1

Social Systems of Primates

Part I: Introduction: what are primates? Part II: Laws of social behaviour

Competition and conflict regulation Cooperation and relationships

Part III: Socioecology of females Costs and benefits of group living Socioecological Paradigm

2

Part I: Introduction: what are primates?

a rather unspecialized (primitive), small to medium-sized mammal

with rather mobile digits with nails (rather than claws) ( arboreal)

with an emphasis on vision relative to smell with forward-pointing eyes, stabilized by the

postorbital bar ( visual predators) with larger than average brain size for its body size which lives longer than average for its body size With a tendency to live in permanent, mixed-sex

groups

3

The Primate Syndrome What is a primate?

a rather unspecialized (primitive), small to medium-sized mammal

with rather mobile digits with nails (rather than claws) ( arboreal)

with an emphasis on vision relative to smell with forward-pointing eyes, stabilized by the

postorbital bar ( visual predators) with larger than average brain size for its body size which lives longer than average for its body size With a tendency to live in permanent, mixed-sex

groups

Primate diversityAfrica Madagascar Americas Asia

N species 79 68 132 78

N genera 21 15 19 16

N families 4 6 5 5

N spp+ subsp

174 70 200 183

% (semi-) terrestrial

35.4 3.0 0.0 20.3

From CI Orlando workshop 2000; Oates (2005)

5

Why not study primates?

1. Large animals that live at low densities and live long lives:

Small data sets, even after long study2. Primates are difficult and expensive to keep

in captivity3. Difficult to do experiments on primates,

even if they only involve social manipulations (ethical considerations)

Field data are often correlative In captivity, simple experiments are possible

6

Why study primates nonetheless?1. Spectacular social diversity:

Great opportunity to do comparisons to test explanatory frameworks for primate (and human) behavior

2. Social complexity unmatched among mammals Especially social relationships and behavioral dynamics

in them3. Easy to observe in detail:

Most are diurnal, visually oriented, can be habituated to observers

4. Humans are primates as well! Phylogeny matters for understanding a species behavior

7

Humans are a great ape, split off from African great apes ca 6-8 Mya

14 8 6.5 2

Human

Jeffry Oonk

8

Primate specializations: hands and brains

Features of hands (and feet) grasping hands sensitive finger tips flat nails on fingers & toes opposable big toe (except us)

galago

rhesus macaque

chimpanzee

9

Primates are brainy mammals

10

Variation in relative brain size among primates

MacLeod 2004

11

Hypothesized selective advantages of greater cognitive abilities

Social strategizing (Machiavellian intelligence)

Spatio-temporal distribution of resources (spatial memory, mental maps)

Acquiring hidden or protected foods: extraction, processing (Technical intelligence)

Arboreal clambering

Byrne & Whiten 1988

Milton 1988

Parker & Gibson 1977; Byrne 1997

Povinelli & Cant 1995

12

A very popular idea: Machiavellian intelligence

Barrett, Henzi & Dunbar 2003

But:Uncertainty about best scaling method (body size effect)Is group size best proxy for social complexity?

apes monkeys prosimians

13

Difficulties with the Machiavellian intelligence hypothesis

Some major contrasts in intelligence are not explainedSocial complexity in great apes not greater than in many monkeys

versus

14

Other difficulties with the social strategizing hypothesis

Some major contrasts in intelligence are not explainedWhy are some lemurs not just as smart as monkeys?

versus

15

Other difficulties cannot distinguish between the benefits

whenever cognitive abilities are domain-general

Impossible to disentangle selective agent

selects forimproves ability to deal withsocial

challenges

improvedcognitive skills

spatio-temporal food distr.

feeding challenges

16

Characterizing primate life histories

17

Important primate featuresFeatures of life history

Small litters Long mother-

infant bond Slow

development Long life span

Features of social life

Almost always in groups Groups tend to be stable

(permanent) Groups contain adults of

both sexes (mixed-sex, or bisexual groups)

Complex social behavior

18

Implications of the primate peculiarities

Arboreality slow life history Diurnality large, mobile groups Hands dextrous foraging Relative brain size ecological and social cognition Life history time for learning, group stability, social

relationships Infant carrying nomadism in ranging, risk of infanticide

19

Lorises & Galagos

Anthropoids

Primate Primate RadiationsRadiations

Tarsiers

Lemurs

Prosimians

Strepsirrhini

Haplorrhini

20

Modern prosimian primates

Nycticebus(Lorisoidea)

Eulemur(Lemuroidea)

Tarsius(Tarsioidea)

21

Modern anthropoid primates

New World monkeys

(Ceboidea)Apes

(Hominoidea)

Old World monkeys(Cercopithecoidea)

22

Conditions favoring evolution of complex social behavior & social cognition

1. Gregariousness= group living: opportunities for frequent social

interactions 2. Individual recognition (= Stable

groups): allows for social relationships

3. Slow life history: allows establishment of long-term

relationships4. Diurnal activity period:

allows vocal + visual communication, hence differentiation of messages to targets

23

The importance of phylogeny

Prosimians versus anthropoids

Old World Primates versus New World Primates

Great apes versus monkeys

24

Lorises & Galagos

Anthropoids

Primate Primate RadiationsRadiations

Tarsiers

Lemurs

Prosimians

Strepsirrhini

Haplorrhini

25

Shared-Derived Traits of Anthropoids(relative to tarsiers + strepsirhines)

Far more likely to be diurnal And therefore more likely to range widely

Larger body size (except for the extinct lemurs) Always carrying offspring

More nomadic, slower development Greater risk of infanticide

Reduced reliance on olfaction and increased reliance on vision Visual communication creates more opportunities for complex

sociality Larger brain size relative to body size

accompanied by superior cognitive abilities Systematically gregarious in mixed-sex groups

Usually accompanied by sexual dimorphism

26

Modes of infant care

Affects:- range use, mobility: central place foraging vs nomadism- reproductive biology, vulnerability to infanticide: male-female association

cache carry

27

Activity period and gregariousness in primates

van Schaik, unpubl. N.B. Cathemeral included in diurnal

28

Social life of anthropoids

Prosimians not as socially complex as anthropoids

(even if gregarious)

versus

Extensive coalitions only in anthropoids

29

Anthropoids: heritage of visual communication- facial expressions

QuickTime and aTIFF (LZW) decompressor

are needed to see this picture.

30

Shared-Derived Traits of Old World Primates (relative to Plathyrhines)

More likely to be terrestrial More likely to have large body size, and hence Greater sexual dimorphism in size and weapons

More evidence for sexual harassment and forced matings by males

More systematically trichromatic vision Lower reliance on olfaction (no scent-marking) Longer gut retention time

Better able to digest high-fiber diets

Ecological contrasts between NW-OW monkeys

New World Monkeys

Old-World Monkeys

Gut Retention Time

Short Long

Home range area per group weight

Larger Smaller

Group sizes Mainly small Often large

Prevalence of pairs

High (incl. coop breeding)

Very low

32

Shared-Derived Traits of Great Apes(relative to Old World Monkeys)

Larger body size Less vulnerable to predation (provided in trees) More vulnerable to competition (nutritious foods)

Larger brain size & superior cognitive abilities e.g. mirror self-recognition; theory of mind Far greater tool use abilities

Sociality despite fission-fusion: Male-female association and female sexual activity as much as

ecologically possible Tendency toward social tolerance in most dyads, incl. food sharing,

cooperation among non-relatives Relatively very slow life history, including long periods of

development and learning Nest-building

33

Patterns in primate socioecology(mainly based on Clutton-Brock & Harvey 1977a, b)

Body size: Nocturnal species tend to be small (up to ca 1-2 kg), and live in small social

units, as compared to diurnal ones; Insectivores tend to be smaller than frugivores which tend to be smaller than

folivores; Terrestrial species tend to be bigger than arboreal ones; Larger species tend to show increased sexual dimorphism in body size.

Group size: Insectivores are often solitary; frugivorous groups tend to be larger and more

wide-ranging than folivorous ones; Species living in open savanna tend to live in larger groups than forest-living

species; Bigger species tend to live in larger groups; Group size has strong effects on range use: daily travel distance, home range

area.

Population density: Larger animals tend to live at lower densities; Densities of folivores> frugivores > insectivores.

34

Part II: The Rules of Social Behavior

35

Social definitions used in this course

Sociality = involving interactions with known conspecifics (note: group-living is not required, but individual recognition is)

Social organization = spatial distribution of individuals = (composition of the social units) + dispersal mode (which sex)

Social relationship = reflection of the history of interactions between two individuals with respect to their content, quality, and patterning over time, and is a variable that allows us to predict future interactions

Social structure = structure of the social relationships, incl. bonds, of individuals.

Social system = social organization + social structure Social unit = a concrete case of a social system Mating system = N of males, N of females mating in a given

social unit

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Living in Groups

Fundamental problem: beneficial

General benefit from being gregarious Allows specific cooperative endeavors benefiting all

individuals Costly

Living in close proximity increases competition over access to limiting resources

Fundamental conclusion: All group life inevitably involves both competition

and cooperation

37

Classifying social interactions by fitness outcome

Recipient

Actor GAIN LOSS

GAINCooperation(mutualism)

Selfish(exploitation, competition)

LOSSService

(altruism)Spite

Virtually all social behavior in animals contains elements of both competition and cooperation

38

Competition & Aggression

Competition ensues when there is not enough of a critical resource to satisfy the needs of each individual (= conflict of interest) i.e. increased access to this resource increases fitness

Two possible responses to competition, depending on benefits of excluding others (which is costly): Contest: exclusion from resource possible (also interference

competition) Scramble: exclusion from resource impossible or too

expensive relative to value (also exploitation competition) Successful contest requires aggression

Aggression is instrumental, not pathological

39

Dominance

Critical precondition: individual recognition + repeated interactions

Repeated interactions: no escalation needed --displays and signals A is dominant to B if A can predictably provoke submissive

behaviors in B or B will spontaneously signal subordinate status

Cheap and effective way of dealing with conflict of interest (when there is also some overlap in interests!)

Dominance is a feature of a relationship, not of an individual same animal can be dominant to some, subordinate to others

40

More on dominance

Dominance in space: territories Dominance is linked to spatial position

Dominance in groups Independent of spatial position or context

How does dominance produce increased fitness? Exclusion from limiting resources Exploitation of subordinates work (e.g. forced grooming, ) Reproductive inhibition (adaptation of subordinate!) Harassment/ killing of subordinates (where no valuable

relationship)

41

Dominance hierarchies

Dominance hierarchies are traits of groups Features:

Linearity % of dyads that deviate from linearity (linked to uni-

directionality within dyads) Linearity expected if dyadic dominance is reflection of FA

Steepness Reduction in access to critical resource for each rank down

Degree of correlation with kinship (nepotistic hierarchy)

Relatives cluster together, as a result of coalitions Stability

Especially where co-residing relatives provide mutual support Often upheld by third parties (maintenance of status quo )

42

Dominance and nepotism among female primates

Nepotistic: rank inheritance: daughters, once adult, rank directly below mothers.Ranks stableGenerally, higher-ranking matrilines out-reproduce others

Individualistic: no rank inheritance.

Ranks unstable, often reverse age-graded, with youngest mature females

on top.Little variation among

females in lifetime reproductive success

43

strictdespotic

dominance style

relaxedtolerant

aggression

interventions in conflicts

de-escalation mechanisms

reconciliation

tolerance of proximity

kin bias in the above variables

respect for possession

Observed features varying in relation to dominance styles

44

dom

inan

ce s

tyle

Macaca mulatta SBT subordinate

Macaca fascicularis SBT subordinate

Macaca nemestrina SBT subordinate

Macaca arctoides mock-bite dominant

Macaca sylvanus RM threat dominant

Theropith. gelada RM threat dominant

Macaca silenus none

Macaca tonkeana none

strict

relaxed Preuschoft & van Schaik 2000

Interspecific variation in dominance style

45

Conflict Regulation(friends and non-friends alike)

Dyadic, affiliative: Reconciliation Conflict anticipation: prevent escalation

In zoos, often pronounced peak in grooming preceding feeding time Dyadic, agonistic:

Dominance itself! Redirection, aimed disproportionately at kin of the former opponent (Aureli) Retribution (attack former opponent at later moment- not possible in

despotic species) Opportunistic joining of attacks on former opponent (winner support)

Polyadic policing behavior: neutral interventions, supporting fights

46

Conflict RegulationReconciliation

Selective (partner-specific) affiliative social contact soon after a conflict (sooner than expected from baseline or matched control observations)

Expected to lead to reduction of anxiety and reoccurrence aggression

Expected only among partners with a valuable relationship

Aureli, de Waal

47

Evidence for post-conflict

friendly reunions and for selective

attraction between former

opponents

Aureli et al. 2002

48Palagi et al. 2006

Bonobo:Conflict

prevention

49

Male Policing in pig-tailed macaques

0

0.5

1

1.5

2

2.5

3

Fena

le--

fem

ale

cont

act a

ggre

ssio

n(fr

eq/fe

m/2

0 m

in te

st)

0.5 1 1.5 2 2.5 3 3.5

Removal of adult male

Before During After

Oswald & Erwin 1976

Note:a self-serving explanation is plausible-- only one male per groups, all benefits accrue to him

but why dont others police?

50

The Rules of Social Behavior II

Cooperation in relationships

51

Cooperative or altruistic behavior is common in primate groups

Examples:- Coalition formation- Grooming- Food sharing- Communal attacks or defense- Alarm calling or mobbing predator- Cooperative hunting- Communal nursing- Helping breeders rear offspring/ allomothering

52

Classifying social interactions by fitness outcome

Recipient

Actor GAIN LOSS

GAINCooperation(mutualism)

Selfish(exploitation, competition)

LOSSService

(altruism)Spite

How can natural selection ever favor service interactions, or even cooperation if it is risky?

53

Evolutionary explanations of altruistic interactions among animals

Group selection but free-riders spread within groups much faster than pro-social

groups displace others Kin selection

but does not explain altruism toward non-relatives Reciprocity

Works well for nonhuman primates, especially in the relationshipversion

Also explains exchange of different behaviors, but does not explain group service

Costly signaling Group service enhances reputation of altruist, who gets repaid

later by other group members

54

I. Altruism toward kin: Hamiltons rule

Altruism directed (at least on average) toward relatives is favored by natural selection if:

where B = benefit, C = cost, r= relatedness, and i and j are individuals

Bi > Ci B j rij > Ci

Relatedness = probability that two animals share a gene on a locus through descent from a common ancestor Calculating relatedness between two individuals i and j:

ri, j = (0 .5)L

Where: = number of paths between i and j,L = number of steps in a given path

j

i

Here: 1 path, and 2 steps: (0.5)2=0.25

55

Coefficients of relatedness and thresholds for altruism

Kin category r

Mother offspring 0.5

Half siblings 0.25

Full siblings 0.5

Aunt niece 0.125 -0.25

Cousins 0.0625-0.125

Grandmother-grandchild

0.2500.250.50.751

Relatedness

Benefit/Cost Ratio

20

40

60

80

100

120

140

bj > 2cibj > 8ci

56

Deployment of proximity and

cooperative behavior toward kin in female

macaques

Chapais & Blisle 2004

Note-1: curves steeper for the more risky altruism

Note-2: cooperation requiring competence/skill less likely to be as kin-biased

Females preferentially interact with kin

Papio cynocephalus

Approach Grunt Groom0

0.1

0.2

0.3

0.4

0.5

0.6

Act

s pe

r hou

r NonkinKin

Silk et al. 1999

58

Kin selection: kin recognition

1. Spatial distribution: kin is whoever is encountered in a particular location By parents: inside the nest By offspring: whichever adult is nearby (maternal imprinting)

2. Familiarity rule: kin is whoever has become familiar during early life Easily tested by cross-fostering experiments (humans,

nonhuman primates)3. Phenotype matching: kin is whoever passes matching against innate

template Tested by bringing together relatives that were reared apart Referents for the phenotypic template:

Self (many insects, vertebrates: dedicated (olfactory) systems, incl. MHC)Mother

Rendall 2004

59

Primate mothers rely largely on familiarity to recognize kin

Mothers dont recognize own infants right away

Extended mother-infant contact provides cues about other kin (remember switched

babies in hospitals in humans)

60

But can primates also recognize paternal kin?

Usually, paternity is uncertain: Pair-bonded species

Extra-pair copulations One-male groups

Incursions from nonresident males, secret matings with outside males

Multi-male groups females mate with many males no long-term pair bonds

But males might use rules of thumb to make pretty good guess about paternity, or do they recognize kin?

61

Male rules often lead to recognition of their own infants

Infanticidal males avoid killing own infants

Male baboons are more likely to aid juveniles born after they arrive in group than other juveniles

Male langurs protect infants, but only if they were present when infant was conceived and had mated with mother

62

Male baboons protect their own juvenile

offspring more than expected

Buchan et al. 2003

But how do they do it?

63

Reciprocal altruism

If altruists take turns giving and receiving benefits, reciprocal altruism can evolve

Reciprocal altruism requires1. Frequent opportunities to interact in future2. Keep track of help given and received3. Must only help if receive help

Primates are good candidates for reciprocal altruism Stable social groups, good memories,

flexible behavior But how to deal with cheating risk?

64

Grooming in primates

Original function: Hygiene: removal of dirt and parasites

Associated proximate mechanism: Strong preference for being groomed -

pleasurable experience Derived function:

Use grooming as means to appease dominants, or to pay for receipt of services

But almost exclusively in Old World Primates only

Trading grooming for aid: experimental confirmation

0

2

4

6

8

10

Prior Grooming No Grooming

Experimental Condition

Dur

atio

n of

Res

pons

e

Seyfarth & Cheney 1984

1. Observe pair grooming1a. Observe same pair without contact2. Play back scream of former groomer to groomee

3. Videotape response

66

Market effects on reciprocation and exchanges of services

Back-and-forth of services not necessarily symmetric: should depend on leverageLeverage may vary over time

One major source of variation is demographic: number of potential partners

Example baboon baby-grooming market

Barrett &

Henzi2006

67

Cooperation at group-level

Group-level cooperation: Mutualistic (if all share) Problem: free-riding (collective action

problem)

68

0

25

50

75

100

% "

freq

uent

"

Single-Male Multi-Male

(n=5)

(n=7)

Presbytis entellusHrdy (1977)

0.00

0.02

0.04

0.06

SM MM

Southeast Asian Presbytisvan Schaik et al. (1992)

* *

B-G

r. en

c. (N

/hr)

0.2

0.4

0.6

0.8

1.0

1.2

B-G

r. en

c. (N

/d)

SM MM

Propithecus verreauxiiRichard (1978)

Propithecus tattersalliMeyers (1993)

0.04

0.06

0.08

0.10

B-G

r. en

c. (N

/hr)

SM MM

Groups with a single male are more likely to engage in escalated between-group encounters

Between-group antagonism

van Schaik 1996

69

0.0

25.0

50.0

75.0

100.0

% L

ow R

ange

Ove

rlap

1M, 1F 1M, mF mM, mF

(n=11)

(n=8)

(n=20)

Group composition and range overlap

Groups with a single male and/or a single female are more likely to defend their range against neighboring groups

van Schaik 1996

70

Major exception: chimpanzees

Communal hunting Potentially lethal communal

violence between communities patroling & incursions

71

Hunting in primates

Many primates eat meat, when they can obtain it e.g. orangutans catch slow

loris

However, hunting (chase or pursuit followed by capture) is extremely rare:Chimpanzees (very common)Capuchin monkeys (common)Bonobos (few cases)

Similarities between chimpanzees and capuchins:Mainly males, often togetherAccompanied by food sharing

72

Part III: Socioecology Basic principles

Sex differences in limiting factors Group living Sex differences in dispersal

Female strategies: Females in large groups

Competitive regimes Alliances and bonding patterns

Female strategies in small groups Competition for membership

Females without female associates Territoriality and infanticide avoidance

Male strategies: Female defense polygyny Male alliances & bonding patterns

73

Batemans Principle

NB: Species with life-long monogamy tend to have equal variance for the two sexes

74

Food limits female reproduction: provisioning and birth rates

Cowlishaw & Dunbar (1999)

75

Social strategies predicted Females

Lifetime reproductive success limited by access to shelter or food

Social strategies should serve to improve access to safety or food

Safety best achieved in groups Males

Lifetime reproductive success limited by mating access to females

Social strategies should serve to improve this access

Optimal male strategies depend on female distribution and behavior

76

The Socioecological Paradigm

Distribution of +Relationships among

males

length + synchrony of

estrus

IntersexualConflict

male-femaleAssociation + Relationships

Resources Risks

Distribution of +Relationships among

females

(predators, disease)(food, shelter)

77

Major primate predatorsRaptors

Harpy Eagle Crowned Hawk-Eagle

78

Major primate predatorsFelids

Leopard

79

Grouping and predator detection

van Schaik et al. 1983a

Larger groups detect predators at greater distances(same found for 3 other species in same forest)

Macaca fascicularis, Ketambe

80

In larger groups, there are more eyes to detect predators

81

Predation rate among African forest animals, mainly primates

Negatively correlated with group sizeHigher for terrestrial species than for arboreal onesPositively correlated with group density (encounter rates, search images and specialization by predators?)

Shultz et al. 2004

terrestrial

arboreal

Demographic evidence for link between grouping and predation risk

82

Comparative evidence for link between group size and predation risk

0

2

4

6

8

10

12

Num

ber F

emal

es

ContrastsHighLow Medium

Predation Risk Levels

Nunn & van Schaik 2000

83

Between-species association reduces predation risk

Diana monkey Red colobus

Ground predators

Aerialpredators

Associating with another species:ecologically cheaper than

increasing own group + different species have different

vigilance patternsprovided range use is compatible

Absent in Madagascar & Southeast Asia: no large diurnal raptors!

Often by species with complementary anti-predation tactics

84

Feeding and grouping: costs

Incompatible feeding schedules and strategies Different classes may prefer different food

species or patches Different classes may prefer feeding bouts of

different lengths Feeding competition

Depends on numbers of individuals and size/ number of patches

85van Schaik et al. 1983

The pushing forward effect,..

leading to longer daily travel distance in larger groups

Costs of grouping: scramble competition

86

Group size effect:stronger when food is scarce

Beehner et al. 2006

87

Integrating benefits and costs:optimum group size

88

Competition dissected

Two kinds: Scramble Contest

Two levels: Within groups Between groups

89

The distribution of food, relative to group size, affects the nature of competition

Dispersed, low value resources generate scramble competition Food is distributed evenly Food items not worth fighting over Scramble to get enough food, no direct

competition

Clumped, valuable resources generate contest competition Resources are scarce & valuable Resources are worth fighting over Contest access to particular resources(assuming animals must stay together)

90Janson & van Schaik 1988

WGC only

WGC + WGSBGC only

WGS only

WGC- within-group contestWGS- within-group scrambleBGC- between-group contest

a)- dominance effect only (effect of group size on mean gain rate is entirely due to dominance effect)b)- group-size effect only (no dominance effect)c)- only effect is that of group-dominancerelative to other groups

I. Females in groupsbasic components of competitive regime

(c)

91

Socioecological model for females:more general cases

van Schaik 1989

92

The model: main predictions

Strong WG-contest component: female dominance ranks, coalitions, philopatry

Weak WG-contest component: no female bonding, females are willing to disperse-migrate when

conditions are favorable High potential for BG-contest:

incentives for low-rankers granted by high-rankers to ensure their cooperation

93

Food, competition, and female social behavior: summary

Dominance Hierarchy

Contest Competition

Distributionof food

AlliancesValuable

CloseBonds

FemalePhilopatry

94

+

-

+ -Macacamost PapioCercopithecus aethiopsCebusSaimiri sciureusLemur catta

Cercopithecus othersErythrocebus

Papio hamadryas

Saimiri oerstedi

Presbytis thomasi

Papio ursinus p.p.

Eulemur fulvus

BrachytelesAteles paniscus

Gorilla g. beringei

Theropithecus

7

15

Cercocebus atys

Propithecusverreauxi

0

Presbytis entellus?

1?

Testing the model: Decided dominance and coalitions among females

Sterck et al. 1997

decided dominance relations

nepotistic coalitions

95

+

-

+ -Macacamost PapioCercopithecus aethiopsCebusSaimiri sciureusLemur catta

Cercopithecus others

Erythrocebus

Papio hamadryas

Saimiri oerstedi

Presbytis thomasiP. ursinus p.p.

Eulemur fulvus

Brachyteles

Gorilla g. beringeiPan

Theropithecus

7 2

110

Colobusbadius

decided dominance/ coalitions

Testing the model:Philopatry and female bonding

femalephilopatry

Sterck et al. 1997

96

Testing the model:two squirrel monkeys

Mitchell, Boinski & van Schaik 1991

97

Explaining tolerant female social structure in primate groups

Original model: increased BGC requires restraint on part of top females Sulawesi macaques

Variant: communal predator defense No evidence

New alternative: communal defense against coercive males No good tests yet

Non-adaptive alternative: multiple stable solutions, arbitrary ?

98

Special case: Small groupsexample Thomas Langurs

anatomical adaptation to folivory small groups:

no strong scramble (group size) effects; no strong contest (dominance) effects

single adult male females disperse, and most groups have gradual beginning and

end (groups last ca 6.5 years)

infanticide common (12% of infants born) sneak attacks by extra-group males after loss of male

Sterck 1995; Steenbeek 1999

99

Group Tenure Phases: significant differences

EARLY MIDDLE LATE

stable

other mm attracted: m actively herds ff in mate defense

ff test new male: seek out extra-group mm, delay reproduction until m proves effective

m gives up mate defense; hidesfrom other groups, may move range

ff with infants often harassed by extra-group mm, avoid them, less alone, rest lower in canopy

infant mortality twice rate of middle phase

Steenbeek 2000

100

Understanding Thomas langur social organization

Female rules to minimize infanticide risk:

1 Attach to strong new male, and begin to reproduce when he effectively wards off other males

2 Stay with male until he becomes ineffective protector3 Attach to next male when without dependent infant

and:4 Keep groups small (minimizes risk of violent takeovers by extra-

group males)

101

Group size and infanticide risk in Thomas langurs

0

0.1

0.2

0.3

0.4

0.5

0.6Ta

ke-o

ver r

ate

per g

roup

yea

r

1 2 3 4 5 6Female group size

mean group size

Steenbeek & van Schaik 2001

102

Group size and infanticide risk in Red Howlers

103

Female social relationships: Integrating ecological and social drivers

Infanticide risk

Female(s) associated with male

Female gregariousness

Females share protector male(s)

Larger groups(WGS, WGC, BGC)

Social relationships

Predation risk

Infanticide limits Ecology limits

Small group

Social relationships

(competition over membership)

104

Females without female associates: low predation risk and high vulnerability to competition

Near-solitary, no territories (+ no permanent association with a single male) Daughters stay in/near natal area (philopatric)

e.g. orangutans

Daughters emigrate from natal area (dispersal) e.g. chimpanzees

Solitary and territorial (+ range shared with a male) Bonded with male: associated pairs

e.g. gibbons

Not-bonded with male: dispersed pairs e.g. dwarf lemur

105Pusey et al 1997

Females (semi-)solitary:competition, but no alliances

Chimpanzees(Gombe)

Females philopatric

Females disperse

106

Origins of pair-living in primatesO

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107

Evolutionary pathways to pairs(as reconstructed from phylogenetic tree)

To:

From:

DispersedPairs

AssociatedPairs

Solitaryforagers 4 1

Bisexualgroups 0 12

(Fisher exact test: P = 0.0021)van Schaik & Kappeler 2003

108

Evolution of obligate pairs

Reconstruction of historical transitions:

Conditions favoring transitions:

Ancestral State(not pairs)

Facultative Pairs

Conditions that produce failed polygyny (e.g. low productivity)

Obligate Pairs

Conditions that produce pairs (almost) all the time, usually because one or both have preference for pairs (e.g. minimizing takeover risk!)

109

Small platyrhines: males and older immatures as helpers

Males invest in offspring Carry infants Share food with infants

Males guard females vsrivals

Closely bonded to mate

marmosettamarin Dusky titi monkeys

Notes:Cooperative breeding: caring males and older immatures not parentsNo risk of infanticide by males

110

Gibbons and siamangs form pair bonds and defend territories

Sing duets in territorial displays Females have priority of access

111

Dispersal patterns potential for kin support

Dispersal: Traditional explanation: response to local density or aggression (not

usually supported) Current explanation: avoidance of inbreeding (passive through

dispersal + active through refusal to mate ) Reduces risk of expressing deleterious mutations Reduces homozygosity, and thus increases developmental stability

Almost always clear sex difference in tendency toward philopatry: Birds: males Mammals: females Explanation: Kin Support Principle

Which sex of offspring can be helped most by parents? Birds: males defend territory and sons can inherit or move next door Mammals: mothers have range and daughters can inherit or move next door

112

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P< 0.001

113

Where male philopatry?1. Difficult to take over a group or a territory, and son may

inherit territory Territory: e.g. gibbons, callitrichids Group: e.g. gorillas

2. Males form large alliance that collectively defends a large range

e.g. chimpanzees

Notes: in case 1, female philopatry is opportunistic, because

male philopatry is opportunistic (inbreeding avoidance!) in case 2, females are forced to become the dispersing

sex (inbreeding avoidance!)

