doi:10.

1093/bjc/azr029

BRIT. J. CRIMINOL. (2011) 51, 535555 Advance Access publication 15 April 2011

BIOLOGY AND THE DEEP HISTORY OF HOMICIDE

Randolph Roth* Social science historians are discovering deep patterns in the history of homicide rates. Murders of children by parents or caregivers correlate inversely with fertility rates and appear to be a function of the cost of children relative to parental resources and to parental ambitions for themselves and their children. Murders among unrelated adults correlate with feelings towards government and society. These patterns may represent facultative adaptations to variable or unstable habitats (including social habitats) that may favour the nurture or neglect of children in the rst instance, or cooperation or aggression among unrelated adults in the second. Human neural and endocrine systems may have evolved to facilitate such shifts in behaviour. Keywords: biocriminology, child murder, facultative adaptation, homicide, hormones

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Introduction As Nicole Rafter argues in her superb book, The Criminal Brain (2008), criminologists have for centuries been fascinated by biological theories of crime. Most biological theories proved bankrupt or even dangerous because of the prejudices they fostered or justied. But the biological sciences have changed since the Second World War in ways that are making it possible, in Rafters opinion, to create a biosocial criminology that avoids the pitfalls of early biocriminology. For the rst time, she writes, there is a genuine possibility for collaborations between social scientists and cognitive, genetic, and neurological scientists working on crime. Biologists no longer belittle the possibility that social factors might affect criminal behavior, because they recognize that the way in which genes are expressed depends on social factors (Rafter 2008: 243, 246). Brain damage, lead poisoning, childhood traumas, stress, poor diet, drug abuse and other factors can reshape our bodies in ways that predispose us to antisocial behaviour. Genes play a role in human behaviour, but they do not determine it. Further, biologists today emphasize human similarities as much as differences, which makes it impossible to draw a sharp physical line between criminals and non-criminals, between us and them. That is why Rafter is so excited by recent research on acquired biological decits, cognitive decits, genetics and neuroscience. Recent research will not improve our understanding of crime, however, unless historians and social scientists acknowledge that biological factors affect crime (Rafter 2008: 246). That acknowledgement is well underway, thanks to the pioneering work of scholars such as Margo Wilson and Martin Daly (1988) and Sarah Blaffer Hrdy (1999; 2009), who have taken a deep interest in neurology, endocrinology, primatology and evolutionary science (Walsh 2009). Of course, much of the work to date remains provisional. It will take decades
* Department of History, Ohio State University, Columbus, Ohio, USA; roth.5@osu.edu.

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The Author 2011. Published by Oxford University Press on behalf of the Centre for Crime and Justice Studies (ISTD). All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

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or perhaps centuries for the knowledge of history, society and biology to reach the level of precision at which we can speak denitively about the patterns and causes of particular crimes. But, given the strides that scholars have made in the past 65 years through collaboration and cross-disciplinary research, it is time, as Anthony Walsh argues in his recent plea for a biological synthesis (2009), to take stock of the deep patterns that criminologists have discovered in human behaviour and to consider the possible biological causes and consequences of those patterns. As a social science historian, my primary concern is to map the incidence of various kinds of crime, particularly homicide, and to determine why such crimes are prevalent at some times and in some places and nearly absent in others. Why do some societies take the lives of a third or more of living children, when, in others, neonaticides, infanticides and murders of older children by parents or caregivers are rare? Why do homicide rates among adults rise into the tens or hundreds per 100,000 adults per year in some circumstances and drop below 1 per 100,000 in others? As primatologist Franz de Waal observes, we are a bipolar species (de Waal 2005: 22750). Our capacity for cooperation, teamwork, love, friendship, empathy, kindness, forbearance, forgiveness, compromise and reconciliation is unparalleled, because our happiness and survival depend on the strength of our social groups (especially our families) and on our commitment to them. But we also have an unparalleled capacity for competition, factionalism, hostility, sadism, cruelty, intransigence and domination. Which side of our nature prevails depends on historical circumstances. But, in a larger sense, many social animals are bipolar. As biologists have long known, animals that live in social groups may change their behaviour drastically when circumstances change. They can be cooperative in one instance and ruthlessly competitive and aggressive in another. Biologists consider such behaviours the products of facultative adaptation. In variable or unstable habitats (including social habitats), natural selection favours organisms that can sense changes in their environment and respond to them behaviourally to maximize their reproductive tness (Sober and Wilson 1998: 12730). A classic example is the honeybee. Worker bees (all of them female) dedicate their lives to helping their queen, raising her brood and defending her hive to the death. Doing so makes sense in evolutionary terms, because the queen is the mother (or, during a month of succession, at least a half-sister) of each worker bee. Workers propagate their genes far more effectively by labouring cooperatively and sacricing themselves for the good of their mothers brood than if they were to try to raise broods on their own. Worker bees are not infertile. They are capable of laying eggs that will develop into male bees (male bees are haploid, meaning they carry only the genes of their mothers, whereas female bees, which carry genes of their mothers and fathers, are diploid). But, while the queen is alive, or while there are larvae of new queens ready to emerge, the reproductive systems of worker bees are suppressed by pheromones from the brood, so few are capable of laying eggs. Those that do are attacked by their fellow workers and their eggs are destroyed, since worker bees prefer to raise the broods of their mothers rather than the broods of their sisters, which have only a small chance of having the same fathers (since queens typically mate with a dozen or more males). Workers can detect the difference between eggs of fellow workers and the queen because of a pheromone that the queen applies to each of her eggs. Most worker eggs are destroyed within two hours of being laid, which is why, although 10 per cent of all eggs are laid by workers, only 0.1 per 536

