found in mean levels. The latter point is important when evaluating G
E
interactions across studies using these different approaches, since different patterns
can emerge from them. For example, it is possible that certain adverse environments (e.g., low socioeconomic status (SES)) may lead to some genes exerting
stronger effects (mean levels), while overall, the relative variance explained by

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genes (heritability) may be greater in other environments (e.g., high SES). The
approach used for testing G
E interactions can vary across study design, such that
adoption designs or studies with measured genes are generally required for the
mean levels approach, while the moderated variance components approach may be
used in both twin and adoption studies in the absence of measured genes.
In molecular genetic studies, both genes and environment are measured,
rather than inferred from correlations among family members. G
E interactions
can therefore be tested in the general population, that is, without necessary
reliance on a twin or adoption design. There are still advantages, nonetheless,
to include measured genes and measured environments in the context of a familybased design, including twins and other siblings as well as parents and offspring.
Evidence of G
E interaction in aggressive behavior has been reported
in twin and adoption studies, and more recently in molecular genetic studies.
Below is a summary of some of the G
E interaction findings in aggressive
behavior from adoption, twin and molecular genetic studies. We also discuss
two potential moderators of genetic and environmental influences on aggressive
behavior, exposure to media violence, and alcohol use.

A. Potential moderators of genetic influence found in adoption and

twin studies

1. Family adversity and social disadvantage

G
E interaction for aggressive behavior has been found in several of the early
adoption studies, using a mean levels approach. What these early adoption study
findings generally showed was that early adverse environments had a greater
negative impact on genetically higher risk children. Adopted children with
criminal biological parents reared by a family where there was adversity showed
higher rates of antisocial and aggressive behavior than adopted children with
antisocial biological parents not raised in a home with adversity, and than
adopted children raised in adversity who are not at higher genetic risk. For
example, the interaction of inherited and postnatal factors was examined in
about 800 Swedish men adopted at an early age. When both inherited factors
and environmental risk factors were present, 40% were found to be criminal; if
only genetic factors were present, 12.1% were criminal; if only environmental
factors were present, 6.7% were criminal; and with neither inherited nor environmental factors being present, 2.7% were criminal (Cloninger et al., 1982).
The fact that 12.1% plus 6.7% is less than 40% would thus be an indication of
G
E interactions. This finding was later replicated in females (Cloninger and
Gottesman, 1987). It should be pointed out, however, that in the adoption
design, the genetic risk factors themselves are considered in a general way,
such that the exact nature of the genes is left unspecified, both in terms of

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which loci or alleles may be involved and what underlying mechanisms may be
involved in the path from genes to phenotype. Similarly, the environmental risk
factors as indexed by certain traits in the adoptive parents or characteristics of
their home do not necessarily specify the exact nature of the childs experiences
or how these lead to various outcomes.
Further, maltreatment places children at risk for psychiatric morbidity,
especially conduct problems. However, not all maltreated children will develop
conduct problems. A recent twin study tested whether the effect of physical
maltreatment on risk for conduct problems was strongest among those who were
at high genetic risk for these problems using data from the E-risk study, a representative cohort of 1116 5-year-old British twin pairs and their families. Maltreatment
was found to be associated with a greater increase in the probability of developing
conduct problems among children who had a high genetic liability for conduct
disorder compared to children who had a low genetic liability (Jaffee et al., 2005).
This finding is consistent with the G
E interaction found in adoption studies of
antisocial and aggressive behavior, in which genetic effects were more pronounced
in adverse environments. This clearly suggests that children in risky environments
would benefit from interventions. However, another view of this interaction is that
favorable genotypes can play a protective role on childrens risk for conduct
problems, especially under circumstances of maltreatment.
There are also a few studies based on twin samples that have used the
moderated variance components approach to examine whether measured environmental (risk) factors moderate the genetic and environmental variances for
aggressive behavior. For example, the heritability of conduct problems was found
to be lower in children growing up in dysfunctional families and higher in
children growing up in families where dysfunction was absent (Button et al.,
2005). Another twin study used DeFries-Fulker regression analysis to examine
whether genetic and environmental influences on aggressive behavior varied
depending on levels of family warmth (DeFries and Fulker, 1985). Genetic
influence on aggressive behavior was found to be higher in schools with higher
average levels of family warmth. In contrast, environmental influences (both
shared and nonshared) were more important in schools with lower average levels
of family warmth (Rowe et al., 1999). These findings suggest that genetic effects
are more likely to explain individual differences in aggression in more benign
environments, whereas in more disadvantaged environments negative familyrelated factors and context-dependent risks may play a greater role than genetic
predispositions in aggressive and antisocial outcomes.
Many early theories about the causes of delinquency and crime assumed
that delinquents come from socially disadvantaged backgrounds. For example,
Merton postulated that antisocial behavior resulted from the strain caused by the
gap between cultural goals and the means available for their achievement
(Merton, 1957). Social disadvantage and poverty constitute a reasonable robust,

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although not always a strong, indication of an increased risk for antisocial and
aggressive behavior, assessed by self-reports and official convictions (Leventhal
and Brooks-Gunn, 2000; Rutter et al., 1998). SES has also been found to moderate
the relative influence of genetic factors on antisocial and aggressive behavior. In a
sample of Swedish 1617-year-old twins, heritability for antisocial and aggressive
behavior was higher in the more affluent neighborhoods (boys, 37%; girls, 69%)
compared to the less advantaged neighborhoods (boys, 1%, girls, 61%). Conversely, the shared environment was higher in the less advantaged neighborhoods
(boys, 69%; girls, 16%) compared to better-off neighborhoods (boys, 13%; girls,
6%). Following the social push hypothesis, Raine (2002) would suggest that the
genetic factors on antisocial and aggressive behavior are more expressed in a
socioeconomically advantaged environment where the environmental risk factors are absent. On the contrary, genetic factors for antisocial behavior will be
weaker and the shared environment more important in a socioeconomically
disadvantaged environment because the environmental risk factors will camouflage the genetic contribution (Tuvblad et al., 2006).
These studies using the moderated variance components approach (e.g.,
Button et al., 2005; Rowe et al., 1999; Tuvblad et al., 2006), all examine whether
an environmental (risk) factor moderates genetic and environmental variance
on antisocial and aggressive behavior. Findings from these studies show that
heritable influences on aggressive behavior vary depending on environmental
context, indicating the importance of the environmental risk factors in the
development of aggressive behavior as well as for gene expression.

2. Violent media exposure

There is an ongoing debate about whether exposure to violent video games
increases aggressive behavior, and it is very possible that exposure to media
violence could moderate the influences of genetic and environmental influences
on aggressive behavior. One line of research argues that mass media exposures
contribute to a childs socialization. A primary process in such socialization is
observational learning (Bandura, 1973). Children and adolescents mimic what
they see and acquire complicated scripts for behaviors, beliefs about the world,
and moral precepts about how to behave in the long run from what they observe
(Huesmann, 2010). In contrast, another line of research argues that there is little
empirical evidence for a link between media exposure and violence. This line of
research argues that media violence cannot have any important psychological
effect on the risk for aggressive behavior (Ferguson and Kilburn, 2010).
A recent meta-analysis that included 136 studies examined the effects
of violent video games on aggressive behaviors. The evidence suggested that
exposure to violent video games is a risk factor for increased aggressive behavior,

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aggressive cognition, and aggressive affect, and for decreased empathy and
prosocial behavior. Moderator analyses showed significant research design
effects, weak evidence of cultural differences in susceptibility and type of measurement effects, and no evidence of sex differences in susceptibility. Sensitivity
analyses were also carried out and they revealed these effects to be robust, with
little evidence of selection (publication) bias (Anderson et al., 2010).
Others studies examining the relationship between violent video games
and aggressive acts have found little evidence for a relationship. A recent review
included a total of 25 studies comprising 27 independent observations. The
corrected overall effect size for all included studies was only r 0.08 (Ferguson
and Kilburn, 2009). The mixed findings in the literature clearly suggest that more
research is needed to resolve whether there is a link between exposure to violent
video games and aggressive behavior. Also, some studies have found that exposure
to violent video games only explains a small fraction of the variance. An explanation for this paradox could be that exposure to violent video games moderates
the influence of genetic and environmental effects on aggressive behavior, rather
than exerting direct effects. No genetically informative studies have examined
violent video game exposure as a possible moderator of genetic influence on
aggression, however, leaving this as an important area in need of study.

3. Alcohol use
It has long been known that some individuals become aggressive after consuming
alcohol, and the relationship of violence and aggression with alcohol is well
established (Bushman and Cooper, 1990; White et al., 2001). For example, a
review including 130 independent studies found that alcohol was correlated with
both criminal and domestic violence (Lipsey et al., 1997). Despite this, there is so
far no behavioral genetic study that had examined whether alcohol use moderates the influence of genetic and environmental factors on aggressive behavior.
However, the genetic and environmental relationship among alcohol
use and aggressive behavior as well as other disruptive and problem behaviors
within the disinhibitory spectrum such as antisocial behavior, ADHD, conduct
disorder, impulsive and sensation seeking personality traits has been examined in
several large population-based twin studies. On a phenotypic level, disruptive
and problem behaviors within the disinhibitory spectrum can be united by a
common higher order externalizing factor (Krueger et al., 2002, 2005, 2007).
This higher order externalizing factor has been found to be largely influenced by
genetic factors. For example, the genetic influences on a common externalizing
factor describing conduct disorder, substance use, ADHD, and novelty seeking
was found to account for more than 80% of the variation in an adolescent sample
(Young et al., 2000). Strong heritable influences on an externalizing factor of

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203

antisocial behavior, substance abuse, and conduct disorder has also been found
among adults (Kendler et al., 2003). Together these studies provide important
insight into our understanding of externalizing behaviors. It seems that behaviors
and disorders within the externalizing spectrum, including aggressive behavior,
share a common genetic liability.

III. SPECIFIC GENES FOR AGGRESSIVE BEHAVIOR: FINDINGS FROM

MOLECULAR GENETIC STUDIES
Increasing evidence suggests the importance of heritable factors in the development of aggressive behavior (Burt, 2009; Miles and Carey, 1997; Rhee and
Waldman, 2002). The first study that showed a link between a specific genotype
and aggressive behavior examined the genetic material of members of a large
Dutch family. This specific family had for decades been found to be prone to
violent, aggressive, and impulsive behavior, including fighting, arson, attempted
rape, and exhibitionism. Some of the male family members were also intellectually disabled. The aggressive males in this large family were shown to share a
mutation in the gene that codes for the enzyme MAO (monoamine oxidase A).
MAO breaks down brain chemicals (neurotransmitters) such as serotonin, noradrenaline, and dopamine, which transmit messages from one nerve cell to the
next. In the afflicted males, however, a mistake in the coding sequence governing
proper production of MAO was detected. As a result, abnormally large quantities
of these neurotransmitters were found in the blood of the affected males
(Brunner et al., 1993). Although this genetic defect remains the first such link
to aggressive behavior in humans, exactly how the genetic defect causes aggressive, impulsive behavior, or mental retardation is not known.
Apart from MAO, only a few candidate genes have been linked to
aggressive behavior to date. The candidate genes that have been found to be
associated with aggressive behavior in humans have, in many cases, been replicated in animal studies. The majority of these candidate genes are genes of the
dopamine, serotonin, and norepinephrine neurotransmitter systems. The dopamine system is involved in mood, motivation and reward, arousal, as well as other
behaviors. The serotonin system is involved in impulse control, affect regulation,
sleep, and appetite, whereas the epinephrine and norepinephrine system facilitate
fight-or-flight reactions and autonomic nervous system activity (Niv and Baker,
2010). For example, dopaminergic candidates, including dopamine receptor
DRD4, has been found to be involved in ADHD and externalizing behavior,
and DRD2 has been found to be involved in substance abuse and disinhibition
(Niv and Baker, 2010). The DRD3 polymorphism has been found to be associated
with impulsivity. This association was significant in violent, but not in nonviolent individuals, and there were no association between DRD3 and violence per se

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(Retz et al., 2003). Dopamine transporter gene DAT1 has also been linked to
ADHD (Waldman et al., 1998), as well as with violent behavior and delinquency
in adolescents and young adults (Guo et al., 2007). Cateocholamine-O-methyltransferase (COMT) has been examined primarily in children and adults with
ADHD, and mixed evidence emerged for its association with conduct disorder
and aggression (Caspi et al., 2008). Several studies have provided evidence that
the low activity VNTR alleles of 5HTTLPR show associations with aggression,
violence, aggressive symptoms of conduct disorder, and other forms of externalizing behavior (Haberstick et al., 2006b; Linnoila et al., 1983). Aggressive behavior
has also shown associations with SNPs of epinephrine and norepinephrine. A
recent study linked two SNPs of PNMT to cognitive and aggressive impulsivity in
children and adolescents (Oades et al., 2008).

A. G
E interaction involving specific genes for aggressive behavior

Advances in the field of molecular genetics have also made it possible for
researchers to identify G
E interactions much more specifically. One of the
most influential studies examining G
E in antisocial and aggressive behavior is
Caspi et al. (2002), a famous study from 2002. The relationship between a
functional polymorphism in the MAO-A gene encoding the neurotransmittermetabolizing enzyme and early childhood maltreatment was examined in the
development of antisocial behavior in males. A significant G
E interaction
was detected, in that maltreated boys with a genotype conferring low levels of
MAO-A were found to be more likely to later develop antisocial problems,
including conduct disorder, adult violent crime, and antisocial personality disorder, than maltreated boys who had a genotype conferring high levels of MAO-A
(Caspi et al., 2002). So far, there have only been a few replications of this
important finding (Foley et al., 2004; Kim-Cohen et al., 2006; Nilsson et al.,
2006). For example, Kim-Cohen et al. (2006) found that the MAO-A polymorphism moderated the development of psychopathology after experiencing physical abuse in a sample of 975 seven-year-old boys. This finding was extended to
the maltreatment exposure closer in time as the subjects were 7-years-old
compared with previous work by Caspi et al. (2002) in which the subjects were
26-years-old, and therefore the possibility of a spurious finding by accounting for
passive and evocative G
E correlation could be ruled out. Passive G
E
correlation, as discussed earlier, refers to the association between the genotype
a child inherits from his/her parents and the environment in which the child is
raised, and evocative G
E correlation occurs when an individuals (heritable)
behavior evokes an environmental response. Further, the authors also conducted
a meta-analysis including the following five studies: Caspi et al. (2002), Foley
et al. (2004), Haberstick et al. (2005), Kim-Cohen et al. (2006), and Nilsson et al.
(2006). The association between maltreatment and mental health problems

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205

was significantly stronger in the group of males with a genotype conferring low
versus high MAO-A activity. This provides strong evidence that the MAO-A
gene influences vulnerability to environmental stress and that this biological
process can be initiated early in life. However, there is at least one published
failure to replicate (Haberstick et al., 2005), and this finding has been replicated
neither in females (Sjoberg et al., 2007) nor in African Americans (Widom and
Brzustowicz, 2006).
A G
E interaction between the DRD2 A1 allele and risk-level in family
environments has been suggested in a sample of adolescents with criminal offenses,
the National Longitudinal Study of Adolescent Health (Ad-Health). Polymorphisms in genes related to the neurotransmitter dopamine were associated with age of
first police contact and arrests, but only for youth from low-risk family environments. More specifically, among those adolescents with a history of criminal
offending, those at greatest risk for later onset were those with the A1 allelic
form of the DRD2 gene, in combination with favorable home environments as
defined by maternal attachment, involvement, and engagement (DeLisi et al.,
2008). It is important to emphasize that this finding involves the age of onset of
first police contact and not the overall risk for offending versus not offending.
There is also some evidence for a G
E interaction in the 5HTTLPR
genotype with adult violence, whereby home violence, familial economic difficulties, and educational or home-life disruptions during childhood were found to
predict violent behavior later in life only in individuals with the short promoter
alleles present (Reif et al., 2007). A similar G
E interaction between the short
allele of 5HTTLPR and childhood adversity has also been reported for ADHD
(Retz et al., 2008).
The ability to detect G
E interactions in molecular genetic studies is
both exciting and controversial. The identification of specific genetic markers
and specific experiences provides the opportunity to evaluate genetic and
environmental risk factors at the individual level. This significantly increases
opportunities for developing effective treatments and preventions for antisocial
and aggressive behavior as well as other forms of psychopathology, which is
exciting. At the same time, increased understanding of individual risks has
often been considered cautiously because of the potential for bias and discrimination of those individuals who are identified as being at highest risk for being
afflicted with disorders.

IV. CONCLUSIONS
Studies (and meta-analyses) including both twin and adoption samples show
that about half (50%) of the variance in aggressive behavior is explained by
genetic influences in both males and females, with the remaining 50% of the

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variance being explained by nonshared environmental factors. Form of aggression (reactive, proactive, direct/physical, indirect/relational), method of assessment (observation, self, teacher, parent/caregiver), and age of the subjectsall
seem to be significant moderators of the magnitude of genetic and environmental influences on aggressive behavior. Neither study design (twin vs.
sibling adoption design) nor sex, on the other hand, seems to impact the
nature or magnitude of these genetic and environmental influences on
aggression.
Although we are unaware of any twin or adoption studies of aggression
induced in authoritative situations such as in the Milgram or Stanford Prison
studies, the vast evidence for genetic influences in most forms of aggression that
have been studied could suggest that individual differences in those early
studies might have stemmed in part from different genetic propensities in
their subjects. Findings from G
E studies on aggressive behavior suggest that
not all individuals will be affected to the same degree by these environmental
exposures, and also that not all individuals will be affected to the same degree
by the genetic predispositions. Adoption and twin studies rely on relationships
between family members when examining G
E interaction effects, whereas
molecular genetic studies are using both a measured environmental (risk) factor
and a measured genetic factor. To date, there have only been a few twin/
adoption and molecular studies that report finding G
E in aggressive behavior,
either using the mean levels approach or the moderated effects approach. These
studies have shown that various measures of family adversity and social disadvantage interact (or act as moderators) with genetic factors on aggressive
behavior.
Today, we have the potential to identify genetic risks at the level of
specific genes, and identify aspects of the environment that make some individuals more vulnerable than others. Yet, there will always be groups of individuals with the same combination of genetic risk and environmental
vulnerability who will not engage in aggressive behavior. So, it is still only an
increased (probabilistic) risk and not a biological determinism. In spite of such
strong support for a genetic basis to aggressive behavior, the importance of
potential interventions which are environmentally based must not be ignored.
Environmental interventions could be developed, for example, through family
or school-based programs, to reduce aggressive behavior. In fact, a general view
held by behavioral genetics researchers is that the best way to understand
environmentand hence develop effect treatment interventionsis through
genetically informative designs such as twin and family data. By using twin and
family data, it is not only possible to estimate the influence of heritable factors
on a trait or a phenotype, but also the influence of environmental factors.
Modern methods for identifying and understanding G
E interactions will
provide a means for doing exactly this.

