CHAPTER
26
The Ecology and Evolution of Social
Behavior and Cognition in Primates
Christophe Boesch
Abstract
The social lives of animals present them with a constant yet varying series of challenges that they
must solve daily if they want to survive and reproduce.An evolutionary approach to the evolution
of social behavior and cognition predicts the convergent emergence of similar patterns and
abilities in animal species facing similar challenges, as well as the emergence of a large diversity
of behavioral and cognitive abilities within species facing different socio-ecological challenges.
In primates, evidence supporting these predictions contradicts a Cartesian approach that many
psychologists have adopted favoring captive studies and minimizing the role of experience and
ecology. Social grouping is largely the result of a balance between increased predation protection,
which is higher in larger groups, and decreased intragroup feeding competition, which is less
intense in smaller groups. However, within such optimally sized groups, a great deal of flexibility
in how social life can be organized is still possible. Cooperation, altruism, and reciprocity are
observed with different levels of prevalence by individuals living in different ecological niches. In
many monkeys and chimpanzees, we see that ecological factors play a decisive role in favoring
the evolution of cooperation and altruism. The underlying cognitive abilities required to master
them will develop according to how important the abilities are for the survival of the individuals.
Different aspects of the ecological niche select for different abilities, which prevents a simple
model of the evolution of social behavior and cognition. As a rule, the captive environment, a
habitat that is particularly unchallenging and safe, selects for less demanding social cognitive
development in many primate species, including humans. If we want to gain a better understanding
of the evolution of social behavior and cognition, more research should be directed toward
primates that face different types and levels of ecological challenges.
Key Words: ecology, sociality, cooperation, altruism, ecological validity, primates, chimpanzees
forms of life due to common ancestry are to this
Holyoak, & Povinelli, 2008; Povinelli,
2000; Shetdeworrh, 1998; Tomasello, Carpenter,
Call, Behne, & Moll 2005). Two main approaches
day hard for some to swallow. If evolutionary
to comparative behavioral and cognitive studies
thinking has reached a consensus about anatomy,
have dominated. The first follows a Darwinian
Introduction
Darwinian
Penn,
ideas of continuity between all
genetics, development, and neuroscience, it has
approach, which endorses an open and unbiased
remained very controversial when it comes to cog­
search for similarities between species living in
nitive and mental abilities (e.g., Barren, Henzi,
& Rendall,
their natural environments. Animals have inter­
acted with the world for generations and have
&
needed to successfully exploit the structure of their
2007; Boesch 2007, 2010; Cheney
Seyfarth, 2007; de Waal, 2001; Hauser 2006,
environment to survive. Therefore, natural selec­
caution and critical minds (Barren et al., 2007;
tion has favored behavioral and cognitive mecha­
nisms that have enabled individuals to cope wi rh
Boesch, 2007, 201 0; Cheney & Seyfarth, 2007;
life in their particular ecological niches. As a result,
the Cartesian approach, results of captive studies
ir is not unexpected that they may have different
skills than humans and be able to perform in spe­
most reliable due to their greater detail and better
de Waal, 2001), whereas, for those who support
are accepted uncritically as they are considered
cific domains better than us, but this need not
control of possible confounding factors (Hauser,
manifest itself in other domains (Barren, Henzi, &
2000, 2006; Penn et al., 2008; Tomasello & Call,
Rendall 2007; Boesch, 2007, 2008, 2010; Cheney
1997; Tomasello et al., 2005). In reality, expe­
& Seyfarth 1990, 2007; Emery & Clayton 2004;
rience has proven to be essential for the devel­
de Waal 2001, 2008; de Waal & Ferrari 2010,
opment of behavioral and cognitive abilities in
Fitch, Huber, & Bugnyar, 2010; Shetdeworth,
many different species, such as food-storing bird
1998). The second approach follows a Cartesian
species, like the Clark's nutcracker (Shetdeworth,
view, which assigns much less importance to ecol­
1998), macaque and rhesus monkeys (Harlow &
ogy and experience in the development of social
Harlow, 1962; Kempes, Den Heijer, Korteweg,
behaviors and cognitive skills, and it concentrates
Louwerse, & Sterck, 2009; Mason 1978; Mathew
instead on rhe presence of human cognitive abili­
et al., 2003; Sanchez, Hearn, Do, Rilling, &
ties in other animal species living in human-made
Herndon,
environments (e.g., Moll & Tomasello, 2007;
2001), chimpanzees (Gardner & Gardner, 1989),
Penn et al., 2008; Povinelli, 2000; Suddendorf &
and humans (Berry, Poortinga, Segall, & Dasen,
1998;
Sanchez,
Ladd,
&
Plotsky,
Corballis, 2007; Tomasello et al., 2005; Wolpert
2002; Cordon, 2004; Fox, Levin, & Nelson,
2007). This has resulted in a confusing and con­
2010; Nelson et al., 2007; Smyke, Zeanah, Fox,
tradictory series of claims and counterclaims in the
Nelson, & Guthrie, 2010). In full support of a
literature on cognitive faculties in primates, which
Darwinian approach that stresses the importance
has made this literature very difficult for external
of socio-ecological conditions, many studies have
readers to understand.
documented the long-term effect of early expe­
The distinction between a Darwinian and a
rience on brain development, brain activity, and
Cartesian approach is also visible in the attitudes
cognitive abilities. For example, bonnet macaques
toward the continuity or discontinuity of behav­
exposed to varying degrees of difficulty in access­
ioral and cognitive traits in the animal kingdom.
ing food at an early age have been shown to pres­
The evolutionary approach predicts continuity in
ent long-lasting alterations in the functioning
the animal kingdom, including between humans
of the prefrontal cortex and cognitive functions
and our closest living relative, the chimpanzee.
(reviewed in Sanchez et al., 2001; Mathew et
In particular, possibly unique human traits are
al., 2003). Similarly, children who were institu­
expected to have a long evolutionary history, and,
tionalized for extended periods early in life have
therefore, comparative studies are essential in
shown deficits in specific aspects of visual atten­
order to understand how such traits evolved and
tion and memory as well as visually mediated
what factors promoted them. In addition, cogni­
learning (Pollack et al., 2010). Models of the role
tive traits are viewed as adaptations to particular
of experience in neural development and mount­
socio-ecological selection pressures on top of what
ing information on molecular processes in neu­
is possible given the evolutionary constraints,
ral plasticity indicate that neural activities (i.e.,
including the morphological, physiological, and
activity-dependent processes) are critical to brain
generic characteristics of the species considered.
development (Fox et al., 2010). This implies that
The Cartesian approach tends to postulate a qual­
in addition to the stimuli available in the envi­
itative difference within the animal kingdom by
ronment, active engagement of the environment
which humans distinguish themselves from all
may be essential in order for some aspects of cog­
other living species in several important traits.
nitive development to occur (Greenfield, 1999;
Following Descartes' propositions, animals are
Smyke et al., 2010). Furthermore, an important
rigidly programmed and the influence of socio­
effect of experience later in life on general intelli­
ecological conditions on the development of
gence has also recently been shown in birds, mice,
behavioral and cognitive traits is minimal to neg­
and humans (Emery & Clayton, 2004; Jaeggi,
ligible (see Figure 26.1). This explains why evolu­
Buschkuehl, Jonides & Perrig 2008; Light et al.,
tionary researchers view captive studies with great
2010).
BOESCH
I 487
Evolution of social cognition
Figure 26.1 Schematic illustration of the
predictions of two theoretical approaches
to the evolution of social cognition.
"
The Darwinian approach predicts that
!!l
animals adapt to the socio-ecological
-�
conditions they face and will develop
more sophisticated abilities while living
nj
u
:c
0.
0
V>
under more challenging conditions,
while a Cartesian approach expects very
limited effects of ecological conditions
Cognition
on individual cognition and therefore
considers captive studies to be generally
valid.
<1.1
c..
E
v;
Simple
It is important to be aware of these different
Socio-ecological niche
Complex
cognitive solutions. Among the primates, humans
approaches because some social behavioral and cogni­
and chimpanzees have adapted to the largest num­
tive traits have recently been proposed to be distinctive
ber of different environmental conditions and are,
traits that characterize humans and separate us from
therefore, predicted to adopt more diverse behav­
ioral and cognitive solutions (Boesch, 2009).
all other living animals. These traits include extended
cooperation, altruism, altruistic punishment, empa­
thy, and concerns about welfare for others (Fehr and
Evolution of Social Grouping
Gachter 2002; Hauser 2006; Hrdy 2009; Penn et
Individuals are expected to adapt to the living
al., 2008; Tomasello et al., 2005; Silk et al., 2005).
conditions they are facing in order to maximize
Because most data supporting such claims come from
their survival and reproductive outputs. Group liv­
captive studies in which all individuals have been liv­
ing has been considered to be such an adaptation,
ing in deprived ecological conditions and artificial
one that permits the reaction to situations in which
social groups, the uncritical acceptance of such claims
lone individuals fare worse than individuals in
by some is surprising. A detailed review of such claims
groups. Generally, two types of factors are proposed
has been made in this volume by Silk and House for
to favor social grouping. First, predation pressure is
altruism (chapter 20), and by Warneken and Melis for
considered to be the main factor that brings animals
cooperation (chapter 21). Therefore, in this chapter, I
together, as lone individuals will always suffer higher
will restrict myself to reviewing the evidence for social
risks than two or more individuals together (this is
behavioral evolution in wild populations of primates
called the dilution effect, because two individuals
and stress how an evolutionary approach to the ques­
are 50 percent less likely to be caught than when
tion, "What makes us human?" can promote unbi­
alone, three individuals are 66 percent less likely,
ased and ecologically valid answers.
An evolutionary approach views behavior and
and so on) (e.g., Alcock, 1989; Krebs & Davies,
. 1991). In addition, individuals in groups will gain
cognition as adaptive responses to the ecologi­
advantages as a result of information provided by
cal challenges faced by the individuals (Barren
other group members, for example, about predator
et al., 2007; Boesch 2005, 2007, 2010; Cheney
presence or food-patch distribution. On the other
and Seyfarth 1990, 2007; de Waal 2001; Pitch
hand, feeding competition will always be higher in
et al., 2010; Shettleworth 1998). Following such an
groups than for lone individuals, and this will lead
approach, more demanding socio-ecological chal­
to the emergence of optimal group size rather than
lenges faced by individuals of different animal spe­
and cognitive abilities and lead to important con­
maximum group size (e.g., Krebs & Davies, 1991).
