Abstract
The aim of this study is to explain the occurrence of food sharing across primates. Defined as the unresisted transfer of food, evolutionary hypotheses have to explain why possessors should relinquish food rather than keep it. While sharing with offspring can be explained by kin selection, explanations for sharing among unrelated adults are more controversial. Here we test the hypothesis that sharing occurs with social partners that have leverage over food possessors due to the opportunity for partner choice in other contexts. Thus, we predict that possessors should relinquish food to potential mates or allies, who could provide or withhold matings or coalitionary support in the future. We used phylogenetic analyses based on both maximum likelihood and Bayesian approaches in a sample of 68 primate species to test these predictions. The analyses strongly indicate that (1) sharing with offspring is predicted by the relative processing difficulty of the diet, as measured by the degree of extractive foraging, but not overall diet quality, (2) food sharing among adults only evolved in species already sharing with offspring, regardless of diet, and (3) male–female sharing co-evolved with the opportunity for female mate choice and sharing within the sexes with coalition formation. These results provide comparative support for the hypothesis that sharing is “traded” for matings and coalitionary support in the sense that these services are statistically associated and can thus be selected for. Based on this, we predict that sharing should occur in any species with opportunities for partner choice.
This is a preview of subscription content, access via your institution.




Notes
Other hypotheses explaining sharing in humans or other animals such as costly signaling are not discussed here because there is no convincing evidence supporting them in primates.
References
Amat JA (2000) Courtship feeding, food sharing, or tolerated food theft among paired red-crested pochards (Netta rufina)? J Ornithol 141:327–334
Aureli F, Schaffner CM, Verpooten J, Slater K, Ramos-Fernandez G (2006) Raiding parties of male spider monkeys: insights into human warfare? Am J Phys Anthropol 131:486–497
Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512
Blurton Jones NG (1984) A selfish origin for human food sharing: tolerated theft. Ethol Sociobiol 5:1–3
Blurton Jones NG (1987) Tolerated theft: suggestions about the ecology and evolution of sharing, hoarding, and scrounging. Soc Sci Inf 26:31–54
Bowler M, Bodmer M (2009) Social behavior in fission–fusion groups of red uakari monkeys (Cacajao calvus ucayalii). Am J Primatol 71:976–987
Brandon-Jones D, Eudey AA, Geissmann T, Groves CP, Melnick DJ, Morales JC, Shekelle M, Stewart CB (2004) Asian primate classification. Int J Primatol 25:97–164
Brown GR, Almond REA, Van Bergen Y (2004) Begging, stealing, and offering: food transfer in nonhuman primates. Advances in the Study of Behavior 34:265–295
Cashdan EA (1997) Comment on Bliege bird and bird: delayed reciprocity and tolerated theft. Curr Anthropol 38:69–70
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Clutton-Brock TH (2009) Cooperation between non-kin in animal societies. Nature 462:51–57
Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84:3–27
Connor RC (2007) Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Philosophical Transactions of the Royal Society B: Biological Sciences 362:587–602
Connor RC, Mann J, Tyack PL, Whitehead H (1998) Social evolution in toothed whales. Trends Ecol Evol 13:228–232
Cords M (1997) Friendships, alliances, reciprocity and repair. In: Whiten A, Byrne RW (eds) Machiavellian intelligence II: extensions and evaluations. Cambridge University Press, Cambridge, pp 24–49
de Waal FBM (1989) Food sharing and reciprocal obligations among chimpanzees. J Hum Evol 18:433–459
de Waal FBM (1997) The chimpanzee's service economy: food for grooming. Evol Hum Behav 18:375–386
de Waal FBM (2000) Attitudinal reciprocity in food sharing among brown capuchin monkeys. Anim Behav 60:253–261
East ML, Hofer H (1991) Loud calling in a female-dominated mammalian society: II. Behavioural contexts and functions of whooping of spotted hyaenas, Crocuta crocuta. Anim Behav 42:651–669
Emery NJ, Seed AM, von Bayern AMP, Clayton NS (2007) Cognitive adaptations of social bonding in birds. Philosophical Transactions of the Royal Society B-Biological Sciences 362:489–505