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207

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Perinatal Risk Factors in

the Development of
Aggression and Violence
Jamie L. LaPrairie, Julia C. Schechter, Brittany A. Robinson,
and Patricia A. Brennan
Department of Psychology, Emory University, Atlanta, Georgia, USA

I. Introduction
II. The Neurobiological and Psychophysiological Systems Involved in
the Regulation of Aggression and Violence
A. Types of aggressive behavior
B. Neurobiological bases of aggression and violence
C. Neurochemical signals of aggression and violence
D. Hormones
E. Autonomic response measures
F. Electro cortical response measures
III. Perinatal Factors Related to the Development of Aggression
A. Birth complications
B. Preterm birth and low birth weight
C. Prenatal drug and alcohol exposure
D. Smoking
E. Maternal psychological stress
F. Environmental context
IV. Genetic Contributions
A. Genetic factors as explanatory
B. Gene by environment (G  E) interactions
C. The role of epigenetics
V. Conclusions
References

Advances in Genetics, Vol. 75

Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00004-6

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ABSTRACT
Over the past several decades, the relative contribution of both environmental
and genetic influences in the development of aggression and violence has been
explored extensively. Only fairly recently, however, has it become increasingly
evident that early perinatal life events may substantially increase the vulnerability toward the development of violent and aggressive behaviors in offspring
across the lifespan. Early life risk factors, such as pregnancy and birth complications and intrauterine exposure to environmental toxins, appear to have a
profound and enduring impact on the neuroregulatory systems mediating violence and aggression, yet the emergence of later adverse behavioral outcomes
appears to be both complex and multidimensional. The present chapter reviews
available experimental and clinical findings to provide a framework on perinatal
risk factors that are associated with altered developmental trajectories leading to
violence and aggression, and also highlights the genetic contributions in the
expression of these behaviors. 2011, Elsevier Inc.

I. INTRODUCTION
Aggressive behavior and violent offending are significant burdens not only to the
individual but also to society at large; incurring costs upward of 2.3 million dollars
per individual in the most severe cases in the United States (Cohen et al., 2010).
In contrast to popular belief, longitudinal epidemiological research indicates that
the sudden onset of physical aggression in adolescence or adulthood is unusual
(Tremblay, 2008). Rather, physically aggressive behaviors can already be detected
by 12 months of age, and their frequency peaks by 24 years of age (Cote et al.,
2006; Tremblay, 2008). Indeed 85% of children exhibit aggression and tantrums
by age 2 (Potegal and Davidson, 2003). In the majority of children, the frequency
of physical aggression gradually decreases toward the end of the preschool period,
reflecting an increase in cognitive control of behavior, the acquisition of alternate
problem-solving strategies, and the influence of socialization (Nagin, and
Tremblay, 1999; Tremblay, 2008). A 60-year longitudinal study of juvenile delinquents concluded that very few show a lifespan high frequency of violent offending
(Sampson and Laub, 2003), and among those who do express chronic physical
aggression, impaired executive functioning is evident in adolescence and early
childhood, even after controlling other cognitive deficits (Barker et al., 2007).
Longitudinal follow-up studies of elementary school children with continued high
levels of physical aggression demonstrate that they are at greater risk for numerous
adjustment problems throughout their lifetime, including substance abuse, academic failure, antisocial behavior, suicide, depression, spouse abuse, and neglectful
parenting (Broidy et al., 2003; Tremblay et al., 2004).

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217

The neurobiological substrates underlying the individual variability in

the development of aggression and violence are many (Loeber and Pardini, 2008),
and current research suggests that some of the most relevant risk factors for a
trajectory of consistently high aggression are predicted by perinatal life events
including pregnancy and birth complications and intrauterine exposure to tobacco, drugs, and alcohol (Brennan and Mednick, 1997; Cannon et al., 2002).
Genetic studies of aggressive behavior also indicate that childhood aggression is
highly heritable (Brendgen et al., 2005; Hicks et al., 2004). Together, these
congenital factors appear to produce neuropsychological deficits in the nervous
system of offspring, manifesting as subtle neurocognitive difficulties, altered temperament, delayed motor development, and hyperactivity (Moffitt and Caspi,
2001). The two most commonly characterized developmental trajectories for
aggression and violence are: (1) an early-onset persistent offender and (2) a lateonset adolescent-limited offender (Moffitt, 1993; Patterson et al., 1989). In the
early-onset offender, behavioral problems typically manifest early in life, develop
into serious juvenile delinquency during adolescence, and ultimately evolve into a
long-term adult history of criminal behavior. Alternatively, late-onset adolescentlimited individuals typically do not begin offending until middle to late adolescence and cease violent and criminal behavior by their mid-1920s (Moffitt, 1993).
These two distinct trajectories are associated with substantial variation in severity,
chronicity, etiology, and prognosis. In fact, adolescent-limited offending can be
considered normative and functional, given the developmental demands on adolescents in modern society (Moffitt, 1993). Adolescent-limited offending may also
be explained by normative changes in brain development in postpubertal children.
Life-course-persistent offending, in contrast, is not socially sanctioned, functional,
or reflective of normative changes in brain development. Instead, this type of
offending is likely caused by genetic and perinatal factors which lead to deficits in
neurocognitive and neurophysiological functioning throughout the life course.
Prior to reviewing the current research on perinatal factors and violence, it is
important to briefly describe the neurophysiological processes that are involved in
the regulation of aggression and violence. Then we will describe how these factors
may mediate that relationship between perinatal risk and aggressive outcomes.
Finally, we will attempt to highlight what is known about the genetic contributions to this developmental process.

II. THE NEUROBIOLOGICAL AND PSYCHOPHYSIOLOGICAL SYSTEMS

INVOLVED IN THE REGULATION OF AGGRESSION AND VIOLENCE
The central nervous system (CNS) and autonomic nervous system (ANS)
maintain homeostasis and monitor physiological responses in humans from the
perinatal period throughout the lifespan. These systems are also involved in the

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mediation of aggressive, violent, and antisocial behavior. Although neurophysiological systems have been the focal point of studies on aggression for decades
(Scarpa and Raine, 1997), significant technological advances over the past
20 years have allowed researchers to advance their investigation of the biological
basis underlying violent and aggressive behaviors. Indeed, researchers are now
able to ask questions concerning the neural underpinnings of aggression and how
the interactions between genes and environment may result in later violence;
ultimately leading to a more complete picture of the development of aggression
and violence throughout the lifespan.

A. Types of aggressive behavior

Two forms of aggression are present in both experimental animal and human
models. Throughout the animal literature, predatory aggression has been differentiated from defensive aggression (Scarpa and Raine, 1997). Similarly, human
studies often discriminate between instrumental/proactive aggression and hostile/reactive or impulsive aggression (Crick and Dodge, 1996; Nelson and
Trainor, 2007). Reactive aggression is characterized as aggressive behavior occurring in the context of anger and high emotionality. It is often more impulsive,
less controlled, and occurring in reaction to a provocation or frustration (Scarpa
and Raine, 1997). Instrumental aggression is qualified as being more goal-oriented and relatively nonemotional. Studies suggest that this latter type of aggression
is regulated by higher cortical systems rather than brain regions (i.e., limbic
systems) associated with impulsiveness (Nelson and Trainor, 2007).
Of note, instrumental aggression is characteristic of psychopathy, a
subtype of aggression often associated with particularly low levels of physiological arousal (Raine, 2002a). While psychopathological disorders are outside the
scope of this chapter, understanding that individuals may display different types
of aggressive behavior is essential to conceptualizing physiological research
findings and the development of violence, in general.

B. Neurobiological bases of aggression and violence

Recent technological advances have allowed scientists to observe parallel neurochemical and anatomical correlates that are activated during aggression in
both human and nonhuman animals (Nelson and Trainor, 2007). Neurobiological literature regarding aggression appears to focus on substrates that are implicated in either the expression of aggressive behavior or inhibitory control of
aggression (Siegel and Victoroff, 2009). Below is a brief synthesis of the animal
and human literature that pertains to the neurobiological systems that have been
implicated in the development and modulation of aggression and violence.

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219

1. Amygdala
The amygdala is part of the limbic system and is considered to play a central role in
both emotional regulation (Joseph, 1999) and fear conditioning (Susman, 2006).
Lesion studies in animals have been critical to the understanding of the relationship
between the amygdala and aggression. Lesioning of the medial amygdala reduces
aggression in rats (Kruk, 1992). Male rhesus monkeys with amygdalar lesions display
significant increases in aggressive behavior in a group setting (Machado and
Bachevalier, 2006), while decreases in aggressive behavior are observed when
animals are tested within a dyad (Emery et al., 2001). An explanation for these
divergent findings may be that reintroduction into a group is a more fearful situation,
thus leading to increases in amygdalar responsiveness (Nelson and Trainor, 2007).
Functional abnormalities in the amygdala have also been noted in human
studies in childhood, adolescence (Marsh et al., 2008; Sterzer et al., 2005), and
adulthood (Veit et al., 2002); however, these studies have provided mixed results.
The posteroventral medial amygdala appears to be involved in the regulation of
reactive aggression, as in defensive situations, while the posterodorsal medial amygdala appears to be associated with instrumental or offensive situations (Swanson,
2000). Coccaro et al. (2007) found that amygdalar activation is positively associated
with scores on the Lifetime History of Aggression scale for adults with intermittent
explosive disorder and healthy controls. Notably, only individuals with intermittent
explosive disorder display increased activation of the amygdala in response to angry
faces (Coccaro et al., 2007). Conversely, Sterzer et al. (2005) found a negative
correlation between aggression and the left amygdala in response to negative affective images in a group of boys diagnosed with conduct disorder (CD). However, the
inverse relationship (i.e., positive correlation between amygdala activation and
aggression) was found in youth with comorbid anxiety and depression, symptoms
often found to be associated with CD (Loeber et al., 2000). Reduced responsiveness of
the amygdala in response to fearful faces has been suggested to reflect impairment in
the processing of distress cues (Marsh et al., 2008), which may result in a lack of
empathy and increases in instrumental aggressive behavior (Blair, 2001). One
explanation for these discrepant findings across samples is that aggressive individuals
may appear hyporesponsive when faced with detecting threat or distress, but hyperresponsive to distressful situations that can lead to aggression (Decety et al., 2009).
Further, these mixed findings highlight that the amygdalas role in the mediation of
aggression may be based largely on the type of aggression expressed.

2. Anterior cingulate cortex

The anterior cingulate cortex (ACC) is also a part of the brains limbic system
and has been implicated in emotional and cognitive processing (Bush et al.,
2000). Lesions of the ACC have led to a range of outcomes, including

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inattention, dysregulation of autonomic functions, and emotional instability

(Kennard, 1954; Tow and Whitty, 1953). ACC lesions as a treatment for
affective disorders in humans have produced decreased distress and emotional
liability (Corkin, 1979). More recently, deactivation in the dorsal ACC, an area
associated with cognitive monitoring and behavioral regulation (Bush et al.,
2000), has been noted in aggressive youth compared to controls (Sterzer et al.,
2005). Reduced activation in the ACC is also associated with novelty seeking
(Cloninger, 1987), a dimension of temperament encompassing a quick-tempered
personality and high impulsivity (Stadler et al., 2007). Thus, reduced activation
of the ACC may be a connection between temperament, behavior, and emotion
processing (Sterzer et al., 2005).

3. Prefrontal cortex
The prefrontal cortex (PFC) modulates subcortical behavior (Siever, 2008),
specifically by inhibiting connections between the amygdala and hypothalamus,
thereby resulting in increased aggression (Davidson, 2000). Prefrontal lesions in
humans as a result of tumors, trauma, or metabolic disturbances have been
instrumental in illustrating the role of the PFC in aggressive behavior (Siever,
2008). The well-known case of Phineas Gage, a stable and dependable railroad
worker who became irritable, angry, and showed poor judgment following an
accident in which a rod entered his skull at the frontal cortex, is a prime example
of the critical role of the PFC in monitoring aggression.
Imaging studies exploring brain functioning have further elucidated the
role of the frontal cortices in modulation of aggression. Individuals with lowerthan-average baseline activity in the frontal cortex demonstrate higher levels of
reactive or impulsive aggression (Coccaro and Kavoussi, 1997; Soloff et al., 2003;
Volkow et al., 1995). Moreover, the ventromedial prefrontal cortex (vmPFC) has
been specifically implicated in the calculation of reward expectation (Elliott and
Deakin, 2005), and increased activation is observed in the vmPFC when errors
are made during a reversal learning task (Finger et al., 2008). Reversal learning
tasks are designed to frustrate participants and measure their ability to adjust
behavior in response to changing reinforcement (i.e., avoid frustration; Rolls
et al., 1994), a deficit observed in individuals with psychopathic traits (Blair
et al., 2001; Budhani and Blair, 2005). Violations of reward expectations (i.e.,
expecting but not receiving reinforcement) have been linked to frustration and
reactive aggression (Berkowitz, 1989), which may be a result of not achieving an
expected reward (Sterzer et al., 2005). Thus, increased vmPFC responses to
violations of expectations may indeed be associated with an increased risk of
frustration and subsequent aggressive or violent behaviors (Blair, 2010).

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Experimental animal studies indicate a connection between the orbitofronal cortex (OFC) and aggressive behavior, particularly with regard to the
interpretation of social cues and behavioral responses in social contexts (Nelson
and Trainor, 2007). OFC lesions in male rhesus monkeys increase aggression in
dominant but not in subordinate animals (Machado and Bachevalier, 2006).
Butter and Snyder (1972) observed similar results, but these effects diminished
over several months. In humans, structural abnormalities in the OFC, such as
reduced levels of gray-matter volume in youth with CD (Huebner et al., 2008)
and early brain damage in this region have also been associated with conduct
problems (Anderson et al., 1999). Overall, dysfunction in the prefrontal regions
of the brain appears to underlie impaired regulation of affective responses and
reduced inhibition of aggression (Davidson, 2000).

4. Hypothalamus
The hypothalamus is another critical brain structure involved in the development of aggression. Research with nonhuman primates suggests that electrical
stimulation of the ventromedial hypothalamus is linked to vocal threats and
aggressive behaviors in marmosets (Lipp and Hunsperger, 1978), while lesions of
the anterior hypothalamus reduce vocal threats toward a male intruder (Lloyd
and Dixson, 1988). Electrical stimulation of the anterior hypothalamus increases
vocalizations in rhesus monkeys (Robinson, 1967) and aggression toward insubordinate male rhesus monkeys (Alexander and Perachio, 1973). Similar findings
have been found with electrical stimulation of the hypothalamus in male rats
(Kruk, 1992) and cats (Siegel and Victoroff, 2009). In humans, the frontal cortex
inhibits circuits in the hypothalamus that increase aggression (Davidson, 2000).
During a period in the mid-twentieth century, electrolytic lesions of the hypothalamus were used as a treatment for excessive aggression (Heimburger et al.,
1966). Although conclusions from such studies should be interpreted cautiously
for both methodological and ethical reasons (Scarpa and Raine, 1997), these
lesions were found to inhibit aggression in humans.

C. Neurochemical signals of aggression and violence

Specific signaling molecules have provided additional information about neural
circuits underlying aggression. As experimental research has turned to the brain
for answers regarding the development of aggression and violence, the neurochemistry of aggressive behavior has also come to the forefront. In general,
neurotransmitters in the brain either increase or inhibit aggressive behavior.
Below is a brief review; a more extensive review of this area of research can be
found in a separate chapter in this volume.

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1. Neurotransmitters-serotonin
Given the connection between emotion, cognition, and aggression, it seems
fitting that many studies have focused their investigation on serotonergic neurotransmission, a system predominantly involved in the regulation of emotional
states. Serotonin (5-HT) receptors in specific regions of the brain, such as the
OFC and ACC, are involved in the modulation and suppression of aggressive
behavior (Siever, 2008). Moreover, low levels of 5-HT are associated with
increased aggression in humans (Chiavegatto et al., 2001) and nonhuman primates (Higley et al., 1992). Many studies have investigated the role of 5-HT in
neuronal functioning and aggression. For example, Frankle et al. (2005) reported
reduced 5-HT transporter distribution in the ACC of patients with aggressive
personality disorder compared to healthy controls. Reduced prefrontal activation
was observed in response to a serotonergic releasing agent (d, 1-fenfluramine) in
individuals with impulsive aggression, such as those diagnosed with borderline
personality disorder (Soloff et al., 2003), and in depressed patients with a history
of suicidal behavior (Mann et al., 1992). Using positron emission tomography
(PET) technology, Parsey et al. (2002) found a negative association between
scores on the Lifetime History of Aggression scale and 5-HT receptor-binding in
the PFC and amygdala. Further, individuals with high levels of impulsive aggression display reduced activation in the PFC (Coccaro and Kavoussi, 1997).
Further, New et al. (2004) found that individuals with borderline personality
disorder, who underwent 12 weeks of selective serotonin reuptake inhibitor
(SSRI) treatment, increased baseline PFC activation, which was negatively
correlated with ratings of aggression.

2. Neurotransmitters-dopamine
Dopamine (DA) has been implicated in the initiation and exhibition of aggression (de Almeida et al., 2005), yet its precise role remains unclear. Ferrari et al.
(2003) found that rats can be conditioned to increase dopamine secretion and
decrease levels of 5-HT in anticipation of aggressive interactions, whereby DA
and 5-HT levels in the nucleus accumbens were measured during and following a
confrontation with another rat using microdialysis. Heart rate (HR) also
increased 1 h prior to the regularly scheduled interactions. Antagonists of both
D1 and D2 receptors appear to reduce aggression in male mice (de Almeida et al.,
2005). Further, animal studies suggest that the activation of catecholaminergic
brainstem neurons (e.g., ventral tegmental area) project to dopaminergic structures in the forebrain, such as the hypothalamus and the limbic system (e.g.,
amygdala, hippocampus, PFC, and ACC). In humans, both proactive and reactive aggressions are associated with dopamine (Siegel and Victoroff, 2009). In
clinical populations, decreased D1 receptors have been observed in depressed

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individuals suffering from anger attacks (Dougherty et al., 2006). Psychopharmacological agents most frequently employ compounds that act on dopaminergic
systems in the brain (McDougle et al., 1998). Risperdone, a D2 antagonist,
effectively reduces aggression in humans (Nelson and Trainor, 2007). Moreover,
haloperidol, another D2 antagonist, is used in the treatment of aggression in
psychotic patients (Fitzgerald, 1999), of violent outbursts in adults with borderline personality disorder and dementia, and of aggression in children and adolescents (Beauchaine et al., 2000).

