Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Testing adaptive hypotheses of alloparenting in Agta foragers

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Predictors of carer–child interactions.
Fig. 2: Relatedness, need and reciprocity and carer–child interactions.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

References

  1. 1.

    Campbell, K. L. & Wood, J. W. in Natural Human Fertility (eds Diggory, P., Teper, S. & Potts, M.) 39–69 (Macmillan Publishing, 1988).

  2. 2.

    Hill, K. & Hurtado, A. M. Cooperative breeding in South American hunter-gatherers. Proc. R. Soc. B Biol. Sci. 276, 3863–3870 (2009).

    Google Scholar 

  3. 3.

    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).

  4. 4.

    Bogin, B., Bragg, J. & Kuzawa, C. Humans are not cooperative breeders but practice biocultural reproduction. Ann. Hum. Biol. 41, 368–380 (2014).

    PubMed  Google Scholar 

  5. 5.

    Meehan, C. L. Allomaternal investment and relational uncertainty among Ngandu farmers of the Central African Republic. Hum. Nat. 19, 211–226 (2008).

    PubMed  Google Scholar 

  6. 6.

    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).

  7. 7.

    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).

  8. 8.

    Hawkes, K. & O’Connell, J. Grandmothering, menopause, and the evolution of human life histories. Proc. Natl Acad. Sci. USA 95, 1336–1339 (1998).

    CAS  PubMed  Google Scholar 

  9. 9.

    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).

    PubMed  Google Scholar 

  10. 10.

    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).

    Google Scholar 

  11. 11.

    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).

    Google Scholar 

  12. 12.

    Snopkowski, K. & Sear, R. Kin influences on fertility in Thailand: effects and mechanisms. Evol. Hum. Behav. 34, 130–138 (2013).

    Google Scholar 

  13. 13.

    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).

    PubMed  Google Scholar 

  14. 14.

    Kramer, K. L. & Veile, A. Infant allocare in traditional societies. Physiol. Behav. 193, 117–126 (2018).

    CAS  PubMed  Google Scholar 

  15. 15.

    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).

    PubMed  Google Scholar 

  16. 16.

    Foster, K. R., Wenseleers, T. & Ratnieks, F. L. W. Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57–60 (2006).

    PubMed  Google Scholar 

  17. 17.

    Rand, D. G. & Nowak, M. A. Human cooperation. Trends Cogn. Sci. 17, 413–425 (2013).

    PubMed  Google Scholar 

  18. 18.

    Clutton-Brock, T. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 (2002).

    CAS  PubMed  Google Scholar 

  19. 19.

    Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964).

    CAS  PubMed  Google Scholar 

  20. 20.

    Ivey, P. K. Cooperative reproduction in Ituri Forest hunter-gatherers: who cares for Efe infants? Curr. Anthropol. 41, 856–866 (2000).

    Google Scholar 

  21. 21.

    Crittenden, A. N. & Marlowe, F. W. Allomaternal care among the Hadza of Tanzania. Hum. Nat. 19, 249–262 (2008).

    PubMed  Google Scholar 

  22. 22.

    Apicella, C. L. & Crittenden, A. N. in The Handbook of Evolutionary Psychology (ed. Buss, D. M.) 1–20 (Wiley, 2013).

  23. 23.

    Chapais, B. in Cooperation in Primates and Humans (eds Kappeler, P. M. & Van Schaik, C. P.) 47–61 (Springer, 2006).

  24. 24.

    Schino, G. & Aureli, F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol. Lett. 13, 45–50 (2010).

    PubMed  Google Scholar 

  25. 25.

    Crittenden, A. N. & Zes, D. A. Food sharing among Hadza hunter-gatherer children. PLoS One 10, e0131996 (2015).

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Lukas, D. & Clutton-Brock, T. Cooperative breeding and monogamy in mammalian societies. Proc. R. Soc. B Biol. Sci. 279, 2151–2156 (2012).

    Google Scholar 

  27. 27.

    Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).

    CAS  PubMed  Google Scholar 

  28. 28.

    Gurven, M. The evolution of contingent cooperation. Curr. Anthropol. 47, 185–192 (2006).

    Google Scholar 

  29. 29.

    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).

    Google Scholar 

  30. 30.

    Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971).

    Google Scholar 

  31. 31.