This interplay of ecological factors favoring and
limiting group size has been shown in many species
vergent evolution. Second, animal species includ­
and could be demonstrated by field experiments, in
cies will select for more sophisticated social behavior
ing humans that face more new socio-ecological
which the presence of predators or food availabiliry,
challenges will acquire different behavioral and
for example, could be manipulated.
I
THE ECOLOGY AND EVOLUTION OF SOCIAL BEHAV!OR
Moreover, the type of groups found is affected by
form temporary bands and gather as large troops
rhe ability of males to monopolize females. Here,
at rare bur predator-safe sleeping cliffs (Kummer,
different factors play a role in the sense that, the
1968; Schreier & Swedell, 2009). In habitats rich
more synchronous food productivity becomes, the
in palm fruits, both bands and clans are larger and
more females will come into estrus simultaneously.
contain more one-male groups than other regions.
At the same time, this makes it more difficult for
Chimpanzees (Pan troglodytes) seem to follow a sim­
rhe males to monopolize the females against male
ilar pattern, because populations facing both higher
rivals. In other words, food production patterns can
predation pressure and more food availability live in
directly affect the number of sexually active females,
larger parties, which is a name given to temporary
which in turn influences the number of males and
associations of individual members from the same
the group structure (one-male versus multimale
community, the stable grouping unit in that species
groups). In addition, in primates, infanticide by
(Anderson Nordheim, Boesch, & Moermond, 2002;
adult males has been proposed to play an important
Boesch, 2009; Mitani, Watts, & Lwanga, 2002). In
role in influencing long-term associations between
some populations, food availability is a direct predictor
females and males; the higher the risk of infanticide,
of parry size, whereas in others, sexual opportunities,
the more important such affiliations are to females
in terms of the number of estrus females present, will
because males will protect their infants from infan­
more directly influence parry size. However, females,
ticidal males (Palombit, 1999; van Schaik, 1996;
who are more dependent on food for breast feeding
van Schaik & Kappeler, 1997). It is important to
their infants, are more sensitive to food scarcity and
note here that limiting infanticide risk can be com­
will tend to use less of the community's home range
plementary to predator avoidance, because both
when less food is available to them (Boesch, 2009;
can be improved by having more individuals in a
Langergraber, Mitani, & Vigilant, 2009; W illiams,
group; however, infanticide risks should be further
Pusey, Carlis, Farm, & Goodall, 2002). The contrast
improved if females associate permanently with the
in female social position is large between the more
fathers of their offspring (van Schaik, 1996).
solitary and narrower-ranging females from Gombe
Many primate species live in groups. Thanks
National Park and the highly social and wide-ranging
ro the increasing number of studies on different
ones from Ta"i National Park. However, recent obser­
populations within the same species, group size has
vations of the social behavior of female chimpanzees
proven to be highly variable and predominantly
at Ngogo and Goualougo indicate that females can
affected by the different ecological conditions each
be even more flexible. What seems to be emerging is a
population encounters. For example, Hanuman
species that is very flexible and presents both flexible
langurs (Semnopithecus entellus) have been studied
parry size and flexible sex-specific responses to local
in many sites throughout the Indian subcontinent,
conditions.
and it has been shown that one-male groups pre­
The importance of ecological factors in explain­
dominate in environments with high food availabil­
ing the specificity of the social grouping parameters
ity, high visibility, and with the number of females
observed in different primate species is in line with
that can be monopolized by one male, whereas mul­
the biological knowledge we have of those species
timale groups were observed more regularly in envi­
where not only the behavior but also morphology
ronments with more and more predictable food,
and physiology reflect an adaptation to living con­
lower visibility, more predators, and larger numbers
ditions. However, social behavior is not limited to
of females (review in Koenig & Borries, 200 1).
only social grouping patterns, and we should expect
Such differences in group patterns were shown to
many different aspects of social behavior to be
have a direct impact on the reproductive success of
precise adaptations to a group's living conditions.
both males and females, because infanticide is much
I will now review some evidence obtained from
more frequent in one-male groups. Baboons living
observations of wild populations of primates, which
in many parts of the Mrican continent have been
illustrates how complex and subtle the influence
shown to adapt their group size in similar ways. The
of the environment can be in promoting different
classic example is the Hamadryas baboons (Papio
aspects of social behavior, such as cooperation and
hamadryas hamadryas), which are found only in the
altruism.
dry regions of Ethiopia and the Arabic peninsula.
They possess a rigid one-male grouping pattern, bur
Evolution of Cooperation
add to that a flexible fission-fusion layer by which
Cooperation has been defined as the joint action
one-male groups can associate in larger clans, which
of two or more individuals to achieve or attempt
BOESCH
I 489
to achieve a common goal that would be more
rarely achieved by an individual alone (Axelrod &
Hamilton, 1981; de Waal, 2008; Dugatkin, 1997;
Hamilton, 1964; Hauser, McAuliffe & Blake,
2009; Krebs & Davis, 1991; Maynard-Smith,
1982; Packer & Ruttan, 1988) (see Box 26.1).
Such interactions have also been called "mutualist"
or "mutual benefit." Some have expanded coop­
eration to encompass any social interactions in
which the receiver obtains a benefit from the actor,
which would then include altruism (Clutton­
Brock, 2009; Fehr & Gachter, 2002; Henrich &
Henrich, 2006; McNamara, Barta, Fromhage, &
Box 26.1 Terminology about coopera­
tion and altruism
This table shows the cost and benefit outco m es
of four main social interactions generally distin­
guished in the social domain: Cooperation is
when both partners profit from an interacrio
�;
Selfish is when the actor gains but the recipie
loses, Altruism is when the actor loses bur the
recipient gains, and Spite is when both partners
incur costs (e.g., Axelrod & Hamilton, 1981·
Houston, 2008; West, Griffin, & Gardiner, 2007).
There are strong reasons to maintain a distinc­
tion between the terms altruism and cooperation,
because the outcomes of the two are quite distinc­
tive for the two partners and, therefore, they rep­
resent two distinctive evolutionary challenges (see
later). Cooperation, as defined earlier, has been
observed in many animal species and in many
different contexts. These contexts range from
group hunting, as seen in Harris hawks, some
fish, hunting dogs, lions, hyenas, and chimpan­
zees, to group defense against predators or neigh­
hors, as seen in many species of birds, carnivores,
and primates (e.g., Boesch 2002, 2009; Bshary,
Grutter, W illener, & Leimar, 2008; Dugatkin,
1997; Packer & Ruttan, 1988; Raihani, Grutter,
& Bshary, 2010). In as much as cooperation is
successful and leads to higher benefits to the par­
ticipants than would try to attain a goal alone,
the evolution of cooperation is easy to understand
(Dugatkin, 1997; Maynard-Smith, 1982; West
et al., 2007). However, it has proven more dif­
ficult to document the effective benefit increase
resulting from cooperative actions, as the net ben­
efit of any actions in the wild is dependent on the
specific ecological conditions encountered when
individuals cooperate. For example, hunting suc­
cess will be strongly influenced by the availabil­
ity of prey, and the ease with which prey can be
subdued, as well as how detectable both the prey
and hunters are (Boesch & Boesch, 1989; Packer
& Ruttan, 1988). Within the same species, this
�
Hamilton, 1964; Maynard-Smith, 1982; Triv
ers, 1971, 1985).
Cooperation
Actor
Recipient
+
+
Altruism
Selfish
+
+
Spite
This original classification, proposed by Hamil­
ton, was followed for a long time, despite difficul­
ties with measuring costs and benefits in the wild.
Recently, some economists and anthropologists
have started to use the term cooperation inter­
changeably with altruism, which suggests that the
important aspect is the recipient side of the inter­
actions (e.g., Bowles, Choi & Hopfensitz, 2003;
Boyd, Gintis, Bowles & Richerson, 2003; Fehr
& Gachter, 2002). Furthermore, as an altruistic
act could be reciprocated by the recipient at a
later time, if one counts the cost/benefit for such
longer time periods, the outcome will resemble
that of cooperation. Thereafter, it was suggested
to reserve the terms mutualism, mutually benefi­
cial cooperation, and direct cooperation to cooper­
ation as defined in the table above (e.g., Wells
et al. 2007). Others have started to talk about
"costly cooperation" or "altruistic cooperation"
when they intended to mean "altruism" as in the
table above (e.g., West et al. 2007). Distinguish­
ing the two terms, however, is important because
in evolutionary terms, the evolution of coopera­
tion has been quite directly explained, while the
evolution of altruism remains a puzzle.
can result in hunters being very successful when
hunting alone under some ecological conditions,
unsuccessful under other ecological conditions,
or only being successful if hunting in a team.
African lions provide a perfect illustration of
(1972) showed that pairs of lions in the Serengeti
in Tanzania are more successful than lone hunters
at hunting Thompson gazelles. For a long time,
this remained a textbook example of the benefits of
such a situation: they were originally proposed to
cooperation. However, a more recent and extensive
be a good example of successful cooperators from
study of lions within the same habitat showed that
a limited set of observations;
lions would be more successful when hunting alone
490
I
George Schaller
THE ECOLOGY AND EVOLUTION OF SOCIAL BEHAVIOR
or in large groups, bur rhar rhey are mainly seen
1992). However, they are not the only primate spe­
ro hunt in middle-sized groups (Packer, Scheel, &
Pusey, 1990). However, with increasing studies of
cies that have been seen to hunt. The olive baboons
different lion popularions, rhe situation became
rnore complex; in Chobe National Park, Botswana,
baboon population seen to hunt young antelopes
]ions hunt more sy stematically in groups in order to
defend their kills when compering with the pow­
performed solely by the dominant male, and meat
erful hyenas (Cooper, 1991),
he tolerated to recover meat scraps that had fallen
as
do lions in Etosha
of Gilgil in Kenya were famous for being the only
for meat (Strum, 1981). However, the hunt was
was passively shared with other individuals, who
National Park, Namibia, where living in an open,
on the ground. Once this dominant male lost his
high visibility, semi-arid environment requires
group coordination for hunting to be successful
position to a y ounger male, the newcomer started
(Srander, 1992; Stander & Albon, 1993). The lion
male who, thereafter, rapidly stopped hunting. As a
example perfectly illustrates how careful we need to
result, hunting disappeared from this group (Strum,
to forcefully steal the meat from the old dominant
be when discussing the evolution of cooperation,
1981). This shows that, besides ecological factors,
because, within rhe same species, different ecologi­
we need to consider that social factors also affect the
cal factors may select for different levels of coopera­
presence of cooperation.
don. In addition, when lions work in teams,
in
The most striking aspect of hunting in chim­
Namibia, individual hunters monitor rhe actions of
panzees is that group hunting tendencies diverge
rhe other hunters so
as
to make rhe success of the
strongly among different popularions (see Figure
joint goal possible-for example, drivers push prey
26.2a) and that, when hunting in groups, the orga­
as
roward where rhe other lions are ambushed (Srander
nization within the hunters differs strongly between
& Albon, 1993).
populations (see Figure 26.2b) (Boesch, 1994, 2009;
The best example of a hunting primate is the
Boesch & Boesch-Achermann, 2000; Gilby er al.,
chimpanzee. In all chimpanzee popularions stud­
2006; Gilby, Eberly, & Wrangham, 2008; Goodall,
ied today with enough detail, males have been seen
1986; Nishida et al., 1992; Watts & Mitani, 2002).
ro hunt monkeys, duikers, and bushpigs for meat
In fact, Tal and Ngogo chimpanzees were observed to
(Boesch
hunt mostly in groups, whereas Gombe and Mahale
& Boesch-Achermann,
2000;
Boesch,
2009; Goodall, 1986; Mirani &Warts, 2001; Mirani
chimpanzees primarily hunted solitarily. The level
et al., 2002; Mirani, 2009b; Nishida, Hasegawa,
of coordination between hunters during a group
Hayaki, Takahara, & Uehara, 1992). In all those
hunt seems to differ, too, with Gombe and Mahale
popularions, chimpanzees have been seen to hunt
male chimpanzees hunting independently but at the
in groups and, when successful, rhey have been seen
same time on the same group of prey, whereas Ta·i
ro share the meat in one way or another with group
male chimpanzees coordinate their actions by pre­
members (Boesch & Boesch-Achermann, 2000;
dominantly performing complementary and differ­
Gilby, Eberly, Pintea & Pusey, 2006; Nishida er al.,
ent hunting roles. The Ngogo chimpanzees live in
Gombe
Mahale
Ta'i
Ngogo
Ngogo
0
25
50
Proportion of hunts
75
100
������
0%
25%
75%
50%
100%
Proportion of group hunts
Figure 26.2. Comparison of the level of group hunt (a) and cooperation (b), in the sense of the level of coordination between
hunters acting at the same time (sensu Boesch and Boesch 1989) among the chimpanzees of Go mbe Stream and Mahale Mountains
National Parks, Tanzania, Tai National Park, Cote d'Ivoire, and Ngogo in Kibale National Park, Uganda.
BOESCH
I 491
a much larger community, and up to 25 males can
hunt at the same time, which makes it difficult to
determine the level of coordination between hunt­
ers (Watts & Mitani, 2002).
W hat is also fascinating is that male chimpan­
zees belonging to different populations share prey
meat according to different social rules (Boesch
1994, 2002, 2009; Gilby 2006; Goodall, 1986;
Mitani, 2009b; Mitani & Watts, 2001; Nishida et
al., 1992). The Ta! chimpanzee males share meat
primarily according to the contribution each indi­
vidual male has made during the hunt, so that hunt­
ers get more meat than nonhunters, and those who
perform more important hunting roles receive more
meat than other hunters. This meat-sharing rule
clearly supports cooperators. The Gombe chimpan­
zee males, on the other hand, seem to give in to
chimpanzees. Although such team work in territo­
rial encounters has been observed in all chimpanzee
populations, support help for outnumbered in di­
viduals seems to vary according to population: Ta1
chimpanzees were seen to support group members
in 30 percent of intergroup encounters, but it seems
to be much rarer in other chimpanzee populations
(Boesch et al., 2008).
A third context in which cooperation has been
systematically observed in chimpanzees is wh en
they face predators, such as leopards (Boesch 1991
d
2009). In the tropical rainforests of Africa, leopar
density is quite high, with seven to ten individuals
per 10 km2. Direct observations have revealed that
Ta! chimpanzees are regularly attacked, injured, and
killed by leopards, and during a five-year period, an
individual risks an attack every third year (Boesch,
pressure from harassing beggars so that meat shar­
1991; Boesch, 2009). Following a typical prey­
ing seemed to be forced upon the meat owners; beg­
predator arms race, Ta! chimpanzees try to decrease
gars are seen to prevent meat owners from eating by
the costs associated with predation by cooperatively
either covering their mouths or pulling the piece of
chasing leopards away each time they notice their
meat away from the meat owners, behavior patterns
presence, as well as countering them whenever they
never seen during meat-eating sessions in Ta! chim­
have attacked a group member. Here again, sup­
panzees. Finally, N gogo and Mahale chimpanzee
port is provided systematically and very rapidly to
males seem to use meat as a "political currency," and
attacked group members, and this has been seen to
they share meat preferentially with their social allies.
save the lives of the attacked individuals (Boesch,
Thus, in chimpanzees, cooperation in the context of
2009).
hunting is embedded in a series of different social
Naturalistic observations with primates show
patterns that contribute to whether the cooperative
that cooperation is observed in many contexts and
action is beneficial or not.
has some important consequences for the social
Team work has also been systematically observed
life of the individuals. It is not so much the exis­
during territory defense in chimpanzees (Boesch,
tence of cooperation with unrelated individuals
2009; Boesch & Boesch-Achermann, 2000; Boesch
that contrasts chimpanzees from humans, as has
et al., 2008; Goodall et al., 1979; Goodall, 1986;
often been proposed, but rather the fact that coop­
Watts & Mitani, 2001; Watts, Muller, Amsler,
eration can involve larger numbers of individuals to
Mbabazi & Mitani, 2006). This situation is some­
an extent rarely, if ever, seen in other primate spe­
how different than hunting, because cooperation in
cies. However, in both chimpanzees and humans,
this context is less about increasing benefits and more
this seems directly influenced by the demographic
about decreasing the costs of encountering aggres­
properties of the society; and since humans live in
sive neighbors; in chimpanzees, such aggression can
decidedly larger groups than chimpanzees, we more
lead to the death of outnumbered individuals. Even
frequently observe large cooperative groups of unre­
at the onset of patrol, adult males come together and
lated individuals in humans.
wait for enough of them to join before leaving to
patrol the boundaries of their territory. Once they
spot neighbors, the chimpanzees will face them as a
An Evolutionary Approach to the Study of
Cooperation
close team, and victory seems to clearly lean in favor
From this background, it is intriguing that
of larger teams. It is important to note that such
so
team work can include an impressive number of
with captive chimpanzees have resulted in nega­
many
experimental
studies
on
cooperation
males; in the exceptionally large Ngogo community,
tive results and that so much attention has been
up to 27 males have been seen to join forces to attack
14.6 males) (Watts & Mitani,
devoted to them (see reviews of experimental stud­
ies on this topic in Warneken & Melis, chapter 21
200 1). Thus, depending on the demographic condi­
of this volume, Tomasello et al., 2005). The main
tions, team work can reach impressive dimensions in
point to remember when trying to make sense out
neighbors (average
492
I
=
THE ECOLOGY AND EVOLUTION OF
SOCIAL
BEHAVIOR
of the sometimes very contradicrory results that
human subjects tend ro show much more willing­
have emerged from experimental captive studies in
ness ro cooperate or help in artificial laborarory
comparison with naturalistic observations is that
conditions than in real life (see Bradsley, 2008;
animals adapt to the specific socio-ecological con­
Lesorogol, 2007; Levin & List, 2008; List, 2006,
ditions they face in nature and will be selected ro
2007). In addition, by manipulating experimental
use some behavioral parrerns only if the conditions
procedures, it is possible ro dramatically influence
experienced favor them (see Figure 26.2). In other
the tendency ro share in humans from different cul­
words, cooperation will be observed only if the con­
tural backgrounds. Therefore, as in the economic
diti ons are such that teamwork pays off. Therefore,
sciences, one of the greatest challenges of captive
to understand this, we must first turn roward the
psychological studies is to demonstrate its applica­
conditions in the wild, because only animals can reil
bility in the real world (see Alien, 2002; Bekoff &
us what those favorable socio-ecological conditions
Alien, 1997; Boesch, 2007, 2008; de Waal 2001)
can be.
Some have argued that only experimental captive
The general and often uncritical acceptance of
experimental studies with primates seems to rest
srudies can provide answers about the proximate
on an unformulated Cartesian assumption (Penn et
mechanisms explaining the facrors underlying some
al. , 2008; Penn & Povinelli, 2007; Tomasello et al. ,
cognitive abilities, such as those necessary ro coop­
2005), whereby the role of the environmental con­
erate or help (Galef, 1990; Heyes, 1993; Povinelli,
ditions on the cognitive development of individu­
2000; Tomasello & Call, 1997). Notwithstanding,
als is considered ro be minimal (see Figure 26.2).
rhe general consensus is that "fieldwork is pri­
Cooperation in wild chimpanzees, as we saw, con­
mary. It tells us what animals do; it sets the prob­
centrates on some specific ecological situations, like
lem" (Tomasello & Call 2008, p. 451). Therefore,
hunting, and predator and terrirorial defense, which
we could have expected that experimental setrings
are not present in captive conditions. Ideally, experi­
would have presented problems similar ro those that,
mental studies should measure the ability for cooper­
in the wild, elicited the behavior or ability under
ation in chimpanzees in those three specific contexts.
srudy. Sadly, this seems not ro have been the priority
However, this has never been done. Obviously
of the majority of experimental studies. However,
duplicating or mimicking such situations in captiv­
"laborarory experiments can illuminate a species'
ity is far from simple, but at the least, this strong
abilities only if their results can be placed within the
limitation in the "ecological validity" of any captive
context of an animal's natural social behavior. In the
study of cooperation should be addressed. The low
absence of such grounding, rhey remain difficult, if
level of cooperation found in captive chimpanzees
not impossible, to interpret" (Cheney & Seyfarth,
might simply reflect the impossibility of provid­
2007, p. 26). The results of experiments may simply
ing ecologically valid situations in such setrings, as
be artifacts of experimental procedures used, which
well as the difficulties of mimicking conditions that
may tell us rather little about natural abilities.
might, from the chimpanzee's point of view, require
In humans, it has now been shown that subjects
cooperation (Boesch, 2007, 2010; de Waal, 200 1).
respond quite differently ro experimental condi­
Recently, higher consideration for the social dimen­
tions compared ro real life situations, and, as a rule,
sion of cooperation has led to better performance
Figure 26.3 Schematic illustration of the effect of socio­
Cross-species comparison of social cognition
ecological conditions on the development of social cognitive
skills in humans and chimpanzees, two species living in very
different ecological conditions. The arrows illustrate two types
of comparative approaches: the first (A) compares populations
of two species living in very different socio-ecological
conditions as is too often done with captive chimpanzee
Social skills
"U
�
u
-�
:.c
a.
0
Vl
studies, and the second (B) shows a preferable comparison,
one between species living under comparable socio-ecological
co nditions.
Ql
a.
E
Vi
Simple
Socio-ecolo�icalniche
BOESCH
Complex
I
493
by subjects in captive experimental settings (Hirata
& Fuwa, 2007; Melis, Hare, & Tomasello, 2006).
It remains that providing individuals with constant
and overabundant food in human-planned social
groups with no life-threatening challenges may be
far from ideal for mimicking the socio-ecological
situations under which we see chimpanzees cooper­
ate in the wild (see Figure 26.3). "Ecological valid­
ity" in captive conditions is a central limitation and
makes the use of captive studies very unsatisfYing
for studying such complex social behavior as coop­
eration, altruism, and reciprocity.
Evolutionary theory predicts that cognitive abili­
ties will be shaped by the daily challenges encoun­
tered during the life of an individual, in that the
abilities that have been successfully solved by other
captive chimpanzees living in larger age-grad ed
groups. Therefore, this limitation may reflect a dif­
ference in the upbringing conditions experienced by
these individuals and not a species-specific limita­
tion (Alien, 2002; Boesch, 2010). The discussion
about the influence of methods used during experi­
ments is still very much in its infancy in comp ar ative
psychology (see Barth, Reaux & Povinelli, 2005; de
Waal & Ferrari, 2010).
Recently, a shift has been proposed in some of
the psychological literature stating that it is nor
the mere fact of cooperating that is suggested to
be unique to humans but more the precise motiva­
tion underlying such an action. Human coopera­
more challenging the situation is, the more sophis­
tion is rooted in a general tendency toward shared
ticated the cognitive solutions will be (Barren et al.,
2007; Boesch, 2007, 2010; Cheney & Seyfarth,
goals and intentions, whereas animal cooperation
is a purely individualistic optimizing act (M�ll &
1990, 2007; de Waal, 2001) (see Figure 26.3).
Tomasello, 2007; Tomasello et al., 2005). Detailed
Therefore, in all animal species, including humans,
observations of cooperative hunting behavior in
we should expect to see different levels of cognitive
chimpanzees completely contradict such claims (see
performances, the more diverse the ecological condi­
Boesch, 2002, 2005, 2010), because the perfor­
tions faced by different populations in those species.
mance of some hunting roles, like driving the prey,
Extensive differences in folk psychology, coopera­
are not compatible with an individual optimization
tion, altruism, and logic have been documented in
interpretation; such roles rarely lead to a capture,
different human societies living under very diverse
and the amount of meat received by the hunters is
ecological and economic conditions (Arran, Medin,
relatively low. The more general issue when stating a
& Ross, 2005; Henrich et al., 2005, 2006, 2010;
difference in motivation is that such a proposition is
Marlowe et al., 2008; Nisbett & Miyamoto, 2005).
basically not testable with nonspeaking animal spe­
W henever we make comparisons between spe­
cies in natural conditions, and as such, it is more an
cies, it is essential that we consider this aspect and
act of faith than a scientific hypothesis. In addition,
limit our comparisons to populations facing similar
when the proponents of such ideas tend to deny the
socio-ecological challenges (see Figure 26.3, where
conclusive value of data collected from naturalistic
comparison B should be privileged over comparison
observations (see Povinelli 2000; Penn et al., 2008;
A) (Boesch, 2007, 2010). If we do not do this, there
Tomasello & Call, 1997; Tomasello et al., 2005),
is no way we can determine if the differences we
the discussion is not a matter of scientific enquiry
observe are due to differences between the two spe­
but of intellectual preference.
cies or differences within one species due to differ­
ent socio-ecological conditions. For example, from
Evolution of Altruism
studies done with a very small peer group of chim­
Altruism has been defined as a costly act that
panzees separated from their mothers and kept in
one individual provides to another individual, who
artificial living conditions, it has been proposed that
directly benefits from it (see Box 26.1; Axelrod &
chimpanzees cannot understand nonvisible rela­
Hamilton, 1981; de Waal, 2008; Hamilton, 1964;
tions (Povinelli, 2000), and this has subsequently
Krebs & Davies, 1991; Maynard-Smith, 1982;
been proposed as a key difference distinguishing
Trivers, 1971; West & Gardner, 2010). As such,
humans from chimpanzees (Penn et al., 2008). The
altruism is a puzzle because it is not expected to
experience faced by those individuals is very similar
occur under an evolutionary framework in which
to those faced by a socially deprived rhesus macaque
individuals are expected to be selfish and to invest
group that has been shown to be socially incom­
only when it is beneficial to themselves. However,
petent compared to individuals reared in larger
many behavioral patterns that have been seen in
animals look as if they are altruistic, such as the
age-graded social groups (Kempes et al., 2009). In
addition, this peer group of chimpanzees failed in
numerous instances of food sharing seen in many
many tests of abilities seen in wild populations, and
animal species, instances of helping injure d
494
I
THE ECOLOGY AND EVOLUTION OF SOCIAL BEHAVIOR
or
needy
adoptions. Two main
species for different lengths of time. Adoption is
evolutionary mechanisms have been proposed to
explain the evolution of altruism. The first is kin
individuals,
and
a very costly behavior because it involves carry­
selection, whereby individuals would behave altru­
istically only to closely related individuals and so
infant for many months (Boesch, Bole, Eckhardt
would indirectly benefit themselves (Hamilton,
Thierry & Anderson, 1987). In many instances,
ing, suckling, protecting, and caring for the foster
& Boesch, 2010; Goodall, 1986; Riedman, 1982;
1964). The second mechanism that would lead
the adoption is performed by related group mem­
ro the evolution of altruism is reciprocal altruism
between unrelated individuals, by which individu­
bers, mostly siblings of the orphans, but they are
also performed by unrelated group members. In
als would reciprocate altruistic acts preferentially
chimpanzees, adoption has been seen regularly and
roward individuals who have been altruistic with
since orphans younger than five years of age do not
rhem (Axelrod & Hamilton, 1981; Trivers, 1971).
survive, adoption is hugely important to them. In
Because altruism between genetically related
TaY chimpanzees, half the orphans are adopted and
individuals indirectly contributes to the inclusive
fiwess of the individual, it is altruism between
Specifically, adult males have been seen to adopt
nonrelated individuals that has drawn more atten­
orphan males and females that they are not related
males do half these adoptions (Boesch et al., 2010).
tion. As seen in primates, reciprocal altruism will
to, and some of these adoptions lasted for years.
work in small stable social groups in which indi­
Skeptics of altruism in animals have suggested that
viduals always have certain likelihoods of interact­
adoption could be attributed to errors, whereby the
ing with one another in the future. In very large
males would mistakenly view the orphan as his own
and anonymous groups, as seen in some human
offspring, but this argument certainly does not hold
societies and many insect and bird species, this
up with adoptions by adult females, who perform
is less certain, and the evolution of altruism is
50 percent of the adoptions in the TaY chimpan­
more difficult to understand. However, it has
zees. An additional contradiction comes from the
been shown that individuals within groups do
fact that chimpanzee males seem to recognize their
nor interact with others at random but tend to
own offspring (Lehmann, Fickenscher, & Boesch,
bias their interactions toward a limited number of
2006).
group members, and, as confirmed in models, this
In chimpanzees, some of the altruistic behaviors
would then make the evolution of altruism much
suggest that they have a notion of the needs of oth­
more likely (Barrett, Gaynor, & Henri, 2002; de
ers, and that they are willing to take a great deal
Waal, 2008; Nowak, 2006).
of risk to help others (e.g., Boesch, 2009; de Waal,
To confirm this, sharing and helping are two
2008). Altruism in the form of risky help is regularly
forms of altruism that have been regularly observed
seen, as was already mentioned, toward individu­
in wild chimpanzee populations as well as other pri­
als in difficult situations, such as during predator
mate species (Boesch et al., 2008, 2010; de Waal,
attacks or intergroup encounters (Boesch, 2009;
2001, 2008; Mitani et al., 2002). Furthermore,
Boesch & Boesch-Achermann, 2000). It is impor­
in chimpanzees, meat sharing between unrelated
tant to note that leopard or chimpanzee attacks are
adult males happens in all populations and the
not immediately fatal and, therefore, there is always
sharing rules are influenced by the social proper­
a time window in which individuals can successfully
ties of the population. This suggests that specific
rescue the victim. This may explain why such help
benefits are pursued by the meat owner. However,
is seen more often in large primates, like chimpan­
meat is shared with many more individuals than
zees, rather than in smaller primates, like baboons,
only the male hunters or his allies, and in many of
where leopard attacks are generally fatal (Cheney &
these instances, they include nonrelated individu­
Seyfarth, 2007). It is puzzling that such altruistic
als. In addition, meat is spontaneously and actively
support seems to be provided with different fre­
offered by meat owners to other group members
quency in different chimpanzee populations (Boesch
(e.g., in Tai· chimpanzees, up to 7 percent of all
et al., 2008; Boesch, 2009). In fact, TaY chimpan­
bystanders by
zees have been reported to regularly help victims in
the meat owner and 32 percent of the meat access
such situations, whereas such help is rarely reported
meat transferred is actively given
to
is actively facilitated by the meat owner; Boesch &
in the Gombe or Ngogo chimpanzee communities.