3. Neurotransmitters-norepinephrine
Norepinephrine (also known as noradrenaline) is a monoamine found in the
ANS. It is associated with arousing situations and has been specifically cited in
the development of both proactive and reactive aggression (Siegel and Victoroff,
2009). Interestingly, a meta-analysis of central (cerebrospinal fluid) measures of
norepinephrine found a negative association between norepinephrine and antisocial behavior (Raine, 1993). Plasma levels of norepinephrine are also associated with induced hostile behavior during experiments with healthy controls
(Gerra et al., 1997). Pharmacological manipulation studies of noradrenaline
levels and noradrenergic receptors suggest that this catecholamine facilitates
the development of aggression (Miczek et al., 2002). Further evidence from the
animal literature demonstrates that DA beta-hydroxylase knockout mice are
unable to produce noradrenaline and display reduced levels of aggression, but
normal levels of anxiety (Marino et al., 2005).

D. Hormones
Hormonal factors have long been studied in relation to aggressive behavior,
particularly as scientists sought an explanation for the notable gender differences
in the rates of violence. Androgens, and in particular testosterone, have received
the most attention in this regard. Research on hormones and aggression has not
demonstrated a one to one relationship between these factors. Instead, empirical
findings suggest that the type of aggressive behavior and the structure and quality
of the social environment are likely important moderators in the association
between hormones and aggression.

1. Testosterone
A positive relationship between testosterone and aggression is well established in
the animal literature, but less support for this association has emerged in humans
(Archer, 1991). Injections of testosterone increase aggression in a variety of

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animals (Monoghan and Glickman, 1992), and aggression has been positively
associated with territorial behavior in birds (Wingfield and Hahn, 1994). Moreover, testosterone increases the display of dominance behaviors in rhesus
monkeys (Rose et al., 1971). Further, the castration of lizards (Greenberg and
Crews, 1983) and male mice (Vom Saal, 1983) leads to reduced aggression.
While some research with humans indicates that testosterone is associated with
anger and aggression (Olweus, 1986), evidence from the broader literature is
mixed (Archer, 1991). Some studies have revealed positive relationships between testosterone and aggression, some report negative relationships, and no
association is found in others (van Bokhoven et al., 2006). Specifically, testosterone measured in cerebrospinal fluid, serum, and saliva have been linked to
chronic aggression (Ehrenkranz et al., 1974), violent crimes (Dabbs et al., 1987),
antisocial personality disorder (Dabbs and Morris, 1990), and peer ratings of
toughness (Dabbs et al., 1987). However, many studies have not replicated
these results (Bain et al., 1987) and a metanalytic study of community and
selected samples found only modest correlations (i.e., between 0.08 and 0.14)
between testosterone and aggression (Archer et al., 2005). Mixed findings have
similarly been observed in adolescents (Olweus et al., 1988; Susman et al., 1987).
These inconsistent results may be partially attributable to social and developmental factors (Rowe et al., 2004), as well as other hormones, such as cortisol
(Popma et al., 2007b).

2. Cortisol
Cortisol is the end product of the hypothalamic-pituitary-adrenal (HPA) axis,
the human bodys stress response system, and is often used as a marker of stress
responsiveness. Literature regarding the relationship between cortisol and aggression is mixed. Although numerous studies suggest that lower basal cortisol
levels are associated with increased disruptive behaviors in males (Hawes et al.,
2009; Popma et al., 2007a), other studies report the opposite, with CD and
aggression being associated with higher levels of cortisol (Alink et al., 2008;
Van Bokhoven et al., 2005). Still other studies have not established any link
between cortisol and aggressive behavior (Alink et al., 2008; Scerbo and Kolko,
1994; van Goozen et al., 2000). A significant amount of research has focused on
an association between an underreactive HPA axis and aggressive behaviors.
Theoretically, this underreactivity may be associated with reduced comprehension of distress cues, which has been related to reduced empathy and behavioral
inhibition (Marsh et al., 2008). Lower levels of cortisol are also linked with
reductions in fear responsiveness (Cima et al., 2008), which may lead to persistent aggressive behavior (McBurnett et al., 2000). In reviewing the divergent
findings linking cortisol levels and aggression, Hawes et al. (2009) proposed two

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hormonal pathways to antisocial behaviorone which links stress exposure to

high cortisol and aggression and the other which links low cortisol to aggression
through callous-unemotional traits. In support of this proposal, a recent empirical study found that changes in cortisol levels in response to a stressor were
positively associated with reactive (but not proactive) aggression in boys (LopezDuran et al., 2009).

3. Oxytocin
Recently, the hormone oxytocin has been investigated as a possible link in the
development of aggression. Oxytocin is a hormone that is involved in trust and
affiliative behaviors (Insel and Winslow, 1998; Young et al., 2001), thereby
reduced oxytocin is thought to be associated with increased aggression. This
hypothesis has been supported in the animal literature as oxytocin knockout
mice exhibit increased aggressive behavior (Ragnauth et al., 2005). In humans,
adults administered oxytocin intranasally are significantly better at identifying
happy facial expressions compared to other expressions (Marsh et al., 2010).
Oxytocin has also been found to reduce activation in the amygdala (Kirsch,
2005). Taken together, data suggest that deficits in oxytocin may
influence mistrust and hostility which can contribute to aggression and violence
(Siever, 2008).

E. Autonomic response measures

Autonomic arousal is most commonly measured via HR and electrodermal
activity (EDA). In general, research regarding autonomic arousal and aggressive
and violent behavior has yielded findings suggesting a pattern of lower baseline
levels of autonomic arousal and higher autonomic reactivity in children and
adolescents (Patrick, 2008). Although less consistent, research on aggressive
adults indicates an increase in autonomic activity in response to a stressor
(Patrick, 2008). A met analysis by Lorber (2004) found a reliable but modest
association between the autonomic measures of HR and EDA and aggression and
conduct problems. Below is a brief review of the specific associations between
HR and EDA and aggression and violence.

1. Heart rate and electrodermal activity

Low resting HR is a common phenomenon among aggressive children (Scarpa
and Raine, 1997) and is associated with conduct problems throughout childhood, adolescence, and adulthood (Lorber, 2004). Evidence for HR reactivity is
less consistent. It appears that aggressive children have increased HR in response

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to a stressor (Lorber, 2004), and this finding is particularly robust in children

displaying reactive aggression rather than proactive aggression (Hubbard et al.,
2002). HR reactivity and its association with aggression in adults are also mixed.
EDA refers to small changes in electrical activity of the skin, usually
occurring 13 s following the onset of a stimulus (Scarpa and Raine, 1997).
Lorber (2004) found that conduct problems in childhood were associated with
reduced EDA in the absence of stimulation, and reduced EDA during a task, but
only in the presence of nonnegative stimuli. This met analysis also revealed a
positive association between adult aggression and EDA reactivity. Scarpa and
Raine (1997) suggested that EDA under arousal may be associated with specific
forms of crime, such as crimes of evasion. Skin conductance levels have also been
shown to interact with markers of the HPA axis to predict later externalizing
behaviors in children (El-Sheikh et al., 2008). Results indicate that children with
higher levels of EDA and higher levels of cortisol display increased levels of
externalizing behaviors.

F. Electro cortical response measures

Electroencephalography (EEG) uses electrodes placed around the scalp at specified points to measure electrical activity of the brain. EEG evidence suggests that
slow-wave activity during adolescence may predict later antisocial behavior
(Raine et al., 1990). These findings have been interpreted to suggest that cortical
immaturity leads to reduced inhibition (Volavka, 1999) and increased impulsive
behavior. EEG abnormalities, specifically under arousal and cortical immaturity,
have been reported in violent recidivistic offenders (Raine et al., 1990).
Event-related potential (ERP) refers to the averaged changes in electrical brain activity in response to a stimulus. Literature on ERP and aggressive
behavior is mixed. One consistent finding has been the association between
reduced amplitude of the P300 wave response, an ERP elicited by infrequent
stimuli, among aggressive and impulsive individuals (Gerstle et al., 1998). The
P300 is thought to reflect online updating of cognitive representations (Donchin
and Coles, 1988), thus the reduced amplitude may suggest impairment in higher
cognitive functioning (e.g., working memory) in these individuals (Patrick,
2008). Reduced P300 has been reported in antisocial personality disorder
(Bauer et al., 1994), as well as other disorders that involve impaired impulsivity
such as child CD and ADHD, drug dependence, and nicotine dependence
(Iacono et al., 2002). Therefore, reduced P300 amplitude may be a reflection of
impulse control, a characteristic of reactive aggression (Patrick, 2008).
The physiological findings presented above illustrate the apparent
biological underpinnings involved in the development of aggression and violence. Research from physiological and neurobiological studies has provided
significant evidence for the biological basis of violent and aggressive behavior.

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Taken together, the neurobiological and psychophysiological findings suggest a

model in which aggression arises due to dysfunction in brain areas responsible for
emotion processing, inhibition, and reactivity (Davidson, 2000). Repeated aggression may contribute to deficits in recognizing and processing of emotion, as
well as the regulation and modulation of aggressive behavior in response to
threat. Reduced activation and distribution of neurotransmitters in areas of the
brain implicated in the development of violent behavior, in combination with
dysregulation of the bodys hormonal responsiveness, may add to difficulties in
controlling aggressive outbursts. Furthermore, reduced arousal to distressing
stimuli, as evidenced by a diminished physiological response and electrical
activity in the brain may contribute to further deficiencies in appropriate
responses to increased arousal. Further research is necessary to provide additional
evidence for this suggested model.
As the field progresses, particular attention should be paid to the
subtypes of aggressive behavior that may be characterized by unique physiological patterns. Future studies should focus on parsing the different types of aggression to elucidate the specific pathways underlying violent behaviors. A better
understanding of these pathways allows for earlier intervention that may be able
to reduce or prevent severe aggressive behavior later in life. With the knowledge
of the psychophysiology associated with the development of violence throughout
the lifetime, we now turn specifically to the perinatal period to better understand
how these biological pathways can be altered to prevent or lead to later violence.

III. PERINATAL FACTORS RELATED TO THE DEVELOPMENT

OF AGGRESSION
The notion of a mothers health affecting that of her unborn infant is one that
has pervaded common knowledge for centuries. Only recently, however, have
scientists begun to empirically study the specific factors influencing fetal development. Preterm birth, delivery complications, maternal mental illness, gender,
and exposure to drugs, alcohol, and tobacco are all topics that have been
explored in relation to their impact on fetal development. These factors have
been shown to have maladaptive effects on fetal brain development following
prenatal exposurea finding that makes pregnancy a critical window for the
prevention of unfavorable outcomes throughout the lifespan of the offspring.
One such risk that has been identified in relation to these perinatal factors is the
development of aggression. It has been suggested that through disruptions in
neural development, the fetus incurs neuropsychological deficitsnamely neural
impairments in executive and verbal functioning that may result in an irritable
disposition, poor behavioral regulation, or aggression (Brennan et al., 2003). This
tendency toward aggression tends to persist throughout adolescence and into

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adulthood, manifesting itself through externalizing behaviors, internalizing problems (depression, loneliness, etc.), poor peer relationships, psychological disorders (CD, oppositional defiant disorder, etc.), recurring criminal behaviors,
and violence. Because of the extensiveness of the risks associated with aggression, it has many potentially negative outcomes both in the developing infant, as
well as in the significant economic and social burdens it places on society. In this
section, the potential influences of the aforementioned perinatal factors will be
explored in their relation to the development of aggression and violence. It is
important to note that these risks do not necessitate the development of aggression in offspring but rather are important in understanding certain conditions in
which aggressive traits may be more likely to arise.

A. Birth complications
Many studies have found associations between birth complications and negative
behavioral outcomes in offspring. Specifically, irritable temperament in childhood, violent offending in adolescence and adulthood, and aggressive behaviors
throughout the lifespan are among the offspring outcomes that have been
associated with higher rates of birth complications. Birth complications typically
refer to the following three factors: (1) prenatal complications, such as hypertension, mental illness, stress, drug and alcohol exposure, and viral infections
experienced by the mother; (2) perinatal complications, which include difficult
fetal delivery (e.g., breech birth), premature breaking of the membrane, assisted
delivery (forceps and cesarean), fetal distress (i.e., difficulty breathing), preeclampsia, and umbilical cord prolapsed; and (3) postnatal complications as
indicated by either cyanosis or treatment with oxygen (Liu et al., 2009).
The mechanisms through which birth complications may influence the
development of aggression are unknown, but they are hypothesized to involve
damage to the PFC, hippocampus, and dopamine systems (Brennan et al., 1997;
Cannon et al., 2002; Mednick and Kandel, 1988; Raine, 2002b). More specifically, preeclampsia, maternal bleeding, and maternal infection may cause an
inadequate supply of blood to the placenta, fetal hypoxia or anoxia (lack of
oxygen), and disrupted development of the hippocampus, dopamine systems, and
other parts of the brain (Cannon et al., 2002; Liu, 2004; Mednick and Kandel,
1988). Animal research has supported these findings by suggesting that perinatal
complications surrounding anoxia in rats may reduce central dopamine transmission (Brake et al., 2000). Dopaminergic neurotransmission appears to be
involved in impulse control, aggression, and violence (Chen et al., 2005; Retz
et al., 2003). Animal research also suggests that perinatal complications may
limit neurotransmitter functioning in the left PFCan effect that has been one
of the most frequently replicated indicators of violent offending in the brain
imaging literature (Henry and Moffitt, 1997). It is important to note, however,

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that birth complications alone are unlikely to predispose infants to externalizing

behavior and aggression. Instead, these complications interact with various
psychosocial risk factors (i.e., poverty, poor parenting, parental rejection, negative peer relationships, bad neighborhoods, etc.), and likely genetic factors, to
influence aggressive tendencies (Raine et al., 1994).
Prenatal, perinatal, and postnatal health care interventions aimed at
reducing birth complications may help to decrease risks of later development of
aggression and violence. If women who may be at risk for birth complications are
identified and educated, these mothers may be in a better position to take steps
toward keeping their pregnancies and their babies healthy. If, however, birth
complications do occur, early enrichment programs, that improve cognitive
ability or enhance the parentchild relationship, may be effective in preventing
the emergence of aggressive and violent behavior in adolescence and adulthood.

B. Preterm birth and low birth weight

Research supporting the role of neuropsychological deficits in mediating birth
complications and adverse outcomes is consistent with preterm and low birth
weight literature. White et al. (1994) have shown that medical and congenital
risk factors, such as low birth weight and preterm birth, may lead to neuropsychological deficits and CNS damage that result in an increased likelihood for
criminal offending. Evidence also suggests that preterm birth may be involved in
the development of externalizing behaviors and aggression, and that these
negative behavioral outcomes worsen with age (Bhutta et al., 2002).
Low birth weight and preterm birth serve as strong and consistent
predictors of neuropsychological deficits that may result in subsequent aggression
and antisocial behavior (McCormick, 1985). Low birth weight infants were three
times more likely to experience neurological deficits than controls (McCormick,
1985). Moreover, such CNS deficits (Moffitt, 1993) may manifest themselves in
a variety of ways, including temperamental difficulties, cognitive deficits, inattention, antisocial behavior, subnormal growth, learning difficulties, hyperactivity, behavioral problems, poor academic achievement, CNS damage, and
psychiatric disorders (Piquero and Tibbetts, 1999).
Preterm birth and low birth weight have been found to be correlated
with maternal tobacco use, lack of prenatal care, drug and alcohol use by the
mother during pregnancy, low socioeconomic status, poor diet, psychotropic drug
use during pregnancy, and low parental educational level (Piquero and Tibbetts,
1999). Because of the range of factors that might cause preterm birth and low
birth weight in an infant, preventative efforts are critical.
It is important to note that the effects of preterm birth and low birth
weight on psychological functioning and aggression may vary depending on the
sex of the child. For example, low birth weight boys exhibit a significantly more

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aggressive and delinquent acts in comparison to their female counterparts (Ross

et al., 1990). There is also considerable evidence suggesting that disadvantaged
home environments and maternal interactive style may moderate the relationship between these risks and aggressive behaviors (Piquero and Tibbetts, 1999).
Therefore, a number of factors, such as sex, home environment, and maternal
interactive style, are involved in the phenotypic expression of aggression in
premature and low birth weight infants.
Despite the decrease in infant mortality over the past 30 years, the
prevalence of preterm birth and low birth weight has actually increased to
approximately 12.5% of births in the United States. Given the prevalence of
preterm birth and low birth weight in the United States, it is understandable why
risk factors associated with this population are such a major public health
concern (Berman and Butler, 2006). Preventative measures and public awareness
campaigns focusing on the risks involved in preterm birth and low birth weight
are a necessary next step in addressing these issues.