    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).

    Google Scholar 

  32. 32.

    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).

    CAS  PubMed  Google Scholar 

  33. 33.

    Carter, G. G., Wilkinson, G. S. & Carter, G. G. Food Sharing in Vampire Bats: Reciprocal Help Predicts Donations More Than Relatedness or Harassment (2013).

  34. 34.

    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).

    Google Scholar 

  35. 35.

    Nolin, D. A. Food-sharing networks in Lamalera, Indonesia: reciprocity, kinship, and distance. Hum. Nat. 21, 243–268 (2010).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Koster, J. Interhousehold meat sharing among Mayangna and Miskito horticulturalists in Nicaragua. Hum. Nat. 22, 394–415 (2011).

    PubMed  Google Scholar 

  37. 37.

    Wilkinson, G. S. Reciprocal food sharing in the vampire bat. Nature 308, 181–184 (1984).

    Google Scholar 

  38. 38.

    Gurven, M. Reciprocal altruism and food sharing decisions among Hiwi and Ache hunter–gatherers. Behav. Ecol. Sociobiol. 56, 366–380 (2004).

    Google Scholar 

  39. 39.

    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).

    Google Scholar 

  40. 40.

    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).

    PubMed  Google Scholar 

  41. 41.

    Hames, R. Garden labour exchange among the Yekwana. Ethol. Sociobiol. 8, 259–284 (1987).

    Google Scholar 

  42. 42.

    Thomas, M. G. et al. Kinship underlies costly cooperation in Mosuo villages. R. Soc. Open Sci. 5, 171535 (2018).

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    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).

    CAS  Google Scholar 

  44. 44.

    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).

    CAS  PubMed  Google Scholar 

  45. 45.

    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).

    PubMed  Google Scholar 

  46. 46.

    Jaeggi, A. V. & Gurven, M. Natural cooperators: food sharing in humans and other primates. Evol. Anthropol. 22, 186–195 (2013).

    PubMed  Google Scholar 

  47. 47.

    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).

    CAS  PubMed  Google Scholar 

  48. 48.

    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).

    Google Scholar 

  49. 49.

    Page, A. E. et al. Hunter-gatherer social networks and reproductive success. Sci. Rep. 7, 1153 (2017).

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Dyble, M. et al. Sex equality can explain the unique social structure of hunter-gatherer bands. Science 348, 796–798 (2015).

    CAS  PubMed  Google Scholar 

  51. 51.

    Hill, K. R. et al. Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331, 1286–1289 (2011).

    CAS  PubMed  Google Scholar 

  52. 52.

    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).

    Google Scholar 

  53. 53.

    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).

    Google Scholar 

  54. 54.

    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).

  55. 55.

    Baker, A. J. Evolution of the Social System of the Golden Lion Tamarin (Leontopithecus rosalia) (Univ. Maryland, 1991).

  56. 56.

    Salo, A. L. & French, J. A. Early experience, reproductive success and development of parental behaviour in Mongolian gerbils. Anim. Behav. 38, 693–702 (1989).

    Google Scholar 

  57. 57.

    Zahavi, A. in Cooperative Breeding in Birds: Long Term Studies of Ecology and Behaviour 103–130 (1990).

  58. 58.

    Tardif, S. D. in Cooperative Breeding in Mammals (eds Solomon, N. G. & French, J. A.) 11–33 (Cambridge Univ. Press, 1997).

  59. 59.

    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).

    Google Scholar 

  60. 60.

    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).

    PubMed  PubMed Central  Google Scholar 

  61. 61.

    Kramer, K. L. Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 417–436 (2010).

    Google Scholar 

  62. 62.

    Sear, R. & Coall, D. How much does family matter? Cooperative breeding and the demographic transition. Popul. Dev. Rev. 37, 81–112 (2011).

    PubMed  Google Scholar 

  63. 63.

    Jetz, W. & Rubenstein, D. R. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78 (2011).

    CAS  PubMed  Google Scholar 

  64. 64.

    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).

    Google Scholar 

  65. 65.

    Kokko, H., Johnstone, R. A. & Clutton-Brock, T. H. The evolution of cooperative breeding through group augmentation. Proc. Biol. Sci. 268, 187–196 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Smith, D. et al. Camp stability predicts patterns of hunter-gatherer cooperation. R. Soc. Open Sci. 3, 160131 (2016).

