Cooperative breeding and its significance to the demographic success of humans.

The demographic success of humans compared with other closely related species can be attributed to the relatively rapid pace of reproduction and improved chances of survival. The assistance that mothers receive from others to help raise children is a common theme in explaining this gain in surviving fertility. Cooperative breeding in its broad definition 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.

[1]  G. McMillan,et al.  The Effect of Labor‐Saving Technology on Longitudinal Fertility Changes , 2006, Current Anthropology.

[2]  Kim Hill,et al.  Cooperative breeding in South American hunter–gatherers , 2009, Proceedings of the Royal Society B: Biological Sciences.

[3]  J. Tanner,et al.  Worldwide Variation in Human Growth , 1991 .

[4]  K. Anderson.  Relatedness and investment in children in South Africa , 2005, Human nature.

[5]  B. White.  The Economic Importance of Children in a Javanese Village , 1976 .

[6]  Anne E. Pusey,et al.  BEHAVIOURAL CHANGES AT ADOLESCENCE IN CHIMPANZEES , 1990 .

[7]  Ronald Lee,et al.  Counting women's labour: A reanalysis of children's net production using Cain's data from a Bangladeshi village , 2008, Population studies.

[8]  S. Emlen.  An evolutionary theory of the family. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Kim Hill,et al.  Female subsistence strategies among Ache hunter-gatherers of Eastern Paraguay , 1985 .

[10]  J. Bongaarts,et al.  Determinants of fertility in developing countries. , 1984 .

[11]  W. Irons.  7 – Human Female Reproductive Strategies , 1983 .

[12]  D. Leonetti,et al.  In‐law Conflict , 2007, Current Anthropology.

[13]  Karen L. Kramer,et al.  Variation in juvenile dependence , 2002, Human nature.

[14]  R. Trivers.  The Evolution of Reciprocal Altruism , 1971, The Quarterly Review of Biology.

[15]  Robin I. M. Dunbar,et al.  Helping‐at‐the‐Nest and Sex‐Biased Parental Investment in a Hungarian Gypsy Population , 2002, Current Anthropology.

[16]  Joel E. Cohen,et al.  Human Population: The Next Half Century , 2003, Science.

[17]  P. Turke.  Evolution and the demand for children. , 1989 .

[18]  K. Hawkes,et al.  Men's time allocation to subsistence work among the Ache of Eastern Paraguay , 1985 .

[19]  Molly Fox,et al.  Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality † , 2010, Proceedings of the Royal Society B: Biological Sciences.

[20]  Paula K. Ivey,et al.  An Interview with Edith Turner1 , 2000, Current Anthropology.

[21]  K. Kramer.  Maya Children: Helpers at the Farm , 2005 .

[22]  R. Trivers.  Parental investment and sexual selection , 1972 .

[23]  S. Emlen,et al.  BREEDING BIOLOGY OF WHITE-FRONTED BEE-EATERS AT NAKURU: THE INFLUENCE OF HELPERS ON BREEDER FITNESS , 1991 .

[24]  Peter M. Kappeler,et al.  Cooperation in Primates and Humans , 2006 .

[25]  Griffin Pb,et al.  Fathers and childcare among the Cagayan Agta. , 1992 .

[26]  S. Tax,et al.  An Anthropological Approach to the Study of the Economic Value of Children in Java and Nepal [and Comments and Reply] , 1978, Current Anthropology.

[27]  S. Preston,et al.  Empathy: Its ultimate and proximate bases. , 2001, The Behavioral and brain sciences.

[28]  M. Villena,et al.  Helping patterns and reproductive success in Aymara communities , 2002, American Journal of Human Biology.

[29]  T. Clutton‐Brock.  Cooperative breeding in mammals , 2006 .

[30]  K. Hawkes,et al.  Hunting and Nuclear Families , 2001, Current Anthropology.

[31]  J. W. Wood,et al.  Birth spacing patterns in humans and apes. , 1990, American journal of physical anthropology.