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cent of drones in a hive with a living queen are derived from worker eggs (Seeley 1985: 5 8, 225, 28, 301; 1995: 913). If the queen dies, however, and there are no successors in the larval stage, the ovaries of worker bees develop. Within 15 days, 5 per cent are capable of laying eggs and, within 30 days, 50 per cent. A erce struggle ensues. The workers maul each other and destroy each others eggs in the hope of raising a son who will carry their genes and mate with a queen from another hive. In these circumstances, natural selection favours competitors who stop at nothing in the ght to propagate their genes. Thus, the worker beethe epitome of the cooperative, social animalis capable of ruthless aggression when circumstances dictate. Facultative adaptation facilitates cooperation and sacrice in one social situation, and aggression and self-aggrandizement in another. It makes sense, therefore, to consider how facultative adaptation has shaped the bipolar behaviour of humans. What social or environmental circumstances elicit aggression and violence, and which cooperation, forbearance and nurture? And how have our neural and endocrine systems evolved to facilitate such shifts in behaviour? The answers to these questions can help us understand the deep history of homicide, to determining why rates of violence against children or adults have varied so markedly.1

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Homicides of Children by Adult Relatives or Caregivers Compared to most animals, humans are capable of extraordinary acts of care, concern and sacrice for children, including children who are not biologically their own. In biological terms, humans are cooperative breeders. Their children are raised not only by mothers, but by fathers and a wide range of alloparents who can, if necessary, shoulder all or part of the parental rolegrandparents, older siblings, step-relatives, neighbours, guardians and others. A fth of all primates engage in some form of cooperative child rearing, but the system of cooperative breeding is most complex and interdependent among humans because of the extraordinary energy required to nurture children. Humans must consume roughly 13 million calories to reach maturity. No mother has the capacity to provide by herself for a single child, let alone a family of children. The human system of cooperative breeding co-evolved with the prolonged period of childhood dependency and neural development, each facilitating the other (Hrdy 2009; Konner 2009). Humans, like other mammals that engage in cooperative breeding, are physiologically primed for an intense commitment to children. Mothers experience surges after birth in prolactin, oxytocin and estradiolhormones that help them bond with their infants by reducing anxiety, elevating mood and activating neural circuits associated with romantic love, empathetic social relationships, pain suppression and physical pleasure (Numan et al. 2006; Hrdy 2009: 21215; Konner 2009: 3215). Adult mothers (but not teen mothers), in response to cries from their infants during the rst months after birth, experience increases in heart rate
1 The term deep history is borrowed from Daniel Lord Smail (2008: ixx, 16), a pioneering scholar who believes there is a need for histories that are informed by natural history, evolution, and the theory of natural selection.

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and the stress hormone cortisol that make them acutely alert, attentive and affectionate (Fleming and Gonzalez 2009). Fathers experience parallel changes in hormones, particularly a decline in testosterone and an increase in estradiol, that facilitate paternal care and pair bonding with the mothers of their children (Berg and Wynne-Edwards 2001; Gray et al. 2006; Gray and Campbell 2009). The physiology of alloparental care is not yet well understood, but some evidence suggests that such care is facilitated by lower levels of testosterone, higher levels of prolactin and a dense network of receptors for oxytocin, a hormone that promotes calm and connection. Oxytocin lowers blood pressure, slows the heart rate, reduces anxiety and stimulates parenting behaviour and more intimate relationships with non-kin (Konner 2009: 4478; Sanchez et al. 2009: 31921; Feldman et al. 2010; Naber et al. 2010). In and of itself, experience with infants and children stimulates the desire to nurture in mammalian cooperative breeders, even in prepubescent humans. But physiology as well as experience facilitates cooperative child rearing.2 But there is a dark side to cooperative breeding. It works effectively when children are born in the right numbers, at the right time and with the right qualities into a world of abundance, strong families and strong social support. But, when those conditions do not prevail, cooperative breeders face a difcult choice, given the time, effort and sacrice required to raise their offspring. Does it make sense to invest in a particular child under particular social or environmental circumstances, or to invest instead in older children, or in children who could be conceived at a later date under more favourable conditions? Maternal neonaticide and infanticide, which are rare in nature, are common among cooperative breeders, including not only humans, but a number of other primates. As Melvin Konner observes, Mothers are designed by evolution not to produce idealized infant and child care under all circumstances but adaptively to adjust their investment depending on the offspring and the circumstances. Because cooperative breeders have been shaped by facultative adaptation, we should expect that mothersconsciously or not, with deliberation or in the midst of a psychotic depressionmake strategic choices about their investment in offspring. For instance, female tamarins and marmosets neglect or kill newborns if they sense that they do not have the resources or social support to raise them to maturity. Human mothers and fathers make the same calculations. When switched on, the parental instincts of cooperative breeders are very powerful, but, like all motives and sentiments, they can be modulated, muted, or switched off when circumstances change (Konner 2009: 544, 4225; Hrdy 2009: 82109; Penn and Smith 2007; Ziegler and Snowdon 2009). Adoption, fosterage, abandonment, selective neglect, abuse and homicide are all possible when natural or social conditions are unfavourable. The physiology of the dark side of cooperative breeding is less well understood for humans than for other mammals. Research has only begun and has largely been
2 The debate among scientists is ongoing, however, over the exact nature of the neurological and endocrinological mechanisms that facilitate cooperative breeding in mammals, and the relative importance of physiology and of parental or alloparental experience. See, for instance, Wynne-Edwards and Timonin (2007), Schradin (2007), Wynne-Edwards (2007), and Ziegler and Snowdon (2009).