    PubMed  PubMed Central  Google Scholar 

  67. 67.

    Dyble, M., Gardner, A., Vinicius, L. & Migliano, A. B. Inclusive fitness for in-laws. Biol. Lett. 14, 20180515 (2018).

    PubMed  PubMed Central  Google Scholar 

  68. 68.

    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).

    Google Scholar 

  69. 69.

    Barclay, P. Strategies for cooperation in biological markets, especially for humans. Evol. Hum. Behav. 34, 164–175 (2013).

    Google Scholar 

  70. 70.

    Davies, N. B., Krebs, J. R. & West, S. An Introduction to Behavioural Ecology (Wiley-Blackwell, 2012).

  71. 71.

    Fried, J. J. The Role of Juvenile Pine Voles (Microtus pinetorum) in the Caretaking of their Younger Siblings (North Carolina State Univ., 1987).

  72. 72.

    Silk, J. B. Kidnapping and female competition among captive bonnet macaques. Primates 21, 100–110 (1980).

    Google Scholar 

  73. 73.

    Hrdy, S. B. Mothers and Others: The Evolutionary Origins of Mutual Understanding (Harvard Univ. Press, 2009).

  74. 74.

    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).

    Google Scholar 

  75. 75.

    Kramer, K. L., Veile, A. & Otárola-Castillo, E. Sibling competition & growth tradeoffs. Biological vs. statistical significance. PLoS One 11, e0150126 (2016).

    PubMed  PubMed Central  Google Scholar 

  76. 76.

    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).

    Google Scholar 

  77. 77.

    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).

    Google Scholar 

  78. 78.

    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).

    PubMed  Google Scholar 

  79. 79.

    Scelza, B. A. The grandmaternal niche: critical caretaking among Martu Aborigines. Am. J. Hum. Biol. 21, 448–454 (2009).

    PubMed  Google Scholar 

  80. 80.

    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).

    PubMed  Google Scholar 

  81. 81.

    Barclay, P. & Reeve, H. K. The varying relationship between helping and individual quality. Behav. Ecol. 23, 693–698 (2012).

    Google Scholar 

  82. 82.

    Minter, T. The Agta of the Northern Sierra Madre: Livelihood Strategies and Resilience Among Philippine Hunter-Gatherers (Leiden Univ., 2010).

  83. 83.

    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).

    CAS  PubMed  Google Scholar 

  84. 84.

    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).

    PubMed  Google Scholar 

  85. 85.

    Migliano, A. B. et al. Characterization of hunter-gatherer networks and implications for cumulative culture. Nat. Hum. Behav. 1, 0043 (2017).

    Google Scholar 

  86. 86.

    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).

    CAS  PubMed  Google Scholar 

  87. 87.

    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).

    CAS  PubMed  Google Scholar 

  88. 88.

    Isella, L. et al. What’s in a crowd? Analysis of face-to-face behavioral networks. J. Theor. Biol. 271, 166–180 (2011).

    PubMed  Google Scholar 

  89. 89.

    Hewlett, B. S., Lamb, M. E., Leyendecker, B. & Schölmerich, A. in Adaptation and Human Behaviour: an Anthropological Perspective 155–177 (2000).

  90. 90.

    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).

    Google Scholar 

  91. 91.

    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).

    Google Scholar 

  92. 92.

    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).

    Google Scholar 

  93. 93.

    Kramer, K. L. The evolution of human parental care and recruitment of juvenile help. Trends Ecol. Evol. 26, 533–540 (2011).

    PubMed  Google Scholar 

  94. 94.

    Konner, M. in Hunter-Gatherer Childhoods: Cultural, Developmental, & Evolutionary Perspectives (eds Hewlett, B. S. & Lamb, M. E.) 19–64 (Aldine Transaction, 2005).

  95. 95.

    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).

    PubMed  Google Scholar 

  96. 96.

    Gurven, M. To give and to give not: the behavioral ecology of human food transfers. Behav. Brain Sci. 27, 543–583 (2004).

    Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Abigail E. Page.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information: Primary Handling Editor: Stavroula Kousta.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Tables 1–9, Supplementary Figs. 1–3 and Supplementary References.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing