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

Part I: Introduction: what are

primates?
a rather unspecialized (primitive), small to mediumsized 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
2

The Primate Syndrome

What is a primate?
a rather unspecialized (primitive), small to mediumsized 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

Primate diversity
Africa

Madagascar

Americas

Asia

N species

79

68

132

78

N genera

21

15

19

16

N families

N spp+
subsp

174

70

200

183

% (semi-)
terrestrial

35.4

3.0

0.0

20.3

From CI Orlando workshop 2000; Oates (2005)

Why not study primates?

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

Small data sets, even after long study

2. Primates are difficult and expensive to keep

in captivity
3. 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
5

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 them

3. 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

6

Humans are a great ape, split off from

African great apes ca 6-8 Mya

Human

14

6.5

2
7
Jeffry Oonk

Primate specializations: hands and brains

chimpanzee

Features of hands (and feet)

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

rhesus macaque

galago

Primates are brainy mammals

Variation in relative brain size among

primates

MacLeod 2004

10

Hypothesized selective advantages

of greater cognitive abilities

Social strategizing (Machiavellian

intelligence)

Byrne & Whiten 1988

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

Milton 1988

Acquiring hidden or protected foods:

extraction, processing (Technical
intelligence)

Parker & Gibson 1977;

Byrne 1997
Povinelli & Cant 1995

Arboreal clambering

11

A very popular idea:

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

apes

monkeys

prosimians
12

Barrett, Henzi & Dunbar 2003

Difficulties with the

Machiavellian intelligence hypothesis
Some major contrasts in intelligence are not explained
Social complexity in great apes not greater than in many monkeys

versus

13

Other difficulties with the

social strategizing hypothesis
Some major contrasts in intelligence are not explained
Why are some lemurs not just as smart as monkeys?

versus

14

Other difficulties
cannot distinguish between the benefits

whenever
cognitive
abilities are
domaingeneral
Impossible to
disentangle
selective agent

feeding
challenges
social
challenges

improves
selectsability
for to deal with

improved
cognitive skills

spatio-temporal
food distr.

15

Characterizing primate life histories

16

Important primate features

Features of life history
Small litters
Long motherinfant 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

17

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

18

Primate
Radiations
Lemurs
Lorises &
Galagos

Strepsirrhini

Prosimians

Tarsiers

Haplorrhini
Anthropoids

19

Modern prosimian primates

Eulemur
(Lemuroidea)

Tarsius
(Tarsioidea)
Nycticebus
(Lorisoidea)

20

Modern anthropoid primates

New World
monkeys
(Ceboidea)

Apes
(Hominoidea)

Old World monkeys

(Cercopithecoidea)

21

Conditions favoring evolution of complex social

behavior & social cognition
1.

Gregariousness= group living:

2.

opportunities for frequent social

interactions

Individual recognition (= Stable

groups):

3.

allows for social relationships

Slow life history:

4.

allows establishment of long-term

relationships

Diurnal activity period:

allows vocal + visual communication,

hence differentiation of messages to
targets
22

The importance of phylogeny

Prosimians versus anthropoids
Old World Primates versus New World
Primates
Great apes versus monkeys

23

Primate
Radiations
Lemurs
Lorises &
Galagos

Strepsirrhini

Prosimians

Tarsiers

Haplorrhini
Anthropoids

24

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

25

Modes of infant care

cache

carry

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

26

Activity period and gregariousness

in primates

van Schaik, unpubl.

27

N.B. Cathemeral included in diurnal

Social life of anthropoids

Prosimians not as socially complex as anthropoids
(even if gregarious)

versus

Extensive coalitions only in

anthropoids

28

Anthropoids:
heritage of visual communication- facial expressions

QuickTime and a
TIFF (LZW) decompressor
are needed to see this picture.

29

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

30

Ecological contrasts between NW-OW monkeys

Gut Retention
Time

New World
Monkeys

Old-World
Monkeys

Short

Long

Home range area Larger

per group weight

Smaller

Group sizes

Mainly small

Often large

Prevalence of
pairs

High (incl. coop

breeding)

Very low

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
32

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.

33

Part II: The Rules of Social

Behavior

34

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

35

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
36

Classifying social interactions by fitness

outcome
Recipient
GAIN

LOSS

GAIN

Cooperation
(mutualism)

Selfish
(exploitation,
competition)

LOSS

Service
(altruism)

Spite

Actor

Virtually all social behavior in animals contains elements of both

competition and cooperation
37

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
38

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
39

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)
40

Dominance hierarchies
Dominance hierarchies are traits of groups
Features:
Linearity
% of dyads that deviate from linearity (linked to unidirectionality 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 ) 41

Dominance and nepotism among

female primates
Nepotistic: rank
inheritance: daughters,
once adult, rank directly
below mothers.
Ranks stable
Generally, 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

42

Observed features varying in relation to

dominance styles
strict
despotic

dominance
style

relaxed
tolerant

aggression
interventions in conflicts
de-escalation mechanisms
reconciliation
tolerance of proximity
kin bias in the above variables
respect for possession
43

Interspecific variation in dominance style

dominance style

strict

relaxed

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

Preuschoft & van Schaik 200044

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

45

Conflict Regulation
Reconciliation
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

46

Evidence for
post-conflict
friendly
reunions and
for selective
attraction
between former
opponents

Aureli et al. 200247

Bonobo:
Conflict
prevention

Palagi et al. 2006

48

2.5

(freq/fem/20 min test)

Fenale--female contact aggression

Male Policing in pig-tailed

macaques

1.5

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

0.5

0
0.5

Before

1.5

During

2.5

After

Removal of adult male

3.5

but why dont others

police?
49

Oswald & Erwin 1976

The Rules of Social Behavior

II

Cooperation in relationships

50

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
51

Classifying social interactions by fitness

outcome
Recipient
GAIN

LOSS

GAIN

Cooperation
(mutualism)

Selfish
(exploitation,
competition)

LOSS

Service
(altruism)

Spite

Actor

How can natural selection ever favor service interactions,

or even cooperation if it is risky?

52

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 relationship
version
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
53

I. Altruism toward kin:

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

B i > C i B j rij > C i

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

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 )

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

Here:
1 path, and 2 steps:
(0.5)2=0.25
54

Coefficients of relatedness and thresholds for

altruism
Kin category

Mother offspring

0.5

Half siblings

0.25

140
120

Full siblings

0.5

100

bj > 2ci

80

Aunt niece

0.125 0.25

Cousins

0.06250.125

Grandmothergrandchild

0.25

Benefit/Cost
60
Ratio

bj > 8ci

40
20

0.75

0.5

0.25

Relatedness
55

Deployment of
proximity and
cooperative behavior
toward kin in female
macaques

Note-1: curves
steeper for the more
risky altruism
Note-2: cooperation
requiring
competence/skill less
likely to be as kinbiased
Chapais & Blisle 2004 56

Females preferentially interact with kin

Acts per hour

Papio cynocephalus
0.6

Nonkin
Kin

0.5
0.4
0.3
0.2
0.1
0

Approach

Grunt

Groom

Silk et al. 1999

Kin selection: kin recognition

1.

Spatial distribution: kin is whoever is encountered in a particular location

2.

By parents: inside the nest

By offspring: whichever adult is nearby (maternal imprinting)
Familiarity rule: kin is whoever has become familiar during early life

3.

Easily tested by cross-fostering experiments (humans,

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

Tested by bringing together relatives that were reared apart

Referents for the phenotypic template:

9
9

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

MHC)
Mother

58

Rendall 2004

Primate mothers rely largely on

familiarity to recognize kin
Mothers dont
recognize own
infants right away
Extended motherinfant contact
provides cues about
other kin
(remember switched
babies in hospitals in
humans)
59

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?
60

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

61

Male baboons protect

their own juvenile
offspring more than
expected

But how do they do it?

Buchan et al. 2003

62

Reciprocal altruism
If altruists take turns giving and
receiving benefits, reciprocal altruism
can evolve
Reciprocal altruism requires
1. Frequent opportunities to interact in future
2. Keep track of help given and received
3. 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?