[32]  S. Hrdy,et al.  Mothers and Others , 2009 .

[33]  R. Gallimore,et al.  My Brother's Keeper: Child and Sibling Caretaking [and Comments and Reply] , 1977, Current Anthropology.

[34]  N. Newton-Fisher.  The diet of chimpanzees in the Budongo Forest Reserve, Uganda , 1999 .

[35]  R. Mace,et al.  Maternal grandmothers improve nutritional status and survival of children in rural Gambia , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  N. Nicolson.  Infants, mothers, and other females , 1987 .

[37]  Ronald Lee,et al.  Children's Economic Roles in the Maya Family Life Cycle: Cain, Caldwell, and Chayanov Revisited , 2002 .

[38]  F. Marlowe.  A critical period for provisioning by Hadza men: Implications for pair bonding , 2003 .

[39]  B. Chapais.  Primate Nepotism: What is the Explanatory Value of Kin Selection? , 2001, International Journal of Primatology.

[40]  Hillard Kaplan,et al.  Evolutionary and wealth flows theories of fertility: empirical tests and new models. , 1994 .

[41]  A. Zeller.  A Role for Women in Hominid Evolution , 1987 .

[42]  M. Gurven,et al.  “ It ’ s a Wonderful Life ” : signaling generosity among the Ache of Paraguay , 2000 .

[43]  M. Flinn,et al.  Local Resource Enhancement and Sex‐biased Breastfeeding in a Caribbean Community1 , 2005, Current Anthropology.

[44]  G. Jasienska,et al.  The fertility of agricultural and non-agricultural traditional societies. , 1993 .

[45]  Tim Clutton-Brock,et al.  Breeding together: kin selection and mutualism in cooperative vertebrates. , 2002, Science.

[46]  B. Strassmann,et al.  Are humans cooperative breeders?: Most studies of natural fertility populations do not support the grandmother hypothesis , 2010 .

[47]  A. Baali,et al.  Do “helpers at the nest” increase their parents' reproductive success? , 2001, American journal of human biology : the official journal of the Human Biology Council.

[48]  Kim Hill,et al.  A theory of human life history evolution: Diet, intelligence, and longevity , 2000 .

[49]  S. Pavard.  Substitute Parents: Biological and Social Perspectives on Alloparenting in Human Societies , 2010 .

[50]  F. Marlowe.  Male Contribution to Diet and Female Reproductive Success among Foragers1 , 2001, Current Anthropology.

[51]  G. Stecklov.  Evaluating the economic returns to childbearing in Côte d'Ivoire , 1999 .

[52]  Eckart Voland,et al.  Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn , 2001, Behavioral Ecology and Sociobiology.

[53]  W. Denham.  INFANT TRANSPORT AMONG THE ALYAWARA TRIBE, CENTRAL AUSTRALIA , 1974 .

[54]  E. Skoufias.  Market wages, family composition and the time allocation of children in agricultural households , 1994 .

[55]  David A. Nolin,et al.  Rousseau’s Whale Hunt? , 2002, Current Anthropology.

[56]  Kim Hill,et al.  The Evolution of Life History, Intelligence and Diet Among Chimpanzees and Human Foragers , 2000 .

[57]  C. Engel,et al.  Cost/benefit oriented parental investment by high status families: The Krummhörn case , 1991 .

[58]  R. Trivers.  Reciprocal altruism: 30 years later , 2006 .

[59]  P. Jamison,et al.  Are all grandmothers equal? A review and a preliminary test of the "grandmother hypothesis" in Tokugawa Japan. , 2002, American journal of physical anthropology.

[60]  A. Romaniuk.  Increase in natural fertility during the early stages of modernization: evidence from an African case study, Zaire. , 1980, Population studies.

[61]  K. Kramer.  Children's Help and the Pace of Reproduction: Cooperative Breeding in Humans , 2005 .

