Cooperative Breeding and Its Significance to the Demographic

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Cooperative Breeding and its Signiﬁcance to the Demographic Success of Humans

Karen L. Kramer

Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138; email: [email protected]

Annu. Rev. Anthropol. 2010. 39:417–36 Key Words First published online as a Review in Advance on life history, intergenerational transfers, allocare, demography June 21, 2010

The Annual Review of Anthropology is online at Abstract anthro.annualreviews.org The demographic success of humans compared with other closely re- This article’s doi: lated species can be attributed to the relatively rapid pace of reproduc- 10.1146/annurev.anthro.012809.105054 tion and improved chances of survival. The assistance that mothers re- Copyright c 2010 by Annual Reviews. ceive from others to help raise children is a common theme in explaining All rights reserved this gain in surviving fertility. Cooperative breeding in its broad deﬁni- 0084-6570/10/1021-0417$20.00 tion describes such a social system in which nonmaternal helpers support offspring who are not their own. In traditional societies, kin and nonkin of different ages and sex contribute both to child care and to provisioning older children. This review discusses empirical evidence for human cooperative breeding and its demographic signiﬁcance and highlights the ways in which humans are similar to and different from other cooperative breeders. An emphasis is placed on cross-cultural comparison and variability in allocare strategies. Because helping in humans occurs within a subsistence pattern of food sharing and labor cooperation, both kin selection and mutualism may explain why children are often raised with nonmaternal help. Cooperative breeding is relevant to debates in anthropology concerning the evolution of human life history, sociality, and psychology and has implications for demographic patterns in today’s world as well as in the past.

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INTRODUCTION Are Humans Cooperative Breeders? The human capacity for population growth Definition of the term cooperative breeding has is one of the remarkable stories of our evo- undergone recent debate and reconsideration lutionary history. Demographically it can be (Clutton-Brock 2006, Cockburn 1998, Russell attributed to short birth intervals and high 2004, Strassman & Kurapati 2010). Because its survivorship. But it is also fundamentally usage lacks consensus, especially in its appli- shaped by features of human parenting, social- cation to humans, cooperative breeding is used ity, and economic organization. Cooperative here in its broadest historic sense as a social sys- breeding combines these features and is a tem in which nonmaternal individuals help sup- useful framework to consider child-rearing port offspring who are not their own. Another patterns characteristic of humans. term, such as social parenting, may also be suit- Cooperative breeding refers to a parent- able. In lieu of developing a new vocabulary, the ing and social system in which nonparental cooperative breeding literature provides a rich members of the social group help support theoretic and empirical background with which offspring. Cooperative breeding models were to comparatively situate human parenting. originally developed to describe the parenting Because human mothers routinely rely on behavior of certain insects, birds, and mammals the help of others to raise young, humans (Brown 1974, Emlen 1991[1978], Skutch 1987, share many features in common with other Solomon & French 1997). Turke’s (1988) sem- cooperative breeders. But human parenting inal study among Micronesian islanders first in- and reproduction are also distinct in several troduced humans as cooperative breeders into key ways. First, the formation of cooperative anthropology. Turke showed that mothers who breeding in many species of birds and mammals bore girls, who are valuable helpers to their is broadly associated with delayed dispersal. mothers, early in their reproductive careers had Sexually mature offspring may delay leaving greater completed fertility than if their first- their natal territory and initiating reproduc- born children were boys. Since then, anthropol- tion when constraints exist either in mating ogists have paid increasing attention to humans opportunities or in the availability of resources as cooperative breeders. or territory to reproduce successfully (Emlen Cooperative breeding has been documented 1995, Woolfenden & Fitzpatrick 1984). In for ∼3% of bird species and for a similar per- several studies of historic Europe, late age centage of mammals. Although uncommon, at marriage has been related to ecological cooperative breeding occurs across diverse constraints (Strassman & Clarke 1998, Voland mammalian taxa: predominantly wild canids, et al. 1991). Delayed dispersal, however, is not foxes, meerkats, rodents, and several species a necessary condition for human cooperation in of primates, including humans (Brown 1987, raising children. Second, cooperative breeding Clutton-Brock et al. 2001, Emlen 1991[1978], in many species of birds and mammals tends Nicolson 1987). Among nonhuman cooper- to be associated with female reproductive ative breeders, helpers may guard, nurse, or suppression and reproduction by one or a small transport young, help forage for food, defend group of dominant females. In contrast, human territory boundaries, or build and clean nests. mothers acquire help without suppressing The occurrence of these helping behaviors the reproductive effort of other females in across species ranges from rare to habitual. the group. This may be partly because two Reflecting this pattern, the classification of classes of helpers common in traditional so- species as cooperative breeders varies among cieties but not among nonhuman cooperative researchers depending on definitional criteria. breeders—juveniles and grandmothers—are Cooperative breeding occurs in other primates not competing for mating opportunities or but is not a parenting strategy shared by our direct reproductive help. Nor do they compro- closest relatives. mise their own reproductive effort during life

