Abstract
Human children are frequently cared for by non-parental caregivers (alloparents), yet few studies have conducted systematic alternative hypothesis tests of why alloparents help. Here we explore whether predictions from kin selection, reciprocity, learning-to-mother and costly signalling hypotheses explain non-parental childcare among Agta hunter-gatherers from the Philippines. To test these hypotheses, we used high-resolution proximity data from 1,701 child–alloparent dyads. Our results indicated that reciprocity and relatedness were positively associated with the number of interactions with a child (our proxy for childcare). Need appeared more influential in close kin, suggesting indirect benefits, while reciprocity proved to be a stronger influence in non-kin, pointing to direct benefits. However, despite shared genes, close and distant kin interactions were also contingent on reciprocity. Compared with other apes, humans are unique in rapidly producing energetically demanding offspring. Our results suggest that the support that mothers require is met through support based on kinship and reciprocity.
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The data that support the findings of this study are available from the corresponding author upon request.
References
Campbell, K. L. & Wood, J. W. in Natural Human Fertility (eds Diggory, P., Teper, S. & Potts, M.) 39–69 (Macmillan Publishing, 1988).
Hill, K. & Hurtado, A. M. Cooperative breeding in South American hunter-gatherers. Proc. R. Soc. B Biol. Sci. 276, 3863–3870 (2009).
Meehan, C. L., Helfrecht, C. & Malcom, C. D. in Childhood: Origins, Evolution and Implications (eds Meehan, C. L. & Crittenden, A. N.) 199–220 (SAR Press, 2016).
Bogin, B., Bragg, J. & Kuzawa, C. Humans are not cooperative breeders but practice biocultural reproduction. Ann. Hum. Biol. 41, 368–380 (2014).
Meehan, C. L. Allomaternal investment and relational uncertainty among Ngandu farmers of the Central African Republic. Hum. Nat. 19, 211–226 (2008).
Meehan, C. L. & Hawks, S. in Different Faces of Attachment: Cultural Variations on a Universal Human Need (eds Otto, H. & Keller, H.) 113–140 (Cambridge Univ. Press, 2014).
Meehan, C. L. & Hawks, S. in Attachment Reconsidered: Cultural Perspectives on a Western Theory (eds Quinn, N. & Mageo, J. M.) 85–113 (Palgrave Macmillan, 2013).
Hawkes, K. & O’Connell, J. Grandmothering, menopause, and the evolution of human life histories. Proc. Natl Acad. Sci. USA 95, 1336–1339 (1998).
Helfrecht, C. & Meehan, C. L. Sibling effects on nutritional status: intersections of cooperation and competition across development. Am. J. Hum. Biol. 28, 159–170 (2016).
Lawson, D. W. & Mace, R. Trade-offs in modern parenting: a longitudinal study of sibling competition for parental care. Evol. Hum. Behav. 30, 170–183 (2009).
Sear, R. & Mace, R. Who keeps children alive? A review of the effects of kin on child survival. Evol. Hum. Behav. 29, 1–18 (2008).
Snopkowski, K. & Sear, R. Kin influences on fertility in Thailand: effects and mechanisms. Evol. Hum. Behav. 34, 130–138 (2013).
Meehan, C. L., Helfrecht, C. & Quinlan, R. J. Cooperative breeding and Aka children’s nutritional status: is flexibility key? Am. J. Phys. Anthropol. 153, 513–525 (2014).
Kramer, K. L. & Veile, A. Infant allocare in traditional societies. Physiol. Behav. 193, 117–126 (2018).
Meehan, C. L., Quinlan, R. & Malcom, C. D. Cooperative breeding and maternal energy expenditure among Aka foragers. Am. J. Hum. Biol. 25, 42–57 (2013).
Foster, K. R., Wenseleers, T. & Ratnieks, F. L. W. Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57–60 (2006).
Rand, D. G. & Nowak, M. A. Human cooperation. Trends Cogn. Sci. 17, 413–425 (2013).
Clutton-Brock, T. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 (2002).
Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964).
Ivey, P. K. Cooperative reproduction in Ituri Forest hunter-gatherers: who cares for Efe infants? Curr. Anthropol. 41, 856–866 (2000).
Crittenden, A. N. & Marlowe, F. W. Allomaternal care among the Hadza of Tanzania. Hum. Nat. 19, 249–262 (2008).
Apicella, C. L. & Crittenden, A. N. in The Handbook of Evolutionary Psychology (ed. Buss, D. M.) 1–20 (Wiley, 2013).