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restricted to women. But the evidence gathered thus far shows that, under stress from a lack of social support, economic reversals or disruption in their intimate relationships, women are less likely to conceive children, more likely to miscarry and less likely to bond with their children emotionally and care for them attentively. These are exactly the facultative adaptations we would expect for cooperative breeders facing adverse conditions. A pioneering study of the impact of stress on reproductive success, which followed women in a Mayan community in the highlands of Guatemala, found that high levels of cortisol steroidsthe hormonal indictors of chronic stressinterfere with reproductive hormones. Elevated cortisol levels cause untimely increases in gonadotrophin and progestin during the follicular phase of the menstrual cycle and a decrease in progestin during the middle of the luteal phase. All these changes lower the chance of conception. Women suffering from elevated cortisol levels who do conceive are three times more likely to miscarry during the rst three weeks of gestation (Nepomnaschy et al. 2004; 2006; Nepomnaschy and Flinn 2009: 3657). Other studies have found that mothers who suffer high levels of cortisol from chronic stress are less attentive and attached to their newborn children, because their response to short-term stressors (such as the cries of their infants) is blunted by a stress response that is always on (Fleming and Gonzales 2009: 30516). And, over the longer term, high cortisol levels are associated with depression, unhappiness and more negative interactions with infants. Postpartum depression, which severely weakens attachment to infants and increases the likelihood of maternal violence, also correlates with a mothers belief that she has little social support, with unplanned or unwanted pregnancies, with stressful experiences in the year before birth and with stress over the care of older children (Wile and Arechiga 1999; Miller 2002; Hagen and Barrett 2007). Chronic stress and social isolation thus lead to physical responses that diminish maternal investment and increase the risk of maternal neglect and abusefacultative adaptations to social and environmental circumstances that are unfavourable to cooperative breeders. The history of child homicide makes sense in light of these facultative adaptations. Homicide rates for children follow a clear pattern from the mid-sixteenth through the nineteenth centuries in locations that have been studied to date in North America and Western Europe. The rates move up and down in long, smooth curves that are visible only when traced over 100 years or more. The rates at which children are murdered by parents or guardians follow the inverse of the birth rate. Low murder rates for neonates, infants and children correlate with:
      

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higher birth rates; lower ages of mothers at the births of their rst children; higher proportions of women who marry at least once; higher rates of premarital pregnancy; lower rates of abortion-related deaths; longer life expectancy for children; higher adult heights (a function of net nutrition).

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These correlations hold for data gathered from multiple sources in New England, Ohio, Virginia and Maryland, and for the ofcial data on neonaticides and infanticides from Philadelphia, England and Wales, and France. They do not hold for the murders of children by other children or by unrelated adults; these follow the sharp ups and downs of the homicide rate among unrelated adultsa rate that has a very different set of correlates (Roth 2001a; 2001b; 2009).3 How are birth rates, premarital pregnancy, marriage, abortion, life expectancy and height related to murders of children by parents or guardians? The child murder rate and the fertility rate appear to be driven by the same forces. The child murder rate is a function of the cost of children relative to parental resources and to parental ambitions for themselves and their children (an investment strategy). When real wages dropped by more than a third for the poorest 40 per cent of the population in England in the late-sixteenth and early-seventeenth centuries, young women and men found it harder to marry and raise families. The birth rate dropped, life expectancy dropped, heights fell, premarital pregnancy rates fell, the age of the mother at rst birth rose, fewer women married and the neonaticide indictment rate jumped vefold. When real wages rose in the lateseventeenth and early-eighteenth centuries, the trends reversed and the neonaticide indictment rate fell to its previous level (Roth 2001b). The rise in child homicides in the mid-nineteenth century was driven more by rising ambitions than economic want, even though most murderous parents were poor. Real wages rose among the poor, but ambitions rose faster. Women in particular embraced new educational opportunities, sought economic independence through work outside the home in teaching, needle trades and factory work, became more active in community affairs and voluntary organizations, and raised their economic expectations for themselves and their children.4 These rising ambitions made children more costly in terms of time and money, so parents limited their child-rearing duties and nancial obligations by beginning childbearing later and ending it sooner through abstinence,
3 The research conducted by the author on colonial Maryland and Virginia, and on selected counties in Ohio and Virginia, 1785 1900, has not yet been published. For a description of the sources, see Roth (2009: 4804, 486). On Philadelphia, see Philadelphia County Court Indictments, 18701901, and Philadelphia Board of Health Annual Reports, 18701901. The statistics on neonaticide, infanticide and manslaughters of infants in England and Wales are from the annual reports of the Registrar-General, 1837/38 to 1900, and the statistics on arrests and prosecutions for concealing the birth and death of illegitimate infants are from Judicial Statistics, 18291900. The series are available in the Parliamentary Papers of the British House of Commons. The earliest murder statistics available from the Registrar-General (for 1837 and 1838) are implausibly low, however. Arrest statistics are not available before 1856, so the earlier data on prosecutions for concealing the birth and death of illegitimate infants are spliced to the arrest data in 1856, based on the ratio of prosecutions to arrests, 185660. The data on prosecutions before 1829 are not used, because they are implausibly low. Reporting procedures appear to have changed in 1829. The statistics on births through 1871 are calculated from Wrigley et al. (1997: 61415), spliced thereafter to the statistics in Mitchell (1988: 29 30). On the limitations of ofcial statistics and of the practices of many local coroners in England and Wales, see Jones (1894: 59 64), Behlmer (1979), Rose (1986: 5760) and Sauer (1978). On the publics continuing interest in detecting and punishing neonaticides and infanticides, see Monholland (1989: 1217, 16983). The statistics on arrests and prosecutions for neonaticide and infanticide in France are from the Compte ge ne ral de la justice criminelle, published annually since 1825. They are available in Brouardel (1897: 1417), Chesnais (1982: 111), Fuchs (1984: 105) and Lalou (1986: 181). They include statistics on cases tried by the courts (infanticides juge s), concealed deaths of newborns (suppressions denfant), manslaughters of infants (homicides involontaires), infanticide cases dismissed by justices (non-lieux) and infanticide cases not carried forward by prosecutors (sans suite). The statistics on births are from Bourgeois-Pichat (1965: 498 9, 506). See also Bechtold (2001). 4 The literature on the rising ambitions of women in the Western world in the late-eighteenth and early-nineteenth centuries is voluminous. Ambitions rose when it came to work, marriage, family, romance, education, fertility control and civic involvement. On the United States, for example, see Cott (1977), Mohr (1978), Dublin (1979), Ryan (1981), Hewitt (1984), Rothman (1984), Stansell (1986), Graff (1987), Gilmore-Lehne (1989), Lystra (1989) and Faust (1996).