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stages when they help. Third, among humans, schooling, and institutional subsidies alter childrearing help occurs within the broader the need and economic options for providing context of food sharing in which individuals help. The final section explores implications Life history: age- of all ages and sex participate. One reason co- of cooperative breeding for postdemographic related time and operative breeding may be uncommon among transition populations. energy allocations to mammalian species is because dependency growth, reproduction, of young terminates with weaning, limiting and survival across the opportunities for help (Russell 2004). Since HUMAN LIFE HISTORY AND life course human juveniles are also dependent, it intro- COOPERATIVE BREEDING Natural fertility duces the potential for helping behaviors aside Human mothers and children are unusual with population: a population in which from child care. Because juvenile provisioning respect to a number of life-history features fertility is not limited, and other forms of help occur within a general compared with our closest primate relatives regulated, or subsistence pattern of food sharing and labor (Figure 1). Children are weaned at a young controlled through cooperation, the costs, benefits, and pathways age, reach sexual maturity late, and are more conscious means to cooperative breeding in humans may be than twice as likely to survive to reproductive Subsistence very different than those for other animals. age (Kaplan et al. 2000). The common explana- population: ahunter- The goal of this overview is to discuss tion for this remarkable improvement in child gatherer, agricultural, or pastoral society with the importance of and empirical evidence for survivorship is that, unlike other primates who little involvement in human cooperative breeding and to consider are independent of their mothers once they are wage labor or market its demographic significance. The first section weaned, human children continue to be fed, economy, and in which outlines key human life-history characteristics clothed, sheltered, and otherwise assisted. Non- households generally associated with cooperative breeding. The human primate mothers may let juveniles for- consume what they produce, and produce second section identifies helpers and addresses age in close proximity, offer agonistic support, what they consume the roles that fathers, older adults, and siblings and help negotiate social position. But before Demographic play in helping raise human young. The third the birth of the next offspring, juveniles are in- transition: the trend and fourth sections discuss two important dependent food providers. In contrast, human in recent centuries cooperative breeding questions: Does help juveniles are subsidized throughout much of toward declining benefit mothers and young, and why should their growth and development. mortality and fertility partners help? The fifth section addresses Short birth intervals, a relatively high prob- the demographic implications of cooperative ability of survival, and postweaning dependency breeding in relationship to the quality/quantity commit mothers to raising children of various trade-off. The cross-cultural examples in these ages concurrently. Many mammals have litters, sections focus on modern natural-fertility, and mothers support multiple young of the subsistence populations. In these small-scale same age. But raising dependents of different populations, typically wealth is labor-based ages presents a unique challenge to human and children grow up in close proximity to kin mothers because infants, young children, and and have little access to health care/education. older children require different time and energy Given the variation in labor patterns among investments. Infant survival is dependent on modern foragers and the overlap in demo- mother’s milk. Young children, whose dental graphic parameters and child-rearing practices and digestive maturation is incomplete, yet with subsistence agriculturalists and pastoral- whose brain growth is calorically demanding, ists (Bentley et al. 1993, Kramer & Boone need calorie-rich, but easily digestible food 2002), natural fertility, rather than subsistence (Bogin 1999). Older children eat adult foods classification, is considered the more meaning- and often require investments in training, ful criteria for discussing cooperative breeding. education, and status to become competitive A distinction is made between natural-fertility adults. Because of these disparate time and and postdemographic transition populations energy expenditures, mothers are faced with because family planning, paying for child care, a time allocation problem throughout their

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Menarche IBI 9.2(6.1–10.4) Orangutans I J

Weaning First Birth

IBI 3.9(3.0–7.3) Gorillas I J TFR 3

IBI 5.5(4.0–7.3) Chimpanzees I J TFR 2

IBI 3.1(2.4–4.1) Humans I C J TFR 6.1(4.7–8.3)

0 5 10 15 20 25 30 35 40 45 50 55 60 Age

Figure 1 Comparative primate life-history parameters showing mean age at weaning, age at menarche, age at first birth. Error bars show ranges for age at menarche and first birth. Arrows show life expectancy given survival to reproductive age. Birth intervals (IBI) and total fertility rate (TFR) given where available. Sources: Orangutans age at weaning (Galdikas & Wood 1990); age at first birth, birth intervals, life span (Wich et al. 2004, p. 393); age at menarche (Knott 2001). Gorillas age at weaning (Fossey 1979); age at menarche, age at first birth, birth intervals (Watts 1991); TFR (Kaplan et al. 2000). Chimpanzees age at weaning (Pusey 1983); age at menarche (Pusey 1990); age at first birth, birth intervals (Knott 2001); TFR, life span (Kaplan et al. 2000). Humans age at weaning (Kaplan et al. 2000); age at menarche (Eveleth & Tanner 1990, pp. 162–65); age at first birth (Kaplan et al. 2000, mean for Ache, !Kung, Hiwi, and Hadza); life span (Kaplan et al. 2000); TFR (Bentley et al. 1993, mean for 57 groups of foragers, horticulturalists, and agriculturalists); birth intervals (Alvarez 2000, mean for Ache, !Kung, Amele, and Turkana), lower range (Kramer 2002), upper range (Howell 1979, 2000).

reproductive careers: how to provide high- is not adjustable, regardless of the availability quality child care without sacrificing activities of helpers. Cross-cultural research suggests that support older children (Hewlett 1991a, that mothers with a nursing infant and older Hill & Hurtado 1996, Hill & Kaplan 1988, children balance the competing demands of Hrdy 1999). providing for children of different ages by In managing these competing demands, reducing time spent in domestic activities, mothers tend not to compromise the time foraging activities, or field work, activities that they allocate to child care, but instead adjust more directly benefit older children (Hames time spent in other activities. The care that 1988; Hurtado et al. 1985, 1992; Kramer 2004; infants receive from their mothers is similar Marlowe 2003). How mothers resolve this cross-culturally. Table 1 includes all known reduction in time spent in other activities has published sources of the proportion of child led to provocative debate in anthropology care that young children receive from various about who helps mothers raise their young. caretakers. Mothers on average provide only ∼50% of the care a young child receives. This regularity partly reflects that breastfeeding WHO HELPS MOTHERS RAISE constitutes a predictable and large proportion THEIR YOUNG? of child care. Although rare instances of Numerous cross-cultural studies document the allonursing occur in humans, under most social support mothers receive to help raise circumstances the time mothers spend nursing young. Although a variety of kin and nonkin