C. Prenatal drug and alcohol exposure

1. Alcohol
Sixteen percent of children born in the United States are exposed prenatally to
alcohol, making alcohol the most common neurobehavioral teratogen affecting
fetal development (Sood et al., 2001). Overall, children who are prenatally
exposed to alcohol are 3.2 times more likely to develop aggression and delinquent behavior than nonexposed children. Further, children exposed to low
levels of alcohol prenatally show higher scores for aggressive and externalizing
behaviors on the Child Behavior Checklist (CBCL) and children exposed to
moderate levels have higher scores on delinquent and total problem behavior on
the CBCL (Sood et al., 2001). This suggests a higher threshold for the development of delinquency in children, as opposed to aggressive and externalizing
behaviors. However, it also negates claims that low levels of alcohol consumption during pregnancy are tolerable with evidence that suggests that even a small
dose may have adverse effects on fetal development. More generally speaking,
the literature supports a doseresponse continuum where a more heavily exposed
fetus shows a greater magnitude of these adverse effects (Driscoll et al., 1990).
Fetal alcohol spectrum disorder (FASD) and fetal alcohol syndrome
(FAS) are conditions that may arise when children are prenatally exposed to
alcohol. These disorders are characterized by physical and mental birth defects
that may result in impaired interpersonal skills and social deficits. Some of the
behaviors that are commonly observed among populations of FAS individuals
are tendencies to demand attention, interrupt others, lie, show impaired moral
judgment (especially with regard to social relationships), overreact to situations

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with excessively strong emotional responses, monopolize conversations, and

demonstrate unawareness of the consequences of ones actions. This population
may also suffer major language and social communication deficits, which further
hamper their social competence (Kelly et al., 2009).
Animal studies have helped in linking prenatal alcohol exposure to the
development of aggressive behaviors. Specifically, evidence suggests that alcohol
exposure during prenatal development causes CNS damage. Rats provide an excellent model for understanding the development of aggression, because their social
behavior has been shown to follow similar patterns to that of humans. Their social
behavior results from a combination of influences including genetic makeup, teratogenic influences, early maternalinfant interactions, and later social learning.
Primates, too, offer a suitable model for studying the effects of prenatal alcohol
exposure, as their gestation characteristics and early developmental stages are
similar to that of humans. In both animals and humans, prenatal alcohol exposure
is not considered a singular cause of social deficits, but rather a probabilistic
contributor serving as a risk factor for the developing child (Kelly et al., 2000).
Because there are socialfamilial influences associated with prenatal
exposure to alcohol, one might ask how it can be determined that alcohol
exposure has any actual teratological effect. Animal models provide a means
through which alcohol- and environment-related factors can be separated in an
experimental fashion. For example, removing a newborn pup from its alcoholusing mother and transferring it to a foster-parent environment results in rates
of aggression that are analogous to those remaining in the care of their alcoholusing mothers, suggesting that changes in aggressive behavior are initiated by
the pups prenatal exposure to alcohol, rather than by its environment. This type
of experiment, for obvious reasons, would be ethically impossible to conduct in
human populations (Kelly et al., 2000).
Animal models have contributed essential components to our understanding of the specific mechanisms through which prenatal ethanol (alcohol)
exposure and aggression are linked. Rodent studies suggest that the behavioral
deficits that result from ethanol exposure in utero are linked to ethanol-induced
changes in the CNS. These changes in the CNS, however, are not uniform, and
some brain regions (i.e., neocortex, hippocampus, cerebellum) are more affected
than others. Notably, the HPA axis and beta-endorphin (b-EP) systems become
dysregulated and hyperresponsive to social situations, which is demonstrated by
heightened and prolonged concentrations of hormones, such as corticosterone
(CORT) and adrenocorticotropin (ACTH), as well as elevated plasma levels and
reduced pituitary content of b-EP compared to controls. Further, ethanol-exposed
neonates show heightened sensitivity to stressors, significantly increased corticotrophin release factor (CRF) biosynthesis and expression, and more prolonged
CORT and ACTH elevations during and after stress. These effects, which persist
throughout the neonates lifespan, indicate deficits in pituitaryadrenal response

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inhibition and in recovery from stress. It is through these mechanisms that

prenatal alcohol exposure may manifest in aggressive tendencies and externalizing
behaviors in the lives of effected offspring (Weinberg et al., 1996).

2. Drugs
Drug use by pregnant women has increased steadily. Despite general awareness of
detrimental effects, drug use during pregnancy continues its upward trend with
prevalence estimates ranging from 0.3% to 46%. Prenatal drug exposure is associated with behavioral abnormalities, such as excessive irritability, poor socialattachment behavior, and aggression (Johns et al., 1994). The neurobiological
processes through which these deficits emerge primarily involve the effects of
drugs on fetal organogenesis, especially fetal brain development (Mayes, 1994).
Evidence suggests that an increase in aggressive or violent behaviors associated with
prenatal drug use may arise from alterations in the CNS. More specifically, aggressive behaviors can be linked to changes in fetal neurotransmitter systems, particularly within the limbic system (Miller et al., 1991). Cocaine (including crack
cocaine) is one of the most commonly studied CNS stimulants in the literature on
prenatal drug exposure. Cocaine affects monoaminergic neurotransmitter (dopamine, norepinephrine, and 5-HT) systems in the CNS by blocking the reuptake of
dopamine, norepinephrine, and 5-HT leaving more of these neurotransmitters
within the synaptic space (and therefore the peripheral blood). An excess in the
amount of these neurotransmitters results in psychological effects, such as pleasure
and euphoria, as well as specific behaviors and physiological reactions. Physiologically, chronic cocaine use may lead to tolerance whereby increasing amounts of the
drug are necessary to achieve a desired effect.
In the developing fetus, monoaminergic neurotransmitters play a critical role in fetal brain development by influencing cell proliferation, neural
outgrowth, and synaptogenesis (Lauder, 1988; Mattson, 1988). Cocaine and
other drugs may affect these neural processes throughout gestation through
their effects on the release and metabolism of monoamines. The importance of
monoamine neurons in fetal brain development has been demonstrated in both
human and animal models. For example, in the rats second week of gestation,
norepinephrine neurons appear in the locus coeruleus, 5-HT neurons are found
in the raphe nuclei, and dopaminergic neurons in the substantia nigra are
functional (Lauder and Bloom, 1974). By the end of the second month of
human gestation, 5-HT and norepinephrine neurons can be found. In both
animals and humans, these monoamine neurons are rapidly generating axonal
connections with the forebrain and actively influencing the production and
differentiation of cell structure in these regions (Lidov and Molliver, 1982a,b;
Wallace and Lauder, 1983).

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Further evidence of these effects can be demonstrated by administering

cocaine to rats during the early postnatal period when synaptogenesis begins in
the forebrain. This early postnatal period in rats is functionally equivalent to the
third trimester in human gestation during which axonal and dendritic growth
take place. When brain glucose metabolism is used as an indicator of activity,
animal models exhibit the greatest percentage change in brain regions with high
dopaminergic activity in comparison to untreated controls (Dow-Edwards et al.,
1988, 1989). Several brain structures associated with the mesocortical and
mesolimbic systems, including the cingulate cortex, PFC, nucleus accumbens,
amygdala, septum, ventral tegmental area, and ventral thalamic nucleus, appear
highly affected by dopamine activity (Goeders and Smith, 1983; Shepard, 1988).
Each of these areas is thought to be involved in an organisms arousal, attention,
and ability to regulate anxiety and emotional responses (Mayes, 1994).
The neural processes mentioned above may lead to the development of
aggression when abnormalities in fetal brain development later manifest themselves in social and behavioral ways. Basic processes, like the regulation of
attention, response to sensory stimuli, and the modulation of mood states may
all be linked to prenatal drug exposure through the drugs alterations of neurotransmitter activity. Several studies have found that infants exposed to drugs
prenatally are often easily irritable and difficult to engage. Evidence also suggests
that prenatal drug exposure results in crying patterns that indicate a general
excitable tendency within affected infants. Human infants exposed prenatally
to cocaine have also shown elevated HRs and norepinephrine levels at 2 months
of age; lending further support to the influence cocaine has on monoaminergic
systems (Mayes, 1994; Mirochnick et al., 1991). Rodent models have demonstrated an increased susceptibility to stressors, higher vulnerability to the environment, and increased rates of aggressive behaviors in response to social
competition among offspring prenatally exposed to drugs (Spear et al., 1998).
The influence of prenatal exposure to drugs and alcohol on social and
aggressive behavior has serious implications for crime prevention. Early identification and intervention among infants and children who may be affected by
prenatal drug or alcohol exposure is necessary to prevent delinquency and poor
social relationships within these populations (Johns et al., 1994). Such steps are
also necessary for gaining a better understanding of the behavioral differences
that may exist within educational, occupational, and social settings due to
prenatal exposure to drugs and alcohol.

D. Smoking
Smoking during pregnancy remains a critical public health concern. Nearly half of
all women who smoke continue to do so even while pregnant, despite some womens
intentions to refrain from doing so. Despite common knowledge of the adverse

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effects of maternal smoking during pregnancy among the American public, more
than half a million infants per year in the United States are prenatally exposed to
maternal smoking (Wakschlag et al., 2002). This is of even greater concern when
one considers the failure of public health smoking cessation campaigns for the
10.2% of women in the United States who continue to smoke through their
pregnancies. Adverse outcomes, which include low birth weight, premature delivery, spontaneous abortion, and infant mortality, have been the primary focus of
these campaigns (Weaver et al., 2007). In comparison, relatively little attention has
been paid, from a public health standpoint, to the relationship between prenatal
smoking and the development of aggression and violence in offspring.
Prenatal smoking predicts childrens likelihood of displaying high aggression from as early as 1.5 years and throughout adulthood (Huijbregts et al.,
2008). Several externalizing behaviors, including impulsivity, truancy, hyperactivity, attentional difficulties, and delinquency, have all been found to be
associated with maternal prenatal smoking through the fetus exposure in
uterine.
Potential neurobiological mechanisms through which prenatal nicotine
exposure may increase the offsprings risk for aggressive behaviors include the
HPA axis and the CNS (Brennan et al., 1997). Substantial evidence suggests
that nicotine crosses the placental barrier and causes neurotoxicity in the fetus.
Neurotoxicity occurs via hypoxic effects on the fetal-placental unit (e.g., reduction of fetal blood flow) and teratological effects on the developing fetal brain.
Two recent human studies support this contention, noting associations between
maternal prenatal smoking and decreased frontal lobe volumes in infants (Ekblad
et al., 2010), and a thinning of the cerebral cortex in adolescents (Toro et al.,
2008). Within the HPA axis, nicotine produces a heightened ACTH response to
stress in adult rats (Poland et al., 1994). Other studies have found that elevated
levels of ACTH increase aggressive and defensive behaviors in both rats and
nonhuman primates, suggesting that this hormone may be related to the development of aggression (Higley et al., 1992; Veenema et al., 2007). However, lower
levels of ACTH have also been found within human criminal and antisocial
populations in comparison to controls, so these results are mixed and should be
interpreted with caution (Coccaro and Siever, 2002; Virkkunen et al., 1994).
Nicotinic acetylcholine receptors (nAChRs) are responsible for the
regulation of many vital phases of brain maturation. These receptors are present
in the brain early in gestation and develop throughout prenatal, postnatal, and
adolescent periods, suggesting that nicotinic signaling plays a crucial role in neural
development. During these developmental periods, NAChRs are particularly
sensitive to environmental stimuli and, as specific nicotine-sensitive receptors,
are especially vulnerable to exogenous nicotine. Nicotine affects fetal development primarily through its effect on nicotinic-binding sites in the cerebral cortex.
More specifically, nicotine has been found to alter the neocortex, hippocampus,

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235

and cerebellum during the early postnatal period within rats (the equivalent of the
third trimester in humans; Dwyer et al., 2009). Evidence suggests that prenatal
nicotine-induced defects within these particular brain regions may increase the
likelihood of dopamine-mediated disorders like attention deficit hyperactivity
disorder and substance abuse. Patterns of continuous maternal smoking (i.e., the
tendency to smoke in a way that maintains plasma nicotine levels at a steady state)
cause more negative effects than more periodic patterns of use, which allow the
CNS to recover between episodes. The stimulation to nicotinic receptors interacts
with the genes that influence differentiation of cells, causing permanent changes
in cell functioning. It has been suggested that these processes disrupt the maturation of the fetal brain and produce adverse effects in fetal development that can
later manifest themselves in aggression or violence (Wakschlag et al., 2002).
Animal models demonstrate many of the biological effects of prenatal
smoking on neonatal behavior. Rats exposed to nicotine prenatally show deficits
in learning and memory, as well as in social behavior. Benowitz (1998) found
that nicotine infusion in rats causes interference with neural cell replication and
abnormal synaptic activity. These, in turn, produce neuroendocrine and behavioral abnormalities that could potentially lead to aggression. Rodent models have
also shown similar adverse effects linked to second hand smoke, as well as
maternal use of nicotine replacement therapy (NRT), a pharmacotherapy of
smoking cessation thought to be less detrimental than smoking cigarettes during
pregnancy (Dwyer et al., 2009). Findings of adverse effects related to maternal
use of NRT are particularly disturbing, since (1) NRT does not seem to increase
the likelihood of successful smoking cessation during pregnancy and (2) NRT
has actually been recommended by a number of public health authorities,
including the Food and Drug Administration (Bruin et al., 2010). NRT (as
well as cognitive-behavioral therapy (CBT)) has been shown to be effective
among nonpregnant smokers, so prevention rather than smoking cessation
during pregnancy should be the aim for reducing adverse outcomes attributed
to prenatal nicotine exposure. Further, interventionists should keep in mind that
any prenatal nicotine exposure, even through modes of transmission not related
to smoking, can be detrimental to fetal development.
As with most toxins, the effects of prenatal smoking exposure are dosedependent and thus strongest among offspring of heavy smoking mothers ( 10
cigarettes/day). Further, the effects of prenatal smoking are exacerbated when
accompanied by low socioeconomic status, poor parenting, family dysfunction,
paternal absence, and parental history of antisocial behavior. However, the
relationship still exists even when these variables are controlled for (Huijbregts
et al., 2008). Evidence suggests that gender might moderate the relationship
between maternal prenatal smoking and externalizing behaviors in that the
relationship is stronger among male offspring in predicting CD and stronger
among female offspring when predicting substance abuse (Brennan et al., 2002).

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E. Maternal psychological stress

Prenatal stress is so common an occurrence that it seems unlikely that it could
have any significant effects or unfavorable life-long outcomes on child development. However, it is, in fact, associated with low birth weight, preterm birth,
preeclampsia, spontaneous abortion, growth-retardation (specifically reduced
head circumference), developmental delays, heightened emotionality, externalizing behaviors, irritability, psychopathology, and deficits in attention, cognition, and neurodevelopment (Clarke et al., 1994, 1996; Gutteling et al., 2005;
Mulder et al., 2002). Effects involving birth outcomes are relevant to the
development of aggression in the ways previously described. However, prenatal
stress, more broadly speaking, also affects fetal neurodevelopment in a different
way. Prenatal stress may stem from a variety of sources including, but not limited
to inadequate social support, low socioeconomic status, unwanted pregnancy,
and sexual, physical, or verbal abuse. These stressors may take the form of one
traumatic event, several recurrent ones, or more chronically on a daily basis
(Mulder et al., 2002). When the stressor is experienced, the HPA axis and the
sympathetic nervous system are activated, as the bodys response to a particular
threat the individual perceives in her environment. This physiological response
has evolutionary value in that it places us in fight or flight mode, increasing our
awareness of problems that may exist and preparing us to find ways of solving
them. This process becomes maladaptive, however, when our perception of a
threat or stressor is inconsistent with its actual magnitude and relevance to our
lives, and alternatively, when the physiological response following a stressor is
prolonged (Clarke et al., 1994, 1996; Gutteling et al., 2005; Mulder et al., 2002).
The connection between prenatal stress and HPA axis activity has been
demonstrated in rodent, animal, and human studies, and in all of these, both
prenatal stress and heightened HPA axis response have been found to be
predictive of the development of aggression in offspring (Clarke et al., 1994,
1996; Gutteling et al., 2005; Mulder et al., 2002). A number of rodent studies
have introduced stress to a pregnant mother prenatally using electrical shock,
immobilization, or randomly administered bursts of noise. These studies have
demonstrated a dysregulation of the HPA axis in both mother and pup that
eventually leads to heightened emotionality, hostility, and aggression in the
offspring (Clarke and Schneider, 1993; Mulder et al., 2002; Sobrian et al.,
1997; Takahashi et al., 1990; Ward and Weisz, 2011). Similarly, studies of the
offspring of rhesus monkey mothers exposed to stress from mid- to late-gestation
demonstrated low birth weight, impaired neuromotor development, attention
deficits, and disturbed behavior (Clarke et al., 1994, 1996; Schneider, 1992a,b).
These effects were long-term and persisted even into the adolescent period of
development (Clarke et al., 1996). In humans, similar effects of maternal prenatal stress have been reported (Gutteling et al., 2005; Mulder et al., 2002).

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HPA axis regulation involves several hormones, including corticoreleasing hormone (CRH), cortisol, (nor)adrenaline, and ACTH, which are
released into the bloodstream when a stressor is experienced. Small increases
in these hormones within the pregnant mother may lead to disproportionately
large increases in fetal hormonal levels. Excessive levels of these hormones may
potentially inhibit the growth and development of the nervous system, cause
damage to the brain, and produce programming effects on the fetal neuroendocrine system that lead to the developmental deficits mentioned above. This may
be especially true when HPA axis activity is characterized by an exceptionally
strong, sustained response to the stressor. Animal models have supported this
explanation by demonstrating experimentally that levels of these hormones are
higher in neonates prenatally exposed to stress in comparison to controls (Clarke
et al., 1994, 1996; Gutteling et al., 2005; Mulder et al., 2002).
It is important to note that there have been gender differences in the
findings within this area, namely that hostility and aggressive behaviors appeared
to be more prevalent in male offspring than in females. These findings, which are
typically found in rodent studies, suggest that males may be more vulnerable to
the effects of prenatal stress than their female counterparts (Clarke et al., 1996).
However, in general, it seems that prenatal stress may be an important predisposing factor for a number of behavioral deficits among both male and female
offspring, even if to different degrees.
Because stress can be so pervasive in the life of a pregnant mother, it
often manifests itself in a variety of ways. For example, stress might lead a mother
to engage in smoking or alcohol and substance abuse, which, in turn, can
produce fetal neurobehavioral deficits of the kind that have been described in
previous sections. To prevent these types of detriments from occurring, it may be
necessary to assess womens stress levels in early pregnancy, identify those who
are at risk, and provide stress reduction programs throughout their pregnancies.
Educating women about the risks involved with prenatal stress, as well as training
them in relaxation methods, may be helpful in alleviating these effects. Ensuring
that women have the appropriate buffers needed to prevent stress is also essential. Adequate social support and financial resources are just a few factors that
may be necessary to ensure a mothers psychological well-being.

F. Environmental context
It is important to note that the prenatal factors discussed above may not
necessarily operate in a unidirectional manner. It may often be the case that
these factors result in child aggression in the form of coercion or manipulation of
the parent in order to obtain something that is wanted. This coercion is likely to
elicit a negative response from the parent in the form of either negative reinforcement (giving in to the child) or positive reinforcement (giving increased

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attention to the child by chastising or yelling). This reinforcement indirectly

encourages and exacerbates the childs behavior, producing an ongoing cycle of
reinforced aggressive behaviors throughout the childs lifetime. Further, this
cycle may be maintained by preexisting neuropsychological deficits and unintentionally harmful reinforcements from other figures in the childs life, such as
teachers, grandparents, and peers.
Throughout this section, it has been continually noted that neither
social nor biological elements operate alone in contributing to the development
of aggression in offspring. One or the other may predispose a child to developing
aggressive behaviors, but it is the double hazard of perinatal risk and social
disadvantage that places a child at maximal risk for later aggression and externalizing behaviors (Brennan and Mednick, 1997). Understanding the interaction of biological and social risk factors in generating aggression is critical for
preventing both personal costs (few positive social relationships, poor job performance, etc.), as well as social costs (crime rate, prison costs, etc.). Thus,
researchers and policy makers should make it a goal to identify populations
potentially affected by perinatal risk factors in order to more accurately predict
who might benefit from interventions aimed at preventing later aggression,
violence, and criminal offending.

IV. GENETIC CONTRIBUTIONS

As described in detail elsewhere in this volume, aggressive and violent behavior
can in part be accounted for by genetic factors. Because prenatal stress and
teratogenic exposures may be linked to genetic risk, it is important to consider
potential genetic contributions to the association between perinatal factors and
aggression.