Social Systems of PrimatesPart I: Introduction: what are primates? The Primate SyndromePrimate diversityWhy not study primates?Why study primates nonetheless?Humans are a great ape, split off from African great apes ca 6-8 MyaPrimate specializations: hands and brainsPrimates are brainy mammalsVariation in relative brain size among primatesHypothesized selective advantages of greater cognitive abilitiesA very popular idea: Machiavellian intelligenceOther difficulties cannot distinguish between the benefitsCharacterizing primate life historiesImportant primate features Implications of the primate peculiaritiesModern prosimian primatesModern anthropoid primatesConditions favoring evolution of complex social behavior & social cognitionThe importance of phylogenyShared-Derived Traits of Anthropoids (relative to tarsiers + strepsirhines)Modes of infant careActivity period and gregariousness in primatesAnthropoids: heritage of visual communication- facial expressionsShared-Derived Traits of Old World Primates (relative to Plathyrhines)Ecological contrasts between NW-OW monkeysShared-Derived Traits of Great Apes(relative to Old World Monkeys)Patterns in primate socioecology(mainly based on Clutton-Brock & Harvey 1977a, b)Part II: The Rules of Social Behavior Social definitions used in this courseLiving in GroupsClassifying social interactions by fitness outcomeCompetition & AggressionDominanceMore on dominanceDominance hierarchiesDominance and nepotism among female primatesConflict Regulation(friends and non-friends alike)Conflict RegulationReconciliationEvidence for post-conflict friendly reunions and for selective attraction between former opponentsMale Policing in pig-tailed macaquesThe Rules of Social Behavior II Cooperation in relationshipsCooperative or altruistic behavior is common in primate groups Classifying social interactions by fitness outcomeEvolutionary explanations of altruistic interactions among animalsI. Altruism toward kin: Hamiltons ruleCoefficients of relatedness and thresholds for altruismDeployment of proximity and cooperative behavior toward kin in female macaquesFemales preferentially interact with kinKin selection: kin recognitionPrimate mothers rely largely on familiarity to recognize kin But can primates also recognize paternal kin?Male rules often lead to recognition of their own infantsMale baboons protect their own juvenile offspring more than expectedReciprocal altruismGrooming in primatesTrading grooming for aid: experimental confirmation Market effects on reciprocation and exchanges of servicesCooperation at group-levelMajor exception: chimpanzeesHunting in primatesPart III: SocioecologyBatemans PrincipleFood limits female reproduction: provisioning and birth ratesSocial strategies predictedThe Socioecological ParadigmMajor primate predatorsMajor primate predatorsGrouping and predator detectionIn larger groups, there are more eyes to detect predatorsComparative evidence for link between group size and predation riskBetween-species association reduces predation riskFeeding and grouping: costsCosts of grouping: scramble competitionGroup size effect:stronger when food is scarceIntegrating benefits and costs:optimum group sizeCompetition dissectedThe distribution of food, relative to group size, affects the nature of competitionI. Females in groupsbasic components of competitive regimeSocioecological model for females:more general casesThe model: main predictionsFood, competition, and female social behavior: summaryTesting the model:two squirrel monkeysExplaining tolerant female social structure in primate groupsSpecial case: Small groupsexample Thomas LangursGroup Tenure Phases: significant differencesUnderstanding Thomas langur social organizationGroup size and infanticide risk in Red HowlersFemales without female associates: low predation risk and high vulnerability to competitionFemales (semi-)solitary:competition, but no alliancesOrigins of pair-living in primatesSmall platyrhines: males and older immatures as helpersGibbons and siamangs form pair bonds and defend territoriesDispersal patterns potential for kin supportWhere male philopatry?