Boesch, 1989).
Such help can be reciprocated months or years later
Altruism in the form of adoptions of orphans by
adult group members has been seen in many primate
in some instances, but on other occasions, this help
is just provided to aid others.
BOESCH
I
495
An Evolutionary Approach to the Study of
placed on the action space, the imposition of task,
Altruism
the selection rules into the environments, and the
Some have proposed that altruistic acts toward
unrelated group members are unique to humans
and are an essential characteristic of human sociality
(Fehr & Fischbacher, 2003; Fehr & Gachter, 2002;
stakes typically at risk. In contrast to the lab, many
real-world markets operate in ways that make pro­
social behavior much less likely ... Because the lab
systematically differs from most naturally occurring
Hrdy, 2009; Silk et al., 2005; Vonk et al., 2008;
environments on these dimensions, experiments rnay
Warneken, Hare, Melis, Hanus,
not always yield results that are readily generalizable.
& Tomasello,
2007). Luckily, Homo sapiens is the most studied of
(Levitt & List, 2007, p. 168-169)
all animal species and, because altruism is consid­
ered a topic of central importance, we have access
They concluded that "[p]erhaps the greatest chal­
to a great many studies to help us qualify such a
lenge of behavioural economists is demonstrating
strong claim.
its (the laboratory's) applicability in the real world"
First, detailed experimental studies have now
(Levin & List, 2008, p. 909), and that "the data
been performed in many different human societies,
suggest that current interpretations of dictator garne
and the tendency to share has been observed in all of
data likely need revision. Rather than representing
them (Henrich et al., 2006, 2010; Gintis, Bowles,
social preferences as currently modeled in the oft­
Boyd & Fehr, 2003). However, the tendency to
cited literature, the data are consistent with the
share is dramatically different in different human
power of changing the giver and recipient expecta­
societies. For example, the way western university
tions" (List 2007, p. 490). For example, the proso­
students share, which has formed the basis for the
cial or altruistic tendency in humans was extensively
preceding claim, has been shown to be nonrepre­
documented in numerous studies using the Dictator
sentative of humans, who generally share much less
game. Such a game, in which the dictator receives a
and are reluctant to punish those who do not share.
lump sum of money and can give as much as he
In humans, sharing and altruistic punishment have
wants to a receiver who cannot retaliate even when
been shown to decrease in smaller human societies
he gets nothing, has been used in many situations;
(Marlowe et al., 2008) and are less frequent in less
humans tend to always give something. This has
socioeconomically developed societies (Gintis et al.,
been used to support claims of a universal human
2003; Henrich et al., 2010).
tendency to care for the welfare of others. However,
Second, many economists have been concerned
the difficulties any charitable organization encoun­
about the "ecological validity" of the experimen­
ters in collecting enough donations for their activi­
tal work, and they have carefully looked at both
ties show that this conclusion is totally unrealistic.
the effects on the subjects of the procedures used
More precise studies have shown that this conclu­
during experiments and at the differences in reac­
sion holds only as long as the dictator knows that
tions between individuals tested in the laboratory
the receiver is expecting something. In contrast,
and those tested in the real world (see review e.g.,
if the receiver is not aware a game is taking place,
Levin and List, 2007, 2008). Such comparisons
the dictator is willing to exit the game without giv­
have revealed that humans react differently in the
laboratory (subjects tend to be more generous than
ing anything to the receiver in almost 50 percent
of the cases (Dana, Cain, & Dawes, 2006). Such
in real life) and that very different results can be
studies have shown that giving does not necessar­
obtained according to the procedures used during
ily reflect a prosocial tendency bur instead might be
the experiment.
strongly affected by the expectations of others (see
also Bradsley, 2008; Henrich et al., 2010 for similar
We believe that several features of the laboratory
conclusions). Recognizing the specific effects labo­
setting need to be carefully considered before
ratory experiments have on subjects is essential if we
generalizing results from experiments that measure
want to understand the natural social behaviors of
pro-social behaviors to market settings they
human and nonhuman primates.
purport to describe ... Such factors include both
the representativeness of the situation as well as the
representativeness of the population: the nature
and extent of scrutiny, the emphasis on the process
by which decisions are made, the artificial limits
I
THE ECOLOGY AND EVOLUTION OF
From this perspective, it is intriguing that experi­
mental psychologists have so rarely questioned th e
"ecological validity" of their captive experiments.
Studies on altruism and helping with captive chim­
panzees have resulted in negative or mixed results
SOCIAL BEHAVJOR
(see review, chapter 20 of this volume, and e.g.,
demanding (Stevens & Hauser, 2004). In particu­
Brosnan et al., 2009; Jensen, Call & Tomasello,
lar, temporal discounting, numerical discounting,
2007; Silk et al., 2005; Vonk et al., 2008; Warneken
and memory would make reciprocity difficult for
& Tomasello, 2006; Yamamoro & Tanaka, 2010).
animals. However, more thorough reviews of the
From these, comparative psychologists have sug­
evidence support the fact that reciprocity plays an
gested that altruism, in the form of sharing and help­
important role in grooming exchange in primates,
in g, can sometimes be found in captive experimental
situations, but that chimpanzees have limited inter­
a result that is explained as resulting from simpler
cognitive mechanisms (Schino & Aureli, 2010).
est in doing so, either because food sharing is very
A detailed study in Tal chimpanzees illustrates
difficult for them Uensen er al., 2007; Warneken
the question of reciprocity in primates; the symme­
& Tomasello, 2006), or because sharing does not
try of grooming exchanges within dyads increases
co me spontaneously but will follow from a request
as longer time windows are considered (up ro 15
fro m a partner (Yamamoro & Tanaka, 2010), or
months) and reaches more than 83 percent (Gomes
because they are indifferent ro the welfare of oth­
er al., 2009). Because grooming interactions in the
ers (Silk et al., 2005). The contradicrory outcomes
fluid social system of chimpanzees were observed
of such experiments, however, suggest an intrinsic
only between the same dyads every seventh day
problem with the methods used, as has been shown
(range
in humans; captive chimpanzee seems ro be reacting
can only be achieved with some means of keeping
ro the specific procedures used for each of the dif­
track of past interactions. Besides grooming interac­
=
2 ro 18 days), such levels of reciprocity
ferent experimental settings used with them, rather
tions, Tal chimpanzees trade meat for sex as well as
than reacting ro a specific "sharing with other ten­
meat for support with all adult group members, and
dency" (see also a very recent result confirming this
they also reciprocate support interactions (Gomes
by Homer et al., 2011).
& Boesch, 2011). Two proximate mechanisms have
been proposed for individuals ro keep track of past
Evolution of Reciprocity
In stable social primate groups, group members
interactions:
"emotionally mediated"
scorekeep­
ing and calculated reciprocity (de Waal & Luttrell,
can potentially interact over many years, and, there­
1988; Schino & Aureli, 2009). The first is based on
fore, there are plenty of opportunities ro reciprocate
the emotional attitude that develops between part­
aggressive or affiliative interactions. Repeated social
ners as a consequence of prior affiliative or aggres­
interactions would increase the efficiency of coop­
sive interactions. Calculated reciprocity, on the
erative and altruistic interactions because they would
other hand, requires a detailed cognitive accounting
make it possible ro distinguish between potential part­
of the amount of services given and received. When
ners in terms of quality and reliability and, therefore,
distinguishing between these two mechanisms, it is
limit the problem of cheaters. Such a benefit would
important to remember that the amount of groom­
be especially important in animal species that main­
ing and support interchanged as well as the trading
tain long-term associations between certain group
of meat and support varied dramatically within and
members, as has been shown in some primate spe­
between dyads, requiring that an emotion-based
cies (e.g., Lehmann & Boesch, 2005; Mitani, 2009a;
scorekeeping be sufficiently structured so that it
Silk, Alberts & Altmann, 2006b). This, in turn, could
would allow each individual ro precisely differ­
increase rhe survival and reproductive success of indi­
entiate and update among 43 ro 52 adult dyadic
viduals (Silk, Alberts, & Altmann, 2006a).
When a researcher is faced with this large poten­
tial advantage ro long-term social reciprocity, it is
interactions. Such structured emotion-based score­
keeping would possibly be very similar to full blown
calculated reciprocity.
puzzling how hard it was ro find conclusive evidence
of reciprocity in primate species (see Barrett et al.,
Discussion
2002; Gomes, Mundry & Boesch, 2009; Hauser,
The present review of social behaviors and cog­
2006). In some species, only evidence of short-term
nitive abilities in primates supports the evolution­
reciprocity could be found; for others, nothing; and
ary approach by showing the key importance of
for a few, some long-term reciprocity. However, in
the socio-ecological challenges on the behavioral
many cases, alternatives ro reciprocity have been
solutions adopted by the individuals. Convergent
forwarded. Following this, it has been proposed that
evolution of similar social behavior and cognitive
reciprocity in animals must be rare because it is roo
solutions have been seen in such diverse species as
BOESCH
I
497
crows, ravens, scrub jays, dogs, fish, baboons, rhesus
populations to understand the interplay betwee n
monkeys, chimpanzees, and humans (Boesch, 2007;
socio-ecological influences and the expression of
Cheney & Seyfarth, 2007; Bshary et al., 2008; de
the different behavioral patterns. Until shown dif­
Waal, 2008; de Waal & Ferrari, 2010; Pitch et al.,
ferently, at present, we can say that, in chimpan­
2010). Similarly, in species living in different eco­
logical challenges, we observed the adoption of large
numbers of different behavioral and cognitive solu­
tions, and this effect was more pronounced in more
adaptive species (Boesch, 2007, 2009; Henrich et
al., 2010). Such observations are not compatible
with a Cartesian approach to the evolution of social
zees, cooperation is concentrated in social domains
in which teamwork is mandatory for solving chal­
lenges. W hen the conditions vary, however, co op­
eration may disappear and individual solutions
will be preferred. Because teamwork requires all
participants to coordinate their behaviors with one
another in time and space, as well as share the risks
ignored or dismissed as naturalistic anecdotes (Penn
and benefits, we should expect such complex group
actions to be performed only if necessary. Assuming
et al., 2008; Povinelli, 2000; Tomasello & Call,
that animal species possessing the cognitive abilities
behavior and cognition, and have often been simply
1997; Tomasello et al., 2005).
