• This record comes from PubMed

Harsh environments promote alloparental care across human societies

. 2020 Aug 26 ; 287 (1933) : 20200758. [epub] 20200819

Language English Country England, Great Britain Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Alloparental care is central to human life history, which integrates exceptionally short interbirth intervals and large birth size with an extended period of juvenile dependency and increased longevity. Formal models, previous comparative research, and palaeoanthropological evidence suggest that humans evolved higher levels of cooperative childcare in response to increasingly harsh environments. Although this hypothesis remains difficult to test directly, the relative importance of alloparental care varies across human societies, providing an opportunity to assess how local social and ecological factors influence the expression of this behaviour. We therefore, investigated associations between alloparental infant care and socioecology across 141 non-industrialized societies. We predicted increased alloparental care in harsher environments, due to the fitness benefits of cooperation in response to shared ecological challenges. We also predicted that starvation would decrease alloparental care, due to prohibitive energetic costs. Using Bayesian phylogenetic multilevel models, we tested these predictions while accounting for potential confounds as well as for population history. Consistent with our hypotheses, we found increased alloparental infant care in regions characterized by both reduced climate predictability and relatively lower average temperatures and precipitation. We also observed reduced alloparental care under conditions of high starvation. These results provide evidence of plasticity in human alloparenting in response to ecological contexts, comparable to previously observed patterns across avian and mammalian cooperative breeders. This suggests convergent social evolutionary processes may underlie both inter- and intraspecific variation in alloparental care.

See more in PubMed

Jaeggi AV, Gurven M. 2013. Natural cooperators: food sharing in humans and other primates. Evol. Anthropol. 22, 186–195. (10.1002/evan.21364) PubMed DOI

Kramer KL. 2010. Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 417–436. (10.1146/annurev.anthro.012809.105054) DOI

Boyd R, Richerson PJ, Henrich J. 2011. The cultural niche: why social learning is essential for human adaptation. Proc. Natl Acad. Sci. USA 108, 10 918–10 925. (10.1073/pnas.1100290108) PubMed DOI PMC

Tomasello M, et al. 2012. Two key steps in the evolution of human cooperation: the interdependence hypothesis. Curr. Anthropol. 53, 673–692. (10.1086/668207) DOI

Hooper PL, Demps K, Gurven M, Gerkey D, Kaplan HS. 2015. Skills, division of labour and economies of scale among Amazonian hunters and South Indian honey collectors. Phil. Trans. R. Soc. B 370, 20150008 (10.1098/rstb.2015.0008) PubMed DOI PMC

Gurven M, Hill K. 2009. Why do men hunt? A reevaluation of ‘man the hunter’ and the sexual division of labor. Curr. Anthropol. 50, 51–74. (10.1086/595620) PubMed DOI

Hill KR, et al. 2011. Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331, 1286–1289. (10.1126/science.1199071) PubMed DOI

Ross CT, Hooper PL, Borgerhoff Mulder M. 2015. Data on the frequency of non-reproductive adults in a cross-cultural sample of small-scale human societies. bioRxiv 032318 (10.1101/032318) DOI

Burkart JM, et al. 2014. The evolutionary origin of human hyper-cooperation. Nat. Commun. 5, ncomms5747 (10.1038/ncomms5747) PubMed DOI

Miller IF, Churchill SE, Nunn CL. 2019. Speeding in the slow lane: phylogenetic comparative analyses reveal that not all human life history traits are exceptional. J. Hum. Evol. 130, 36–44. (10.1016/j.jhevol.2018.12.007) PubMed DOI

Kaplan H, Hill K, Lancaster J, Hurtado AM. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. 9, 156–185. (10.1002/1520-6505(2000)9:4<156::AID-EVAN5>3.0.CO;2-7) DOI

Isler K, Van Schaik CP. 2012. How our ancestors broke through the gray ceiling: comparative evidence for cooperative breeding in early homo. Curr. Anthropol. 53, S453–S465. (10.1086/667623) DOI

Kaplan H, Gurven M, Hill K, Hurtado AM. 2005. The natural history of human food sharing and cooperation: a review and a new multi-individual approach to the negotiation of norms. In Moral sentiments and material interests: the foundations of cooperation in economic life, pp. 75–113. Cambridge, MA: MIT Press.