[62]  R. Hames,et al.  Birth order, sibling investment, and fertility among Ju/’Hoansi (!Kung) , 2000, Human nature.

[63]  T. Clutton‐Brock,et al.  Contributions to cooperative rearing in meerkats , 2001, Animal Behaviour.

[64]  B. Chapais.  Kinship, competence and cooperation in primates , 2006 .

[65]  T. Dyson,et al.  The Onset of Fertility Transition , 1985 .

[66]  J. Grove,et al.  The compatibility of hunting and mothering among the agta hunter-gatherers of the Philippines , 1985 .

[67]  R. Layton,et al.  Hunter-Gatherers Today: An Aboriginal Economy in North Australia. , 1991 .

[68]  H. Barrett,et al.  Cooperative Breeding and Adolescent Siblings , 2009, Current Anthropology.

[69]  A. Russell.  Ecology and Evolution of Cooperative Breeding in Birds: Mammals: comparisons and contrasts , 2004 .

[70]  W. Hamilton.  The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[71]  K. Hawkes,et al.  Showing off: Tests of an hypothesis about men's foraging goals , 1991 .

[72]  Richard B. Lee.  The !Kung San: Men, Women and Work in a Foraging Society , 1979 .

[73]  K. Hawkes,et al.  Hadza Women's Time Allocation, Offspring Provisioning, and the Evolution of Long Postmenopausal Life Spans , 1997, Current Anthropology.

[74]  C. Erasmus.  Work Patterns in a Mayo Village2 , 1955 .

[75]  S. Wich,et al.  Life history of wild Sumatran orangutans (Pongo abelii). , 2004, Journal of human evolution.

[76]  F. D. Waal.  Putting the Altruism Back into Altruism: The Evolution of Empathy , 2008 .

[77]  P. Ellison,et al.  Girl helpers and time allocation of nursing women among the Toba of Argentina , 2002, Human nature.

[78]  J. W. Whiting,et al.  Culture and human development: The duration of maidenhood across cultures , 1986 .

[79]  E. Cashdan,et al.  Technological Change and Child Behavior among the !Kung , 1988 .

[80]  H. Alvarez,et al.  Grandmother hypothesis and primate life histories. , 2000, American journal of physical anthropology.

[81]  T. Bereczkei.  Kinship Network, Direct Childcare, and Fertility Among Hungarians and Gypsies , 1998 .

[82]  J. French,et al.  Cooperative Breeding in Mammals: Proximate Regulation of Singular Breeding in Callitrichid Primates , 1996 .

[83]  D. Watts.  Mountain gorilla reproduction and sexual behavior , 1991, American journal of primatology.

[84]  A. Hurtado,et al.  Paternal effect on offspring survivorship among Ache and Hiwi hunter-gatherers: implications for modeling pair-bond stability. , 1992 .

[85]  F. Marlowe.  Showoffs or Providers? The Parenting Effort of Hadza Men , 1999 .

[86]  R. Bird.  Cooperation and conflict: The behavioral ecology of the sexual division of labor , 1999 .

[87]  B. Hewlett.  Demography and Childcare in Preindustrial Societies , 1991, Journal of Anthropological Research.

[88]  James F. O'Connell,et al.  Hunting and Nuclear Families: Some Lessons from the Hadza about Men's Work , 2001 .

[89]  E. Fratkin,et al.  Household Variation and Gender Inequality in Ariaal Pastoral Production: Results of a Stratified Time-Allocation Survey , 1989 .

[90]  A. Koenig.  Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus) , 1995, American journal of primatology.

[91]  Russell D. Greaves,et al.  Changing Patterns of Infant Mortality and Maternal Fertility among Pumé Foragers and Horticulturalists , 2007 .

[92]  S. Tardif,et al.  Effects of Allocare-Givers on Fitness of Infants and Parents in Callitrichid Primates , 2000, Folia Primatologica.

[93]  J. Lancaster.  Parenting across the life span , 1987 .