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contraception and abortion. And when unrealized ambition led to frustration and stress, parents killed newborns, infants and older children (Roth 2001a). The child murder rate is also a function of the amount of support parents can expect from society at large (a response to social isolation and stress). Welfare measures have had a considerable impact on the child murder rate, because they affect both the ability of young parents to form families and raise children and the stress that young parents experienced. For instance, the child homicide rate went up for blacks and whites in the South after the Civil War because of hard economic times and the deaths of so many young men of marriageable age. The murder rate fell sharply, however, in Richmond, Virginia, in the 1880s, after a home opened for single mothers. The home did not ask single mothers to give up their children for adoption. Instead, it offered medical care, child-care and employment opportunities so that single women could raise their children on their own. The home was for whites only. Its impact was stark: the homicide rate dropped only for white children in Richmond, not for black children (Green 1999). New welfare policies in Western Europe contributed to the increase in neonaticide and infanticide that occurred there in the mid-nineteenth century. The British government amended the Poor Law in 1834 to make it harder for single mothers and local parishes to sue the fathers of illegitimate children for child support. The new law also forced single mothers who sought poor relief to live with their children in disease-ridden public almshouses and earn their keep. The number of illegitimate children receiving public assistance in England and Wales decreased instantly by 40 per cent (Higginbotham 1985: 17, 28; Rose 1986: 2234). In the 1830s, the French government launched its own campaign to pressure single women to have fewer children and to shoulder the cost of the children they had. In Paris, for instance, in the 1820s, a quarter of all newborns and half of all illegitimate newborns were abandoned at the state-run foundling hospital. The government decided to make it more difcult to abandon children at foundling hospitals and, in return, offered single mothers one month of assistance after the births of their children (Fuchs 1984: xi, 29, 3446, 6479). Under these circumstances, the temptation to abort or murder a child was enormous. Social attitudes towards out-of-wedlock pregnancies have also affected the homicide rate of newborn children. When out-of-wedlock pregnancies were re-stigmatized in the New England during the Great Awakening of the late 1730s and 1740s, the neonaticide rate spiked, because there was tremendous pressure on young people to abstain from premarital sex. More young women chose to try to conceal their pregnancies rather than be shamed publicly, and there were more neonaticides and more hangings of women found guilty of neonaticide. The neonaticide rate also spiked in France after an 1825 law made it illegal to leave an unwanted newborn anonymously at the door of a church or charitable institution. The desire to shame indigent single mothers and to hold them personally and publicly responsible for their unplanned pregnancies had dire consequences. Conversely, when public support and sympathy for single mothers was substantial, neonaticide and infanticide rates fell (Roth 2001a; Fuchs 1984). These historic patterns in child homicide rates are consistent with contemporary patterns in the United States. Because of advances in medicine and forensic science, cooperation among physicians, coroners, social workers and law-enforcement ofcers, and the creation of formal review boards to examine suspicious or unexplained 541