Feistner ATC, McGrew WC (1989) Food-sharing in primates: a critical review. In: Seth PK, Seth S (eds) Perspectives in primate biology, vol 3. Today and Tomorrow's, New Delhi, pp 21–36
Fish JL, Lockwood CA (2003) Dietary constraints on encephalization in primates. Am J Phys Anthropol 120:171–181
Forss SIF, van Noordwijk MA, Jaeggi AV, Meulman EM, van Schaik CP (2009) Social construction of the feeding niche in orang-utans: a comparative study. Folia Primatol 80:117–118
Fragaszy DM, Mason WA (1983) Comparisons of feeding behavior in captive squirrel and titi monkeys (Saimiri sciureus and Callicebus moloch). J Comp Psychol 97:310–326
Gibson KR (1986) Cognition, brain size and the extraction of embedded food resources. In: Else J, Lee PC (eds) Primate ontogeny, cognition and social behaviour. Cambridge University Press, Cambridge
Gilby IC (2006) Meat sharing among the Gombe chimpanzees: harassment and reciprocal exchange. Anim Behav 71:953–963
Gilby IC, Emery Thompson M, Ruane JD, Wrangham RW (2010) No evidence of short-term exchange of meat for sex among chimpanzees. J Hum Evol 59:44–53
Gomes CM, Boesch C (2009) Wild chimpanzees exchange meat for sex on a long-term basis. PLoS One 4:e5116
Gomes CM, Mundry R, Boesch C (2009) Long-term reciprocation of grooming in wild West African chimpanzees. Proceedings of the Royal Society B-Biological Sciences 276:699–706
Groves CP (2001) Primate Taxonomy. Smithsonian Institution Press, Washington DC
Grueter CC (2009) Determinants of modular societies in snub-nosed monkeys (Rhinopithecus bieti) and other Asian colobines. Ph.D. thesis, University of Zurich, Zurich
Grueter CC, van Schaik CP (2009) Sexual size dimorphism in Asian colobines revisited. Am J Primatol 71:609–616
Guinet C, Barrett-Lennard LG, Loyer B (2000) Co-ordinated attack behavior and prey sharing by killer whales at Crozet archipelago: strategies for feeding on negatively-buoyant prey. Marine Mammal Science 16:829–834
Gurven M (2004) To give and to give not: the behavioral ecology of human food transfers. Behav Brain Sci 27:543–583
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
Hamilton WD (1964) Genetical evolution of social behaviour I. J Theor Biol 7:1–16
Hamilton WJ, Bulger J (1992) Facultative expression of behavioral differences between one-male and multimale savanna baboon groups. Am J Primatol 28:61–71
Harding RSO (1981) An order of omnivores: nonhuman primate diets in the wild. In: Harding RSO, Teleki G (eds) Omnivorous primates: gathering and hunting in human evolution. Columbia University Press, New York, pp 191–214
Hawkes K (1993) Why hunter–gatherers work—an ancient version of the problem of public goods. Curr Anthropol 34:341–361
Heinrich B (1988a) Food sharing in the raven, Corvus corax. In: Slobodchikoff CN (ed) The ecology of social behavior. Academic, San Diego, pp 285–311
Heinrich B (1988b) Winter foraging at carcasses by 3 sympatric corvids, with emphasis on recruitment by the raven, Corvus corax. Behav Ecol Sociobiol 23:141–156
Hill K, Kaplan H (1993) On why male foragers hunt and share food. Curr Anthropol 34:701–706
Hockings KJ, Humle T, Anderson JR, Biro D, Sousa C, Ohashi G, Matsuzawa T (2007) Chimpanzees share forbidden fruit. PLoS ONE 2:886 (online 1–4)
Hoelzel AR (1991) Killer whale predation on marine mammals at Punta Norte, Argentina—food sharing, provisioning and foraging strategy. Behav Ecol Sociobiol 29:197–204
Hohmann G, Fruth B (2008) New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Folia Primatol 79:103–110
Hrdy SB (1999) Mother Nature: maternal instincts and how they shape the human species. Ballantine Books, New York
Hrdy S (2009) Mothers and others: the evolutionary origins of mutual understanding. Harvard University Press, Cambridge
Jaeggi AV, Burkart JM, van Schaik CP (2010a) On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality. Philosophical Transactions of the Royal Society B-Biological Sciences 365:2723–2735
Jaeggi AV, Dunkel LP, van Noordwijk MA, Wich SA, Sura AAL, van Schaik CP (2010b) Social learning of diet and foraging skills among wild immature Bornean orangutans (Pongo pygmaeus wurmbii): implications for culture. Am J Primatol 72:62–71
Jaeggi AV, Stevens JMG, van Schaik CP (2010c) Tolerant food sharing and reciprocity is precluded by despotism in bonobos but not chimpanzees. Am J Phys Anthropol 143:41–51
Johnson RH (1982) Food-sharing behavior in captive Amazon River dolphins (Inia geoffrensis). Cetology 43:1–3