Hewlett BS, Winn S. 2014. Allomaternal nursing in humans. Curr. Anthropol. 55, 200–229. (10.1086/675657) PubMed DOI

Kramer KL, Veile A. 2018. Infant allocare in traditional societies. Physiol. Behav. 193, 117–126. (10.1016/j.physbeh.2018.02.054) PubMed DOI

Meehan CL. 2009. Maternal time allocation in two cooperative childrearing societies. Hum. Nat. 20, 375–393. (10.1007/s12110-009-9076-2) DOI

Meehan CL, Quinlan R, Malcom CD. 2013. Cooperative breeding and maternal energy expenditure among Aka foragers. Am. J. Hum. Biol. 25, 42–57. (10.1002/ajhb.22336) PubMed DOI

Isler K, Van Schaik CP. 2014. How humans evolved large brains: comparative evidence. Evol. Anthropol. 23, 65–75. (10.1002/evan.21403) PubMed DOI

Quinlan RJ. 2008. Human pair-bonds: evolutionary functions, ecological variation, and adaptive development. Evol. Anthropol. 17, 227–238. (10.1002/evan.20191) DOI

Hrdy SB. 2009. Mothers and others. Cambridge, MA: Harvard University Press.

Gurven M, Kaplan H, Gutierrez M. 2006. How long does it take to become a proficient hunter? Implications for the evolution of extended development and long life span. J. Hum. Evol. 51, 454–470. (10.1016/j.jhevol.2006.05.003) PubMed DOI

Emmott EH, Page AE. 2019. Alloparenting. In Encyclopedia of evolutionary psychological science (eds Shackelford T, Weekes-Shackelford V). Cham, Switzerland: Springer.

Antón SC, Potts R, Aiello LC. 2014. Evolution of early Homo: an integrated biological perspective. Science 345, 1236828 (10.1126/science.1236828) PubMed DOI

Potts R. 2013. Hominin evolution in settings of strong environmental variability. Quat. Sci. Rev. 73, 1–13. (10.1016/j.quascirev.2013.04.003) DOI

Wynn JG. 2004. Influence of Plio-Pleistocene aridification on human evolution: evidence from paleosols of the Turkana Basin, Kenya. Am. J. Phys. Anthropol. 123, 106–118. (10.1002/ajpa.10317) PubMed DOI

Maslin MA, Susanne S, Martin HT. 2015. A synthesis of the theories and concepts of early human evolution. Phil. Trans. R. Soc. B 370, 20140064 (10.1098/rstb.2014.0064) PubMed DOI PMC

Owen RB, et al. 2018. Progressive aridification in East Africa over the last half million years and implications for human evolution. Proc. Natl Acad. Sci. USA 115, 11 174–11 179. (10.1073/pnas.1801357115) PubMed DOI PMC

Pereda M, Zurro D, Santos JI, Godino IB, Álvarez M, Caro J, Galán JM. 2017. Emergence and evolution of cooperation under resource pressure. Sci. Rep. 7, 45574 (10.1038/srep45574) PubMed DOI PMC

Smaldino PE, Schank JC, McElreath R. 2013. Increased costs of cooperation help cooperators in the long run. Am. Nat. 181, 451–463. (10.1086/669615) PubMed DOI

Smaldino PE, Newson L, Schank JC, Richerson PJ. 2013. Simulating the evolution of the human family: Cooperative breeding increases in harsh environments. PLoS ONE 8, e80753 (10.1371/journal.pone.0080753) PubMed DOI PMC

Shen SF, Emlen ST, Koenig WD, Rubenstein DR. 2017. The ecology of cooperative breeding behaviour. Ecol. Lett. 20, 708–720. (10.1111/ele.12774) PubMed DOI

Mesterton-Gibbons M, Dugatkin LA. 1992. Cooperation among unrelated individuals: evolutionary factors. Q Rev. Biol. 67, 267–281. (10.1086/417658) DOI