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deaths of infants and children, it has been possible in the past decade to study domestic violence against children with great precision. One of the largest studies, organized by the childrens hospitals in greater Pittsburgh and Columbus, Ohio, found a clear and not unexpected pattern. The incidence of child abuse went up during economic downturns. In fact, the researchers recognized the recessions of 2001 and 2007 before economists and government ofcials did because they noted an increase in the number of shaken babies and battered children.5 Historic patterns of child homicide are also consistent with the patterns criminologists have discovered in mortality data compiled by the World Health Organization. Comparisons of nations with adequate statistics (most of them afuent) reveal that high homicide rates for children of all ages are correlated with economic inequality, low government expenditures on welfare and a high rate of female participation in the labour forcea proxy for higher economic need or ambition (Gartner 1990; 1991; Fiala and LaFree 1988; Briggs and Cutright 1994; Sorenson et al. 2002; Hunnicutt and LaFree 2008). Once again, the degree of social support and the economic circumstances and ambitions of parents, especially mothers, appear to determine the homicide rate for children. These patterns are consistent with those found by many anthropologists and comparative primatologists who have studied infanticide and neonaticide in hunter-gatherer, pastoral and peasant societies. Children who come at the wrong time, in the wrong number or with the wrong qualities (disabilities, non-preferred gender, etc.) are at risk, especially if parents are experiencing economic or social stress (Hrdy 1999; 2009). Child murder is thus caused not only by social or environmental circumstances, but by the ways in which evolution has enabled parents and caregivers to respond to those circumstances. Humans, like other cooperative breeders, are well adapted to life in variable or unstable habitats (including social habitats) because they can change their fertility rate, their level of parental investment and their attachment to children as conditions become more or less favourable for forming families and raising children. Homicides among Unrelated Adults Like many other social animals, humans are well adapted to life in cohesive social groups composed largely of non-relatives. Of course, like most social animals, humans compete with each other within their societies, sometimes ruthlessly, for status, power and resources, because they have been shaped by individual-level selection. Selshness can have benets when it comes to reproductive tness. But, because their survival as social animals also depends on the strength and solidarity of their social groups whether bands of hunters and gatherers, or villages of farmers or herders, or modern nationsthey cooperate for mutual advantage and in certain cases sacrice for the good of the whole. Reciprocity and selessness also have benets, because, as social animals, humans have been shaped by group-level selection as well. Mutual aid, reciprocity and altruism can enhance their reproductive tness (or at least the tness of their
5 Incidence of Child Abuse Skyrocketed During Recent Recession, Childrens Hospital of Pittsburgh of UPMC-led Study Finds, Childrens Hospital of Pittsburgh, news release, 10 May 2010, at www.chp.edu/CHP/050110; Recession Linked to Increase in Shaken Baby Syndrome, USA Today, 3 May 2010, at www.usatoday.com/news/health/2010-05-03-abuse03_ST_N.htm; and personal communication with Dr Philip Scribano, Medical Director of the Center for Child and Family Advocacy at Nationwide Childrens Hospital, Columbus, Ohio.

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surviving kin) by enabling their social groups to outcompete rivals (Sober and Wilson 1998; de Waal 2005).6 The ability of humans to cooperate has been enhanced by their capacity, as Michael Tomasello observes, to establish norms and institutions to govern their interactions with other members of their social groups. Unlike other primates, humans create moral rules that bind them to certain standards of conduct within the group. These rules facilitate trust and tolerance among cooperators and legitimize sanctions against bullies, free riders and cheats. Humans also adopt social conventions that encourage identication with the group and conformity to the groups way of doing things. These constitutive rules foster a sense of empathy, fellow feeling and common purpose within the group, and facilitate coordinated action, although sometimes at the price of turning members of the group against outsiders (Tomasello 2009: 2844, 905, 99100). The ability to cooperate has enabled humans to create societies on a vast scalefar beyond the capacities of nonhuman primates, who conne their social groups to kin or to small bands of kin and non-kin and cooperate almost exclusively on the basis of kinship or direct reciprocity. But, as Christopher Boehm observes, human societies are nonetheless rife with conict because of the determination of some individuals to dominate others and the determination of others to resist domination. According to Boehm, bands of hunters and gatherers contain aggression by embracing an egalitarian ethos that mandates that members share power within their bands as equals and respect the personal autonomy of others. Any member who belittles, bullies, or otherwise tries to control another faces sanctions: ridicule, ostracism or even death. Modern nation states contain aggression differently, by asking subordinates to buy into the notion of social and political hierarchy:
Nevertheless, they subject their dominators to a certain kind of cost-benet accounting. If their leaders are fair-minded and attentive to the needs of their people, subordinates remain appreciativeand docile. If they feel the leaders are abusing their powers, however these may be dened locally in terms of political legitimacy, they become ambivalent, hostile, potentially rebellious, and disposed to act forcefully. (Boehm 1999: 669, 169)

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The human capacity for aggression within social groups is thus a facultative adaptation to group living, as is the human capacity for cooperation. When human social groups are stable, and when they further members interests or command respect and loyalty, humans tend to cooperate with others and act in a spirit of tolerance, forbearance, generosity and helpfulness. But, when their social groups are unstablewhen they lose the capacity to protect lives and property or contain the struggle for dominance and no longer serve their members interests, respect their rights or give them a sense of belonging, humans tend to turn against each other and become more hostile, defensive or predatory. These facultative adaptations to group living are nowhere more evident than in homicides among unrelated adults, including homicides that at rst glance appear to have
6 As Charles Darwin recognized, natural selection can act on social groups as well as on individuals or kin groups. Altruists and cooperators may have fewer offspring than non-altruists or free-riders within their groups, because of their willingness to sacrice for the good of others (including non-relatives) or to temper their pursuit of self-interest for mutual benet. But groups of altruists and cooperators may have more offspring than groups of non-altruists and free-riders because of their ability to work together, provide for each other and defend their groups. If the advantages of altruism and cooperation for the social group are great enough, as they appear to be for many group-living animals, including humans, the proportion of altruists and cooperators will increase in the species population over time, even though the proportion of altruists and cooperators may decrease within each particular social group (Sober and Wilson 1998).

