Food Sharing In Humans And Nonhuman Primates

Food Sharing In Humans And Nonhuman Primates
Food sharing universal in humans but also common in some primate species Well studied case for evolution of cooperation, and to a lesser degree prosocial psychology For those trying to understand cooperation in the lab, important to take this naturalistic and comparative perspective Adrian V. Jaeggi & Michael Gurven UC Santa Barbara

Introduction: Food sharing as a window on cooperation
Summary Introduction: Food sharing as a window on cooperation Why food sharing? “Other than suicide, no behavior is more clearly altruistic than the surrender of food” (Wilson, 1975)  Evolution and psychology of cooperation Naturalistic context for interpreting experimental studies of cooperation (economic games, etc.)  Decision rules evolved in customary interactions Prime example for studying evolution and psychology of cooperation Customary behavior rather than reaction norms

Summary Introduction: Food sharing as a window on cooperation Explaining sharing across species (Jaeggi & van Schaik 2011 BES) Sharing with offspring among adults Between sexes Within ? Total sample: 68 species Few prosimians, most NWM, few OWM, all apes: 38 species Some NWM, some apes, few other species: 14 / 9 species No food sharing Homo sapiens 1 species Wide- spread EVOLUTION OF FOOD SHARING

Sharing psychology: Food transfers (Jaeggi, Burkart & van Schaik 2010 Phil Trans B) (n= # studies) ? - ‘Social contacts between squirrel Monkeys during feeding were relatively rare, And if they did occur, they were predominantly agonistic’ (Fragaszy and Mason 1983, p. 314) - ‘In the chimpanzee, infants, rather than mothers, might be responsible for initiating [transfers] and experiencing the diversity of adult foods and for gathering information about them … offered food parts were assumed to be meaningless for the infant in the sense of nutrition and taste, because these were often offered after the mother had eaten all of the palatable parts of them’ (Ueno & Matsuzawa 2003, p. 237) - Chimps: scramble for ownership followed by mainly passive sharing with those in begging cluster (e.g. Nishida et al 1992) - ‘food-transfer by parents and older siblings relates to their level of motivation such that the more highly motivated toward food they are, the more transfers of food occur’ (Feistner & Chamove 1986, p. 449) No data on human adults (Hilly/Hames: what do you need that for?) but requests are hardly ever refused, having a stingy reputation is bad, offering is common

Linking sharing psychology and selection pressures (Jaeggi, Burkart & van Schaik 2010 Phil Trans B) Sharing Psychology (Prosociality) Adults Selection pressures We understand selection pressures pretty well. The challenge is to link them to sharing psychology Tried to do that a little bit in Phil Trans paper, but pretty ramply, here’s a better attempt, in particular with better human data What are intrinsic motivation and external stimuli? Intrinsic motivation = deviation from ‘I want to eat all this’ default  inhibitory control Extrinsic stimuli = evolved decision rules (HBE style): when to do what optimally Respond to need, social distance, etc.

Theoretical concepts Explaining sharing across species: Phylogenetic analyses Linking sharing psychology to selection pressures: Case studies

Theoretical Concepts Characteristics of shared food (Kaplan & Hill 1985) Asynchrony in acquisition Decreasing marginal value

Concept I: Tolerated scrounging (TS)
COwner << BRecipient (Blurton Jones 1987, Winterhalder 1996, Stevens & Stephens 2002) Relative need  Large package sizes, similar RHP

Concept II: Kin selection (KS)
COwner << BRecipient Relative need Producer control Hard-to-acquire food High fertility, fast growth High (inter-)dependence * ROwner-Recipient (Hamilton 1964)

Concept III: Reciprocal altruism (RA)
COwner << BRecipient Relative need Producer control Contingency High variance, high yield: Insurance Economies of scale, Division of labor: Trade Biological markets: Exchange and interchange and vice versa (Trivers 1971)

COwner << BRecipient and vice versa (Trivers 1971) Relative need Producer control Contingency Illustrates the first two points on the previous slide: Meat contingency = insurance All foods = economies of scale from Gurven 2004

COwner << BRecipient and vice versa (Trivers 1971) Relative need Producer control Contingency Jaeggi et al AJPA Food sharing Schino 2007 Behav Ecol Grooming and support Grooming for grooming Biological markets in primates: Grooming is exchanged for grooming over long time periods Grooming is traded for agonistic support Food sharing sometimes is best predicted by past shares Gomes et al Proc Roy Soc (cf. Watts 2002, Schino & Aureli 2008, Frank & Silk 2009, Fruteau et al. 2011) (cf. de Waal 1989, 1997, Mitani 2006)

Concepts IV: Costly signalling (CS)
No control or contingency, independent of need (e.g. Hawkes 1991, Smith & Bliege Bird 2005) Food production = Contribution to public good Sharing = High broadcasting efficiency Smith & Bliege Bird 2005

Concepts IV: Costly signalling (CS)
No control or contingency, independent of need (e.g. Hawkes 1991, Smith & Bliege Bird 2005) Food production = Contribution to public good Sharing = High broadcasting efficiency Signal = Phenotypic quality: Pay-back = Status, EPCs Signal = Cooperative intent: Pay-back = Cooperation partners (== Indirect reciprocity)

Reconciling different concepts
TS = Need + No producer control + No contingency KS = Need + Producer control + No contingency RA = Need + Producer control + Contingency CS = No need + No producer control + No contingency Always some combination of these - Relative need: what are the benefits for offspring? Do they gain anything more than the nutrients the mother could convert into milk by eating all food? - Producer control: Can sharing be selective? Are certain individuals tolerated more than others? Is there even respect for possession? - Contingency: are producers also recipients? Or, do they get other benefits back e.g. insurance against bad times, sometimes never cashed in Relative need? Producer control? Contingency?

Linking sharing psychology and selection pressures
Jaeggi et al Phil Trans B Sharing Psychology (Prosociality) Adults Knowing that multiple models can explain food transfers, we should really ask how certain or how big are the return benefits to donors that’s what should predict how prosocial sharing psychology is And therefore the transition from no sharing to relatively rare, passive sharing, to wide-spread active sharing Selection pressures Wide-spread, active sharing No sharing Rare, passive sharing

> 200 articles 68 species PGLS, GEE (ape in R) RJ MCMC
Jaeggi & van Schaik 2011 BES > 200 articles 68 species PGLS, GEE (ape in R) RJ MCMC (BayesTraits) Use phylogenetic analyses to identify the CONDITIONS for food sharing Sharing with adults conditional on sharing with infants  Explain sharing with offspring first!

Results: Sharing with offspring
EVOLUTION OF FOOD SHARING Total sample: 68 species No food sharing Few prosimians, most NWM, few OWM, all apes: 38 species Sharing with offspring Jaeggi & van Schaik 2011 BES 18

Sharing with offspring:
Case studies Social learning of diet: Feeding tolerance (Jaeggi et al. 2008, 2010 AJP)

Case studies Social learning of diet: Tolerated taking (Jaeggi et al. 2008, 2010 AJP) Mainly passive (cf. Silk 1978, Nishida & Turner 1996)

Case studies High growth rates: Provisioning (Feistner & Chamove 1986) Preferred Non-preferred - Highly dependent offspring: twin births, fast growth rates - Provisioning with high quality items Provisioning by allo-mothers (mom provides milk, others additonal nutrients) Great inhibitory control! Food offering (cf. Izawa 1978, Ferrari 1987, Rapaport 2006, Rapaport & Ruiz-Miranda 2006)

Sharing with offspring: Summary and Predictions
Relative need? Adults have better access to food Offspring gain informational and nutritional benefits Producer control? Adults are stronger Contingency? No  Selection pressures: TS, KS  Predictions More dependent (higher B), more (active) sharing - Highly dependent offspring: twin births, fast growth rates - Provisioning with high quality items Provisioning by allo-mothers (mom provides milk, others additonal nutrients) Great inhibitory control!

Sharing with offspring predicted by processing-difficulty, no effect of diet quality  Learning about difficult-to-access food1 PGLS: P<0.05 Sharing with offspring Analyses, which i‘m not gonna show here in detail, indicate strong co-evolution to the extent that sharing among adults will NEVER evolve in the absence of sharing with infants Extractive Foraging 1cf. Feistner & McGrew 1989, Brown et al 2004, Rapaport & Brown 2008 23

EVOLUTION OF FOOD SHARING Total sample: 68 species No food sharing Easy diet Few prosimians, most NWM, few OWM, all apes: 38 species Sharing with offspring Difficult diet (extractive foraging) Jaeggi & van Schaik 2011 BES 24

Results: Sharing among adults
EVOLUTION OF FOOD SHARING Total sample: 68 species No food sharing Easy diet Few prosimians, most NWM, few OWM, all apes: 38 species Sharing with offspring Difficult diet (extractive foraging) Sharing among adults Some NWM, some apes, few other species: 14 / 9 species Between sexes Within sexes Jaeggi & van Schaik 2011 BES 25

Male-female sharing: Case studies
Squirrel monkeys (Fragaszy & Mason 1983) “ Social contacts between squirrel monkeys during feeding were relatively rare, and when they did occur, they were predominantly agonistic. … attempts to steal were noted, all made by males and accompanied by agonistic overtones” (p. 314) Red colobus (Starin 2006) “Food transfer is predominantly an aggressive male behavior” (p. 181) Knowing that multiple models can explain food transfers, we should really ask how certain or how big are the return benefits to donors that’s what should predict how prosocial sharing psychology is And therefore the transition from no sharing to relatively rare, passive sharing, to wide-spread active sharing

Rhesus macaque consorts: co-feeding (Dubuc et al 2012) Consort as special situation in which females can be more entitled cf. Strum 1981

Male-female sharing: Case studies Orangutan consorts: Tolerated taking (van Noordwijk & van Schaik 2009)

Chimpanzee meat-for-sex (Mitani & Watts 2001 vs. Gomes & Boesch 2009)  Female mate choice! (cf. Muller et al 2011 vs.Stumpf & Boesch 2006) Same estrous cycle (Ngogo) Whole study period (Taï)

Summary and Predictions
Male-female sharing: Summary and Predictions Relative need? Males often have more access to preferred food Females increase feeding rates, gain rare nutrients, social information Producer control? Males are stronger, higher RHP Selective to consort- or long-term social partners Contingency? Long-term contingency with mating due to female choice  Selection pressures: TS, RA Social costs to non-sharing: (In)tolerant males (un)preferred mating partners  Predictions: More female choice, more (active) sharing - Highly dependent offspring: twin births, fast growth rates - Provisioning with high quality items Provisioning by allo-mothers (mom provides milk, others additonal nutrients) Great inhibitory control!

Results: Male-Female Sharing
Female choice: Male-female sharing significantly more likely in multi-male species Within multi-male species, frequency of female mate choice predicts sharing frequency  If females can choose among multiple males, these have to be nice!  Not just more opportunities for sharing, because male-female proximity lower in multi-male groups (van Schaik & van Hooff 1983) Within single-male species, only in monogamous species (but rare) PGLS: P< 0.05 Female mate choice studies Male-female food sharing studies Multi-male species Males share with females GEE: P< 0.05 1 MIGHT ADD THAT MULTI-MALE SIGNIFICANT IF ONLY SUBSET OF SHARERS TESTED, ISI FEMALE CHOICE RATE BEST AIC BUT N.S.

Food Sharing among Chimpanzees and Bonobos
Sharing among adults: Case studies Cebus sharing (de Waal et al 1993) (cf. Perry & Rose 1994, Rose 1997, van Noordwijk & van Schaik unpubl. data)

Sharing among adults: Case studies Chimpanzee sharing (Boesch & Boesch 1989) Allies! (Nishida et al 1992, Mitani 2006)

Sharing among adults: Case studies Chimpanzee and bonobo sharing (Jaeggi, Stevens & van Schaik 2010 AJPA) Chimpanzees: Gossau (CH), 11 adults, 30 Experiments, 82 obs. hours Bonobos: Planckendael (B), 6 adults, 70 Experiments, 125 obs. hours test some basic predictions of reciprocity framework say in a minute what i mean with if dominance hierarchy allows explain how experiments worked

Sharing among adults: Case studies Chimpanzee and bonobo sharing: Linking return benefits and tolerant sharing (Jaeggi, Stevens & van Schaik 2010 AJPA) Chimpanzees: GLMM P<0.01 Bonobos: GLMM P<0.01 Show another case study that illuminates the relationship between return benefits and sharing psychology Food received best predictor of food given in chimps, opposite is true for bonobos cf. de Waal 1989, 1997, Mitani & Watts 2001, Mitani 2006, Gomes & Boesch 2009; Fruth & Hohmann 2002

Sharing among adults: Case studies
Chimpanzee and bonobo sharing: Linking return benefits and tolerant sharing (Jaeggi, Stevens & van Schaik 2010 AJPA) RA TS KS Sorry for the mess, just to show that we didn’t only test for food-for-food reciprocity similarly, also evidence for other return benefits as food given also predicted by relationship quality (grooming, proximity, support) and kinship in chimps, but mainly RHP difference in bonobos  Less control in bonobos!

Sharing among adults: Case studies Chimpanzee and bonobo sharing: Linking return benefits and tolerant sharing (Jaeggi, Stevens & van Schaik 2010 AJPA) * % Unresisted Transfers - expect that chimps would then share more voluntarily  indeed! - now you should be surprised: aren‘t bonobos supposed to be nicer? The hippie primates? But, see de waal (1) This study

Sharing among adults: Case studies Chimpanzee and bonobo sharing: Linking return benefits and tolerant sharing (Jaeggi, Stevens & van Schaik 2010 AJPA) % Unresisted Transfers Hare et al. Etc. Found the opposite result Measured sharing differently  could be the reason Or, both species are highly flexible and expressed sharing generosity could lie on a continuum spanning both species  no final call on which species is nicer! (1) This study; (2) de Waal 1992 (But cf. Hare et al. 2007, Wobber et al. 2010)

Sharing among adults: Summary and Predictions Relative need? Asynchrony of acquisition, rank-biased ownership Access to rare nutrients Producer control? Begging clusters, ‘respect for possession’ Selective to long-term social partners, kin Contingency? Long-term contingency with grooming, support, etc. due to partner choice  Selection pressures: TS, KS, RA Social costs to non-sharing: (In)tolerant males (un)preferred cooperation partners  Predictions: More important cooperation partners, more (active) sharing - Highly dependent offspring: twin births, fast growth rates - Provisioning with high quality items Provisioning by allo-mothers (mom provides milk, others additonal nutrients) Great inhibitory control! Note: you can condition any species to like you with food  easy to do with members of same species

Sharing among adults: Summary and Predictions In some species sharing occurs in all sex-combinations Sharing predicted by kinship, grooming, support, past sharing, etc. But rare overall, not significant contribution to diet  Selective tolerance of preferred social partners  Social costs to intolerance: partner choice (In)tolerant individuals (un)preferred cooperation partner Long-term contingency (grooming, support, etc.) TS, KS, RA More important cooperation partners, more (active) sharing - Highly dependent offspring: twin births, fast growth rates - Provisioning with high quality items Provisioning by allo-mothers (mom provides milk, others additonal nutrients) Great inhibitory control!

Results: Female-Female and Male-Male Sharing
Male-male and female-female sharing Coalition formation explains sharing among males and females 1 Sharing among females GEE: P< 0.05 Female-female coalitions 1 Sharing among males GEE: P< 0.05 Male-male coalitions MIGHT ADD THAT GROOMING RATE IS TREND IN MALE-MALE 1‘S SUBSET

Results: Female-Female and Male-Male Sharing
Male-male and female-female sharing Coalition formation explains sharing among males and females If reduced to only nonkin food sharing, results even stronger!  If you need allies, you have to be nice to them 1 Sharing among unrelated females GEE: P< 0.05 Female-female coalitions 1 Sharing among unrelated males GEE: P< 0.05 Male-male coalitions MIGHT ADD THAT BOTH COALITIONRATE AND GROOMING RATE ARE SIGNIFICANT IN FEMALE-FEMALE 1‘S SUBSET

EVOLUTION OF FOOD SHARING (extractive foraging)
Summary Sharing among adults: Summary EVOLUTION OF FOOD SHARING Total sample: 68 species No food sharing Easy diet Few prosimians, most NWM, few OWM, all apes: 38 species Sharing with offspring Difficult diet (extractive foraging) Sharing among adults Some NWM, some apes, few other species: 14 / 9 species Partner choice (mating / coalitions) Between sexes Within sexes Jaeggi & van Schaik 2011 BES

Discussion: Predictions
Sharing among adults: Predictions Given shareable food items:  Males in groups / species with stronger female choice should share more  One-male vs. multi-male, modular vs. non-modular species1  In any species with coalitions, allies should share: - Ateles2, Cacajao3, Dolphins4, Elephants5, etc. Pygathrix nemaeus Rhinopithecus roxellana Macaca radiata Ateles geoffroyi Cacajao calvus 1Sinha 2005, Sinha et al. 2005, Kavanagh 1972, Zhen Zhang et al. 2008, Grueter 2009 2Aureli et al Bowler & Bodmer Connor Poole & Moss 2008

Summary Sharing among human foragers
Explaining sharing across species (Jaeggi & van Schaik 2011 BES) EVOLUTION OF FOOD SHARING Total sample: 68 species No food sharing Easy diet Few prosimians, most NWM, few OWM, all apes: 38 species Sharing with offspring Difficult diet (extractive foraging) Sharing among adults Some NWM, some apes, few other species: 14 / 9 species Partner choice (mating / coalitions) Between sexes Within sexes Wide- spread Homo sapiens 1 species

Sharing among human foragers
Complexity of human foraging niche (Gurven in press, adapted from Kaplan et al 2000) low CALORIC VALUE high large small DIFFICULTY NUTRIENT DENSITY PACKAGE SIZE sharing

Sharing among human foragers:
Tsimane Production and consumption across lifespan Individuals (Gurven et al 2012) Nuclear families (Hooper et al in prep) (cf. Kaplan & Gurven 2005)

Tsimane Food transfers within extended family (Hooper et al in prep)

Tsimane Likelihood of caloric deficit (Gurven et al 2012)

Tsimane Food transfers between households (Hooper et al in prep)  RA KS (x TS)

Sharing norms in ethnographic record (from Gurven 2004): Distribution rules (Central Eskimo: Damas 1972, Gunwinggu: Altman 1987) Share with those in need (Ache: Gurven 2004, !Kung: Marshall 1976, Lee 1979, Yanomamo: Hames 1990) Never deny requests (Batek: Endicott 1988, Chacobo: Prost 1983, Kaingang: Henry 1941, Kutse: Kent 1993, Pintupi: Myers 1988) Give to those who gave in the past (Agta: Peterson 1978, G/wi: Silberbauer 1981, Maimande: Aspelin 1979, Pintupi: Myers 1988, Siriono: Holmberg 1969) Stinginess is punished (Ache: Bertoni 1941, Agta: Griffin 1982, Maimande: Aspelin 1979, Netsilik: Balikci 1970, Ona: Bridges 1948, Pilaga: Henry 1951, Utku: Briggs 1970, Washo: Price 1975)

Summary Sharing among human foragers Explaining sharing across species (Jaeggi & van Schaik 2011 BES) Sharing with offspring among adults Between sexes Within Difficult diet (extractive foraging) Partner choice (mating / coalitions) Total sample: 68 species Few prosimians, most NWM, few OWM, all apes: 38 species Some NWM, some apes, few other species: 14 / 9 species No food sharing Easy diet Homo sapiens 1 species Interdependence (complex foraging niche) Wide- spread EVOLUTION OF FOOD SHARING

Conclusions: Food sharing as a window on cooperation
Jaeggi et al Phil Trans B Sharing Psychology (Prosociality) Adults We understand selection pressures pretty well. The challenge is to link them to sharing psychology Tried to do that a little bit in Phil Trans paper, but pretty ramply, here’s a better attempt, in particular with better human data What are intrinsic motivation and external stimuli? Intrinsic motivation = deviation from ‘I want to eat all this’ default  inhibitory control Extrinsic stimuli = evolved decision rules (HBE style): when to do what optimally Respond to need, social distance, etc. Selection pressure Interdependence  Norms No cooperation, easy diet  No tolerance Difficult diet  Infants take Partner choice  Selective tolerance High growth rates  Provisioning

Jaeggi et al Phil Trans B Sharing Psychology (Prosociality) Adults One one side, sharing doesn’t get you anything. On the other side, you’re dead! In between, sharing is a necessary evil Selection pressure No benefits to sharing Necessary evil Dead without it!

People cross-culturally share resources (Henrich et al 2001, 2006, 2010) Michael Gurven and the Tsimane David Tracer in PNG

Marmosets but not chimpanzees provision others (Burkart et al 2007 vs. Silk et al 2005; cf. Jensen et al 2006, Vonk et al 2008) Donor Recipient Judith Burkart Food

Chimpanzees do help- but only upon request (Yamamoto et al 2009a, cf. Yamamoto & Tanaka 2009b,c, 2010, Warneken et al 2007) Taps prosocial psychology better than food provisioning tasks evolved rules Jaeggi, Burkart & van Schaik 2010

Evolved decision rules How responsive to extrinsic stimuli? What stimuli (need, social distance, audience, ..) ‘Intrinsic motivation’ (inhibitory control, conscience, ..) Taps prosocial psychology better than food provisioning tasks evolved rules Jaeggi, Burkart & van Schaik 2010

Acknowledgements A. H. Schultz Foundation Carel van Schaik
Michael Gurven Maria van Noordwijk Judith Burkart Jeroen Stevens Chris von Rueden Hilly Kaplan

Food Sharing In Humans And Nonhuman Primates

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