Kaplan H, Gurven M (2005) The natural history of human food sharing and cooperation: a review and a new multi-individual approach to the negotiation of norms. In: Gintis H, Bowles S, Boyd R, Fehr E (eds) Moral sentiments and material interests: the foundations of cooperation in economic life. MIT, Cambridge, pp 75–113
Kaplan H, Hill K (1985) Food sharing among Ache foragers: tests of explanatory hypotheses. Curr Anthropol 26:223–246
Kaplan HS, Hooper PL, Gurven M (2009) The evolutionary and ecological roots of human social organization. Philosophical Transactions of the Royal Society B-Biological Sciences 364:3289–3299
Kavanagh M (1972) Food-sharing behavior within a group of douc monkeys (Pygathrix nemaeus nemaeus). Nature 239:406–407
Kawanaka K (1982) Further studies on predation by chimpanzees of the Mahale Mountains. Primates 23:364–384
Keddy-Hector AC (1992) Mate choice in non-human primates. Am Zool 32:62–70
Launhardt K, Borries C, Hardt C, Epplen JT, Winkler P (2001) Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar. Anim Behav 61:53–64
Lorenz K (1965) Evolution and the modification of behavior. Chicago University Press, Chicago
Marlowe FW (2004) What explains Hadza food sharing? Res Econ Anthropol 23:69–88
Mas F, Kölliker M (2008) Maternal care and offspring begging in social insects: chemical signalling, hormonal regulation and evolution. Anim Behav 76:1121–1131
Massen JJM, Sterck EHM, de Vos H (2010) Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour 147:1379–1412
Mitani JC (2006) Reciprocal exchange in chimpanzees and other primates. In: Kappeler PM, van Schaik CP (eds) Cooperation in primates and humans: mechanisms and evolution. Springer, New York, pp 107–119
Mitani JC, Watts DP (2001) Why do chimpanzees hunt and share meat? Anim Behav 61:915–924
Nettelbeck AR (1998) Observations on food sharing in wild lar gibbons (Hylobates lar). Folia Primatol 69:386–391
Nishida T, Hasegawa T, Hayaki H, Takahata Y, Uehara S (1992) Meat-sharing as a coalition strategy by an alpha male chimpanzee? In: Nishida T, McGrew WC, Marler P, Pickford M, De Waal FBM (eds) Topics in primatology, vol 1, Human origins. University of Tokyo Press, Tokyo, pp 159–174
Noë R, Hammerstein P (1995) Biological markets. Trends Ecol Evol 10:336–339
Noë R, Sluijter A (1995) Which adult male savanna baboons form coalitions? Int J Primatol 16:77–105
Pagel M, Meade A (2011) Bayes traits, 1.0 edn. Reading Evolutionary Biology Group, www.evolution.rdg.ac.uk
Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167:808–825
Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53:673–684
Paradis E (2006) Analysis of phylogenetics and evolution with R. Springer, New York
Paradis E, Bolker BM, Claude J, Cuong HS, Desper R, Durand B, Dutheil J, Gascuel O, Jobb G, Heibl C, Lawson D, Lefort V, Legendre P, Lemon J, Noel Y, Nylander J, Opgen-Rhein R, Strimmer K, de Vienne D (2009) Analyses of phylogenetics and evolution. Institut de recherche pour le développement, Montpellier. http://ape.mpl.ird.fr/
Perry S, Rose L (1994) Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus. Primates 35:409–415
Plavcan JM, van Schaik CP, Kappeler PM (1995) Competition, coalitions and canine size in primates. J Hum Evol 28:245–276
Poole JH, Moss CJ (2008) Elephant sociality and complexity: the scientific evidence. In: Wemmer C, Christen K (eds) Elephants and ethics: towards a morality of coexistence. Johns Hopkins University Press, Baltimore
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rapaport LG, Brown GR (2008) Social influences on foraging behaviour in young nonhuman primates: learning what, where and how to eat. Evolutionary Anthropology 17:189–201
Rowe N (1996) The pictorial guide to the living primates. Pogonias, Charlestown
Scheid C, Schmidt J, Noë R (2008) Distinct patterns of food offering and co-feeding in rooks. Anim Behav 76:1701–1707
Schessler T, Nash LT (1977) Food sharing among captive gibbons (Hylobates lar). Primates 18:677–689
Schino G (2007) Grooming and agonistic support: a meta-analysis of primate reciprocal altruism. Behav Ecol 18:115–120
Schino G, Aureli F (2009) Reciprocal altruism in primates: partner choice, cognition, and emotions. Advances in the Study of Behavior 39:45–69
Silk JB (2002) Using the ‘F’-word in primatology. Behaviour 139:421–446