[94]  T. Gragson.  Allocation of time to subsistence and settlement in a Ciri Khonome Pume village of the Lhanos of Apure, Venezuela. , 1989 .

[95]  J. Mitani,et al.  The evolution of non-maternal caretaking among anthropoid primates: do helpers help? , 1997, Behavioral Ecology and Sociobiology.

[96]  Jerram L. Brown.  Alternate Routes to Sociality in Jays—With a Theory for the Evolution of Altruism and Communal Breeding , 1974 .

[97]  A. Griffin,et al.  Kin selection: fact and fiction , 2002 .

[98]  B. Strassmann,et al.  ECOLOGICAL CONSTRAINTS ON MARRIAGE IN RURAL IRELAND , 1998 .

[99]  D. Leonetti,et al.  DO WOMEN REALLY NEED MARITAL PARTNERS FOR SUPPORT OF THEIR REPRODUCTIVE SUCCESS? THE CASE OF THE MATRILINEAL KHASI OF N. E. INDIA , 2004 .

[100]  A. Hurtado,et al.  Trade-Offs between female food acquisition and child care among hiwi and ache foragers , 1992, Human nature.

[101]  A. Skutch.  Helpers at Birds' Nests: A Worldwide Survey of Cooperative Breeding and Related Behavior , 1987 .

[102]  K. Kramer.  RECONSIDERING THE COST OF CHILDBEARING: THE TIMING OF CHILDREN’S HELPING BEHAVIOR ACROSS THE LIFE CYCLE OF MAYA FAMILIES , 2004 .

[103]  B. Scelza.  The grandmaternal niche: Critical caretaking among Martu Aborigines , 2009, American journal of human biology : the official journal of the Human Biology Council.

[104]  R. Quinlan,et al.  Human Lactation, Pair-bonds, and Alloparents , 2008, Human nature.

[105]  J. Boone,et al.  Why Intensive Agriculturalists Have Higher Fertility: A Household Energy Budget Approach1 , 2002, Current Anthropology.

[106]  Allen Johnson.  Time Allocation in a Machiguenga Community , 1975 .

[107]  A. Pusey.  Mother-offspring relationships in chimpanzees after weaning , 1983, Animal Behaviour.

[108]  Glen E. Woolfenden,et al.  The Florida scrub jay : demography of a cooperative-breeding bird , 1986 .

[109]  S. Hrdy.  Mothers and Others: The Evolutionary Origins of Mutual Understanding , 2009 .

[110]  Ruth Mace,et al.  Who keeps children alive? A review of the effects of kin on child survival , 2008 .

[111]  M. Cain,et al.  The economic activities of children in a village in Bangladesh , 1977 .

[112]  Hillary N. Fouts.  Father Involvement With Young Children Among the Aka and Bofi Foragers , 2008 .

[113]  Ralph Hertwig,et al.  Grandparental investment: past, present, and future. , 2010, The Behavioral and brain sciences.

[114]  J. French,et al.  Cooperative Breeding in Mammals , 2007 .

[115]  S. Vehrencamp.  The adaptive significance of communal nesting in Groove-billed anis (Crotophaga sulcirostris) , 1978, Behavioral Ecology and Sociobiology.

[116]  A. Zeller.  A Role for Children in Hominid Evolution , 1987 .

[117]  R. Mace,et al.  The effects of kin on child mortality in rural gambia , 2002, Demography.

[118]  Nancy Howell.  Demography of the Dobe! Kung , 1979 .

[119]  J. Silk.  Practicing Hamilton’s rule: kin selection in primate groups , 2006 .

[120]  A. Cockburn.  EVOLUTION OF HELPING BEHAVIOR IN COOPERATIVELY BREEDING BIRDS , 1998 .

[121]  K. Hawkes,et al.  Grandmothering and the evolution of homo erectus. , 1999, Journal of human evolution.

[122]  B. Hewlett.  Hunter-Gatherer Childhoods: Evolutionary, Developmental, and Cultural Perspectives , 2005 .