Chapais, B. in Cooperation in Primates and Humans (eds Kappeler, P. M. & Van Schaik, C. P.) 47–61 (Springer, 2006).
Schino, G. & Aureli, F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol. Lett. 13, 45–50 (2010).
Crittenden, A. N. & Zes, D. A. Food sharing among Hadza hunter-gatherer children. PLoS One 10, e0131996 (2015).
Lukas, D. & Clutton-Brock, T. Cooperative breeding and monogamy in mammalian societies. Proc. R. Soc. B Biol. Sci. 279, 2151–2156 (2012).
Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).
Gurven, M. The evolution of contingent cooperation. Curr. Anthropol. 47, 185–192 (2006).
Smith, D. et al. A friend in need is a friend indeed: need-based sharing, rather than cooperative assortment, predicts experimental resource transfers among Agta hunter-gatherers. Evol. Hum. Behav. 40, 82–89 (2019).
Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971).
Jaeggi, A. V. & Gurven, M. Reciprocity explains food sharing in humans and other primates independent of kin selection and tolerated scrounging: a phylogenetic meta-analysis. Proc. R. Soc. B Biol. Sci. 280, 20131634 (2013).
Jaeggi, A. V., Hooper, P. L., Beheim, B. A., Kaplan, H. & Gurven, M. Reciprocal exchange patterned by market forces helps explain cooperation in a small-scale society. Curr. Biol. 26, 2180–2187 (2016).
Carter, G. G., Wilkinson, G. S. & Carter, G. G. Food Sharing in Vampire Bats: Reciprocal Help Predicts Donations More Than Relatedness or Harassment (2013).
Allen-Arave, W., Gurven, M. & Hill, K. Reciprocal altruism, rather than kin selection, maintains nepotistic food transfers on an Ache reservation. Evol. Hum. Behav. 29, 305–318 (2008).
Nolin, D. A. Food-sharing networks in Lamalera, Indonesia: reciprocity, kinship, and distance. Hum. Nat. 21, 243–268 (2010).
Koster, J. Interhousehold meat sharing among Mayangna and Miskito horticulturalists in Nicaragua. Hum. Nat. 22, 394–415 (2011).
Wilkinson, G. S. Reciprocal food sharing in the vampire bat. Nature 308, 181–184 (1984).
Gurven, M. Reciprocal altruism and food sharing decisions among Hiwi and Ache hunter–gatherers. Behav. Ecol. Sociobiol. 56, 366–380 (2004).
Koster, J. M. & Leckie, G. Food sharing networks in lowland Nicaragua: an application of the social relations model to count data. Soc. Netw. 38, 100–110 (2014).
Snopkowski, K. & Sear, R. Grandparental help in Indonesia is directed preferentially towards needier descendants: a potential confounder when exploring grandparental influences on child health. Soc. Sci. Med. 128, 105–114 (2015).
Hames, R. Garden labour exchange among the Yekwana. Ethol. Sociobiol. 8, 259–284 (1987).
Thomas, M. G. et al. Kinship underlies costly cooperation in Mosuo villages. R. Soc. Open Sci. 5, 171535 (2018).
Hawkes, K. Hunting income patterns among the Hadza: big game, common goods, foraging goals and the evolution of the human diet. Phil. Trans. Biol. Sci. 334, 243–250 (1991).
Gurven, M., Allen-Arave, W., Hill, K. & Hurtado, M. ‘It’s a Wonderful Life’: signaling generosity among the Ache of Paraguay. Evol. Hum. Behav. 21, 263–282 (2000).
Sugiyama, L. S. Illness, injury, and disability among Shiwiar forager-horticulturalists: implications of health-risk buffering for the evolution of human life history. Am. J. Phys. Anthropol. 123, 371–389 (2004).
Jaeggi, A. V. & Gurven, M. Natural cooperators: food sharing in humans and other primates. Evol. Anthropol. 22, 186–195 (2013).
Dyble, M. et al. Networks of food sharing reveal the functional significance of multilevel sociality in two hunter-gatherer groups. Curr. Biol. 26, 2017–2021 (2016).
Carter, G. G. & Wilkinson, G. S. Social benefits of non-kin food sharing by female vampire bats. Proc. R. Soc. B Biol. Sci. 282, 20152524 (2015).
Page, A. E. et al. Hunter-gatherer social networks and reproductive success. Sci. Rep. 7, 1153 (2017).
Dyble, M. et al. Sex equality can explain the unique social structure of hunter-gatherer bands. Science 348, 796–798 (2015).
Hill, K. R. et al. Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331, 1286–1289 (2011).