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nothing to do with feelings towards government and society. As Gary LaFree, Manuel Eisner, Roger Gould and I discovered independently in the 1990s, homicide rates among unrelated adultsnearly all of which have been committed historically by malesappear to be determined by such feelings (LaFree 1998; Eisner 2001; Gould 2003; Roth 2009). As I put it in my own work, there have been four correlates of low rates in North America and Western Europe over the past 450 years: (1) the belief that government is stable and that its legal and judicial institutions are unbiased and will redress wrongs and protect lives and property; (2) a feeling of trust in government and the ofcials who run it, and a belief in their legitimacy; (3) patriotism, empathy and fellow feeling arising from racial, religious or political solidarity; (4) the belief that the social hierarchy is legitimate, that ones position in society is or can be satisfactory and that one can command the respect of others without resorting to violence. When these correlates are in place, the homicide rate among unrelated adults can fall below 1 per 100,000 per year. When they are not, the homicide rate can soar to tens or hundreds per 100,000. Homicide rates on contested frontiers and during revolutions, civil wars and hostile military occupations show how quickly humans can become aggressive during periods of political instability. As soon as the political order loses its ability to contain the struggle for dominance and protect lives and property, cooperation and forbearance give way to defensive, hostile and predatory behaviour. Political violence, terrorism and genocide are common in such circumstances, but so too are everyday homicides over honour or property and predatory homicides involving robbery or rape. In eighteenth and nineteenth-century France, for instance, the homicide rate rose during every revolution17891801, 183031, 184850, 187071and not only in places where political violence was common, like Paris, but in places remote from such violence, like Corsica, where there were spikes in feud and honour killings (Gould 2003: 15061). During periods of political instability, warring factions aim to create new stable regimes by dominating or eliminating political rivals. But those homicides are inevitably accompanied by others that may seem at rst glance to be apolitical, but that correlate just as strongly with the lack of political stability. For example, some men become predatory killers, raping, robbing and murdering as individuals or members of gangs. They may begin killing as political partisans, but when they nd themselves on the losing side or at odds with an emerging political order, they may begin to prey not only on political enemies, but on former allies and non-combatants, whom they may resent for their weakness, defeatism or indifference to the cause. They lose their sense of connection with anyone beyond their immediate circle. Old neighbourhood feuds are also likely to turn murderous during periods of political instability. When government breaks down, men kill for what appear to be purely personal reasons, avenging wrongs, settling scores or simply getting rid of people they dont like. They may be moved to do so by a lack of sanctions (because of weak law enforcement), a fear that their enemies will kill them rst or partisanship (if their personal enemies happen to be on the opposite side in the political struggle). Regardless of 544

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motive, these feuds can take on a life of their own and draw in more combatants. Homicide rates can thus reach catastrophic levels during periods of political instability and can remain high for decades. Once learned, homicidal habits can be hard to break and can be passed down for generations. Why does aggression break out during periods of political instability? Because, in evolutionary terms, it can pay off handsomely. The risks of aggression are always considerableinjury, death, the loss of family and friends. But the rewards for successful aggression during periods of political instability are enormous: more power, more resources, more offspring, and a higher rank in the social hierarchy for oneself or ones faction. Intensied aggression is thus a facultative adaptation to life in unstable or failing social groups, just as cooperation is an adaptation to life in nascent or thriving social groups. These adaptations have deep biological roots. Consider, for instance, the behaviour of group-living monkeys and apes during their own periods of political instability, when dominance hierarchies are contested and the personal relationships and coalitions that support them break down. In these circumstances, plasma levels of testosterone increase in adult males in anticipation of aggression (the challenge hypothesis) and the number of ghts doubles or triples, as individuals and new coalitions struggle for power. Formerly pacic relationships turn violent and former subordinates challenge dominants. Males who exhibit the highest levels of testosterone and aggression tend to rise to the top of the new political order, while the level of testosterone and aggression drops for males who experience repeated defeats and fall towards the bottom of the social hierarchyan evolutionarily conservative strategy (conditioned defeat) to protect subordinated individuals from further harm. Once political stability returns, however, plasma levels of testosterone decline generally, as does the number of ghts; and, over time, if stability is maintained, rank depends less on testosterone and aggression than on the ability to form alliances, reassure subordinates and reconcile with former adversaries (Bernstein et al. 1974; Dixson 1980; Goodall 1986: 75, 209, 336, 404, 410; Wingeld et al. 1990; Nelson 2005: 5078; Blanchard and Blanchard 2006: 2856; Simon and Lu 2006: 222; Mehta and Josephs 2006; Fairbanks 2009: 16776).7 Under unstable conditions, serotonin levels decrease in group-living monkeys and apes in anticipation of aggression. Unlike testosterone, which, at natural levels, facilitates assertiveness and controlled, strategic aggression aimed at achieving dominance, low levels of serotonin facilitate impulsive behaviour and sudden, uncontrolled aggression. Experiments have demonstrated that rhesus monkeys with relatively low levels of serotonin are more aggressive than others and that lowering the level of serotonin in an entire troop of vervet monkeys (by depleting the amount in the troops diet of tryptophan, the compound from which serotonin is synthesized) dramatically increases the amount of spontaneous aggression among members of the troop (threatening, hitting,

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7 The relationship between testosterone and dominance or status-seeking behaviours may be mediated, however, by cortisol and other stress-related hormones. Recent research suggests that a high level of testosterone may facilitate aggressive behaviour only if the level of cortisol (i.e. stress) is low. If the level of cortisol is high, a high level of testosterone may impede aggression, by warning a stressed individual (usually subordinate or oft-defeated) not to ght for status now that an intense struggle for status has broken out in the group (Mehta and Josephs 2010). Furthermore, the relationship between high testosterone levels and competitive performance may hold only for competition among individuals. Success in competition among groups may be facilitated by lower levels of testosterone, since individuals with lower levels of testosterone are motivated to cooperate with others (Mehta et al. 2009). Research into such subtleties has only begun. Note, however, that these new ndings support the idea that aggression is a facultative adaptation to life in unstable social groups or contested social hierarchies.