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Table 1 Mean proportion of direct child care received by a childa Other Mothers Fathers Siblings Grandmothers related/unrelated Ye’kwanab (Hames 1988, p. 245) 49% 2.7% ♀ 16.7% 11.2% 20.6% ♂ 1.9% Akac (Hewlett 1988, p. 269) 42.7% 15.8% – – 13.2% Efe (P. Ivey, unpublished data) 50% 6% ♀ 13% 9% 9% ♂ 14% Agta (Goodman et al. 1985, p. 1206) 51.7% 4.4% ♀ 10.2% 7.6% – ♂ 1.1% Maya (Kramer 2005a, p. 227) 46.1% 1.6% ♀ 31.6% 1.2% 11.2%d ♂ 4.6% 2.8% Alyawarae (Denham 1974, p. 264) 53% <1% 31% – 16% Trinidadf (Flinn 1992, p. 66) 44.2% 10.3% 16.3% – 29.3% Mardug (Scelza 2009, p. 451) 32.2% 1.7% 5.0% 14.3% 29.8% (12.6)h Toba (Valeggia 2009) 50% – ♀ 33% 13% – ♂ 4%

aUnless otherwise indicated, direct child care includes nursing, feeding, carrying, holding, and grooming (dressing, bathing, delousing, minor medical). Values are for infants, in most cases deﬁned as children under the age of one year. A dash indicates data not reported for category. Values may not add up to 100%. bIncludes children 0–40 months. cValues for mothers and fathers includes children 1–18 month(s) old. Other may include siblings and grandmothers. dHelp by related individuals shown on top (of this, aunts comprise 8.4%), unrelated on bottom. eValues reported for carrying children only. Values for male and female siblings reported as an aggregate. f Includes children 0–4 years old. Other includes grandparents. Values for male and female siblings reported as an aggregate. gIncludes children 0–3 years old. Values for male and female siblings reported as an aggregate. hPercent of child care observations in which more than one caretaker was present, and most often includes the mother. In an additional 4.4% of observations, no caretaker was present.

help mothers, attention has centered on males, species (Woolfenden & Fitzpatrick 1984), in- older adults, and children. A selection of these cluding nonhuman primates (Bales et al. 2000, studies is discussed below. Goldizen 1987, McKenna 1987). In human societies, males assist relatively little in child care (Table 1). A notable exception is Aka (cen- Male Investment tral African foragers) fathers, who provide a The help of males in avian studies, where ideas high proportion of infant care (Hewlett 1988). about cooperative breeding were developed, While males generally help little with children, was traditionally considered to be parental in- they are important economic contributors in vestment. When genetic testing opened up the many traditional societies (Draper & Hames possibility of ascertaining paternity, it became 2000, Hewlett 1991a, Hurtado & Hill 1991, clear that in many cases male helpers were not Irons 1983, Kaplan et al. 2000, Marlowe 1999). biological fathers. To avoid making assump- In a comprehensive review of male contributions about paternity, current literature often tion to forager diets, Lancaster et al. (2000) ﬁnd refers to male assistance as allocare or allomoth- that males in most societies provide the majority ering (Hrdy 2001). of calories and most of the protein. Male pro- Male investment is unusual among animals visioning may be particularly important dur- but occurs in a number of cooperative breeding ing lactation (Hurtado et al. 1992, Quinlan &

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Quinlan 2008). Hadza women, for example, The few studies for which time allocation forage less, and their husbands more, when they data are reported specifically for older adults have young nurslings (Marlowe 2003). indicate that they remain hard workers until Paternity certainty: the extent to which a Although males make valuable food con- late in life (Hawkes et al. 1989, 1997; Kaplan male is certain he is tributions, these inputs are quite variable. A 1994; Kramer 2005b; Turke 1988). A compara- the biological father number of studies emphasize that this variation tive time allocation study for which age-specific is best understood as a response to how much consumption data are also available shows that a others help (Fouts 2008, Griffin & Griffin high proportion of Piro and Machiquenga, two 1992, Quinlan & Quinlan 2008). For example, groups of Peruvian horticulturalists, and Maya Fouts (2008) finds that among Indian Bofi older adults produce more than they consume. foragers and Kashi agriculturalists the presence As net producers, these older adults not only of a grandmother is associated with decreased continue to support themselves, but also pro- male parenting effort. Among the Agta, for- duce surpluses that can be transferred to un- agers native to the Philippines, fathers spend derproducers (Lee et al. 2002). more time in child care early in a marriage In traditional societies in which residence when a mother does not have a daughter old patterns are primarily kin based, male and fe- enough to assist (Griffin & Griffin 1992). male kin may have differential effects on survival Other studies emphasize that variation in and growth. The willingness to help has been male assistance reflects the value of their help. associated with paternity certainty, with respect Aka fathers, for example, vary their invest- to both fathers and male relatives. A number ment depending on the opportunity costs of of studies have found, for example, that mater- other ways to spend their time. Aka fathers nal grandparents are more inclined to invest in who have fewer resources to offer spend more grandchildren than are paternal grandparents time with their children and provide more child (Fox et al. 2010, Leonetti et al. 2004, Sear et al. care than do wealthier, higher-status fathers 2000, Voland & Beise 2002). (Hewlett 1988). Among the Ache, food provisioning has higher fitness payoffs than does time spent in other activities, such as child care Juveniles (Hill & Kaplan 1988). Although children may Juveniles are an important but often overlooked benefit from male investment, especially where source of help (Kramer 2002, Kramer 2005b). male resources are important to the diet, moti- Children who are still young enough to receive vation for male provisioning has alternatively child care also often care for their younger sib- been explained as mating effort (Bliege Bird lings (Flinn 1988, Hames 1988, Kramer 2005b, 1999, Hawkes 1991, Hawkes et al. 2001). Nag et al. 1978, Weisner & Gallimore 1977, Whiting & Edwards 1988). Although children receive food and resources from mothers and Older Adults others, juveniles in many traditional societies Grandparents in traditional populations often contribute to their own and their siblings’ live in close proximity to or reside with younger needs from a young age. In addition to food generations. Many empirical studies have fo- production, juveniles participate in a range of cused specifically on grandmothers, who may other subsistence and domestic tasks. The time care for young children while daughters spend children allocate to these activities varies widely time away from home foraging or in other eco- across cultures (Figure 2). This figure includes nomic pursuits. In other circumstances, moth- all known published sources on the time chil- ers with newborns reduce time spent in eco- dren spend working in preindustrial societies. nomic activities while grandmothers take on Variation in the time spent in productive activ- these support tasks (Hawkes et al. 1989, 1997; ities crosscuts modes of subsistence. Notably, Hurtado et al. 1992; Leonetti et al. 2005). forager children have both the highest and