63

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

64

Duration of Response

Trading grooming for aid:

experimental confirmation
10
8
6
4
2
0
Prior Grooming

1. Observe pair grooming

1a. Observe same pair without contact
2. Play back scream of former groomer to
groomee
3. Videotape response

No Grooming

Experimental Condition

Seyfarth & Cheney 1984

Market effects on reciprocation and

exchanges of services
Back-and-forth of services not necessarily
symmetric: should depend on leverage
Leverage may vary over time
Barrett & Henzi 2006

One major source of variation is

demographic: number of potential partners

Example baboon baby-grooming

market

66

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

67

Between-group antagonism
Southeast Asian Presbytis
van Schaik et al. (1992)

Presbytis entellus
Hrdy (1977)

0.06

B-Gr. enc. (N/hr)

% "frequent"

100

(n=5)
75

50

0.04

0.02
25

(n=7)

0.00

Single-Male

Multi-Male

SM
Propithecus verreauxii
Richard (1978)
0.10

1.2

B-Gr. enc. (N/hr)

B-Gr. enc. (N/d)

Propithecus tattersalli
Meyers (1993)

MM

1.0

0.8

0.6

0.08

Groups with a single male

are more likely to engage in
escalated between-group
encounters

0.06

0.4
0.04

68

0.2

SM

MM

SM

MM

van Schaik 1996

Group composition and range overlap

% Low Range Overlap

100.0

Groups with a single male

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

(n=11)
75.0

(n=8)

50.0

(n=20)
25.0

0.0

1M, 1F

van Schaik 1996

1M, mF

mM, mF

69

Major exception: chimpanzees

Communal hunting
Potentially lethal communal
violence between
communities
patroling & incursions

70

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 together

Accompanied by food sharing
71

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
72

Batemans Principle

NB: Species with life-long monogamy tend to have equal

variance for the two sexes
73

Food limits female reproduction:

provisioning and birth rates

Cowlishaw & Dunbar (1999)

74

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

75

The Socioecological Paradigm

(food, shelter)

Resources

(predators, disease)

Risks

Intersexual
Conflict

Distribution of +
Relationships among
females
length +
synchrony of
estrus

male-female
Association +
Relationships

Distribution of +
Relationships among
males
76

Major primate predators

Raptors

Harpy Eagle

Crowned Hawk-Eagle

77

Major primate predators

Felids

Leopard

78

Grouping and predator detection

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

van Schaik et al. 1983a

79

In larger groups, there are more eyes to

detect predators

80

terrestrial

Demographic
evidence for link
between grouping
and predation risk

arboreal
Predation rate among African
forest animals, mainly primates

Negatively correlated with

group size
Higher for terrestrial
species than for arboreal
ones
Positively correlated with
group density (encounter
rates, search images and
specialization by predators?)

Shultz et al. 2004

81

Comparative evidence for link between

group size and predation risk
12

Number Females

10
8
6
4
2
0
Low

Medium

High

Contrasts

Predation Risk Levels

Nunn & van Schaik 2000

82

Between-species association reduces

predation risk

Associating with another species:

ecologically cheaper than
increasing own group +
different species have different
vigilance patterns
provided range use is compatible
Absent in Madagascar & Southeast
Asia: no large diurnal raptors!
Often by species with complementary
anti-predation tactics

Diana monkey

Red colobus

Ground
predators

Aerial
predators

83

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
84

Costs of grouping: scramble competition

The pushing forward effect,..
leading to longer daily travel distance in
larger groups

85

van Schaik et al. 1983

Group size effect:

stronger when food is scarce

86

Beehner et al. 2006

Integrating benefits and costs:

optimum group size

87

Competition dissected
Two kinds:
Scramble
Contest

Two levels:
Within groups
Between groups

88

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)

89

I. Females in groups
basic components of competitive regime
WGC only

WGC- within-group contest

WGS- within-group scramble
WGC + WGS
BGC- 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-dominance
relative to other groups

WGS only

BGC only

(c)

90

Janson & van Schaik 1988

Socioecological model for females:

more general cases

91

van Schaik 1989

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 highrankers to ensure their cooperation
92

Food, competition, and

female social behavior: summary
Alliances
Valuable

Distribution
of food

Contest
Competition

Dominance
Hierarchy

Close
Bonds

Female
Philopatry

93

Testing the model: Decided dominance and

coalitions among females
decided dominance relations

+
+
nepotistic
coalitions

Macaca
Theropithecus
most Papio
Cercopithecus aethiops
Cebus
Saimiri sciureus
Lemur catta

Presbytis entellus?

1?

0
Eulemur fulvus
Propithecus
Saimiri oerstedi
verreauxi
Brachyteles
Ateles paniscus
Cercopithecus others
Erythrocebus
Cercocebus atys
Papio ursinus p.p.
Papio hamadryas
Presbytis thomasi
15
Gorilla g. beringei
94

Sterck et al. 1997

Testing the model:

Philopatry and female bonding
decided dominance/ coalitions

+
+
female
philopatry

Macaca
Theropithecus
most Papio
Cercopithecus aethiops
Cebus
Saimiri sciureus
Lemur catta

Cercopithecus others
Erythrocebus

Sterck et al. 1997

7
Eulemur fulvus
Saimiri oerstedi
Brachyteles
Papio hamadryas
P. ursinus p.p.
Presbytis thomasi
Gorilla g. beringei
Pan

Colobus
badius

11
95

Testing the model:

two squirrel monkeys

Mitchell, Boinski & van Schaik 1991

96

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
?

97

Special case: Small groups

example 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

98

Group Tenure Phases:

significant differences
EARLY
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

MIDDLE

stable

LATE
m gives up mate defense; hides
from 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

99

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 protector
3 Attach to next male when without dependent infant
and:
4 Keep groups small (minimizes risk of violent takeovers by extragroup males)

100

Take-over rate per group year

Group size and infanticide risk

in Thomas langurs
0.6
0.5

mean group
size

0.4
0.3
0.2
0.1
0

Steenbeek & van Schaik 2001

2
3
4
5
Female group size

101

Group size and infanticide risk

in Red Howlers

102

Female social relationships:

Integrating ecological and social drivers
Infanticide risk

Female(s) associated
with male

Predation risk

Females share
protector male(s)

Female
gregariousness

Infanticide limits

Small group
(competition over
membership)

Social
relationships

Ecology limits

Larger groups
(WGS, WGC, BGC)

Social
relationships

103

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
104

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

Females
disperse

105

Pusey et al 1997

Otolemur
Galagoides zanzibaricus
Galagoides
Galago
Euoticus
Nycticebus
Loris
Perodicticus
Arctocebus
Phaner
Cheirogaleus
Cheirog. medius
Mirza
Microcebus
Allocebus
Avahi
Indri
Propithecus
Hapalemur
Eulemur
Eulemur rubriventer
Varecia
Lemur
Lepilemur
Daubentonia
Tarsius spectrum
Tarsius pumilus
Tarsius banc. e.a.
Cebuella
Callithrix
Callimico
Leontopithecus
Saguinus
Aotus
Saimiri
Cebus
Callicebus
Pithecia
Chiropotes
Cacajao
Alouatta
Lagothrix
Ateles
Brachyteles
Presbytis
Presbytis potenz.
Semnopithecus
Trachypithecus
Nasalis
Simias
Pygathrix
Rhinopithecus
Colobus
Procolobus
Cercopithecus
Chlorocebus
Erythrocebus
Miopithecus
Allenopithecus
Macaca
Cercocebus
Mandrillus
Lophocebus
Theropithecus
Papio
Hylobates
Pongo
Gorilla
Pan paniscus
Pan trogl.

Origins of pair-living in primates

Pairs
ordered
other

Variable pairs

uniform pairs

106

Evolutionary pathways to pairs

(as reconstructed from phylogenetic tree)

To:

Dispersed
Pairs

Associated
Pairs

Solitary
foragers

Bisexual
groups

12

From:

van Schaik & Kappeler 2003

(Fisher exact test: P = 0.0021)

107

Evolution of obligate pairs

Reconstruction of
historical transitions:

Conditions favoring
transitions:

Ancestral State
(not pairs)

Conditions that produce failed

polygyny (e.g. low
productivity)
Facultative Pairs

Obligate Pairs

Conditions that produce

pairs (almost) all the time,
usually because one or both
have preference for pairs
(e.g. minimizing takeover
risk!)
108

Small platyrhines:
males and older immatures as helpers
Males invest in
offspring
Carry infants
Share food with infants

Notes:
Cooperative breeding: caring males
and older immatures not parents
No risk of infanticide by males

Males guard females vs

rivals
Closely bonded to mate

109
tamarin

Dusky titi monkeys

marmoset

Gibbons and siamangs form pair bonds

and defend territories

Sing duets in territorial displays

Females have priority of access

110

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
111

Male natal dispersal and female group size

% natal males emigrating

100

P< 0.001
M. fuscata
75

M. sylvanus
Papio spp

50

C. aethiops
S. entellus

25

other spp. (6)

0
0

20

40

60

80

number of females in group

112

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!)
113