Social interactions are adaptive responses to the
to cooperate or help should always do so ignores the
costs that are associated with such social behaviors.
specific circumstances encountered by individuals
Therefore, ecological validity is of central impor­
within their social groups. If circumstances change,
tance if we want to understand the evolution of
social behavior.
we would expect individuals to adapt their behav­
ior so that they make the best out of the situations
they face. Long-term studies have proven to be one
Future Directions
of the best approaches to address such issues, and
The field of social cognition has been dominated
they have provided many insights into the flexibil­
by a debate about the value of captive animal experi­
ity of primate social behavior patterns. For example,
ments (e.g., Alien, 2002; Boesch, 2007, 2008; de
female chacma baboons have been shown to adapt
Waal, 2001; Tomasello & Call, 1997). On one side
their social interactions to variations in competi­
of the debate, experiments are the only way to pro­
tion levels (Barrett et al., 2002). A similar flexible
vide answers to cognitive questions, because this is
response to the ecological and social circumstances
the only way to control for all possible factors that
has been shown in the dispersal decisions by males
influence individuals in their natural life (Galef,
in different species of baboons (Alberts & Altmann,
1990; Heyes, 1993; Penn et al., 2008; Tomasello &
1995; Clarke, Henzi, Barrett & Rendall, 2008). In
Call, 1997). This has led some scientific disciplines,
line with this, cooperation has been shown to be
like experimental and comparative psychology, to
flexible and observed mainly in situations in which
concentrate on captive studies to the point that one
the individual is paid off for investing in such joint
has the impression that animals live only in captivity
efforts.
and that wild animals are outliers. To highlight this,
In chimpanzees, cooperation is flexibly
observed when hunting arboreal monkeys, and in
some high-profile experimental studies on animal
communal defense against predators and conspe­
cognition do not cite even a single study of their
cific neighbors. Similarly, altruism is concentrated
study species living under natural conditions. Not
in cases when high-value food resources are shared
surprisingly, on the other side of the debate, captive
and when recipients are provided with large benefits
studies have been strongly criticized for having very
like support and adoptions.
little to no ecological validity and presenting ani­
Comparative studies on potential differences in
mals with extremely artificial situations (Barrett et
social behavior and cognitive abilities have made
al., 2007; Boesch, 2007, 2010; Cheney & Seyfarth,
a great deal of progress thanks to the increasing
2006; de Waal, 2001). The fields of comparative
number of detailed long-term studies with different
and experimental psychology sometimes see captive
primate species, which, for the first time, have pro­
studies from a Cartesian approach, by which the
vided science with insight into "how primates see
differences in upbringing and ecology are consid­
the world" (e.g., Boesch, 2009; Cheney & Seyfarth,
1990, 2007; Goodall, 1986). At the same time, the
ered of very little relevance for understanding the
performance of an animal species. However, until
confirmation of important differences within a spe­
the impact of development and ecology is clearly
cies has greatly complicated the task for compara­
integrated into our thinking, our understanding of
tive studies, because it requires a large number of
species differences will remain totally biased and
'i
I
THE ECOLOGY AND
EVOLUTION OF
SOCIAL
BEHAV!OR
incomplete. To make some progress in solving this
by the infants leads to earlier mirror recognition in
debate, it seems important to have more informa­
both humans and chimpanzees (Bard et al., 2005;
tion on the following points:
1. QuantifY the role of ecological differences on
the development of social behavior and cognition
in different primate species.
It is striking that, after over 100 years of compara­
Ijzendoorn, van Bard, Bakermans-Kranenberg &
Ivan, 2009; Keller et al., 2004). Such pioneering
work should be replicated and applied to many other
behavioral domains to see how different aspects of
social cognition are affected by early experience dur­
ing upbringing. The whole field of cognitive science
tive psychology, no systematic study exists on the
would benefit from following the economic sciences
role of captivity on the development of social behav­
ior and cognition. The closest study was undertaken
by specifically designing studies aimed at quantify­
in the 1960s by Gardner and Gardner (1989) with
mance of the individual subjects.
a small sample size, by comparing only two different
rearing conditions. This study clearly showed that
young chimpanzees differed strongly in all possible
measures. Sadly, such a pioneering study was nor fol­
lowed, and we are left wondering about such effects
ing the role of experience and design in the perfor­
3. Develop an understanding of the specific
factors affecting the evolution of cooperation and
altruism.
Cooperation,
altruism,
and
reciprocity
have
(see, however, Lyn, Russel, & Hopkins, 2010). In
become important social domains in defining
economic science, this has been done to the point
potentially unique differences between humans
rhat some argue that "behavior in the lab might be
and other primate species. However, the whole dis­
poor to real-world behavior" (Levin & List, 2008).
cussion is impaired by a lack of understanding of
In a sense, this important gap in our knowledge
the conditions under which such behavioral pat­
allows psychologists
maintain dramatically differ­
terns evolve. Most observations of cooperation and
ent opinions. It is not that we are missing data on the
altruism have been done in natural social groups
dramatic consequences of strongly deprived captive
and directed toward life-long group members who
conditions, as they still prevailed in the early 1950s
solve challenges they encounter within their envi­
to
(Harlow & Harlow, 1962), but direct comparisons
ronments. On the other hand, most observations
with wild living animals have not been done. We saw
that found primates to be incompletely or unable
that even relatively small deprivations can have large
to cooperate, help, or share with others were done
and long-lasting detrimental effects on an individu­
with captive individuals facing artificial conditions
al's development, and we are simply missing more
(e.g., Povinelli, 2000; Tomasello et al., 2005). New
information of the effect of this on different primate
experiments taking into account the social dimen­
species. Only with such studies will cognitive sci­
sion of cooperation and altruism have tried to pres­
ences be able to scientifically evaluate the applicabil­
ent more natural choices to the tested individuals,
ity of captive studies to the real world.
2. QuantifY the effects of different upbringing
conditions on the cognitive development of the
individuals.
Upbringing has been shown to have very impor­
tant and long-lasting effects in individual humans,
and the field of social psychology has provided data
on how poor socioeconomic conditions are detri­
mental to the development of social cognitive skills.
and they have already shown clear improvements in
performance (Melis et al., 2006). More studies in
this direction will allow us to gain a better under­
standing of the social dimension of such behavior
patterns and provide an explanation of why animals
p
rend to cooperate less and be less hel ful in captive
conditions than in the wild (Boesch, 2010).
4. Study nonhuman animals without
anrhropocentrism.
Recently, more efforts have been done to quantifY
Too often, the field of comparative psychology
some of these effects in chimpanzees facing different
has been guided by an anthropocentric approach,
social conditions in captive settings, and they have
by which humans look to other animal species to
shown strong but specialized effects. For example,
explain specific human abilities (Alien, 2002; Barren
mirror recognition, often considered as a measure of
er al., 2007). Furthermore, many of these anthropo­
self-recognition, has been shown to be strongly influ­
centric approaches are ethnocentric as they do not
enced by maternal style toward babies: more stimu­
take into account that what occidental humans do is
lation by the mothers and independent movements
far from being representative of what all humans on
BOESCH
I-
499
this planet do (Boesch, 2007; Henrich et al., 2010).
Chimpanzees, rhesus monkeys, and ravens are not
humans, and, therefore, it would make more sense
Boesch, C. (2002). Cooperative hunting roles among Tai' chim­
panzees. Human Nature, 13, 27-46.
Boesch, C. (2005). Joint cooperative hunting among wild chim­
panzees: Taking natural observations seriously. Behavioral and
to ask how they solve their specific ecological and
social problems. In this way, we could gain a better
understanding about the evolution of abilities that
are used in nature and on which our ancestors have
built to produce our modern human abilities. Too
Brain Sciences, 28, 692-693.
Boesch, C. (2007). What makes us human (Homo sapiens)? The
challenge of cognitive cross-species comparison. journal of
Comparative Psychology, 121, 227-240.
Boesch, C. (2008). Taking ecology and development seri­
ously when comparing cognition: Reply to Tomasel!o
often, animals are confronted with challenges that
do not address their natural abilities, and the nega­
and Call 2008. journal of Comparative Psycholo gy, 122,
453-455.
tive answers might just reflect our own inability to
Boesch, C. (2009). 7he real chimpanzee: Sex strategies in the forest.
set ourselves in the mind of others.
Cambridge, England: Cambridge University Press.
Boesch, C. (2010). Away from ethnocentrism and anthropocen­
trism: Toward a scientific understanding of "what makes
Alberts, S., & Altmann, J. (1995). Balancing costs and opportu­
Boesch, C., & Boesch, H. ( 1989). Hunting behavior of wild chim­
panzees in the Tai National Park. American journal ofPhysical
nities: Dispersal in male baboons. American Naturalist, 145,
279-306.
Alcock, J. (1989). Animal behavior: An evolutionary approach
Anthropology, 78, 547-573.
695-702.
of the Tai Forest: Behavioural ecology and evolution. Oxf ord
England: Oxford University Press.
panzees in the Tii forest, Cote d'Ivoire. In C. Boesch, G.