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10 Ariaal 9 8 Bangladesh 7 Mayo, Sonora Hadz a Nepal 6 Java Kipsigis 5 India 4 Dominic a Machiguenga Java May a 3 Mikea Hours of daily work Pumé 2 1 Kung 0 Foragers Horticulturalists Mixed econ Agriculturalists Pastoralists

Figure 2 Time that children in natural-fertility populations allocate to food production and domestic tasks. Values include the time children spend foraging, hunting, fishing, working in the fields, caring for animals, hauling water, collecting fire wood, processing and preparing food, and performing other domestic tasks. These values do not include time spent in child care. Age categories reported in published sources vary from group to group but roughly include children ages 3–12. Sources (left to right): Hadza (Hawkes et al. 1997, p. 556), !Kung (Draper & Cashdan 1988, p. 349), Pume´ (K. Kramer & R. Greaves, n.d.), Machiguenga ( Johnson 1975, p. 305), Mikea (Tucker & Young 2005, p. 155), Java (Nag et al. 1978, p. 295), Nepal (Nag et al. 1978, p. 296), Java (White 1975, p. 141), India (Skoufias 1994, p. 340), Bangladesh (Cain 1977, p. 216), Maya (Kramer & Boone 2002, p. 308), Mayo (Erasmus 1955, p. 330), Dominica (Quinlan et al. 2005, p. 475), Ariaal (Fratkin 1989, p. 434), and Kipsigis (Borgerhoff Mulder et al. 1997, p. 43).

the lowest participation in economic activities. mortality schedules, women are more likely to This suggests that children’s help varies with have a surviving mother when they are young. specific subsistence ecologies, the kinds of Later in her reproductive career, when a subsistence tasks available to children, costs to mother is most pressed by competing demands participate, dangerousness of the environment, to care for older and younger children, a and how children learn to become competent mother is more likely to have productive-aged adults, rather than whether a child is a forager, children and adult sisters. Depending on agriculturalist, or pastoralist per se (Kramer society and individual circumstances, husbands 2005b). and male relatives may provide resources and The age patterning of child care differs child care throughout a mother’s reproductive from economic activities in that it is younger, career. Small-scale populations are subject to not older, children who allocate the most time pronounced stochastic variation in age and sex to child care. Children in many traditional distribution. Although grandmothers, fathers, societies allocate considerably more time to and siblings are often posed as alternative economic activities than to child care (Kramer sources of help, different classes of helpers may 2005a, 2009). This is an important point be important at different points in a woman’s because much of the research on the helping reproductive career and under variable behavior of children has focused on child care, ecological and demographic conditions. which while valuable underrepresents their economic role. In sum, researchers emphasize the contribu- DO HELPERS HELP? tions of different age and sex classes of potential Benefits of Help to Mothers helpers. Given that the importance of male and Young and female resources to the diet and mortality schedules varies widely across environments, An important question in the cooperative there is strategic value to mothers having ac- breeding literature is whether help actu- cess to a range of helpers. Under preindustrial ally benefits maternal fitness. Even though