Green JP, Freckleton RP, Hatchwell BJ. 2016. Variation in helper effort among cooperatively breeding bird species is consistent with Hamilton's Rule. Nat. Commun. 7, 12663 (10.1038/ncomms12663) PubMed DOI PMC

Briga M, Pen I, Wright J. 2012. Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny. Biol. Lett. 8, 533–536. (10.1098/rsbl.2012.0159) PubMed DOI PMC

Komdeur J. 1992. Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358, 493–495. (10.1038/358493a0) DOI

Rubenstein DR, Lovette IJ. 2007. Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414–1419. (10.1016/j.cub.2007.07.032) PubMed DOI

Lin YH, Chan SF, Rubenstein DR, Liu M, Shen SF. 2019. Resolving the paradox of environmental quality and sociality: the ecological causes and consequences of cooperative breeding in two lineages of birds. Am. Nat. 194, 207–216. (10.1086/704090) PubMed DOI

Jetz W, Rubenstein DR. 2011. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78. (10.1016/j.cub.2010.11.075) PubMed DOI

Cornwallis CK, Botero CA, Rubenstein DR, Downing PA, West SA, Griffin AS. 2017. Cooperation facilitates the colonization of harsh environments. Nat. Ecol. Evol. 1, 0057 (10.1038/s41559-016-0057) PubMed DOI

Lukas D, Clutton-Brock T. 2017. Climate and the distribution of cooperative breeding in mammals. R. Soc. Open Sci. 4, 160897 (10.1098/rsos.160897) PubMed DOI PMC

Roberts G. 2005. Cooperation through interdependence. Anim. Behav. 70, 901–908. (10.1016/j.anbehav.2005.02.006) DOI

Clutton-Brock T. 2002. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72. (10.1126/science.296.5565.69) PubMed DOI

Kokko H, Johnstone RA. 2001. The evolution of cooperative breeding through group augmentation. Proc. R. Soc. B 268, 187–196. (10.1098/rspb.2000.1349) PubMed DOI PMC

Covas R, Doutrelant C, du Plessis MA. 2004. Experimental evidence of a link between breeding conditions and the decision to breed or to help in a colonial cooperative bird. Proc. R. Soc. B 271, 827–832. (10.1098/rspb.2003.2652) PubMed DOI PMC

Baglione V, Canestrari D, Marcos JM, Griesser M, Ekman J. 2002. History, environment and social behaviour: experimentally induced cooperative breeding in the carrion crow. Proc. R. Soc. B 269, 1247–1251. (10.1098/rspb.2002.2016) PubMed DOI PMC

Guindre-Parker S, Rubenstein DR. 2018. Multiple benefits of alloparental care in a fluctuating environment. R. Soc. Open Sci. 5, 172406 (10.1098/rsos.172406) PubMed DOI PMC

Hawkes K, Coxworth JE. 2013. Grandmothers and the evolution of human longevity: a review of findings and future directions. Evol. Anthrop. 22, 294–302. (10.1002/evan.21382) PubMed DOI

Sear R, Mace R. 2008. Who keeps children alive? A review of the effects of kin on child survival. Evol. Hum. Behav. 29, 1–18. (10.1016/j.evolhumbehav.2007.10.001) DOI

Kramer KL. 2014. Why what juveniles do matters in the evolution of cooperative breeding. Hum. Nat. 25, 49–65. (10.1007/s12110-013-9189-5) PubMed DOI

Quinlan RJ. 2006. Human parental effort and environmental risk. Proc. R. Soc. B 274, 121–125. (10.1098/rspb.2006.3690) PubMed DOI PMC

Jaeggi AV, Hooper PL, Beheim BA, Kaplan H, Gurven M. 2016. Reciprocal exchange patterned by market forces helps explain cooperation in a small-scale society. Curr. Biol. 26, 2180–2187. (10.1016/j.cub.2016.06.019) PubMed DOI

Page AE, et al. 2019. Testing adaptive hypotheses of alloparenting in Agta foragers. Nat. Hum. Behav. 3, 1154–1163. (10.1038/s41562-019-0679-2) PubMed DOI PMC