Altruism in chimpanzees: The case of adoption. PLoS One,
5, e8901.
Boesch, C., Crockford, C., Herbinger, I., Wittig, R., Moebius, Y.,
& Normand, E. (2008). lntergroup conflicts among chimpan­
Hohmann, & L. Marchant (Eds.), Chimpanzee behavioural
zees in Tai' National Park: Lethal violence and the female per­
diversity (pp. 90-101). Cambridge, England: Cambridge
University Press.
Arran, S., Medin, D., & Ross, N. (2005). The cultural mind:
spective. American journal ofPrimatology, 70, 1-14.
Bowles, S., Choi, J., & Hopfensirz, A. (2003). The coevolution
of individual behaviors and social institutions. journal of
Environmental decision making and cultural modeling
within and across populations. Psychological Review, 112,
744-776.
Axelrod, R., & Hamilton, W D. (1981). The evolution of coop­
eration. Science, 211, 1390-1396.
Bard, K., Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M.,
Costal!, A., & Matsuzawa, T. (2005). Group differences in the
Theoretical Biology, 223, 135-147.
Boyd, R., Gintis, H., Bowles, S., & Richerson, P. (2003). The evo­
lution of altruistic punishment. PNAS, 100, 3531-3535.
Bradsley, N. (2008). Dictator game giving: Altruism or artifact?
Experimental Economy, 11, 122-133.
Brosnan, S., Silk, J., Henrich, J., Mareno, M., Lambeth, S., &
Shapiro, S. (2009). Chimpanzees (Pan troglodytes) do not
mutual gaze of chimpanzees (Pan troglodytes). Developmental
develop contingent reciprocity in an experimental task. Animal
Psychology, 41, 615-624.
(2002). A dynamic
interaction between aggression and grooming reciproc­
Cognition, 12, 587-597.
Bshary, R., Grurrer, A., Willener, A., & Leimar, 0. (2008). Pairs
of cooperating cleaner fish provide better service quality than
ity among female chacma baboons. Animal Behaviour, 63,
1047-1053.
Barren, L., Henzi, P., & Rendall, D. (2007). Social brains, simple
minds: Does social complexity really require cognitive com­
plexity. Philosophical Transcriptions ofthe Royal Society, Series
singletons. Nature, 455, 964-967.
Cheney, D., & Seyfarth, R. (1990). How monkeys see the world.
Chicago: The University of Chicago Press.
Cheney, D., & Seyfarth, R. (2007). Baboon metaphysics: 7he
troglodytes) use of gaze cues in object-choice tasks: Different
Press.
Clarke, P., Henzi, S., Barren, L., & Rendall, D. (2008). On the
road again: Competitive effects and condition-dependent dis­
methods yield different results. Animal Cognition, 8, 84-92.
Bekoff, M., & Alien, C. (1997). Cognitive ethology: Slayers,
skeptics and proponents. In R. Mitchell, N. Thompson, &
L. Miles (Eds.), Anthropomorphism, anecdotes and animals:
7he emperor's new clothes? (pp. 314-334). New York: State
persal in male baboons. Animal Behaviour, 76, 55-63.
Clutton-Brock, T. (2009). Cooperation between non-kin in ani­
mal societies. Nature, 462, 51-57.
Cooper, S. (1991). Optimal hunting group size: The need for lions
to defend their kills against loss to spotted hyenas. Aftican
University of New York Press.
Berry, J., Poortinga, Y., Segall, M., & Dasen, P. (2002). Cross­
cultural psychology: Research and applications.
Cambridge, England: Can1bridge University
(2nd ed.).
journal ofEcology, 29, 130-136.
Dana, J., Cain, D., & Dawes, R. (2006). What you don't know
won't hurt me: Costly (but quiet) exit in dictator games.
Press.
Organizational Behavior and Human Decision Processes, 100,
Boesch, C. (1991). The effect of leopard predation on grouping
patterns in forest chimpanzees. Behaviour, 117, 220-242.
Boesch, C. (1994). Cooperative hunting in wild chimpanzees.
THE ECOLOGY AND EVOLUTION OF
193-201.
de Waal, F. (2001). 7he ape and the sushi master: Cultura l reflec­
Animal Behaviour, 48, 653-667.
500
evo­
lution of a social mind Chicago: The University of Chicago
B, 362, 561-575.
Barth, J., Reaux, J., & Povinelli, D. (2005). Chimpanzees' (Pan
'
Boesch, C., Bole, C., Eckhardt, N., & Boesch, H. (2010).
Anderson, D., Nordheim, E., Boesch, C., & Moermond, T.
(2002). Factors influencing fission-fusion grouping in chim­
.
Boesch, C., & Boesch-Achermann, H. (2000). 7he chimpanzees
(4th ed.) Sunderland, MA: Sinauer Associates.
Alien, C. (2002). A skeptic's progress. Biology and Philosophy, 17,
Barren, L., Gaynor, D., & Henzi, P.
us
human". Behavioral and Brain Sciences, 33.
References
SOCIAL
tions ofa primatologist. New York: Basic Books.
BEHAVIOR
de Waal, F. (2008). Putting the altruism back into altruism:
the evolution of empathy. Annual Review of Psychology, 59,
279-300.
Greenfield, P. (1999). Cultural change and human development.
New Directions for Child and Adalescent Development, 83,
37-59.
de Waa1, F., & Ferrari, P. (2010). Toward a bottom-up perspec­
tive on animal and human cognition. Trends in Cognitive
Sciences, 14, 201-207.
Hamilton, W D. (1964). The genetical theory of social behaviour
(I and II). journal of7heoretical Biology, 7, 1-32.
Harlow,H.,& Harlow,M. (1962). Social deprivation in monkeys.
de Waal, F., & Lurrrell, L. (1988). Mechanisms of social reci­
procity in three primates species: Symmetrical relationship
characteristics or cognition? Ethology and Sociobiology, 9,
101-118.
Scientific American, 207, 136-146.
Hauser, M. (2000). Wild minds: What animals really think. New
York: Henry Holt.
Hauser, M. (2006). Moral minds: 7he nature of right and wrong.
D ugatkin, L. (1997). Cooperation among animals: An evolution­
ary perspective. Oxford, England: Oxford University Press.
Emery, N., &
Clayton, N. (2004). Mentality
of
crows:
Convergent evolution of intelligence in corvids and apes.
Science, 306, 1903-1907.
New York: HarperCollins.
Hauser,M.,McAuliffe, K, & Blake, P. (2009). Evolving the ingre­
dients for reciprocity and spite. Philosophical Transactions ofthe
Royal Society, Series B, 364,3255-3266.
Henrich,].,Ensminger,J., Boyd, R., Henrich, N., Bowles, S., Hill,
Fehr, E., & Fischbacher, U. (2003). The nature of human altru­
ism. Nature, 425, 785-791.
K, Camerer, C., Gil-White, F., Fehr, E., Gurven, M., Gintis,
H., Marlowe, F., McElreath, R., Patron,J.,Alvard, M.,Tracer,
Fehr,E.,& Gachter,S. (2002). Altruistic punishment in humans.
Nature, 415, 137-140.
D., & Barr,A. (2005). "Economic man" in cross-cultural per­
spective: Behavioral experiments in 15 small-scale societies.
Fitch,T., Huber, L., & Bugnyar,T. (2010). Social cognition and
the evolution of language: Constructing cognitive phylog­
enies. Neuron, 65, 795-814.
Behavioral and Brain Sciences, 28, 795-855.
Henrich, J., Ensminger, )., McElrearh, R., Barr, A., Barren, C.,
Bolyanatz,A.,Cardenas,J., Gurven, M.,Gwako, E., Henrich,
Fox, S., Levitt, P., & Nelson, C. (2010). How the timing and
quality of early experiences influence the development of
brain architecture. Child Development, 81, 28-40.
N.,Lesorogol,C.,Marlowe,F., Tracer, D., &
Ziker,
J. (2010). Markers,religion,community size and the evolution
of fairness and punishment. Science, 327, 1480-1484.
Galef, B. (1990). Tradition in animals: Field observations and
laboratory analyses. In M. Bekoff, & D. Jamieson (Eds.),
Interpretation and explanation in the study of animal behavior
(pp. 74-95). Boulder, CO: Wesrview Press.
Henrich,]., Heine, S., & Norenzayan,A. (in press). The weirdest
people in the world? Behavioral and Brain Sciences.
Henrich, )., & Henrich, N. (2006). Culture, evolution and the
puzzle of human cooperation. Cognitive Systems Research, 7,
Gardner, B.,& Gardner,R. (1989). Prelinguistic development of
children and chimpanzees. Human Evolution, 4, 433-460.
220--245.
Henrich, J., McElreath, R., Barr, A., Ensminger, J., Barren, C.,
Gilby,I. (2006). Meat sharing among the Gombe chimpanzees:
Bolyanarh,A., Cardenas,J.,Gurven,M.,Gwako,E., Henrich,
Harassment and reciprocal exchange. Animal Behaviour, 71,
N., Lesorogol, C., Marlowe, F., Tracer, D., & Ziker,J. (2006).
953-963.
Costly punishment across human societies. Science,
Gilby, I., Eberly, L., Pintea, L., & Pusey, A. (2006). Ecological
312,
1767-1770.
and social influences on the hunting behaviour of wild chim­
Heyes,C. M. (1993). Anecdotes, training,trapping and triangular­
panzees,Pan troglodytes schweinfurthii. Animal Behaviour, 72,
ing: Do animals attribute mental states? Animal Behaviour, 46,
177-188.
169-180.
Wrangham, R. (2008). Economic
Hirata,S.,& Fuwa, K (2007). Chimpanzees (Pan troglodytes) learn
profitability of social predation among wild chimpan­
to act with other individuals in a cooperative task. Primates,
Gilby, I., Eberly, L., &
zees: Individual variation promotes cooperation. Animal
Gintis, H., Bowles, S., Boyd, R., & Fehr, E. (2003). Explaining
altruistic
behavior
in
48, 13-21.
Homer, V., Carter, D., Suchak, M. and de Waal, F. 2011.