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Table 2 Studies documenting the effect that helpers have on maternal and child outcomes, stratiﬁed by type of helper Males/fathers Grandparents Juveniles Hill et al. 1985 Hawkes et al. 1989, 1997 Bereczkei 1998 Hill & Hurtado 2009 Jamison et al. 2002 Bereczkei & Dunbar 2002 Hurtado et al. 1992 Leonetti et al. 2005 Bove et al. 2002 Lancaster et al. 2000 Sear et al. 2000, 2002 Bulatao & Lee 1983 Lancaster & Lancaster 1983, 1987 Sear & Mace 2008 Cain 1977 Leonetti et al. 2004, 2007 Voland & Beise 2002 Crognier et al. 2001, 2002 Lee 1979 Hagen & Barrett 2009 Kaplan et al. 2000 Kramer 2002, 2005a,b, 2009 Marlowe 1999, 2001, 2003 Lee & Kramer 2002 Quinlan & Quinlan 2008 Reynolds 1991 Turke 1988, 1989 Zeller 1987

mothers may receive assistance, evidence for associated with higher maternal fertility positive effects on fitness across cooperative (Kramer 2005b, 2009; Lee & Kramer 2002; breeding species is inconclusive (overview in Turke 1988). Other research documents that Clutton-Brock 2006, Russell 2004). In hu- mothers and children benefit from male provi- mans, help provisioning juveniles and assisting sioning returns (Kaplan et al. 2000; Lancaster in child care is associated with mothers giv- et al. 2000; Marlowe 2001, 2003). ing birth at younger ages and at shorter birth intervals, and offspring having improved survival probabilities and better growth outcomes Intergenerational Resource Flows (Table 2). However, the complexities of human These studies draw attention to several points subsistence make it difficult to distinguish be- that distinguish human and nonhuman coop- tween the benefits of help per se and the general erative breeders. Because juveniles in other effects of group living, food sharing, and labor species of cooperative breeding mammals are transfers. independent foragers, help is directed primar- The benefits of help on maternal and ily to unweaned young. Helping behaviors such child outcomes have been assessed with both as allonursing, babysitting, and transporting demographic parameters and individual time young are clear examples of the unidirectional allocation and return rate data. Several studies nature of interactions between helpers and in- using demographic variables as an assay for fants. Older individuals help younger individu- help have shown that the presence of a grand- als with no expectation of an infant reciprocat- mother in a household, particularly maternal ing. However, because weaned human children grandmothers, produces positive effects on also receive care, much of what helpers pro- grandchild survival and growth (Fox et al. 2010, vide is support to juveniles. Helping an infant Jamison et al. 2002, Sear et al. 2000, Voland is distinct from helping a juvenile because in- & Beise 2002). Among the Hadza, foragers in fants do not give back, but juveniles in most sub-Saharan Africa, mothers’ foraging efforts traditional societies make food and labor trans- are correlated with children’s weight, but only fers not only to their siblings, but also to older for nonnursing mothers. After the birth of a generations, including those who help them. new child, children’s weight is correlated with Likewise, helpers who provide food and other the foraging efforts of older adults (O’Connell goods also receive subsidies from others, often et al. 1999). Using time allocation data, others times including those they help. These complex have found that sibling contributions are social interactions and bidirectional resource

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flows among individuals of different ages and sex add a layer of complexity to modeling the HAMILTON’S RULE benefits, motivations, and costs of human cooperative breeding. Hamilton’s rule predicts that altruistic behavior among relatives Subsistence economies are characterized by will be favored by natural selection if rb > c, where r is the coef- widespread labor cooperation and food shar- ficient of relatedness, b is the benefit to the recipient, and c is the ing (Alvard & Nolin 2002; Gurven et al. 2000; cost to the helper. Hames 1990, 2000; Smith & Boyd 1990). These resource and labor transfers may occur among individuals within biological families and with These explanations are reviewed with respect more distantly related kin. Cooperating units to their applicability to cooperative breeding in vary in composition and size, but rarely does humans. an individual of any age do all the tasks necessary to grow, survive, and reproduce. Among Pume´ foragers living on the llanos of Venezuela, Kin Selection a father may bring home hunted game that is Prior to Hamilton’s (1964) articulation of in- shared with other members of his extended fam- clusive fitness theory, there was no satisfy- ily, but he also consumes roots that his wife, ing way to explain helping behavior, which daughters, and others collect and process, as was seen as an enigmatic expression of altru- well as fish that his juvenile son catches. A ism. Hamilton’s rule (see sidebar, Hamilton’s Bidirectional Maya boy harvests enough maize to meet his Rule) provided a framework to view helping as resource flows: own consumption as well as that of his siblings. an adaptive behavior by formulating a means resource exchanges However, he does not consume the maize he to weigh whether benefits accrued by helpers and labor flows that harvests until after it has been shelled, leached, compensate for the cost of their help (Brown occur generationally both downward from soaked, ground, and cooked, tasks that his older 1987, Emlen & Wrege 1991, Vehrencamp older to younger sisters and mother perform (Kramer 2005a). 1978). Hamilton’s rule predicts that helping is generations and This pattern of pooled labor and bidirectional favored and more likely to evolve among closely upward from children resource flows raises a question about why related kin. to adults helpers help and the cost to help in human co- Kin selection has broad appeal as the evo- Collective action operative breeding. lutionary basis for cooperative breeding. As an problem: arises when explanation for why helpers help, kin selection an individual or group of individuals partakes is supported by the close genetic relatedness in benefits without WHY HELP? PATHWAYS TO often noted between helpers and those they COOPERATIVE BREEDING providing benefits in support and the amount of allocare they pro- return Although help raising young may benefit moth- vide (Anderson 2005, Emlen & Wrege 1991, Indirect and direct ers, it poses an evolutionary puzzle. Why should Hames 1988, Ivey 2000, Koenig & Mumme benefits (of helping): others help raise offspring that are not their 1991, Skutch 1987). Child rearing in traditional direct benefits enhance own? Why divert valuable time, energy, and societies is typically kin based. If a caretaker a helper’s own survival, mating opportunities, resources to another when they could be di- benefits directly, the benefit is the same regard- or fecundity. An rected to one’s own survival and fitness? This is less of whether he or she helps kin or nonkin. indirect benefit an important question because it addresses the But if the caretaker helps a closely related child, increases the fitness of collective action problem that arises from help- he or she also benefits indirectly. Grandparents closely related kin ing. Traditional explanations for cooperative are closely related to their grandchildren. Full Mutualism: behaviors center on indirect and direct benefits siblings are even more closely related, as are the benefits of a (Emlen 1995) and forms of reciprocity (Trivers biological fathers. Although helpers are often cooperative act shared by both the helper and 1971, 2006). Recently, greater attention has related to the young they help, this relationship the recipient (e.g., been given to mutualism, by-product mu- does not necessarily explain why they provide forms of food sharing) tualism, and coercion (Clutton-Brock 2006). support.

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Kin selection as the explanation for coop- during some seasons Hadza children provide erative breeding has been reexamined from 50% of their own caloric requirements by age two perspectives (Chapais 2001, 2006). First, five (Blurton Jones et al. 1989). When sub- the emphasis placed on indirect benefits may sistence work is defined to include processing eclipse direct benefits to the helper and and household tasks, Maya girls produce 50% overstate the cost to help (Clutton-Brock of what they consume by age six (Robinson 2002, Clutton-Brock et al. 2001, Griffin Sullivan et al. 2008). Detailed time allocation & West 2002). Although help may benefit off- data reveal that juveniles can produce some spring, there may be little fitness cost to helpers. of what they need at the level of their own Second, kin-biased behaviors may be moti- consumption and some in excess of their con- vated by factors other than kin selection (Coall sumption: Fetching water, harvesting, fishing, & Hertwig 2010, de Waal 2008, Silk 2006). foraging for fruit, and collecting shellfish are These reevaluations are particularly relevant to good examples. Children may satisfy their own humans among whom helping young occurs consumption needs through these tasks, but within the general context of food sharing and their surplus at these tasks may be redistributed labor cooperation. among other members of the sharing group. Human subsistence includes many necessary activities in addition to food provisioning. Mutualism and Bidirectional Transfers However, few studies measure the time and The importance of provisioning young is a energy children spend in these food-processing predominant focus in human parenting, re- and domestic tasks. The emphasis on food production, and life-history research. The em- production underestimates juveniles’ economic phasis on children as the recipients of care, contributions. however, overlooks an important aspect of re- Although children receive help, in societies source sharing and labor cooperation in sub- where they make economic contributions (see sistence economies. Transfers flow downward Figure 1), children underwrite a proportion from older to younger generations, but also up- of their own costs, as well as those of others. ward from children to adults. It is not surpris- Where bidirectional transfers between moth- ing that these intergenerational transfers tend ers and young have been quantified, children’s to occur among related kin and in the context subsistence efforts allow their mothers to sup- of sibling help. But they may have important port more children than they otherwise could effects on the cost to raise children, on the cost without help (Kramer 2005b, Lee & Kramer to help, and perhaps on the motivation to help. 2002).

Cost to raise children. Because dependency Cost to help and proximate mechanisms. of human young extends into juvenility, the en- Recent research has questioned whether kin- ergetic burden on others to support children biased behaviors may be motivated by factors is often assumed to increase. While children in addition to kin selection (Coall & Hertwig growing up in industrialized nations are expen- 2010, de Waal 2008, Silk 2006). Some re- sive to raise, children in many traditional and searchers have raised the point that kin se- evolutionary contexts may be less costly than lection is an ultimate cause focused on ﬁtness often characterized. payoffs. Because these payoffs are often time Although juveniles depend on others for delayed, kin selection per se may be insufﬁ- some of what they need to survive, they have cient to explain helping behaviors. Several emo- complex relationships with their caretakers. tional mechanisms have been forwarded as mo- In most traditional societies, children provide tivation: empathy, fairness, sympathy (de Waal some portion of what they need. For instance, 2008, Hrdy 2009, Preston & de Waal 2002).