Lancaster, J. B. Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol. (Basel) 15, 161–182 (1971).
Baker, A. J. & Woods, F. Reproduction of the emperor tamarin (Saguinus imperator) in captivity, with comparisons to cotton‐top and golden lion tamarins. Am. J. Primatol. 26, 1–10 (1992).
Solomon, N. G. & Hayes, L. D. in Substitute Parents: Biological and Social Perspective on Alloparenting Across Human Societies (eds Bentley, G. & Mace, R.) 13–49 (Berghahn Books, 2009).
Baker, A. J. Evolution of the Social System of the Golden Lion Tamarin (Leontopithecus rosalia) (Univ. Maryland, 1991).
Salo, A. L. & French, J. A. Early experience, reproductive success and development of parental behaviour in Mongolian gerbils. Anim. Behav. 38, 693–702 (1989).
Zahavi, A. in Cooperative Breeding in Birds: Long Term Studies of Ecology and Behaviour 103–130 (1990).
Tardif, S. D. in Cooperative Breeding in Mammals (eds Solomon, N. G. & French, J. A.) 11–33 (Cambridge Univ. Press, 1997).
Price, E. C. & McGrew, W. C. Cotton‐top tamarins (Saguinus (o.) oedipus) in a semi‐naturalistic captive colony. Am. J. Primatol. 20, 1–12 (1990).
Rosenbaum, S., Vigilant, L., Kuzawa, C. W. & Stoinski, T. S. Caring for infants is associated with increased reproductive success for male mountain gorillas. Sci. Rep. 8, 15223 (2018).
Kramer, K. L. Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 417–436 (2010).
Sear, R. & Coall, D. How much does family matter? Cooperative breeding and the demographic transition. Popul. Dev. Rev. 37, 81–112 (2011).
Jetz, W. & Rubenstein, D. R. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78 (2011).
Baden, A. L., Wright, P. C., Louis, E. E. & Bradley, B. J. Communal nesting, kinship, and maternal success in a social primate. Behav. Ecol. Sociobiol. 67, 1939–1950 (2013).
Kokko, H., Johnstone, R. A. & Clutton-Brock, T. H. The evolution of cooperative breeding through group augmentation. Proc. Biol. Sci. 268, 187–196 (2001).
Smith, D. et al. Camp stability predicts patterns of hunter-gatherer cooperation. R. Soc. Open Sci. 3, 160131 (2016).
Dyble, M., Gardner, A., Vinicius, L. & Migliano, A. B. Inclusive fitness for in-laws. Biol. Lett. 14, 20180515 (2018).
Carter, G. G., Wilkinson, G. S. & Page, R. A. Food-sharing vampire bats are more nepotistic under conditions of perceived risk. Behav. Ecol. 280, 20122573 (2017).
Barclay, P. Strategies for cooperation in biological markets, especially for humans. Evol. Hum. Behav. 34, 164–175 (2013).
Davies, N. B., Krebs, J. R. & West, S. An Introduction to Behavioural Ecology (Wiley-Blackwell, 2012).
Fried, J. J. The Role of Juvenile Pine Voles (Microtus pinetorum) in the Caretaking of their Younger Siblings (North Carolina State Univ., 1987).
Silk, J. B. Kidnapping and female competition among captive bonnet macaques. Primates 21, 100–110 (1980).
Hrdy, S. B. Mothers and Others: The Evolutionary Origins of Mutual Understanding (Harvard Univ. Press, 2009).
Tardif, S. D., Carson, R. L. & Gangaware, B. L. Infant-care behavior of non-reproductive helpers in a communal-care primate, the cotton-top tamarin (Saguinus oedipus). Ethology 92, 155–167 (1992).
Kramer, K. L., Veile, A. & Otárola-Castillo, E. Sibling competition & growth tradeoffs. Biological vs. statistical significance. PLoS One 11, e0150126 (2016).
Davies, N. B., Hatchwell, B. J., Robson, T. & Burke, T. Paternity and parental effort in dunnocks Prunella modularis: how good are male chick-feeding rules? Anim. Behav. 43, 729–745 (1992).
Baker, A. J., Dietz, J. M. & Kleiman, D. G. Behavioural evidence for monopolization of paternity in multi-male groups of golden lion tamarins. Anim. Behav. 46, 1091–1103 (1993).
Winking, J., Gurven, M., Kaplan, H. & Stieglitz, J. The goals of direct paternal care among a South Amerindian population. Am. J. Phys. Anthropol. 139, 295–304 (2009).