Murdock GP, White DR. 1969. Standard cross-cultural sample. Ethnology 8, 329–369. (10.2307/3772907) DOI

Barry H III, Paxson LM. 1971. Infancy and early childhood: cross-cultural codes 2. Ethnology 10, 466–508. (10.2307/3773177) DOI

Kirby KR, et al. 2016. D-PLACE: a global database of cultural, linguistic and environmental diversity. PLoS ONE 11, e0158391 (10.1371/journal.pone.0158391) PubMed DOI PMC

Dufour DL, Sauther ML. 2002. Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. Am. J. Hum. Biol. 14, 584–602. (10.1002/ajhb.10071) PubMed DOI

Konner M. 2018. Nonmaternal care: a half-century of research. Physiol. Behav. 193, 179–186. (10.1016/j.physbeh.2018.03.025) PubMed DOI

Colwell RK. 1974. Predictability, constancy, and contingency of periodic phenomena. Ecology 1, 1148–1153. (10.2307/1940366) DOI

Lima-Ribeiro MS, Varela S, González-Hernández J, de Oliveira G, Diniz-Filho JAF, Terribile LC. 2015. EcoClimate: a database of climate data from multiple models for past, present, and future for macroecologists and biogeographers. Biodivers. Inform. 10, 1–21.

Revell LJ. 2009. Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258–3268. (10.1111/j.1558-5646.2009.00804.x) PubMed DOI

Jackson JE. 2005. Quartimax Rotation. In Encyclopedia of biostatistics (eds Armitrage P, Colton T). Hoboken, NJ: John Wiley & Sons.

Dirks R. 1993. Starvation and famine: cross-cultural codes and some hypothesis tests. Cross-Cult. Res. 27, 28–69. (10.1177/106939719302700103) DOI

Murdock GP, Provost C. 1973. Measurement of cultural complexity. Ethnology 12, 379–392. (10.2307/3773367) DOI

Page AE, et al. 2016. Reproductive trade-offs in extant hunter-gatherers suggest adaptive mechanism for the Neolithic expansion. Proc. Natl Acad. Sci. USA 113, 4694–4699. (10.1073/pnas.1524031113) PubMed DOI PMC

Murdock GP, Morrow DO. 1970. Subsistence economy and supportive practices: cross-cultural codes 1. Ethnology 9, 302–330. (10.2307/3773028) DOI

Ringen EJ, Duda P, Jaeggi AV. 2019. The evolution of daily food sharing: a Bayesian phylogenetic analysis. Evol. Hum. Behav. 40, 375–384. (10.1016/j.evolhumbehav.2019.04.003) DOI

Barry H, Schlegel A. 1982. Cross-cultural codes on contributions by women to subsistence. Ethnology 21, 165–188. (10.2307/3773435) DOI

Low BS. 1994. Pathogen intensity cross-culturally. World Cult. 8, 24–34.

Olson DM, et al. 2001. Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51, 933–938. (10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2) DOI

Heldstab SA, Isler K, Burkart JM, van Schaik CP. 2019. Allomaternal care, brains and fertility in mammals: who cares matters. Behav. Ecol. Sociobiol. 73, 71 (10.1007/s00265-019-2684-x) DOI

Duda P, Zrzavý J. 2016. Human population history revealed by a supertree approach. Sci. Rep. 6, 29890 (10.1038/srep29890) PubMed DOI PMC

Duda P, Zrzavý J. 2019. Towards a global phylogeny of human populations based on genetic and linguistic data. In Modern human origins and dispersal, words, bones, genes, tools: DFG center for advanced studies series (eds Sahle Y, Reyes-Centeno H, Bentz C), pp. 331–359. Tübingen, Germany: Kerns Verlag.