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biting and chasing) (Chamberlain et al. 1987; Mehlman et al. 1994; Higley et al. 1996; Manuck et al. 2006: 749). Political instability and disruption of the social hierarchy have the same effect, because they prime males for aggression by lowering their levels of serotonin. During periods of instability, when impulsive aggression can bring great rewards, males who have the lowest levels of serotonin tend to rise to the top of the dominance hierarchy. But, during periods of political stability, when cooperativeness, political skill and calculated displays of aggression can bring the greatest rewards, males with moderate levels of serotonin, who are neither impulsive nor passive, tend to rise to the top (Fairbanks 2001; 2009: 17692; Fairbanks et al. 2004). Research on nonhuman mammals has shown further that testosterone and serotonin mediate each others effect on aggression: a low level of testosterone inhibits aggression in low-serotonin individuals and a high level of serotonin inhibits aggression in hightestosterone individuals. But, when testosterone levels are high and serotonin levels are low, these inhibitory effects are neutralized and aggression is fully facilitated, because the areas of the brain that control aggression are rich in receptors for both hormones (Nelson 2005: 51215). Because of the difculty of measuring changes in hormones in uncontrived social situations, endocrinological research on humans is not as advanced as it is for nonhuman primates and other mammals. It is not yet possible to say with certainty that political instability and the disruption of social hierarchies trigger increases in testosterone and decreases in serotonin in human males, which, in turn, facilitate aggression among unrelated adults. There is substantial evidence, however, that testosterone levels increase in human males before and during competitive sporting events, that males with low base levels of serotonin are more impulsive and prone to violence, and that lowering serotonin levels with a tryptophan-depleting beverage increases the likelihood of aggression and retaliation in competitive computer games (Bjork et al. 1999; 2000; Dougherty 1999; Nelson 2005: 5089; Simon and Lu 2006: 222; Manuck et al. 2006: 7990). Some studies suggest that humans, like many other mammals, can be habituated to aggression physiologically if they are subjected repeatedly to dominance challenges or the threat of violence. For example, as Richard Nisbett and Dov Cohen discovered, when young, afuent white men from the Souththe most violent and homicidal region in the United Stateswalk down a hallway unimpeded, they behave no differently than young, afuent white Northern men. But, when Southerners are bumped by a man walking in the opposite direction, they behave differently. They feel insulted; they worry about appearing weak and unmanly; they fantasize about taking revenge; and their glands secrete larger quantities of testosterone and cortisol (a stress hormone) adaptive responses to the greater number of challenges and threats they face in their daily lives. Southern white men carry the violent history of the region with them wherever they go. It is inscribed on their bodies, just as it is on the bodies of nonhuman mammals that have faced an unusual number of threats, challenges or attacks from dominants, subordinates or peers (Nisbett and Cohen 1996: 4155; Miczek et al. 2004; Nelson 2005: 5078; Blanchard and Blanchard 2006: 2826; Berton et al. 2006; Huhman 2006; Garcia-Segura 2009: 2278). The neurological and endocrinological consequences of a loss of trust and empathy in primate societies are not as well understood as the consequences of political instability or the disruption of social hierarchies, because trust and empathy are difcult to measure, even in human societies. Evidence is accumulating, however, that humans are less 546

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aggressive and homicidal when they trust the government and their leaders and when they have a sense of kinship with others in their society or social group. For instance, the strongest correlate of the homicide rate in the United States since the Second World War has been the proportion of Americans who say that they trust the government to do the right thing most of the time and who believe most public ofcials are honest (LaFree 1998). That correlation has tracked separately for various social groups, particularly blacks and white conservatives. In the last ve decades, the black homicide victimization rate peaked between 1971 and 1974, when black trust in government reached a postSecond World War low. The white homicide victimization rate peaked in 1980 during the nal year of the Carter administration, when white trust in government reached its postwar low because of accumulated anger over court-ordered busing to integrate schools, welfare, afrmative action, the American defeat in Vietnam and the seizure of American hostages in Iran. That rate7 per 100,000 white persons per yearwas, by itself, 315 times the homicide rate in other afuent nations. But, as soon as Ronald Reagan and the Republican Partythe champions of those angry whiteswon the White House and the Senate, the white homicide victimization rate fell (Roth 2009: 44866). Why does faith in government have a profound impact on interpersonal violence? How people feel about the government plays an important role in determining how they feel about themselves and society. If people believe that their government shares their values, speaks for them and acts on their behalf, they feel empowered, have greater self-respect and gain condence in their dealings with people outside their families. When people feel that the government is antagonistic toward them and they question its legitimacy, especially on the national level, they can feel frustrated, alienated and dishonoured. And those feelings, in turn, can stimulate the hostile, defensive and predatory feelings that lead to violence against friends, acquaintances and strangers. The degree of empathy and fellow feeling among the members of a society also has a powerful effect on the homicide rate. Nothing suppresses homicide within a social group more powerfully than a sense of connectedness that extends beyond the bounds of family and neighbourhood and forges a strong bond among people who share race, ethnicity, religion or nationality. Consider, for instance, the inverse relationship between the homicide rate among unrelated adults in the United States and the proportion of new counties named after national heroesBritish heroes in the colonial period and American heroes in the national period. When that proportion was highan unconscious way of saying that Americans believed in their nation and in each otherthe homicide rate among unrelated adults was low. When that proportion dropped, the homicide rate soared (Roth 2009: 22, 778, 149, 157, 301, 387). Of course, solidarity is a double-edged sword: it can deter homicide within a group and at the same time incite homicides among members of different social groups. When humans draw the boundary between us and them in a way that excludes a substantial portion of the population, the potential for homicide is high. But, when humans draw the boundary in a way that is encompassing and inclusive, the potential for homicide decreases. It is as yet uncertain whether humans or nonhuman primates respond physiologically to social conditions that foster trust or empathy within their social groups in ways that facilitate cooperation and deter aggression. Perhaps there are neurological, endocrinological and behavioural consequences to living in social groups in which trust and fellow feeling prevail and in groups in which they do not. Certainly, humans have evolved defences that help them distinguish between people they can and cannot trust. Humans 547

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recognize the faces of people they consider untrustworthy more rapidly and accurately than they recognize the faces of people they associate with other traits and they are hesitant to enter relationships with individuals who are known to be manipulative. At the same time, humans are primed to detect altruists who will be trustworthy partners in social exchanges (Mealey et al. 1996; Wilson et al. 1998; Brown and Moore 2000). Humans have also evolved defences that enable them to determine with 170 millisecondsfaster than they can thinkwhether an individual is a member of their own group or a stranger or potential adversary. These defences activate almost instantaneously the neural networks that tell us whether to approach, ght or ee, and whether to evaluate individuals positively or negatively (Ratner and Amodio 2009; Dickter and Gagnon 2009; Gutsell and Inzlicht 2010). Related neural networks prompt us to respond with greater sympathy to the pain or distress of members of our own group (Xu et al. 2009; Yahya et al. 2009). When humans are in the presence of individuals they trust or towards whom they have positive feelings, they usually experience a surge in oxytocin, a neuropeptide that lowers blood pressure, reduces stress and anxiety, and facilitates social interaction (Sanchez et al. 2009: 31926; Neumann 2002; Kosfeld et al. 2005; Bartz and Hollander 2006; Lim and Young 2006; Theodoridou et al. 2009). Higher levels of oxytocin increase the willingness of individuals to trust and cooperate with other individuals, once they have had a chance to interact with them. Oxytocin is not indiscriminate: higher levels of oxytocin impede trust and cooperation with anonymous others whose emotions cannot be read. But, if social cues are available and if the incentives to cooperate are strong, oxytocin facilitates cooperation by reducing activity in the areas of the brain that govern fear and stress and by activating the dopamine reward circuits that foster a sense of happiness and well-being (Declerck et al. 2010; Winslow et al. 2003; Heinrichs et al. 2003; Depue and Morrone-Strupinsky 2005; Kirsch et al. 2005; Baumgartner et al. 2008). If these neural and endocrinological responses prove to be plasticif they become stronger after repeated interactions with trusted institutions and with people with whom we feel a sense of kinshipthey would constitute a facilitative adaptation to life in cohesive social groups with legitimate institutions, just as a dampening of such responses would be an adaptation to life in incoherent social groups with illegitimate institutions. Those adaptations would, in turn, facilitate tolerance and cooperation in cohesive groups and defensive or hostile aggression within incoherent groupsthe pattern evident in homicide rates among unrelated adults.8 It will require many more years of research to understand the precise connections between the social circumstances that increase or decease homicide rates and the neurological and endocrinological mechanisms that facilitate or deter aggression. It is essential, however, that criminologists and social science historians continue their efforts to understand the deep patterns of homicide. As endocrinologist Randy Nelson points out, scientists who study the neurology and endocrinology of animal behaviour have developed sophisticated research tools, but they can only use those tools if there is a clear pattern of behaviour to be explained and if the function of the behaviour is known
8 The neuropeptide vasopressin may play an opposite role in the same facultative adaptation. Vasopressin, which is released under stressful and defensive circumstances and during periods of increased aggression, raises blood pressure, increases anxiety and interacts with serotonin to facilitate aggression in malemale competition (Sanchez et al., 2009: 31931; Lim and Young 2006; Fairbanks 2009: 1645, 169). If it were released in great amounts when trust and empathy declined within social groups, and if it had a plastic effect on the neural and endocrinological mechanisms that facilitate aggression, it, too, could represent a facultative adaptation to life in coherent or incoherent social groups.

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(Nelson 2005: 1221). If social scientists can improve our understanding of the patterns of homicide across time and space, neurologists, endocrinologists, primatologists and evolutionary biologists may be able to improve our understanding of the physiological causes and consequences of violence. Funding The authors studies of homicide have received funding from the National Science Foundation, the National Endowment for the Humanities, the Harry Frank Guggenheim Foundation, and the College of Humanities and the Criminal Justice Research Center at Ohio State University.
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