Slocombe KE, Newton-Fisher NE (2005) Fruit sharing between wild adult chimpanzees (Pan troglodytes schweinfurthii): a socially significant event? Am J Primatol 65:385–391
Stanford CB (1999) The hunting apes: meat eating and the origins of human behavior. Princeton University Press, Princeton
Stevens JR (2004) The selfish nature of generosity: harassment and food sharing in primates. Proceedings of the Royal Society of London Series B-Biological Sciences 271:451–456
Stevens JR, Gilby IC (2004) A conceptual, framework for nonkin food sharing: timing and currency of benefits. Anim Behav 67:603–614
Stevens JR, Hauser MD (2004) Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn Sci 8:60–65
Stevens JR, Stephens DW (2002) Food sharing: a model of manipulation by harassment. Behav Ecol 13:393–400
Strum SC (1975) Primate predation: interim report on the development of a tradition in a troop of olive baboons. Science 187:755–757
Strum SC (1981) Processes and products of change: baboon predatory behavior at Gilgil, Kenya. In: Harding RSO, Teleki G (eds) Omnivorous primates: gathering and hunting in human evolution. Columbia University Press, New York, pp 255–302
Tinbergen N (1952) “Derived” activities; their causation, biological significance, origin, and emancipation during evolution. Q Rev Biol 27:1–32
Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New York
Trivers RL (1971) Evolution of reciprocal altruism. Q Rev Biol 46:35–57
Utami SS, van Hooff JARAM (1997) Meat-eating by adult female Sumatran orangutans (Pongo pygmaeus abelii). Am J Primatol 43:159–165
Vahed K (1998) The function of nuptial feeding in insects: review of empirical studies. Biol Rev 73:43–78
van Noordwijk MA, van Schaik CP (2009) Intersexual food transfer among orangutans: do females test males for coercive tendency? Behav Ecol Sociobiol 63:883–890
van Schaik CP, van Hooff JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85:91–117
van Schaik CP, Fox EA, Sitompul AF (1996) Manufacture and use of tools in wild Sumatran orangutans—implications for human evolution. Naturwissenschaften 83:186–188
von Bayern AMP, de Kort SR, Clayton NS, Emery NJ (2007) The role of food- and object-sharing in the development of social bonds in juvenile jackdaws (Corvus monedula). Behaviour 144:711–733
Watts DP (2002) Reciprocity and interchange in the social relationships of wild male chimpanzees. Behaviour 139:343–370
White F (1994) Food sharing in wild pygmy chimpanzees (Pan paniscus). In: Roeder JJ, Thierry B, Anderson JR, Herrenschmidt N (eds) Current primatology, vol II, Social development, learning and behavior. Université Louis Pasteur, Strasbourg, pp 1–10
Wolovich CK, Feged A, Evans S, Green SM (2006) Social patterns of food sharing in monogamous owl monkeys. Am J Primatol 68:663–674
Wolovich CK, Evans S, French JA (2008a) Dads do not pay for sex but do buy the milk: food sharing and reproduction in owl monkeys (Aotus spp.). Anim Behav 75:1155–1163
Wolovich CK, Perea-Rodriguez JP, Fernandez-Duque E (2008b) Food transfers to young and mates in wild owl monkeys (Aotus azarai). Am J Primatol 70:211–221
Ydenberg RC (1994) The behavioral ecology of provisioning in birds. Ecoscience 1:1–14
Yeager C, Kirkpatrick R (1998) Asian colobine social structure: ecological and evolutionary constraints. Primates 39:147–155
Zahavi A (1990) Arabian babblers: the quest for social status in a cooperative breeder. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge, pp 103–130
Zhang Z, Su YJ, Chan RCK, Reimann G (2008) A preliminary study of food transfer in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Am J Primatol 70:148–152
Acknowledgements
The authors would like to thank Michael Gurven, Karin Isler, Charles Nunn, Gabrielle Russo, Maria van Noordwijk, Janneke van Woerden, the UCSB’s Human Behavioral Ecology Lab, and several anonymous reviewers for discussions and many helpful comments on earlier versions of the manuscript. We also thank Charles Nunn for sharing parts of his forthcoming book “The comparative method in evolutionary anthropology and biology”, which was highly informative for the methods used in this study. Finally, we are very grateful to the Swiss National Science Foundation (grant PBZHP3-133433), the Cogito Foundation (grant S-106/06), and the A.H. Schultz Foundation for financial support to AJ. The authors declare no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Nunn
Electronic supplementary material
Below is the link to the electronic supplementary material.