A. Genetic factors as explanatory

One prenatal risk factor, that has received recent attention in terms of the
potentially confound role of genetic factors, is maternal smoking during pregnancy. For example, twin studies have been utilized to assess whether the
relationship between maternal prenatal smoking and offspring externalizing
behavior remains significant when controlling for genetic influences. In one
such study, the association between maternal smoking and offspring ADHD
was found to persist after controlling for genetic influences (Thapar et al.,
2003). In a separate twin study, researchers found that genetic effects explained
about half of the association between maternal prenatal smoking and child

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239

conduct problems; in this study, controls for both genetic influences and parent
psychopathology accounted for the initial association in its entirety (Maughan
et al., 2004).
Recent advances in infertility treatment (i.e., in vitro fertilization using
donor eggs) have also allowed for the use of a prenatal cross fostering design to
assess the moderating impact of genetic influences on the maternal prenatal
smoking/child externalizing disorder association (Rice et al., 2009). In this novel
study, maternal smoking during pregnancy was only associated with child antisocial outcomes in cases where the mother was implanted with her own egg, as
opposed to an unrelated donors egg. These results suggest that genetic factors are
a necessary component in the noted relationship between maternal smoking and
child antisocial outcomes.
Another novel design strategy has recently been used to evaluate outcomes for siblings discordant for maternal prenatal smoking (DOnofrio et al.,
2010; Lindblad and Hjern, 2010). Results from studies using this design suggest
that familial background factors, rather than environmental exposure effects,
explain associations between maternal prenatal smoking and externalizing problems. However, as acknowledged by their authors, these sibling discordant
design studies did not test for gene by environment interactions, leaving open
the possibility that prenatal exposure to maternal smoking may result in externalizing behavior outcomes for offspring at particular genetic risk.

B. Gene by environment (G  E) interactions

Gene by environment interactions have recently been examined in terms of
their relevance to perinatal risks and child behavioral outcomes. These studies
have primarily focused on polymorphisms linked to the neurotransmitter systems
of dopamine, norepinephrine, and 5-HT, which have been described previously
in terms of their relevance to both perinatal factors and aggressive outcomes.

1. Monoamine oxidase genotype

Monoamine oxidase (MAO) is a critical enzyme involved in the degradation of
neurotransmitters, including norepinephrine, dopamine, and 5-HT. MAO exists
in two forms, MAOa and MAOb. The gene that codes MAOa has functional
variations that influence the level of MAOa (Sabol et al., 1998), which in turn
affects central levels of dopamine and 5-HT and thus, directly regulates behavior. Therefore, this gene has been the focus of molecular genetics studies of
aggressive behavior in both humans (Manuck et al., 2000) and rodents (Cases
et al., 1995) and is the most well-established susceptibility variant for aggression
in several species. MAOa genotype appears to influence the development of

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violent behaviors by altering vulnerability to the effects of early adverse environments (Caspi et al., 2002; Kim-Cohen et al., 2006). Specifically, there is robust
evidence that the interaction between MAOa and childhood maltreatment
predicts child CD and adult antisocial behavior such that males with low
expression of MAOa (L allele), but not males with high expression of MAOa
(H allele) are at increased risk (Kim-Cohen et al., 2006; Nilsson et al., 2007).
Recent evidence also links MAOa-L and low brain MAOa with trait aggression
and neural hypersensitivity to social cues (Alia-Klein et al., 2008; Eisenberger
et al., 2007). Interestingly, MAOa is an X-linked gene (with males carrying only
one allele and females carrying two), which suggests the possibility of sex
differences in genetic and epigenetic regulation and may explain the increased
average aggressiveness in males in comparison to females.
One recent study has noted an interaction between the MAOa uVNTR
(untranslated region variable number of tandem repeats) genotype, gender, and
maternal prenatal smoking in the prediction of CD symptoms (Wakschlag et al.,
2010). Specifically, boys with the low activity MAOa genotype whose mothers
smoked during pregnancy were at an increased risk of CD symptoms, whereas
girls with the high activity MAOa genotype whose mothers smoked during
pregnancy were at increased risk for hostile attribution bias (a characteristic
common to aggressive children) as well as CD symptoms.

2. Genes related to dopaminergic function

Kahn et al. (2003) noted an interaction between a DAT1 genotype and maternal
prenatal smoking in the prediction of oppositional and hyperactive symptoms in
young children. This finding was replicated in an adolescent sample; however,
the G  E effect was specific to hyperactive-impulsive symptoms in males
(Becker et al., 2008). Other studies have failed to replicate this effect for
DAT1 and other dopamine-related genotypes (e.g., Brookes et al., 2006;
Langley et al., 2008); however, relatively few studies have been completed in
this area.

3. Catechol O-methyltransferase
Catechol O-methyltransferase (COMT) is a key modulator of extracellular dopamine levels in the PFC. A common G/A polymorphism produces a valine-tomethionine amino acid substitution at codons 108 and 158 (Val108/158Met;
rs4680), which results in a three- to fourfold variation in COMT activity,
whereby the Val and Met alleles confer high and low activity, respectively
(Lachman et al., 1996). This well-characterized, functional polymorphism has
been associated with atypical neural processing and connectivity in healthy

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241

individuals (Dennis et al., 2010), deficits in executive functioning abilities

(Tunbridge et al., 2006), and with aggression and serious antisocial behavior in
individuals with ADHD (Caspi et al., 2008).
Prenatal exposure to nicotine also leads to persistent abnormalities in
neurotransmitter functioning in the cerebrocortical areas of the rat brain
(Slotkin et al., 2007). Further, both maternal prenatal smoking and COMT
associations with CD appear to be specific to aggressive behavior, rather than
covert antisocial behavior (Monuteaux et al., 2006, 2009). Taken together, these
findings suggest that the combination of the Val/Val genotype and prenatal
exposure to maternal smoking may lead to neural processing deficits that increase
vulnerability for aggression.
One study examining the interaction of prenatal risk and COMT
variation in the prediction of antisocial outcomes found that birth weight
interacted with Val108/158Met to predict antisocial behavior in an ADHD
sample (Thapar et al., 2005); however, this finding has had at least one failure
to replicate (Sengupta et al., 2006). Another recent study (Brennan et al., 2011)
found that individuals with the COMT Val/Val genotype whose mothers also
smoked during pregnancy were at an increased risk for aggressive behavior outcomes in adolescence and young adulthood. These G  E interaction findings are
preliminary but do suggest a potentially important role for genetics in noted
relationships between perinatal risk factors and aggression.

C. The role of epigenetics

The analysis of a G  E interaction is still focused on the fixed nature of the
genomethe DNA sequence itself. The DNA sequence is the same in every cell
of the body and does not change across the lifespan. But there are other
characteristics of genetic makeup that are not as fixed, and that have been
found to change in response to environmental influences over time. These are
known as epigenetic phenomena. Several epigenetic processes have been discovered, but the most commonly studied today is the phenomenon of methylation, a
measurable chemical modification to DNA that can directly alter the expression
of genes.
Methylation patterns change not only in response to toxins and stress
encountered in the environment but also in response to nutritional supplements
and parenting sensitivity. In a series of seminal studies in this area, Meaney and
colleagues discovered that the quality of the parenting (licking and grooming)
that a mother rat provided to her pups during early postnatal development
changed the methylation patterns in the hippocampus of her offspring
(Kappeler and Meaney, 2010). Specifically, higher levels of licking and grooming
made the genes (and the offspring) less responsive to stress in the environment.
In contrast, low levels of licking and grooming resulted in offspring whose

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genetic profile enhanced the release of cortisol in response to stress. Importantly,

either strategy might be considered ideal parenting, depending upon the
environment in which the offspring will have to survive.
Recent research suggests that prenatal factors may also influence DNA
methylation patterns in offspring (Radtke et al., 2011). Specifically, maternal
reports of abuse during pregnancy were found to be correlated with methylation
of the glucocorticoid receptor (GR) gene in offspring ages 1019. In contrast,
maternal experiences of abuse prior to or after pregnancy were not associated
with offspring DNA methylation patterns. Importantly, methylation of the GR
gene directly impacts the functioning of the HPA axis, which (as noted previously) may, in turn, impact levels of aggression and antisocial behavior.
In summary, preliminary evidence suggests that high versus low risk
genotypes may moderate the effects of perinatal exposures by influencing an
individuals susceptibility or resistance to these environmental experiences. In
addition, perinatal risk factors are associated with epigenetic changes that are
evident in and may influence later development. Complex behaviors, like aggression, are likely based on interactions of numerous genes and numerous
environmental factors. Future molecular genetics and epigenetic programming
studies should attempt to unravel the interplay between genes and environment.
Such knowledge will provide a clearer understanding of the role of early risk
factors in the development of aggression and how they can be used as intervention targets to alter developmental trajectories that lead to a lifetime of violence.

V. CONCLUSIONS
It is highly evident based on experimental and clinical studies that deleterious
perinatal exposures can have a profound and enduring impact on the neuroregulatory systems that mediate violence and aggression. Early adverse perinatal
experiences, in combination with predisposing genetic factors, combine with
unstable family environments to substantially increase the vulnerability for a
trajectory of delinquent and aggressive behavior throughout the lifespan; however, these outcomes are both complex and multidimensional. Future studies
should focus on genetic risk factors, as well as novel interventions that may
mitigate or prevent the deleterious effects of an adverse perinatal environment
on the development of aggression. Effective interventions should target prenatal
maternal mental and physical health-related behaviors, address parenting behaviors during critical stages of child development (i.e., infancy, early childhood,
and adolescence), as well as focus on child cognitive and social enrichment
during pre- and elementary-school years. As we are just beginning to understand
the complexity of the intergenerational transmission of these problems during

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pregnancy and early childhood, it is important as a field to focus on the origin,

early development, and prevention of aggression and violence to prevent vulnerable families and at-risk children from a lifetime of adversity.

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10

Neurocriminology
Benjamin R. Nordstrom,* Yu Gao, Andrea L. Glenn,
Melissa Peskin,} Anna S. Rudo-Hutt,} Robert A. Schug,
Yaling Yang,k and Adrian Raine*,},#
*Department of Psychiatry, University of Pennsylvania, Philadelphia, USA

Department of Psychology, Brooklyn College, New York, USA

Department of Child and Adolescent Psychiatry, Institute of Mental Health,

Singapore, Singapore
}
Department of Psychology, University of Pennsylvania, Philadelphia, USA

Department of Criminal Justice, California State University, Long Branch,

USA
k
Laboratory of Neuro Imaging, University of California, Los Angeles, USA
#
Department of Criminology, University of Pennsylvania, Philadelphia, USA

I. Introduction
II. Psychodynamic Theories
III. Neuroimaging
A. Structural imaging studies
B. Functional imaging studies
IV. Neuropsychological Testing
V. Psychophysiological Evidence
A. Electrocortical measures
VI. Genetics
A. Twin studies
B. Adoption studies
C. Molecular genetics
D. ACE model
E. Geneenvironment interaction
VII. Nongenetic Risk Factors
A. Prenatal
Advances in Genetics, Vol. 75
Copyright 2011, Elsevier Inc. All rights reserved.

0065-2660/11 $35.00
DOI: 10.1016/B978-0-12-380858-5.00006-X

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B. Perinatal risk factors

C. Postnatal
VIII. The Limitations and Potential of Neurocriminology
IX. Modifiable Risk Factor Interventions
X. Conclusion
References

ABSTRACT
In the past several decades there has been an explosion of research into the
biological correlates to antisocial behavior. This chapter reviews the state of
current research on the topic, including a review of the genetics, neuroimaging,
neuropsychological, and electrophysiological studies in delinquent and antisocial populations. Special attention is paid to the biopsychosocial model and
geneenvironment interactions in producing antisocial behavior. 2011, Elsevier Inc.

I. INTRODUCTION
In 1977, George Engel wrote an essay in Science to advocate for a new model in
medicine that would serve as a corrective to the biomedical reductionism that he
noted in the field and in psychiatry in particular (Engel, 1977). The model he
suggested was called the biopsychosocial model and, in understanding the disease
in question, took into account the biological aspect of the individual, their
psychological state, and the social context in which they exist. This model has
since become the dominant paradigm in psychiatric treatment.
In recent years, a tremendous amount of research has been done to
elucidate the biological correlates and causes of antisocial behavior. This work
has been conducted in an environment that has been, at times, hostile to this
kind of research, as the dominant paradigm in criminology research has focused
on social theories of crime. What we hope to accomplish in this chapter is to
present the evidence for a biopsychosocial model of crime.
We will present the data that argues that there is an inherited propensity for criminal behavior. The behavioral phenotype of those who criminally
offend is demonstrably and obviously different from those who do not; we will
show that their biological phenotypes are also different. We will marshal the data
that suggest that the various brain areas that perform cognitive processes relevant
to criminal offending are structurally and functionally different in antisocial
people compared to others. We will discuss how these brain differences are also

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257

evident in techniques that elucidate the mindbody connection. We will also

discuss how various social, or environmental, events can have multiplicative
interactions with the biological risk factors to produce criminal offending.
That there is not one standard diagnosis to identify the behavioral
phenotype of interest to criminologists is a limitation of any review of this
literature. Some research teams studying children use the diagnosis of oppositional defiant disorder or conduct disorder. Others use a broader category of
disruptive behavior, attention deficit hyperactivity disorder. Researchers interested in adults may use the diagnosis of antisocial personality disorder to identify
participants, while others might use the more stringent diagnosis of psychopathy.
Other teams use self-reports of violence or aggression, a history of arrests, or
various scores on personality inventories to identify the population of interest.
Our stance on this is that although these differences make it difficult to directly
compare the results of studies using different identifying criteria, all add the
potential to better understand the biological correlates of problematic behaviors.

II. PSYCHODYNAMIC THEORIES

For the first part of the twentieth century, psychoanalytic models of crime and/or
criminality (Holmes and Holmes, 1998; Wittels, 1937), cases of murder
(Abrahamsen, 1973; Arieti and Schreiber, 1981; Bromberg, 1951; Cassity,
1941; Evseef and Wisniewski, 1972; Karpman, 1951a,b; Lehrman, 1939;
Morrison, 1979; Revitch and Schlesinger, 1981, 1989; Wertham, 1949, 1950;
Wittels, 1937), and even homicide wound patterns (DeRiver, 1951) appeared in
the psychiatric literature. A common feature of psychoanalytic criminological
theory centers on unconscious processes (i.e., drives, instincts, and motivations,
and the defense mechanisms used to control them which operate outside of a
persons conscious awareness) which are maladaptive and lead to antisocial and
criminal behavior (Alexander and Staub, 1931).
A number of psychodynamic theorists have posited that early problems
of attachment to parents (especially mothers) can predispose individuals to
unstable personality structure and later criminal offending (Bowlby, 1944,
1969, 1973, 1980). Some theorists have posited that early experiences with
rejecting mothers can lead children to mentally internalize fragments of this
bad mother, which can then be externalized onto later female victims (Liebert,
1972). More recent authors have posited that such malformed attachments
might be at work in cases of serial homicide (Whitman and Akutagawa, 2004).
Although some of these notions of psychodynamic theories may appear
quaint compared to the astonishing technological achievements used in the
studies described later, it is worth noting that the psychodynamic theorists may
be using a different language to describe phenomena other researchers frame in

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more exacting biological terms. For example, we will later turn to discussions of
how biology and environment can interact in ways that increase the likelihood
of criminal offending. We will see that some of this data involves birth complications, and in what might be a partial affirmation of attachment theory,
maternal rejection.

III. NEUROIMAGING
Using neuroanatomy as a tool to study criminal propensity is an idea that dates
back to the early eighteenth century when the German physician Franz Joseph
Gall developed phrenology. Phrenology purported to analyze the shape of cranial
bones to make scientific inferences as to both the size and function of underlying
brain areas. Later technological advances replaced the pseudoscience of phrenology, allowing for the scientific study of how brain structure and function
relate to antisocial behavior. A comprehensive review of the neuroanatomic
literature as it pertains to antisocial behavior is available (Yang et al., 2008).
The two main technological advances that allowed images of the brain
itself to be generated are computerized axial tomography (CAT) scans and
magnetic resonance imaging (MRI) scans. CAT scans are produced using a series
of X-rays taken along the axis of the body. The X-rays pass unevenly through
tissues of different densities, allowing for distinctions between fluid, bone, and
brain tissue to be made. A computer then assembles these slices into a sequence
of cross-sectional images. MRI scans are created by using powerful magnetic
fields to orient all the hydrogen atoms (primarily found in water molecules) in
the brain in the same direction. A radiofrequency electromagnetic field is
introduced which then produces a signal that is detected by the MRI scanners
receiver. These signals are then assembled into high-resolution images that can
distinguish the gray matter from the white matter of the brain. MRI scans dont
use radiation and produce more detailed pictures than do CAT scans, but they
also take much longer to obtain and are much more expensive.

A. Structural imaging studies

Structural neuroimaging studies the size of brain regions of interest (ROI). One
early study found that when CAT scans of the brains of sexual sadists were
studied, about 50% of them had abnormal brain structures, especially in the
temporal lobes (Langevin et al., 1988). Other researchers found that nearly 50%
of 19 murder suspects studied had atrophic brains on CAT scan (Blake et al.,
1995). Later studies using MRI scans found brain atrophy as well, especially in
the frontotemporal region (Aigner et al., 2000; Sakuta and Fukushima, 1998).