Minocher R, Duda P, Jaeggi AV. 2019. Explaining marriage patterns in a globally representative sample through socio-ecology and population history: a Bayesian phylogenetic analysis using a new supertree. Evol. Hum. Behav. 40, 176–187. (10.1016/j.evolhumbehav.2018.11.003) DOI

Blows MW, Brooks R. 2003. Measuring nonlinear selection. Am. Nat. 162, 815–820. (10.1086/378905) PubMed DOI

Myers RH, Montgomery DC, Anderson-Cook CM. 2016. Response surface methodology: process and product optimization using designed experiments, 4th edn Hoboken, NJ: John Wiley & Sons.

Bürkner PC. 2017. brms: An R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28. (10.18637/jss.v080.i01) DOI

Hadfield JD, Nakagawa S. 2010. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508. (10.1111/j.1420-9101.2009.01915.x) PubMed DOI

McElreath R. 2016. Statistical rethinking: a Bayesian course with examples in R and stan. Boca Raton, FL: CRC Press.

Bürkner PC, Charpentier E. In press. Modelling monotonic effects of ordinal predictors in Bayesian regression models. Br. J. Math. Statist. Psychol. (10.1111/bmsp.12195) PubMed DOI

Gelman A, Carlin JB, Stern HS, Dunson DB, Vehtari A, Rubin DB. 2013. Bayesian data analysis. Boca Raton, FL: CRC Press.

McShane BB, Gal D, Gelman A, Robert C, Tackett JL. 2019. Abandon statistical significance. Am. Stat. 73, 235–245. (10.1080/00031305.2018.1527253) DOI

Gelman A, Hwang J, Vehtari A. 2014. Understanding predictive information criteria for Bayesian models. Stat. Comput. 24, 997–1016. (10.1007/s11222-013-9416-2) DOI

Ember CR, Skoggard I, Ringen EJ, Farrer M. 2018. Our better nature: does resource stress predict beyond-household sharing? Evol. Hum. Behav. 39, 380–391. (10.1016/j.evolhumbehav.2018.03.001) DOI

Glowacki L, von Rueden C. 2015. Leadership solves collective action problems in small-scale societies. Phil. Trans. R. Soc. B 370, 20150010 (10.1098/rstb.2015.0010) PubMed DOI PMC

Botero CA, Gardner B, Kirby KR, Bulbulia J, Gavin MC, Gray RD. 2014. The ecology of religious beliefs. Proc. Natl Acad. Sci. USA 111, 16 784–16 789. (10.1073/pnas.1408701111) PubMed DOI PMC

Schiefenhovel W. 1989. Reproduction and sex-ratio manipulation through preferential female infanticide among the Eipo, in the Highlands of Western New Guinea. In The sociobiology of sexual and reproductive strategies (eds Rasa AE, Vogel C, Voland E), pp. 170–193. New York, NY: Chapman and Hall.

Firman RC, Rubenstein DR, Moran JM, Rowe KC, Buzatto BA. 2020. Extreme and variable climatic conditions drive the evolution of sociality in Australian Rodents. Curr. Biol. 30, 691–697. (10.1016/j.cub.2019.12.012) PubMed DOI

Peters MK, et al. 2016. Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level. Nat. Commun. 7, 1–11. PubMed PMC

Tallavaara M, Eronen JT, Luoto M. 2018. Productivity, biodiversity, and pathogens influence the global hunter-gatherer population density. Proc. Natl Acad. Sci. USA 115, 1232–1237. (10.1073/pnas.1715638115) PubMed DOI PMC

Griesser M, Drobniak SM, Nakagawa S, Botero CA. 2017. Family living sets the stage for cooperative breeding and ecological resilience in birds. PLoS Biol. 15, e2000483 (10.1371/journal.pbio.2000483) PubMed DOI PMC

Rubenstein DR, Abbot P (Eds.) 2017. Comparative social evolution. Cambridge, UK: Cambridge University Press.

Bourke AF. 2011. Principles of social evolution. Oxford, UK: Oxford University Press.

Burkart JM, van Schaik C, Griesser M. 2017. Looking for unity in diversity: human cooperative childcare in comparative perspective. Proc. R. Soc. B 284, 20171184 (10.1098/rspb.2017.1184) PubMed DOI PMC

See more in PubMed

figshare
10.6084/m9.figshare.c.5089508

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...