Scelza, B. A. The grandmaternal niche: critical caretaking among Martu Aborigines. Am. J. Hum. Biol. 21, 448–454 (2009).
Meehan, C. L. The effects of residential locality on parental and alloparental investment among the Aka foragers of the Central African Republic. Hum. Nat. 16, 58–80 (2005).
Barclay, P. & Reeve, H. K. The varying relationship between helping and individual quality. Behav. Ecol. 23, 693–698 (2012).
Minter, T. The Agta of the Northern Sierra Madre: Livelihood Strategies and Resilience Among Philippine Hunter-Gatherers (Leiden Univ., 2010).
Page, A. E. et al. Reproductive trade-offs in extant hunter-gatherers suggest adaptive mechanism for the Neolithic expansion. Proc. Natl Acad. Sci. USA 113, 4694–4699 (2016).
Page, A. E., Minter, T., Viguier, S. & Migliano, A. B. Hunter-gatherer health and development policy: how the promotion of sedentism worsens the Agta’s health outcomes. Soc. Sci. Med. 197, 39–48 (2018).
Migliano, A. B. et al. Characterization of hunter-gatherer networks and implications for cumulative culture. Nat. Hum. Behav. 1, 0043 (2017).
Flack, J. C., Girvan, M., de Waal, F. B. M. & Krakauer, D. C. Policing stabilizes construction of social niches in primates. Nature 439, 426–429 (2006).
Brent, L. J. N., Semple, S., Dubuc, C., Heistermann, M. & Maclarnon, A. Social capital and physiological stress levels in free-ranging adult female rhesus macaques. Physiol. Behav. 102, 76–83 (2011).
Isella, L. et al. What’s in a crowd? Analysis of face-to-face behavioral networks. J. Theor. Biol. 271, 166–180 (2011).
Hewlett, B. S., Lamb, M. E., Leyendecker, B. & Schölmerich, A. in Adaptation and Human Behaviour: an Anthropological Perspective 155–177 (2000).
Fouts, H. N., Hewlett, B. S. & Lamb, M. E. Parent–offspring weaning conflicts among the Bofi farmers and foragers of Central Africa. Curr. Anthropol. 46, 29–50 (2005).
Lee, R. D. & Kramer, K. L. Children’s economic roles in the Maya family life cycle: Cain, Caldwell, and Chayanov revisited. Popul. Dev. Rev. 28, 475–499 (2002).
Crittenden, A. N., Conklin-Brittain, N. L., Zes, D. A., Schoeninger, M. J. & Marlowe, F. W. Juvenile foraging among the Hadza: implications for human life history. Evol. Hum. Behav. 34, 299–304 (2013).
Kramer, K. L. The evolution of human parental care and recruitment of juvenile help. Trends Ecol. Evol. 26, 533–540 (2011).
Konner, M. in Hunter-Gatherer Childhoods: Cultural, Developmental, & Evolutionary Perspectives (eds Hewlett, B. S. & Lamb, M. E.) 19–64 (Aldine Transaction, 2005).
Koster, J., Leckie, G., Miller, A. & Hames, R. Multilevel modeling analysis of dyadic network data with an application to Ye’kwana food sharing. Am. J. Phys. Anthropol. 157, 507–512 (2015).
Gurven, M. To give and to give not: the behavioral ecology of human food transfers. Behav. Brain Sci. 27, 543–583 (2004).
Acknowledgements
We thank the Human Evolutionary Ecology Group for comments on earlier drafts, our assistants in the Philippines, and most importantly, the Agta. We also thank L. Barrett, G. Bentley and R. Sear for guidance and useful suggestions to improve this work. This project was funded by Leverhulme Trust Grant RP2011-R 045 (to A.B.M. and R.M.). R.M. received funding from European Research Council Advanced Grant AdG 249347. A.E.P. received funding from the MRC and DFID (grant number MR/P014216/1). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
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A.E.P. conceived and designed the study. A.B.M. led the research project and supervised the study. S.V. and A.E.P. designed the motes. A.E.P. and M.G.T. analysed the data. A.E.P. and A.B.M. wrote the manuscript. A.E.P., M.D., S.V. and D.S. collected the data. M.G.T., M.D., S.V., D.S., N.C., J.T., G.D.S., R.M. and A.B.M. all assisted in writing the manuscript.
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Page, A.E., Thomas, M.G., Smith, D. et al. Testing adaptive hypotheses of alloparenting in Agta foragers. Nat Hum Behav 3, 1154–1163 (2019). https://doi.org/10.1038/s41562-019-0679-2
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DOI: https://doi.org/10.1038/s41562-019-0679-2
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