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Another qualitative structural imaging study found that 6 of 10 of the violent

psychiatric inpatients they studied had atrophic temporal regions (Chesterman
et al., 1994).
A number of studies in structural imaging have used larger samples and
reported their findings in quantitative terms. Raine and colleagues viewed 21
individuals with antisocial personality disorder and compared them to a matched
group of substance users and normal controls (Raine et al., 2000, 2010). This
work reported an 11% reduction in the gray matter of the prefrontal cortices of
the antisocial group. A second study by this group found reduced prefrontal
cortical gray matter volumes in unsuccessful psychopaths (i.e., psychopaths who
had been criminally convicted at least once), compared to successful psychopaths (i.e., psychopaths who had never been convicted of a crime), and normal
controls (Yang et al., 2005). In addition, Yang et al. revealed reduced cortical
gray matter thickness in the frontal and temporal regions in psychopaths when
compared to normal controls (Yang et al., 2009). Other groups have found that,
compared to normal controls, subjects with antisocial personality disorder have
smaller temporal lobes (Dolan et al., 2002; Laakso et al., 2002), as well as
reductions in their dorsolateral, medial frontal, and orbitofrontal cortices
(Laakso et al., 2002).
One team of researchers demonstrated smaller gray matter volumes in
the orbitofrontal and temporal lobes of children with conduct disorder compared
to normal controls (Huebner et al., 2008). Reductions in gray matter concentration have also been observed in the frontal and temporal lobes of criminal
psychopaths compared to normal controls (Muller et al., 2008). Along
these same lines, another research group found insignificant prefrontal lobe
volume reductions, but significant temporal lobe volume reductions, in conduct
disordered children (Kruesi et al., 2004).
Buried deep in the temporal lobe is the amygdala, which is associated
with fear conditioning, and the hippocampus, a structure associated with
learning and memory. Laakso and colleagues found, in a group of violent
offenders with alcoholism and antisocial personality disorder, that smaller posterior hippocampus measures matched higher psychopathy rating scores (Laakso
et al., 2000, 2001). Other researchers report that adolescents with conduct
disorder demonstrate reduced gray matter volumes in the insula and amygdala
compared to normal controls (Sterzer et al., 2007).
A relatively new technique called diffusion tensor imaging (DTI) allows
images to be taken of the structural integrity of the white matter tracts connecting various parts of the brain. One DTI study showed evidence of abnormal white
matter tract structure in the frontotemporal regions of adolescents with disruptive behavior compared to normal controls (Li et al., 2005). A second study
showed similar evidence of abnormal white matter tracts connecting the amygdalas and orbitofrontal cortices of criminal psychopaths when compared to

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normal controls (Craig et al., 2008). Other studies looking at abnormalities in

connectivity have focused on white matter structures. Raine et al. (2003a,b)
found that compared to a normal comparison group, psychopathic, antisocial
subjects had a longer, thinner corpus callosum with overall increased volume.
They also found a correlation between psychopathy scores and larger callosal
volumes (Raine et al., 2003a).

B. Functional imaging studies

Not only does current technology allow us to study the structure and connectivity of brain regions, it also allows us to image the functioning of brain areas as
well. One form of functional neuroimaging is photon emission tomography
(PET). This technique relies on injecting subjects with radioactively labeled
substance such as glucose. Images of their brains can then be obtained. Areas of
higher radioactive signal have more glucose metabolism and are thought to be
more active (Yang et al., 2008). A second form of functional neuroimaging is
single photon emission tomography (SPECT). This form of imaging also
involves the injection of a radioactive tracer. The camera detects the amount
of radiation coming from different parts of the brain. These differences are due to
differences in regional cerebral blood flow (rCBF) and are thought to reflect
different levels of activity in various parts of the brain (Yang et al., 2008)
Functional magnetic resonance imaging (fMRI) studies measure changes in
blood oxygen in ROI in the brain before and after cognitive tasks are undertaken.
These blood oxygen level dependent (BOLD) signals are used as a proxy for how
active a region of the brain is. By comparing subjects of interest with matched
controls, the patterns of activation or inactivation in the brain can be studied to
learn how the functioning of various brain regions relates to the condition at
hand (Yang et al., 2008).
One early PET scan study showed that, compared to controls, antisocial
subjects demonstrated reduced glucose metabolism in the prefrontal and temporal areas of their brains (Volkow et al., 1995). A SPECT study of aggressive
psychiatric patients also found reduced rCBF in the prefrontal cortex, as well as
increased blood flow to the left temporal and the anterior medial frontal cortices
(Amen et al., 1996).
Other PET studies have investigated how glucose metabolism responds
to difficult cognitive tests, such as a continuous performance task (CPT). One
group found that the number of impulsiveaggressive acts perpetrated by subjects
with personality disorders, including antisocial personality disorder, was negatively correlated to glucose metabolism in the orbitofrontal, anterior medial
frontal, and left anterior frontal cortices (Goyer et al., 1994). Raine et al.
(1994a,b) found that after a CPT, a sample of murderers demonstrated reduced
glucose metabolism in the anterior medial prefrontal, orbitofrontal, and superior

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frontal cortices compared to a normal comparison group (Raine et al., 1994b).

A follow up study with a larger sample but a similar methodology found the same
pattern of reduced glucose metabolism in the anterior frontal cortices, and in the
amygdalas and hippocampi as well (Raine et al., 1997a).
The amygdala is a structure in the brain that plays a significant role in
emotion processing. This makes it an important structure in associative learning,
in which individuals assign an affective valence to the consequences of their
actions. These associations can be positive, such as learning to feel good after
helping someone, or negative, such as learning to feel guilty or bad after harming
someone. It has been theorized that associating harmful actions with the distress
of others could thus discourage antisocial behavior (Blair, 2006a,b).
A study using PET technology looked at a sample of normal controls, a
sample of schizophrenic patients with a history of repeated violent offending and
a sample of schizophrenic patients with a history of nonrepetitive violent offending (Wong et al., 1997). This team found that, compared to the normal controls,
the patient samples had reduced glucose metabolism in the anterior inferior
temporal lobes. This reduction was bilateral in the nonrepetitively violent
group, but isolated to the left side in the repetitively violent group. Later, a
research group using SPECT found that, compared to normal controls, antisocial
populations have reduced rCBF to the frontal cortex and temporal cortex, and
that psychopathy scores are negatively correlated with the degree of rCBF
reduction to these areas (Soderstrom et al., 2000, 2002).
One fMRI study looked at patterns of brain activation in 13 adolescent
aggressive conduct disordered males and 14 matched controls as they looked at
neutral pictures and pictures with a strong negative affective valence. It was
found that when the conduct disordered youth viewed the distressing pictures
they had significantly reduced activity to their left amygdalas compared to the
control subjects (Sterzer et al., 2005). Similar findings have been described in
adult populations (Kiehl et al., 2004; Muller et al., 2003).
Another group used a similar methodology to study the reaction of a
sample of 36 children and adolescents as they viewed photographs of neutral,
angry, or fearful faces. 12 of the participants had callousunemotional traits and
oppositional defiant disorder or conduct disorder, 12 had attention deficit hyperactivity disorder and 12 were comparison subjects. When compared to the other
two groups, the group with callousunemotional traits demonstrated significantly
reduced amygdala activation on viewing the fearful (but not the angry or
neutral) faces (Marsh et al., 2008). In addition, in a functional connectivity
analysis, the callousunemotional children showed reduced connectivity between the ventromedial prefrontal cortex and the amygdala. Further, the degree
of reduction in this connectivity was negatively correlated with the score on the
scale that measured the degree of callousunemotional traits. This is particularly
interesting as the ventromedial prefrontal cortex has been implicated in

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processing punishment and reward (Rolls, 2000), affective theories of the mind
(Shamay-Tsoory et al., 2005), response inhibition (Aron et al., 2004; Vollm
et al., 2006), and emotional regulation (Ochsner et al., 2005).

IV. NEUROPSYCHOLOGICAL TESTING

Neuropsychological tests provide another method for testing the capabilities and
functioning of various brain areas. One of the most consistent findings in the
neuropsychological aspects of criminality is that antisocial populations have
lower verbal IQs compared to nonantisocial groups (Brennan et al., 2003; Dery
et al., 1999; Raine, 1993; Teichner and Golden, 2000). Researchers have found
that verbal deficits on testing at age 13 predict delinquency at age 18 (Moffitt
et al., 1994). A number of authors have found evidence that such neuropsychological deficits show interactive effects when they are present in children with
social risk factors (Aguilar et al., 2000; Brennan et al., 2003; Raine, 2002a,b).
Executive functioning is another neuropsychological function of interest in criminology (Moffitt, 1990, 1993). Executive functioning refers to the
group of cognitive processes that produce goal-directed, flexible, and strategically
effective behavior (Lezak et al., 2004; Luria, 1996; Spreen and Strauss, 1998).
Executive dysfunction involves impairments in impulse control, self-regulation,
abstract reasoning, concept formation, sustained attention, planning, organization, problem solving, and cognitive flexibility (Raine, 2002a,b). A meta-analysis of 39 studies incorporating data from 4589 individuals studied the relationship
between executive dysfunction and antisocial behavior(Morgan and Lilienfeld,
2000). These authors found significant effect sizes (d 0.86 for juvenile delinquency and d 0.46 for conduct disorder) for the association between antisocial
behavior and executive dysfunction.
Another neuropsychological test that has been studied in antisocial
populations tests selective attention, or the ability to attend to one or more
stimuli while ignoring others. The dichotic listening test is used to probe selective
attention by having subjects wear headphones and then sending different auditory stimuli to each ear, while instructing them to respond to only 1 ton and ignore
others. Both adult (Hare and Jutai, 1988) and juvenile (Raine et al., 1990a)
populations with psychopathic traits have been shown to have abnormalities on
this test when verbal stimuli are used. These researchers have hypothesized that
this reduced lateralization of linguistic processes might indicate that people with
psychopathic traits have a reduced use of language to regulate their behavior.
Other neuropsychological tests have focused on how antisocial populations respond to affectively charged stimuli. Loney et al. (2003) found that
juveniles with callousunemotional traits showed slower reaction times after
being presented with emotionally negative words, while those with impulsive
traits showed faster reaction times to such stimuli. Adult psychopaths have been

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found to have deficits in passive-avoidance learning tasks (Newman and Kosson,

1986) and adolescent psychopaths have been shown to demonstrate hyperresponsivity to rewards (Scerbo et al., 1990). Taken together, these data suggest
that psychopathic individuals will be less sensitive to punishment and more
sensitive to the possibility of rewards as a consequence to their behavior. Also,
given the executive functioning literature, they may be less able to plan, act in a
rationally self-interested fashion, control their impulses and respond flexibly to
the various problems encountered in everyday life.

V. PSYCHOPHYSIOLOGICAL EVIDENCE
The autonomic underarousal and hyporesponsivity noted in various electrophysiological studies have given rise to fearlessness theory. This theory posits that the
low level of arousal noted in the somewhat stressful testing situations can be
taken as evidence of a lack of normal fear (Raine, 1993, 1997). An alternative to
fearlessness theory is the stimulation-seeking theory, which presumes that the
observed hypoarousal is experienced by affected individuals as unpleasant, and is
compensated for using risk-taking/thrill-seeking behaviors. Supporting this hypothesis is the observation that 3-year-old children who show high levels of
sensation seeking and lower levels of fearlessness demonstrate increased levels of
aggression at age 11 (Raine et al., 1998).
It is likely that stimulation-seeking and fearlessness explain some part of
the low resting heart rate shown in antisocial youth, but a causal link between
the low resting heart rate and criminal behavior is more elusive (Raine, 2002a,b).
A third theory, the prefrontal deficit theory, argues that the low arousal seen
arises from abnormalities in the prefrontal corticalsubcortical circuits involved
with arousal and stress response (Raine, 2002a,b).
A number of psychophysiological studies have also elucidated biological
correlates of criminal behavior. These studies have typically focused on heart
rate, skin conductance and electrocortical measurements. In-depth descriptions
of the methodologies used in psychophysiological research are available
(Cacioppo et al., 2007).

A. Electrocortical measures

1. Electroencephalogram (EEG)
The electrical activity in the cerebral cortex can be measured by a noninvasive
test, the EEG (Hugdahl, 2001). In an EEG, the subject has electrodes placed in
specific points over the scalp. These electrodes detect the brains electrical
impulses, which are then recorded and analyzed by a computer. The frequency
and amplitude of the resultant signals are then interpreted.

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Increasing frequency is associated with increasing arousal, and lower

frequency is associated with lower arousal (Hugdahl, 2001). Slower EEG activity
in children and adolescents is associated with later criminal behavior (Mednick
et al., 1981; Petersen et al., 1982). Raine and colleagues demonstrated that,
compared to their peers with higher arousal, 15-year-old boys with lower arousal
as measured by resting EEG were more likely to become criminals at age 24
(Raine et al., 1990b). Children with externalizing and antisocial behaviors have
been noted to demonstrate abnormal patterns of EEG asymmetry in their frontal
lobes (Ishikawa and Raine, 2002; Santesso et al., 2006).
It has been noted that dominant EEG frequencies increase with age
(Dustman et al., 1999). The EEG abnormalities noted with respect to criminal
behavior have been hypothesized to be due to cortical immaturity (Volavka,
1987). It has been suggested that abnormal frontal EEG asymmetry might belie
language and analytic reasoning deficits, thus impairing emotion regulation
(Santesso et al., 2006).

2. Event-related potentials (ERPs)

A stimulus perceived by the brain will cause a change in the brains electrical
activity. An ERP is a measure of the magnitude of that change after the
presentation of specific stimuli. The change, or deflection, may be positive or
negative in direction, and occurs within milliseconds of the onset of the stimulus.
Typically an ERP is measured several times, and the average of all the trials is
taken (Hugdahl, 2001). The P300 is a waveform that typically occurs approximately 300 ms after the presentation of a stimulus. Early onset of drug abuse and
criminal behavior has been shown to be related to smaller P300 amplitudes
(Iacono and McGue, 2006). Other studies have demonstrated that greater
negative amplitude at 100 ms and faster latency at 300 ms at age 15 are predict
criminal behavior at age 24 (Raine et al., 1990b). A meta-analysis of studies of
ERP in antisocial populations found that, in general, antisocial individuals have
smaller P300 amplitudes and longer latencies (Gao and Raine, 2009).

3. Low resting heart rate

Low resting heart rate is the best-replicated biological correlate of antisocial
behavior in juvenile samples (Ortiz and Raine, 2004). In a meta-analytic review
of 29 samples, the average effect size was 0.56. This effect was demonstrated in
both genders and irrespective of measurement technique (Raine, 1996). This
relationship is not artifactual, as confounding variables such as height, weight,
body composition, muscle tone, poor school performance, low IQ, hyperactivity,

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low attention, drug and alcohol use, participation in sports and exercise, social
class, and family size and composition have all been ruled out (Farrington, 1997;
Raine et al., 1990b, 1997b; Wadsworth, 1976).
The finding that low resting heart rate predicts later crime has been
replicated in the United States, Germany, England, Canada, Mauritius, and New
Zealand (Farrington, 1997; Mezzacappa et al., 1997; Moffitt and Caspi, 2001;
Raine et al., 1997b; Rogeness et al., 1990; Schmeck and Poustra, 1993). In
longitudinal studies, low resting heart rate has been shown to accurately identify
individuals who are at risk for later developing antisocial behavior. This finding
is specific for antisocial behavior (Rogeness et al., 1990) and has not been shown
in other psychiatric syndromes.
In the Cambridge Study in Delinquent Development, a series of six
regression analyses were used to identify the best independent risk factors of
violence (Farrington, 1997). Only two risk factors, low resting heart rate and
poor concentration, were found, independently of all other risk factors, to predict
violence. This same study found evidence of an interaction between low resting
heart rate and several environmental risk factors (e.g., coming from a large
family, having a teenaged mother, being of low socioeconomic status) in producing violent behavior. Lastly, it has been shown that having a high resting heart
rate is negatively correlated with later violent behavior (i.e., a high resting heart
rate is a protective factor against developing crime development) (Raine et al.,
1995).

4. Skin conductance
The ease with which the skin can conduct electrical impulses is a function of
sympathetic nervous system activity. Increased sweating leads to improved
electrical conductance along the surface of the skin. In times of stress, sympathetic nervous system activity increases, and skin conductance will also increase.
A classically conditioned fear response (as measured by an increase in skin
conductance) can be produced by pairing a stressful stimulus, such as a noxious
sound, with a neutral stimulus, such as a light turning on. Studying skin conductance under different paradigms can thus provide insight into the functioning of
the sympathetic nervous system.
Low skin conductance has been shown to be associated with conduct
problems (Lorber, 2004). Boys with conduct disorder have been shown to have
reduced fluctuations in skin conductance and impairments in conditioned fear
responses (Fairchild et al., 2008; Herpertz et al., 2005). Longitudinal studies have
demonstrated that reduced skin conductance arousal at age 15 has been associated with criminal offending at age 24 (Raine et al., 1995) and that low skin
conductance at age 11 predicts institutionalization at age 13 (Kruesi et al., 1992).

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Impaired fear conditioning as measured by skin conductance at age 3 has been

shown to predict aggression at age 8 and criminal behavior at age 23 (Gao et al.,
2010a,b).
Low sympathetic reactivity has been shown in psychopathy-prone adolescents and in children with conduct disorder and callousunemotional traits
(Anastassiou-Hadjichara and Warden, 2008; Kimonis et al., 2006; Loney et al.,
2003). At age 3, having an abnormal skin conductance response to unpleasant
stimuli is a risk factor for displaying psychopathy in adulthood (Glenn et al.,
2007).

VI. GENETICS
As described in more detail in a separate chapter in this volume, a growing body
of evidence has shown that there is a strong genetic contribution to juvenile
delinquency (Popma and Raine, 2006). Although a number of genes have been
shown to have an association with antisocial behavior, no one gene seems to
explain criminal behavior (Goldman and Ducci, 2007). Investigating the
potential genetic basis for complex behaviors is inherently complicated as they
are likely to involve multiple genes, in contrast to conditions where there is a
single-gene effect, as in classic Mendelian genetics (Uhl and Grow, 2004).
Studies report heritability estimates that range widely, although the majority of
investigators find heritability estimates that fall between 40% and 60%
(Arsenault et al., 2003; Beaver et al., 2009; Jaffee et al., 2004, 2005; Lyons
et al., 1995; Moffitt, 2005; Rhee and Waldman, 2002; Slutske et al., 1997).

A. Twin studies
One way to investigate a genetic component to a behavior is by comparing the
frequency with which the disease occurs in different kinds of siblings. Monozygotic (also called identical) twins arise from a single fertilized ovum, meaning
they have exactly the same genetic material. Dizygotic (also called fraternal)
twins arise from two separate fertilized ova. Like any siblings, they share 50% of
the same genes. A twin pair demonstrates concordance when both individuals
demonstrate the condition in question, while twin pairs with only one affected
individual are said to show discordance. The heritability of a disease can be
estimated by comparing the rates of concordance and discordance in both
monozygotic and dizygotic twins (Jorde et al., 1995).
One study that investigated the genetic contribution to childhood
antisocial and aggressive behavior investigated 605 families of 9- to 10-yearold twins and triplets (Baker et al., 2007). In this economically and ethnically
diverse sample, such behavior was strongly heritable. Another study analyzed

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self-report measures of aggression in 182 monozygotic and 118 dizygotic twins

(Coccaro et al., 1997a). The investigators found significant heritability for three
out of the four forms of aggression studied. Although twin studies provide the
opportunity study individuals with identical genetic make-ups or identical prenatal histories, other methodologies have also sought to gain understanding into
the relative contribution of genes and parenting on later problematic behavior.