Online resource 1
Following Pagel and Meade (2006), we plotted the posterior distributions of rate coefficients, i.e., estimated probabilities (q) for evolutionary transitions between states (see Fig. 3). Rate pairs, i.e., the probabilities of gains or losses of one trait in the presence or absence of the other trait, were arranged vertically for easy comparison. Differences between rate pairs provide evidence for correlated evolution, e.g., pairs q13 and q24, which correspond to gains of food sharing with and without another trait of interest. The graphs represent (a) sharing among adults, sharing with infants, (b) sharing from males to females, multi–male groups, (c) sharing among males, male–male coalitions, (d) sharing among unrelated males, male–male coalitions, (e) sharing among females, female–female coalitions, and (f) sharing among unrelated females, female–female coalitions. The written values are the mean ± SD values of q as well as the percentage of models that estimated q to zero (“zero bin”) and are based on six runs for each model (PDF 602 kb)
Online resource 2
This table provides an overview of the harmonic means and the resulting Bayes factors for each analysis across different settings of the rate deviation parameter. The settings that were reported, based on the recommended range of acceptance (0.2–0.4) and visual inspection of the plotted Markov chains to confirm convergence (available on request), are indicated in bold. Each analysis was run six times with each setting and the reported values are means and standard deviations of these six runs. Mean harmonic means for the same model never differ by more than 1 across different parameter settings, differences tend to follow the same direction for dependent and independent models, and the resulting Bayes factors are always, and most often substantially, greater than 2 and thus consistently provide support for dependent evolution despite some variation within and across parameter settings (PDF 82 kb)
Online resource 3
These graphs present the mean harmonic mean of six runs of dependent and independent models, respectively, plotted against the number of iterations of the model. Furthermore, we included histograms of harmonic means in the posterior distribution. In each graph, the lower chain and the histogram to the left, both in red, represent the independent models, whereas the upper chain and the histogram to the right, both in green, represent the dependent models. The x-axis for the histograms has the same range as the y-axis for the Markov chains. The graphs represent (a) sharing among adults, sharing with infants, (b) sharing from males to females, multi-male groups, (c) sharing among males, male–male coalitions, (d) sharing among unrelated males, male–male coalitions, (e) sharing among unrelated females, female–female coalitions, and (f) sharing among females, female–female coalitions. The graphs show that the Markov chains converged and that the differences between the harmonic means of dependent and independent models used to infer evidence for dependent evolution of the two traits were stable along the runs (PDF 189 kb)
Online resource 4
Figure a is a boxplot of the bibliographic frequency of female mate choice showing the significant difference between single-male (0) and multi–male (1) species. Figure b shows the significant correlation of the bibliographic frequencies of female mate choice and male–female food sharing within multi–male groups (N = 23) (PDF 117 kb)
Rights and permissions
About this article
Cite this article
Jaeggi, A.V., Van Schaik, C.P. The evolution of food sharing in primates. Behav Ecol Sociobiol 65, 2125–2140 (2011). https://doi.org/10.1007/s00265-011-1221-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-011-1221-3
Keywords
- Coalitions
- Cooperation
- Food sharing
- Mate choice
- Reciprocal altruism
- Social bonds
- Provisioning