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Helpers, especially children, may be coerced or care and other unidirectional helping behaviors strongly urged to help (Becker 1981) or pun- where the individual who is being helped is not ished for not cooperating. Alternatively, what likely to reciprocate. However, mutualism in appears to be altruistic help may more appropri- addition to kin selection may pertain to juve- ately be characterized as an aspect of the long- nile food provisioning where both the helper term mutualism (or short-term reciprocal altru- and the individual being helped are often en- ism) of food sharing and labor transfers that are gaged in a long-term economic relationship. the basis of human subsistence. It is important While juveniles depend on subsidies from oth- to emphasize that kin selection, coercion, and ers, the challenge is to distinguish help per se mutualism are not mutually exclusive explana- from general economic interdependence that tions for cooperative breeding but may explain extends across ages/sex. Although adults may different aspects of very complex human eco- produce surpluses that exceed the levels of their nomic and social interactions. own consumption (Hawkes et al. 1989, Kaplan In subsistence economies, self- and allo- 1994, Kramer 2005b), they also rely on ex- provisioning are often part of the same gen- changes from others, including from younger eral suite of subsistence activities, e.g., some generations. portion of the returns from the time a grandmother spends digging for roots she consumes and some portion her grandchild consumes. DEMOGRAPHIC SIGNIFICANCE Other than child care, the time and energy spent OF COOPERATIVE BREEDING provisioning juveniles, who consume adult re- The quality/quantity trade-off, developed both sources, are integrated into the same suite of in evolutionary biology and in economics tasks helpers otherwise do to support them- to model optimal reproductive solutions, is a selves. This point is obvious, but it is not well useful heuristic to compare parental investment incorporated into ideas about the costs of food strategies across species. The quantity/quality sharing, cooperation, and helping. trade-off predicts that offspring survival will Relative to other primates, humans are either plateau or decline at higher levels impressively efficient food producers. Chim- of fertility (Trivers 1972). This expectation panzees spend 50%–75% of their daily follows from the principle of allocation and time budget foraging (Newton-Fisher 1999). its implication for reproduction. Because time Human foragers spend about half that time and resources are limited, mothers cannot both (Altmann 1987, Gragson 1989, Lee 1979). This have more children and produce higher-quality efficiency reduces costs associated with helping. offspring, often measured by survivorship. Or For example, postreproductive Pumewomen´ can they? have significantly higher return rates than do Compared with other closely related reproductive-aged women for wild roots, which species of similar size, human mothers have comprise about 35% of the diet. These older both higher fertility rates and offspring who women do not spend more time foraging, indi- are twice as likely to survive to reproductive cating that the difference in return rates is be- age (Kaplan et al. 2000). An alteration of the cause they are more efficient at the task. Their quality/quantity trade-off is not uncommon greater efficiency may have some energetic cost, in cooperative breeders (Hrdy 2005). Because but the increase in total cost to provide some of resources available to invest in offspring often their food returns to others is not expected to vary among parents, problems with phenotypic be great. correlation can obscure trade-offs within In sum, cooperative breeding in humans and populations (Hill & Hurtado 1996, Smith & other animals is often kin based. Indirect ben- Fretwell 1974). However, one explanation why efits may explain why helpers assist in child the quality/quantity trade-off is resituated in

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cooperative breeders is that resources available development are debated topics beyond the for reproduction and parental care are not scope of this review. Humans solving compli- solely a function of maternal production. cated problems of access to a great variety of For most mammals, the energy available for high-quality foods using technology, food pro- reproduction is limited by a mother’s ability to cessing, and large foraging ranges establishes produce energy. Mothers must increase their a time allocation constraint for any individual foraging efforts to fund the metabolic costs of to be self-reliant. Economic interdependence reproduction and lactation. For cooperative co-occurs with behaviors that reduce both a breeders, these costs may be mitigated to mother’s sole responsibilities to fund child rear- some extent by helpers. For example, among ing and the risk of juvenile self-reliance. Socially nonhuman primates, help carrying infants supported resource provisioning and offspring allows mothers to forage more efficiently and care have become elaborated beyond a sexual reallocate energy from carrying, an energeti- division of labor to include both bidirectional cally demanding activity, to lactation and the transfers and complex reciprocity. These strate- production of young (French 1997, Goldizen gies have made humans successful reproducers 1987, Koenig 1995, Mitani & Watts 1997, through both an increase in the pace of re- Tardif 1997). The association of helpers with production and improved chances of offspring a reduction in maternal time spent in energeti- survival. cally costly activities, such as food provisioning, has also been observed in humans (Hurtado et al. 1985, 1992; Kramer 2004; Marlowe 2003). IMPLICATIONS FOR If the energy available for reproduction and THE PRESENT childrearing is not limited by a mother’s pro- Two distinct demographic processes are on- duction, it attenuates constraints on the pace of going in the world today. Developed nations reproduction. This has particular significance have passed through the demographic transi- to humans because investment in offspring is tion and population growth rates are low, in decoupled from lactation. Young weaned chil- some cases below replacement. Yet, in many de- dren (under age 7) are similar to infants in veloping nations and traditional societies, fer- their almost complete dependency on others for tility and population growth rates remain high. growth and survival. However, from a mother’s The implications of cooperative breeding to perspective, there is a significant distinction. pre- and postdemographic transition popula- The shift in dependency from milk to food al- tions are discussed separately because family lows mothers to bear children at shorter birth planning and economic options available to intervals because they are not energetically con- raise children, which affect the need for and strained by lactation. In addition to early wean- cost of help, are very different in contracepting, ing compared with closely related primates, market-economy contexts and natural fertility help allows mothers to produce higher-quality populations. juveniles without compromising the rate of reproduction. The modern human diet poses challenges to Predemographic Transition juveniles, and also to adults, to be self-sufficient. Populations Compared with other primates, day ranges In most natural fertility societies today, and for are enormous, annual ranges are vast, food is much of human history, reproduction and par- often transported long distances back to camp, enting occur in the context of extended families and many foods require sophisticated tech- and under circumstances in which maternal nology and skills to access and process. When work and child care are easily combined and these changes occurred and their sequential shared among family and kin. The persistence

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of high fertility following the reduction in although mothers make allocation decisions child mortality in many nonindustrialized and and rely on help, the central evolutionary ques- traditional communities can be seen as a further tion about why helpers help no longer pertains expansion of cooperative breeding. Assistance if caretakers are paid. The child care indus- in raising young, which traditionally came try rests on a relationship between parents and from kin and others, is today augmented by caretakers that is based in money and trust. governments and institutions. In many natural The benefits of help in postdemographic- fertility populations, child survival has in- transition contexts are difficult to identify when creased through nonkin sources of nutritional evaluated against traditional measures of fitness and medical assistance. Concomitant with the because of the confounding effects of the demo- increase in child survival, birth rates have also graphic transition. Currencies other than re- increased, leading to rapid population growth productive success, such as risk adversity, may (Dyson & Murphy 1985, Kramer & Greaves be more appropriate in evaluating helper ef- 2007, Kramer & McMillan 2006, Romaniuk fects in posttransitional industrialized societies. 1980). Although many traditional kin roles may be supplanted, grandparenting, for example, con- tinues to have an important effect on the fertility Postdemographic Transition decisions of working mothers (Coall & Hertwig Populations 2010). Mothers in postdemographic transition populations face new challenges to the same time allocation dilemma of how to provide compe- CONCLUDING REMARKS tent child care while maintaining their eco- Similarities and differences between human nomic production. In postdemographic tran- and nonhuman cooperative breeders are sition populations, childbearing occurs much rooted in the diverse social and economic less often in a kin-based context. As genera- interactions that characterize human behavior. tional time lengthens and families are more For example, that children offset some portion prone to geographic dispersion, child-rearing of their own costs, by helping their siblings support networks often diminish or evapo- while also receiving help, underscores the rate. The reduction of completed family size complexity of demonstrating the dynamics of to approximately two children means that in human cooperative breeding in as comparably both the current and the immediately pre- clear costs and benefits as described for other vious generation, siblings, aunts, and uncles animals. Resolving how humans fit into the are in short supply (Cohen 2003). Unlike the framework of cooperative breeding will benefit trend in traditional societies, mothers who from further theoretical debate and empirical work outside the home often spend more time research. Because humans target high-quality in economic pursuits and less time in child resources with complex access problems, care. both juveniles and adults are constrained In these populations, mothers can solve from being self reliant. High fertility and the competing demands of providing for chil- survival rates are accomplished through our dren of different ages by delaying first birth, particular subsistence and social behaviors and extending birth intervals, and limiting family by utilizing many forms of offspring support. size through contraception. Even though fam- Human cooperative breeding is embedded in a ilies are small, help from others is often still complex sociality, food sharing, and long-term essential, but support shifts to nonkin-based reciprocal relationships that occur across all assistance, paying for child care or institu- ages and sex. These conditions provide rich tional assistance. An interesting outcome is that, fodder for future research directions.

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SUMMARY POINTS 1. The combined effects of short human birth intervals, juvenile dependency, relatively high fertility, and survivorship commit mothers to raise young of different ages. Because mothers routinely depend on the help of others, human parenting has been characterized as cooperative breeding. Males, older adults, a mother’s children, other kin, and nonkin help support mothers, their infants, and older children. Although different classes of helpers (father, grandmothers, siblings) often are posed as alternative sources of help, the range of evidence for nonmaternal support of young suggests that who helps is facultative and varies across a mother’s reproductive career. 2. Unlike other cooperative breeders among whom help is directed primarily to unweaned young and their mothers, human juveniles also are subsidized, not only with food, but with shelter, material goods, etc. Although they are subsidized in part, juveniles in most subsistence populations also help support their siblings and make food and labor transfers to older generations. The analytic challenge is to distinguish help per se from general economic interdependence. 3. Because cooperative breeding occurs within a subsistence pattern of food sharing and labor cooperation, it affects helping behavior in two significant ways. First, the economic relationship between older and younger generations is bidirectional. If these transfers are considered, children growing up in traditional societies may not be as costly as often characterized. Second, the opportunity and energetic cost for adults to help juveniles may be relatively low because the time and energy spent provisioning others are embedded in the same set tasks they do to support themselves. 4. Although helpers often are closely related to those they help, kin selection may not be the only explanation for human cooperative breeding. Help directed to infants may be motivated by inclusive fitness benefits. But provisioning juveniles may be based in long- term mutualistic food-sharing and labor cooperation in which juveniles also participate.

FUTURE ISSUES 1. Within-population comparisons (e.g., Hill & Hurtado 2009) across a greater range of populations will further illuminate the relative importance of various age and sex classes of helpers and the extent to which help is facultative or a determined life-history trait. A wider range of data on children’s age-speciﬁc production and consumption will improve our understanding of the need and opportunities for help and their cross-cultural variation. 2. Many studies infer helper effects from demographic stipulation (the number of grandparents, siblings, or other relatives living or resident in household). The extent to which the presence of a potential helper is an adequate proxy for allocare, resource provisioning, or other forms of help is unclear. Supporting time allocation, economic, and resource ﬂow data are critical to distinguish statistical association from causation and further develop causal links and comprehensive explanations of the effects of help on child and maternal outcomes.

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3. Modern human cooperative breeding occurs within a subsistence strategy that itself involves cooperation and sharing across all ages and sex. Combining what is known more generally about cooperation and food sharing will improve the understanding of human cooperative breeding. 4. Alloparenting in other cooperative breeders is often associated with delayed dispersal. In many traditional societies, parents encourage girls to marry and initiate childbearing at a young age. In other societies, the lapse between sexual maturity and age at ﬁrst birth may last up to a dozen years (Whiting et al. 1986). Examining cross-cultural differences in the activity proﬁles of the marriage and ecological constraints of girls who remain in their natal families well past sexual maturity may clarify the role of delayed dispersal in human compared with nonhuman cooperative breeders.

DISCLOSURE STATEMENT The author is not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS Researchers working with cooperative breeding birds and mammals have laid much of the foun- dation for our understanding of cooperative breeding. This rich background provides many interesting parallels to human cooperative breeding. Much appreciation goes to the Maya and Pume´ for the many years spent observing the interactions of mothers, children, and extended families at work and play. This overview beneﬁted from discussions with Sarah Hrdy, Peter Ellison, Russell Greaves, Hilly Kaplan, Jane Lancaster, and Benjamin Chabot-Hanowell.

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