B. Adoption studies
Adoption studies provide another mechanism for studying the genetic versus the
environmental contributions to antisocial behavior. In such studies, the characteristics of a childs biological and adoptive parents are considered relative to
the childs own behavior. One early such study (Bohman, 1978) found evidence
for a genetic predisposition to alcohol, but not to criminality, while another
study from that same year (Cadoret, 1978) found evidence for heritability of
antisocial behavior. A study of 862 Swedish male adoptees found that genetic
influences were the most significant contributor to later criminal behavior
(Cloninger et al., 1982). Another large sample of adoptees in Denmark similarly
found strong evidence for a genetic propensity for criminal behavior (Gabrielli
and Mednick, 1984).

C. Molecular genetics
Although it was previously noted complex behavioral syndromes dont follow
ordinary Mendelian patterns of inheritance, there is a notable exception to this.
One group of researchers identified a family that demonstrated X-linked inheritance of borderline intellectual functioning and abnormal behavior. (Brunner
et al., 1993) The behaviors exhibited by affected males included aggression, rape,
exhibitionism, and arson. The researchers found that all had inherited a deficiency in the gene that coded for monoamine oxidase A (MAO-A).

D. ACE model
In behavioral genetic research, the heritability (i.e., the portion of the phenotypic variance explained by genetic factors) is represented by the letter A. The
letter C is used to represent the family-wide, common, or shared environment.
This includes influences that siblings would share, such as parenting styles or
neighborhood characteristics. The letter E is used to represent environmental
conditions uniquely encountered by an individual, such as getting a head injury.
These are also called nonshared environmental influences.

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One such study investigated the genetic basis for psychopathy (Larsson
et al., 2006). The researchers found that A accounted for 63% of the variance,
C accounted for 0%, and E accounted for 37% of the variance.
One meta-analytic study that used the ACE model found that, in
children, genes (A) and shared environment (C) were equally important in
explaining aggressive behavior (Miles and Carey, 1997). The researchers also
found that heritability was slightly higher for males than for females, and that in
adulthood the role of heritability increased while the role of shared environment
fell to inconsequential levels.
Another meta-analytic study of over 100 behavioral genetic studies
showed that 4050% of the variance of antisocial behavior is due to heritability,
30% is due to the nonshared environmental influences, and 1520% is due to
shared environmental influences (Rhee and Waldman, 2002).
It has been demonstrated that the influence of genes on criminal
behavior varies over the life course (Goldman and Ducci, 2007). The majority
of reports find that heritability estimates for antisocial behavior are lower, and
shared environmental effects on antisocial behavior are higher, in childhood
than in adolescence (Jacobson et al., 2002; Lyons et al., 1995; Miles and Carey,
1997). It further seems that some genes affect the propensity for criminal
involvement in adolescence, while others exert their effects in adulthood
(Goldman and Ducci, 2007).
The effects of genetics are also moderated by the type of criminal
offending being considered. Heritability estimates for aggressive offending are
higher than those for nonaggressive offending, such as rule breaking and theft
(Eley et al., 2003). The opposite appears to be true for nonaggressive offending,
which may be influenced more by shared environmental factors, such as family
criminality, family poverty, and poor parenting, although research suggests that
genetic influences also affect several of these risk factors (Moffitt, 2005).

E. Geneenvironment interaction
Other studies have focused on how a persons genetic endowment interacts with
the environment in which the person lives. In the Swedish adoption study
described above (Cloninger et al., 1982), the researchers found that if a person
had both a biological parent and an adoptive parent who were criminals, then
the persons likelihood of criminal behavior was greater than the sum of the
individual risks. In other words, there was a multiplicative effect of having a
biological predisposition to crime and then being raised in a criminogenic
environment.
Another large study of geneenvironment interaction identified people
who carried a genotype that conferred a low expression of MAO-A activity
(Caspi et al., 2002). The researchers looked at the people with high versus low

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MAO-A activity and also whether or not the individual had been abused as a
child. They found evidence of a strong interaction between low MAO-A activity
and childhood maltreatment in the likelihood of developing conduct disorder.

VII. NONGENETIC RISK FACTORS

There are many different types of the kinds of environmental risk factors
captured by the ACE model. Researchers have identified a number of intriguing
risk factors, some of which could be shared by siblings, some of which are less
likely to be, which have been associated with later problematic behavior. These
risk factors can be broken into those that arise during pregnancy (prenatal),
those that arise during birth (perinatal) and those that arise in childhood
(postnatal).

A. Prenatal

1. Minor physical anomalies (MPAs)

MPAs are subtle physical defects such as having a curved fifth finger, a single
palmar crease, low seated ears, or a furrowed tongue, are thought to arise from
abnormalities in fetal development. These are thought to serve as biomarkers for
abnormalities in neural development as well. MPAs may have a genetic basis, but
they might also be due to anoxia, bleeding, or infection (Guy et al., 1983). Early
studies showed an increase in the prevalence of MPAs in school-aged boys
exhibiting behavioral problems (Halverson and Victor, 1976). MPAs have also
been shown to be correlated to aggressive behaviors in children as young as 3
years old (Waldrop et al., 1978). It has also been shown that MPAs identified at
age 14 predict violence at age 17 (Arsenault et al., 2000).
Mednick and Kandel studied MPAs in a sample of 129 12-year-old boys
(Mednick and Kandel, 1988). They found MPAs were related to violent offending as assessed 9 years later when subjects were 21 years old. Interestingly, when
subjects were divided into those from unstable (i.e., non-intact) homes versus
those from stable homes, a biosocial interaction was observed. MPAs only
predicted violence in those individuals raised in unstable home environments.
Similarly, a study of 72 male offspring of psychiatrically ill parents found
that those with both MPAs and family adversity had especially high rates of adult
violent offending (Brennan et al., 1997). Another study showed that the presence of MPAs significantly interacted with environmental risk factors (e.g.,
poverty, marital conflict) to predict conduct problems in adolescence (Pine
et al., 1997).

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2. Tobacco
There is a significant body of evidence that demonstrates that maternal smoking
during pregnancy predisposes children to developing antisocial behavior
(Wakschlag et al., 2002). Maternal prenatal smoking predicts externalizing behaviors in childhood and criminal behavior in adolescence (Fergusson et al., 1993,
1998; Orlebeke et al., 1997; Rantakallio et al., 1992b; Wakschlag et al., 1997).
Researchers have elucidated a clear dose-dependent relationship between smoking
and later criminal behavior (Brennan et al., 1999; Maughan et al., 2001, 2004).
Although the mechanism by which smoking produces these effects is
unknown, basic science research has shown that the byproducts of smoking may
affect the brains dopaminergic and noradrenergic systems (Muneoka et al.,
1997) and glucose metabolism (Eckstein et al., 1997). Smoking may affect
various brain structures, for example, the basal ganglia, cerebral, and cerebellar
corticesimplicated in the deficits observed in violent offenders (Olds, 1997;
Raine, 2002a,b).

3. Alcohol
There is also a great deal of evidence that prenatal exposure to alcohol predisposes individuals to antisocial behavior (Fast et al., 1999; Olson et al., 1997;
Streissguth et al., 1996). Although Fetal Alcohol Syndrome (FAS) does not arise
in all children exposed to alcohol in utero, evidence shows that children who do
not display the full FAS syndrome can have some of the functional deficits
characteristic of the syndrome (Schonfeld et al., 2005). Children who do not
meet diagnostic criteria for FAS, yet were exposed to high levels of alcohol in
utero, are at increased risk of antisocial behavior (Roebuck et al., 1999).

B. Perinatal risk factors

Obstetrical complications are untoward events that occur at the time of delivery
and include such things as maternal preeclampsia, premature birth, low birth
weight, use of forceps in delivery, transfer to a neonatal intensive care unit,
anoxia, and low Apgar scores. Maternal complications have been shown to have
deleterious effects on neonatal brain function (Liu, 2004; Liu and Wuerker,
2005). Newborns who suffer obstetrical complications are more likely to exhibit
externalizing behaviors at age 11 than those without complications (Liu et al.,
2009). Obstetrical complication was found to mediate the relationship between
low IQ and externalizing behaviors.
It has also been demonstrated that obstetrical complications interact
with other environmental factors to predict later antisocial behavior. Raine et al.
(1994a,b) investigated a cohort 4269 Danish men. The investigators found that

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birth complication significantly interacted with severe maternal rejection (e.g.,

efforts to abort the pregnancy, reporting the pregnancy as unwanted, or attempting to give up custody of the baby) to predict violent crime in adolescence (Raine
et al., 1994a). This study has since been replicated in the United States, Sweden,
Finland, and Canada, and has repeatedly shown that birth complications interact
with a number of psychosocial risk factors to produce antisocial behavior
(Arsenault et al., 2002; Hodgins et al., 2001; Kemppainen et al., 2001; Tibbetts
and Piquero, 1999).

C. Postnatal
Poor nutrition has been investigated as a risk factor for criminal behavior for
some time. An association between aggressive behavior and vitamin and mineral
deficiency has been described (Breakey, 1997; Werbach, 1995). The exact
mechanism by which malnutrition affects later antisocial behavior is not well
understood, it has been hypothesized that proteins or minerals may either
regulate neurotransmitters and hormones, or ameliorate neurotoxins (Coccaro
et al., 1997b; Liu and Raine, 2006).
Although most studies have focused on nutrition in the postnatal period,
one study investigated the role of malnutrition in the prenatal period in producing
antisocial behavior (Neugebauer et al., 1999). This group studied the offspring of
women who were pregnant during the German food blockade of Dutch cities in
World War II. The blockade produced near starvation and severe food shortages.
The researchers found that the male offspring of women who were in the first and
second trimesters (but not the third trimester) of pregnancy during this time had
two and a half times the rate of antisocial personality disorder than did the
offspring of women who were not affected by food shortages.
Another study of prenatal nutrition studied a sample of 11,875 pregnant
women. Those women who ate less seafood (i.e., less than 340 g a week), which
is rich in omega-3 fatty acids, had offspring that demonstrated significantly lower
scores on a number of neurodevelopmental outcomes, including prosocial behavior, than the offspring of mothers who ate more seafood (Hibbeln et al.,
2007).
Studies have also shown that deficiency in nutrients such as proteins,
zinc, iron, and docosahexaenoic acid (a component of omega-3 fatty acid) can
lead to impaired brain functioning and a predisposition to antisocial behavior in
childhood and adolescence (Arnold et al., 2000; Breakey, 1997; Fishbein, 2001;
Lister et al., 2005; Liu and Raine, 2006; Rosen et al., 1985).
Longitudinal studies have shown that malnutrition in infancy is associated with aggressive behavior and attentional deficits in childhood (Galler and
Ramsey, 1989; Galler et al., 1983a,b). Liu et al. conducted a prospective longitudinal study to investigate how early malnutrition can predispose to behavior

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problems later in life (Liu and Raine, 2006). The researchers found that, compared
to controls, children with protein, iron, or zinc deficiencies at age 3 had significantly more aggressive and hyperactive behavior at age 8, more antisocial behavior
at age 11, and more excessive motor activity and conduct disorder at age 17.
Significantly, this team also found a dose-dependent relationship between the
extent of malnutrition and the extent of later behavior problems.

1. Traumatic brain injury (TBI)

Another risk factor that has been studied in relation to antisocial behavior is
TBI. One group of investigators found that half of the juvenile delinquents in
their sample had a history of TBI, and a third of the delinquents with TBI were
thought by their parents to have neuropsychological sequelae from their injuries
(Hux et al., 1998). Another study, which used more severe criteria in the
definition of TBI than the previous study, found that 27.7% of the delinquents
in their sample had a history of TBI (Carswell et al., 2004). A number of large,
longitudinal studies of have repeatedly shown an increased incidence of delinquent behavior among youth with a history of TBI (Asarnow et al., 1991; Bloom
et al., 2001; Butler et al., 1997; McAllister, 1992; Rantakallio et al., 1992a; Rimel
et al., 1981; Rivera et al., 1994).

VIII. THE LIMITATIONS AND POTENTIAL OF NEUROCRIMINOLOGY

The field of neurocriminology has struggled to free itself from associations to
earlier efforts to incorporate biology into the field of criminology. The reductionism of Lombrosos biological positivism, the pseudoscience of phrenology,
and the appalling racism of social Darwinists have all cast long shadows that
have affected how contemporary efforts have been received by sociologically
oriented criminologists.
There is a danger that the kind of neurocriminological data could be
used in a sensationalistic or superficial manner to implicate or exculpate individual offenders. Although the current state of imaging and other forms of biological
research have not advanced to the point where an individuals data could be
confidently compared against a reliable database of normal controls, the possibility exists that such databases could be created and validated (Yang et al.,
2008). Until such time, however, it is important to note that studies of the sort
reviewed in this chapter cannot be taken to imply that any one biological factor
causes criminal behavior. Rather, the presence of these factors only increases the
probability that problematic behavior will be present in people with a given
biological risk factor.

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We have now reviewed a number of studies that describe such increased

probabilities of biological risk factors in criminal behavior. The sociological roots
have crime have also been widely studied. This chapter has also reviewed a
number of examples of how biological and environmental forces can interact to
produce problematic behavior. We can see that criminal behavior can be investigated and explained at many different levels of abstraction.
The psychiatrist and philosopher Kenneth Kendler illustrates this phenomenon with a hypothetical case of a pharmacologist running a randomized
controlled trial of a medication for a psychiatric condition (Kendler, 2005).
Although it is undoubtedly true that the medication is a molecule, and molecules
are made up of atoms and atoms are made up of subatomic particles, it does not
necessarily make sense to consult with a particle physicist in conducting the
study. Thus, some levels of abstraction may be more or less efficient in explaining
the phenomenon in question. However, each time a new level is identified, new
possibilities for intervention arise as well. In uncovering biological leads relevant
to crime the potential for new strategies for crime prevention are created as well.

IX. MODIFIABLE RISK FACTOR INTERVENTIONS

Not all risk factors for criminal behavior (e.g., male gender, having a biological
parent with a history of criminal behavior) are modifiable. There are a number of
risk factors (e.g., smoking, nutrition), however, that can be modified. Successful
interventions have been developed to reduce prenatal alcohol exposure (Chang
et al., 1999, 2005). Interventions have also been designed to reduce smoking in
pregnancy, but these have been notably less effective than the interventions for
alcohol use (Ershoff et al., 2004). Of note, women who persist in smoking
throughout pregnancy are more likely than those who quit to have a personal
history of conduct disorder (Kodl and Wakschlag, 2004).
Other studies have sought to correct nutritional deficits. One randomized, double blind, placebo-controlled study was performed in a sample of 486
public schoolchildren to see if a daily multivitamin and mineral supplement
could reduce antisocial behavior (Schoenthaler and Bier, 2000). The researchers
found that, compared to the placebo group, the treatment group had a 47%
reduction in antisocial behavior after 4 months. Previously, this team had
investigated the effect of vitamin and mineral supplementation in a group of
juvenile delinquents confined to a correctional setting. The results of this
randomized, double blind, placebo-controlled trial showed that, compared to
the placebo group, the treatment group had significantly less violent and nonviolent antisocial behaviors (Schoenthaler et al., 1997). Another randomized,
double blind, placebo-controlled trial of omega-3 fatty acid supplementation
was done in a sample of 50 children. Compared to the placebo condition, the

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intervention group had a 42.7% reduction in conduct disorder problems (Stevens

et al., 2003). A study using omega-3 fatty acid supplementation in ADHD failed
to reveal a benefit (Hirayama et al., 2004).
Other interventions address more than one risk factor at a time. For
example, one highly successful intervention for prevention of later criminal and
antisocial behavior involves home nursing visits for pregnant and new mothers.
Parenting, health, and nutritional guidance are provided in the sessions (Olds
et al., 1998). Other authors have also shown that prenatal education on nutrition, health, and parenting can lead to reductions in juvenile delinquency at age
15 (Lally et al., 1988).
Another multidimensional intervention was tested in a randomized,
controlled fashion (Raine et al., 2003b). In this study, an intervention consisting
of physical exercise and nutritional and educational enrichment was tested on a
sample of 35 year olds. The study found that the intervention significantly
reduced antisocial behavior at age 17 and criminal behavior at age 23. The
intervention was found to be especially effective for the subgroup of children
who displayed signs of malnutrition at age 3, suggesting the nutritional aspect of
the treatment was particularly beneficial. The intervention was shown to produce lasting psychophysiological changes at age 11, including increased skin
conductance, more orienting, and more arousal on EEG (Raine et al., 2001,
2003b). These changes might then protect against the development of criminal
offending (Raine et al., 1995, 1996).

X. CONCLUSION
Human beings are biological creatures. Whatever the truest essence of our souls
may be, our subjective mental lives are mediated by and expressed through a
system that is undeniably biological. This biological self exists in a specific social
reality, which, in turn, shapes and alters the biological self in ways that will find
some biological expression. What this chapter has sought to do is clarify how
these biological aspects of the self can be used to understand, identify and,
hopefully, predict individuals who criminally offend. Understanding these processes is the first step in then being able to modify risk factors or target at-risk
individuals for services designed to attenuate their criminal propensity.

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Index
A
Adoption study, human aggression
assumption and generalizability, 193194
forms of
BDHI subscales, 192193
etiology, 191192
reactive and proactive aggression, 192
relational, 192
G x E interaction
alcohol usage, 202203
family adversity and social disadvantages,
199201
violent media exposure, 201202
heritability and environmental factors
biological resemblance, 175
effect size for, 175184
meta-analysis of, 175
phenotype, 184
sex-limitation, 185186
vs. twin study, 193
Adrenocorticotropin (ACTH), 231232
Aggression
analysis of, 3
conflict situations, 1
definition, 2
drug-induced
amphetamine, 138
cocaine, 137
in human, 137
neural reorganization, 137
in prairie vole, 136137
in Syrian hamsters, 137138
evolutionary aspects, 8
in human (see Human aggression)
hyperaggressive phenotypes, 23
impulsive, 152
incidence, 216
in mammals
mating opportunities (see Mating)

sexual dimorphism, 1620

(see also Mammals, aggression)
sexual selection (see Sexual selection)
mechanism, 4
perinatal risk factors
alcohol exposure, 230232
birth complications, 228229
drug, 232233
environmental factors, 237238
epigenetics, role of, 241242
genetic factors, 238239
G x E interactions, 239241
maternal psychological stress, 236237
preterm birth and low birth weight,
229230
smoking, 233235
signaling (see Signaling aggression)
in songbirds (see Songbirds)
terminology, 5
types of, 12, 152
and violence, regulation of
autonomic arousal, 225226
electroencephalography (EEG), 226227
hormones, 223225
neurobiological base, 218221
neurochemical signals, 221223
types of, 218
in voles (see Prairie vole, selective aggression)
Agonistic behavior
in cephalopods, 37
definition, 2
game theory models, 38
in prairie vole, 123125
Amphetamine (AMPH), 138
Anabolic-androgenic steroids (AASs), 137
Androgens, aggressive behavior, 134135
Anterior hypothalamus (AH), 9697
Antisocial personality disorder (AsPD), 152, 259
Arginine vasopressin (AVP)
in hamsters, 130132
285

286

Index

Arginine vasopressin (AVP) (cont.)

in human, 129130
in marmoset monkey, 130132
in vole, neuropeptide regulation
distribution pattern of, 128129
mating-induced aggression, 129130
selective aggression, 130131
signaling and structural, 130131
Aromatase, 93
Astatolapia burtoni, 61
Autonomic arousal
heart rate and electrodermal activity, 225226
measurement of, 225
B
Batemans principles, 1011
Bed nucleus of the stria terminalis (BNST)
high Fos expression, 126127
in prairie voles, 128129
social behavior regulation, 127
3-hydroxysteroid dehydeogenase, 94
Black-throated blue warblers, 35
Borderline personality disorder (BPD), 152
C
Catechol O-methyltransferase (COMT),
240241
Cephalopods, visual signaling
chromatic skin patterns, 38
cuttlefish agonistic bouts, 3839
facultative nature, 37
during fight, aggressive motivation, 38
parallel positioning and arm posture, 38
rapid adaptive polyphenism, 37
squid agonistic bouts, 4041
in squid, contact pheromon, 4043
Challenge hypothesis, 86
Chemical signals, 25
Chickens, dominance hierarchies in, 56
Child Behavior Checklist (CBCL), 184
Cichlid fish, 1415, 6768
Clozapine, dibenzodiazepine antipsychotic
agent, 160
Cocaine, 137
Cognitive-behavioral therapy (CBT), 235
Computerized axial tomography (CAT) scan,
258
Corticosterone (CORT), 231232

Crex crex, 3637

Crocuta crocuta, 60
Crustaceans, 57
D
Dendroica caerulescens, 35
Dendroica pensylvanica, 88
Diffusion tensor imaging (DTI), 259260
Dominance relationships and hierarchies
animal models
chickens, 56
crustaceans, 57
fish, 5657
primates, 57
behavioral process
animal cognitive abilities and interaction
process, 74
jigsaw puzzle model (see Jigsaw puzzle
model)
social organization, 70
definition
behavioral measure of, 5354
individual majority, 5455
obtaining desired food, by animal pairs,
5455
two hens interactions, music notation graph
of, 5455
factors, animal pairs
behavioral states, 6263
genetic variations, 6062
physical differences, 5859
physiological differences, 5960
in groups
hierarchy formation, 6467
linear hierarchy formation, 6770
prior attributes hypothesis, 64
Dopamine (DA)
human aggression
in BPD patients, 157158
catecholamine neurotransmitter, 157
in CNS, 157
nucleus accumbens (NAc), 158
receptor antagonist, 158
role, 157
specific gene polymorphism, 157158
in male, aggressive behavior, 99
perinatal risk factors, 240
prairie vole, selective aggression
pathways, 132

287

Index
receptors, 132133
regulation of, 132134
Drug abuse and aggression
amphetamine, 138
cocaine, 137
in human, 137
neural reorganization, 137
in prairie vole, 136137
in Syrian hamsters, 137138
E
Electroencephalogram (EEG)
aggression and violence, regulation of,
226227
neurocriminology, 263264
Endogenous opioid, 100
Environmental Risk Longitudinal Twin study
(E-risk study), 175184
Equal environment assumption (EEA), 195
Estradiol (E2) blocker, 93
Estrildid finches, 101102
Ethnographic Atlas Codebook, 20
Event-related potentials (ERPs)
neurocriminology, 264
perinatal aggression, 226
Evolutionarily stable strategy (ESS), 1516,
2627
F
Fetal alcohol spectrum disorder (FASD),
230231
Fetal alcohol syndrome (FAS), 230231, 270
Field endocrinology, 89
Functional neuroimaging, neurocriminology
fMRI study, 260, 261
PET technique, 260
reduced glucose metabolism, 260261
reduced rCBF, 260
schizophrenic patients, 261
SPECT technique, 260
G
Gallus gallus domesticus, 9192
Game theory, 34
Gamma-aminobutryic acid (GABA)
human aggression
behavioral aggression, role in, 160

in CNS, 160
deficiency in, 161
in human aggression, 161
and serotonin, 161
subtypes, 161
neurochemical regulation, selective
aggression, 135
Gene by environment (G x E) interactions
human aggression
alcohol use, 202203
family adversity and social disadvantage,
199201
specific genes, 204205
violent media exposure, 201202
neurocriminology, 268269
perinatal aggression
catechol O-methyltransferase, 240241
dopaminergic function, 240
monoamine oxidase, 239240
Glutamate, 135
Golden hamsters, 154155
Gonadotropin-releasing hormone (GnRH1), 61
H
HawkDove game, 2628
Hormones
aggression
cortisol, 224225
oxytocin, 225
testosterone, 223224
norepinephrine (NE), 158159
prairie vole, selective aggression, 134135
songbirds (see Songbirds)
territoriality (see Territoriality)
Human aggression
in certain circumstances, 172
genetic and environmental influences
adoption study (see Adoption study, human
aggression)
forms of, 191193
G x E interaction (see Gene by environment
(G x E) interactions)
specific gene, genetic risk at, 203205
study design, 193
twin study (see Twin study, human
aggression)
multidimensional behavior, 152
neurochemistry of
dopamine (see Dopamine)

288

Index

Human aggression (cont.)

GABA (see Gamma-aminobutryic acid
(GABA))
impulsive, 152
norepinephrine (see Norepinephrine)
peptides, 162
serotonin/5-HT (see Serotonin (5-HT),
human aggression)
neurotransmitters, 152
signaling
natural selection, 44
vocal and facial expressions, 4344
vocal frequency, 4344
social factors, 172
6-Hydroxydopamine, 159
5-Hydroxytryptamine (5-HT). See Serotonin
(5-HT), human aggression
I
Impulsive aggression, serotonin
in animal, 156
in human, 153
norepinephrine, 160
Intermittent explosive disorder (IED), 152
International Center for the Study of Aggression,
56
J
Jigsaw puzzle model
in hens, 72
intransitive dominance relationship, 72
modification of, 73
self-structuring, 71
sequences, 71
transitive relationship, 71
L
Lekking birds, 1415
Linear hierarchy
behavioral process
cognitive abilities and interactions, 74
jigsaw puzzle model (see Jigsaw puzzle
model)
social factors influence on
in animal group, 70
cichlid fish, 6768
individual attributes, 68

isolated vs. embedded fish pairs, 6970

round-robin competition, 6768
winner, loser and bystander effects, 6869
Loligo pealei, 4042
Low resting heart rate, 264265
M
Magnetic resonance imaging (MRI) scan, 258
Mammals, aggression
mating opportunities
cost-benefit analysis, 13
harem holder, paternities by, 1415
hawk-dove game, 1516
sequential assessment game, 1314
strategies, 1516
pattern, 20
sexual dimorphism
brain structure, 1920
harem size and body weight, 1617
limited resources, 19
male-biased, 19
patterns of, 1618
phylogenetic tree, 1719
sexual selection
large body size, 11
male domination, 11
weapons, presence and absence of, 11
Mating
male domination, 61
mammals, opportunity in
cost-benefit analysis, 13
harem holder, paternities by, 1415
hawk-dove game, 1516
sequential assessment game, 1314
strategies, 1516
selective aggression, 123125
squids and cuttlefish, 37
VMH contribution, 9394
Melospiza georgiana, 35
Melospiza melodia, 31, 8788
Mesocricetus auratus, 130
Methylation, 241242
Microtus ochrogaster. See Prairie vole, selective
aggression
Minnesota Study of Twins and Families (MFTS),
175184
Minor physical anomalies (MPAs), 269
Monoamine oxidase (MAO), 239240

289

Index
N
Neural circuits
aggression
dopamine, 222223
norephinephrine, 223
serotonin, 222
prairie vole, selective aggression, 124, 127
in selective aggression, 127
songbirds
in BSTm, VT-Zenk colocalization, 101102
dopaminergic mechanism, 100
IEG labelling, 103
neuropeptides, 100
stress-related process, 100101
V1a antagonist, 102
Neurobiology, aggression and violence
amygdala, 219
in animal and human, 218
anterior cingulate cortex (ACC), 219220
hypothalamus, 221
prefrontal cortex, 220221
Neurocriminology
CAT scan, 258
functional neuroimaging
fMRI study, 260, 261
PET technique, 260
reduced glucose metabolism, 260261
reduced rCBF, 260
schizophrenic patients, 261
SPECT technique, 260
genetic contribution
ACE model, 267268
adoption, 267
gene-environment interaction, 268269
molecular genetics, 267
twins, 266267
limitations and potential, 272273
modifiable risk factor interventions
home nurse visiting, 274
nutritional deficits, 273274
during pregnancy, reduce smoking, 273
MRI scan, 258
neuropsychological testing, 262263
nongenetic risk factors
perinatal, 270271
postnatal, 271272
prenatal, 269270
psychodynamic theory
concepts of, 257258

early problems, 257

psychophysiological evidence
electroencephalogram, 263264
event-related potentials, 264
low resting heart rate, 264265
skin conductance, 265266
structural neuroimaging
amygdala and hippocampus, 259
antisocial personality disorder, 259
atrophic brains, 258259
brain ROI, size of, 258259
conduct disoder patient, 259
reduced gray matter volumes/thickness, 259
white matter tracts, 259260
Neuropeptides
in prairie vole, selection aggression, 128132
somatostatin, 62
VT and VIP, 100
Neuropsychology, 262263
Neurotransmitters. See specific
Neurotransmitters
New World sparrows, 8788
Nicotine replacement therapy (NRT), 235
Norepinephrine (NE)
human aggression
activity, 160
clozapine, schizophrenia treatment, 160
fight-or-flight response, 159
impulsive aggression, role in, 160
shock-induced aggression, 159
stress hormone, 159
impulsive aggression, serotonin, 160
perinatal aggression, 232
O
Orthoptera, 25
Oxytocin
and human aggression, 162
perinatal aggression, 225
selective aggression, neurochemical, 128
P
Papio anubis, 57
Paraventricular nucleus of the hypothalamus
(PVN), 97
Parus major, 88
Passer domesticus, 8990
Peptides, in human aggression, 162

290
Perinatal aggression
alcohol exposure
animal models, 231232
in children, 230
disorders, 230231
birth complications, 228229
drugs exposure
CNS alterations, 232
cocaine, 232
dopamine activity, 233
on fetal organogenesis, 232
5-HT and norepinephrine, 232
on social relationship, 233
environmental context, 237238
epigenetic, role of, 241242
genetic risk factors, 238239
G x E interactions
catechol O-methyltransferase, 240241
dopaminergic function, 240
monoamine oxidase, 239240
maternal psychological stress, 236237
neurocriminology, 270271
preterm birth and low birth weight
CNS damage, 229
neuropsychological deficits, 229
prevalence of, 230
sex, depends on, 229230
smoking
animal models, 235
in childerns, 234
effects of, 235
nAChRs, 234235
nicotine exposure, 234
women, in United States, 233234
P300 event-related potentials, 264
Photon emission tomography (PET), 260
Postnatal, neurocriminology, 271272
Prairie vole, selective aggression
drug abuse, 136137
function, 123125
inter- and intrasexual, 122
mating, 123125
molecular genetics of, 136
neural circuitry, 124, 127
neural correlates of, 124, 125127
neurochemical regulation of
dopamine, 132134
neuropeptides, 128132
neurotransmitters, 135

Index
steroid hormones, 134135
offensive and defensive types, 123
pair bonding, 123
residentintruder test (RIT), 123
Pregnancy, risk factors during
alcohol, 270
minor physical anomalies, 269
obstetrical complications, 270271
in postnatal period, nutrition deficiency,
271272
tobacco, 269
traumatic brain injury, 272
Prenatal
alcohol exposure, 230232
birth complications, 228, 229
drug exposure, 232233
neurocriminology, 269270
Primates, aggression in
dominance hierarchies, 57
male-male aggression, 19
nonhuman, 221
prenatal alcohol exposure, 231
sexual selection, 8
Prior attributes hypothesis, 64
Procambarus clarkii, 57
Prolactin, 154155
Psychodynamic theory
concepts of, 257258
early problems, 257
Psychopathy
genetic basis, 268
instrumental aggression, 218
scores, 259260
skin conductance, 266
Psychophysiology
electro cortical response measures, 226227
electroencephalogram (EEG), 263264
event-related potentials, 264
low resting heart rate, 264265
neurocriminology
electroencephalogram, 263264
event-related potentials, 264
low resting heart rate, 264265
skin conductance, 265266
skin conductance, 265266
Q
Quinpirole D2 receptor agonist, 99100

Index
R
Reactive and Proactive Aggression
Questionnaire (RPQ), 184
Residentintruder test (RIT), 123
Regional cerebral blood flow (rCBF), 260
S
Sepia officinalis, 38
Serotonin (5-HT), human aggression
binding potential, 155156
in central nervous system, 156
components, 153
D,L-fenfluramine, releasing agent, 154
enhancing agent, 153
expression, 155
failure, 156157
functions, 152153
metabolism, 153
neuroimaging studies, 156
postsynaptic function, 154
prolactin, 154155
subtypes, 155
Sex
birth control methods, 89
evolutionary explanation for, 89
humans, 89
Sexual selection
Batemans principles, 1011
conflicts of interest, 9
inter- and intrasexual selection, 910
limiting resources, 10
in mammals
large body size, 11
male domination, 11
weapons, presence and absence of, 11
sex role reversal, 10
Signaling aggression
animal models and techniques, 30
cephalopods, visual display in
chromatic skin patterns, 38
cuttlefish agonistic bouts, 3839
facultative nature, 37
during fight, aggressive motivation, 38
parallel positioning and arm posture, 38
rapid adaptive polyphenism, 37
squid agonistic bouts, 4041
in squid, contact pheromon, 4043
chemical signals, 25

291

classic game theory model

ESS strategies, 2627
HawkDove game, 2627
ethological approach, 2526
evolutionary issues, 2930
games
Hawk/Dove models, 28
mutual, 2728
in humans
natural selection, 44
vocal and facial expressions, 4344
vocal frequency, 4344
incomplete honesty challenge, 30
songbirds
aggressive escalation, 33
black-throated blue warblers, 35
display measures, 3334, 34
mate attraction, 31
musculature function, 31
signalers advantages, 3637
singing behaviors, 3233
soft song, 36
song sparrow, spectrograms of, 3132
song types and variants, 31
swamp sparrows, 35
territory defense, 31
threat displays
aggressiveness motivation, 28
modulates, social interaction, 28
performance signals, 2829
resource-holding potential, 28
strategic signals, 29
visual sign, 25
Single photon emission tomography (SPECT),
260
Skin conductance, 265266
Sociogenomics, definition of, 60
Somatostatin, 62
Songbird model, 4
Songbirds
causality, 107
context, 8487
endocrine and neuroendocrine correlation,
105106
hormonal mechanism
evolution and life history, 95
flocks, nonbreeding season, 9193
territoriality (see Territoriality)
neural circuits, brain
in BSTm, VT-Zenk colocalization, 101102

292
Songbirds (cont.)
dopaminergic mechanism, 100
IEG labelling, 103
neuropeptides, 100
stress-related process, 100101
V1a antagonist, 102
phentypic engineering, 107
signaling
aggressive escalation, 33
black-throated blue warblers, 35
display measures, 3334
mate attraction, 31
musculature function, 31
signalers advantages, 3637
singing behaviors, 3233
soft song, 36
song sparrow, spectrograms of, 3132
song types and variants, 31
swamp sparrows, 35
territory defense, 31
transcriptional activity
arginine vasotocin (VT), 9799
Fos-ir cell count, correlations between,
9798
IEG transcript, 9596
limbic areas, similarities in, 9596
paraventricular nucleus, 9799
social behavior network, 9697
white-throated sparrow
genetic basis of, 104
plumage polymorphism, 103104
social behavior, 103104
ZAL2m mapping, 107109
Song sparrow. See also Songbirds
aromatase mRNA expression, 9394
soft song, 33
song rate, 33
song-type matching, 33
spectrograms of, 3132
T treatment of, 95
Spizella pusilla, 8788
Steroid hormone
and central DA, 135
role of, 94
testosterone, 134135
in voles (see Prairie vole, selective aggression)
Sturnus vulgaris, 100
Swamp sparrows
types of calls, 35
wing-waving, 35

Index
Syrian hamsters
aggressive behavior in, 130
drug abuse, during adolescence, 137
T
Taeniopygia guttata, 94
Teachers Report Form (TRF), 184
Teratogens, 230
Territoriality
in breeding season
central perch, 88
distinct species song, 88
feather puffing, 88
high-quality territory establishment, 8788
physical fights, 88
simulated territorial intrusion, 8889
hormones
gonadal hormone secretion, 89
and plasma T, correlation between, 89
plasma T profile, male breeding season,
8990
in nonbreeding season
aromatase activity, in brain, 9394
autumnal aggression, 93
flocking behavior, 9193
gonads and ovaries regression, 91
reduced plasma gonadal steroids, 91
steroid hormones, role of, 94
Testosterone (T)
aggression and territoriality, 8990
aggressive behavior, 134135
low levels of, 8586
perinatal aggression, 223224
Traumatic brain injury (TBI), 272
Twin study, human aggression
additive and nonadditive, 174175
assumption and generalizability
EEA, 195
genetic and environmental influences,
196197
psychiatric disorders, 194
random mating, 195196
vs. singletons, 194195
in child, adolescent and samples, 175
correlation across
age groups, 187188
assessment methods, 189191
effect size for, 175184
between family members, 174

293

Index
forms of, 191193
G x E interaction
alcohol usage, 202203
family adversity and social disadvantages,
199201
violent media exposure, 201202
indirect hostility, 192193
meta-analysis of, 175
monozygotic and dizygotic, 174175
phenotype, 184
sex-limited effects, 185186
shared and nonshared environmental factors,
174175
vs. sibling adoption design, 193
verbal hostility, 192193
V
Vasoactive intestinal polypeptide (VIP), 100
Vasopressin (VP)
PVN, 9799

in voles, selective aggression (see Arginine

vasopressin (AVP))
Vasotocin (VT), 9799
Violence. See Aggression
W
White-throated sparrow
dominance hierarchies, 9192
territorial aggression in, 8687
genetic basis of, 104
plumage polymorphism, 103104
social behavior, 103104
VT administration, 105106
Winner-loser models, 6263
Wood warblers, 31
Z
Zebra finch, 94, 102
Zonotrichia leucophrys, 8788
Zonotrichia querula, 9192