Behaviour, 75, 351-360.
humans. Evolution
and
Human
Behavior, 24, 153-172.
Gomes, C., & Boesch, C. (2009). Wild chimpanzees exchange
meat for sex on a long-term basis. PLoS One, 4, e5116.
Gomes, C., & Boesch, C. (2011). Reciprocity and trades in
Spontaneous prosocial choice by chimpanzees. PNAS. Early
edition,doi: 10.1073/pnas 1111088108.
Hrdy, S. (2009). Mothers and others: 7he evolutionary origins of
mutual understanding. Cambridge, MA: Belknap Press of
Harvard University.
Ijzendoorn,M.,van Bard,K, Bakermans-Kranenberg,M.,& Ivan,
wild West African chimpanzees. Behtwioral Ecology and
K (2009). Enhancement of attachment and cognitive develop­
Sociobiology, published online 26 July 2011. doi: 10.1007/
ment of young nursery-reared chimpanzees in responsive versus
s00265-011-1227-x.
Gomes, C., Mundry, R., & Boesch, C. (2009). Long-term recip­
standard care. DevelopmentaiPsychobiology, 51, 173-185.
Jaeggi, S., Buschkuehl, M., Jonides, ]., & Perrig, W (2008).
rocation of grooming in wild West African chimpanzees.
Improving fluid intelligence with training on working mem­
Proceeding}· ofthe Royal Society B. 276, 699-706.
ory. Proceedings of the National Academy of Science, 105,
Goodall,J. (1986). 7he chimpanzees ofGombe: Patterns ofbehav­
ior. Cambridge,MA: Belknap Press of Harvard University.
Go odall,]., Bandura, A., Bergmann, E., Busse, C., Matam, H.,
Mpongo, E., Pierce,A., & Riss, D. (1979). Inter-community
interactions in the chimpanzee populations of the Gombe
6829-6833.
Jensen, K, Call, ]., & Tomasello, M. (2007). Chimpanzees
are rational maximizers in an ultimate game. Science, 318,
107-109.
Keller, H., Yovsi, R., Borke, J., Karrner, J., Jensen, H., &
National Park. In D. Hamburg & E. McCown (Eds.), 7he great
Papaligoura, Z. (2004). Developmental consequences of
apes (pp. 13-53). Menlo Park,CA: Benjamin/ Cummings.
early parenting experiences: Self-recognition and self-regu­
Cordon, P. (2004). Numerical cognition without words: Evidence
from Amazonia. Science, 306,496-499.
lation in three cultural communities. Child Development, 75,
1745-1760.
BOESCH
501
Kempes, M., Den Heijer, E., Korteweg, L., Louwerse, A., &
Sterck, E. (2009). Socially deprived rhesus macaques fail to
reconcile: Do they not attempt or not accept reconciliation?
Animal Behaviour, 78, 271-277.
Koenig, A., & Borries, C. (200 1). Socioecology of Hanuman
langurs: The story of their success. Evolutionary Anthropology,
10, 122-137.
Krebs,]. R., & Davies, N. B. (1991). An introduction to behav-
ioural ecology (3rd ed.).
Oxford,
England:
Blackwell
Scientific Publications.
Kummer, H. (1968). Social organization ofHamadryas baboons:
A field study. Bibliotheca Primatology, 6. Chicago: University
of Chicago Press.
Langergraber, K., Mitani, ]., & Vigilant, L. (2009). Kinship
and social bonds in female chimpanzees (Pan troglodytes).
American journal ofPrimatology, 71, 1-12.
Lehmann, J. & Boesch, C. (2005). Bisexually-bonded ranging in
chimpanzees (Pan troglodytes verus). Behavioral Ecology and
Sociobiology, 57, 525-535.
panzees:
Current understanding and
Evolutionary Anthropology, 18, 215-227.
future challenges.
Mitani, J., & Watts, D. (2001). Why do chimpanzees hunt a nd
share meat? Animal Behaviour, 61, 1-10.
Mitani,]., Watts, D., & Lwanga, J. (2002). Ecological and so ci al
correlates of chimpanzee party size and composition. In C.
Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural
diversity in
chimpanzees
and bonobos
(pp.
102-111).
Cambridge, England: Cambridge University Press.
Mitani,]., Watts, D., & Muller, M. (2002). Recent development
in the study of wild chimpanzee behaviour. Evolutionary
Anthropology, 11, 9-25.
Moll, H., &Tomasello, M. (2007). Cooperation and human cog­
nition: The Vygotskian intelligence hypothesis. Philosophical
Transcriptions ofthe Royal Society, B., 362, 639-648.
Nelson, C., Zeanah, C., Fox, N., Marshal!, P., Smyke, A., &
Guthrie, D. (2007). Cognitive recovery in socially depri ved
young children: The Bucharest early intervention proj ect.
Lehmann, ]., Fickenscher, G., & Boesch, C. (2006). Kin biased
investment in wild chimpanzees. Behaviour, 143, 931-955.
Lesorogol, C. (2007). The role of context in experimental dictac­
tor games. Current Anthropology, 48, 920-926.
Levitt, S., & List, J. (2007). What do laboratory experiments
measuring social preferences reveal about the real world?
journal ofEconomic Perspectives, 21, 153-174.
Levitt, S., & List, J. (2008). Homo economicus evolves. Science,
319, 909-910.
Light, K., Kolata, S., Wass, C., Denman-Brice, A., Zagalsky, R.,
& Matzel, L. (2010). Working memory training promotes
general cognitive abilities in genetically heterogeneous mice.
Current Biology, 20, 1-6.
Science, 318, 1937-1940.
Nisbett, R., & Miyamoto, Y. (2005). The influence of culture:
Holistic versus analytic perception.
Sciences, 9, 467-473.
Trends in Cognitive
Nishida, T., Hasegawa, T., Hayaki, H., Takahata, Y., & Uehara,
S. (1992). Meat-sharing as a coalition strategy by an alpha
male chimpanzee? In T. Nishida, W C. McGrew, P. Marler,
M. Pickford, &F. de Waal (Eds.), Topics in primatology: Vol
1. Human origins (pp. 159-174). Basel, Switzerland: Karger
AG.
Nowak, M. (2006). Five rules for the evolution of cooperation.
Science, 314, 1560-1563.
Packer, C., & Ruttan, L. (1988). The evolution of cooperative
List, J. (2006). The behavioralist meets the market: Measuring
social preferences and reputation effects in actual transac­
tions. journal ofPolitical Economy, 114, 1-37.
List,]. (2007). On the interpretation of giving in dictator games.
journal ofPolitical Economy, 11 5 , 482-493.
Lyn, H., Russell,]., & Hopkins, W (2010). The impact of envi­
ronment on the comprehension of declarative communica­
tion in apes. Psychological Science, 21, 360-365.
Marlowe, F., Berbesque, ]., Barr, A., Barren, C., Bolyanatz, A.,
Cardenas,]., Ensminger,
Mitani, J. (2009b). Cooperation and compeonon in chim­
]., Gurven, M., Gwako, E.,
Henrich, ]., Henrich, N., Lesorogol, C., McElreath, R., &
hunting. American Naturalist, 132,159-198.
Packer, C., Scheel, D., & Pusey, A. E. (1990). Why lions form
groups:
Food is not enough. American Naturalist, 136,
1-19.
Palombit, R. (1999). Infanticide and the evolution of pair
bonds in nonhuman primates. Evolutionary Anthropology, 7,
117-129.
Penn, D., Holyoak, K., & Povinelli, D. (2008). Darwin's
mistake: Explaining the discontinuity between human
and nonhuman minds. Behavioral and Brain Sciences, 31,
109-178.
Tracer, D. (2008). More "altruistic" punishment in larger
Penn, D., & Povinelli, D. (2007). On the lack of evidence that
Mason, W (1978). Social experience and primate development.
a "theory of mind". Philosophical Transactions of the Royal
societies. Proceedings ofthe Royal Society B, 275, 587-590.
In G.M. Burghardt & M. Bekoff (Eds.), The development of
behavior: Comparative and evolutionary
non-human animals possess anything remotely resembling
Society, Series B, 362, 731-744.
aspects (pp. 233-
Pollack, S., Nelson, C., Schlaak, M., Roeber, B., Wewerka, S.,
Mathew, S., Shungu, D., Mao, X., Smith, E., Perera, G., Kegeles,
Neurodevelopmental effects of early deprivation in postinsti­
251). New York: Garland Press.
L., Perera, T., Lisanby, S., Rosenblum, L., Gorman, ]., &
Coplan, J. (2003). A magnetic resonance spectroscopic imag­
Wiik, K., Frenn, K., Loman, M., & Gunnar, M. (2010).
tutionalized children. Child Development, 81, 224-236.
Povinelli, D. (2000). Folk physics for apes: The chimpanzee's theory
ing study of adult nonhuman primates exposed to early-life
ofhow the world works. Oxford, England: Oxford University
Maynard Smith, J. (1982). Evolution and the theory of games.
Raihani, N., Grutter, A., & Bshary, R. (2010). Punishers benefit
stressors. Biological Psychiatry, 54, 727-735.
Cambridge, England: Cambridge University Press.
McNamara,]., Barta, Z., Fromhage, L., & Houston, A. (2008).
The coevolution of choosiness and cooperation. Nature, 451,
189-192.
Press.
from third-party punishment in fish. Science, 327, 171.
Riedman, M. (1982). The evolution of alloparental care and
adoption in mammals and birds. The Quarterly Review of
Biology, 57, 405-435.
Melis, A., Hare, B., & Tomasello, M. (2006). Chimpanzees
Sanchez, M., Hearn, E., Do, D., Rilling, J., & Herndon, J.
Mitani, J. (2009a). Male chimpanzees form enduring and equi­
cognitive function of rhesus monkeys. Brain Research, 812,
recruit the best collaborators. Science, 311, 1297-1300.
table social bonds. Animal Behaviour, 77, 633-640.
502
(1998). Differential rearing affects corpus callosum size and
38-49.
THE ECOLOGY AND EVOLUTION OF SOCIAL BEHAVIOR
-
Sanchez,M.,Ladd,C.,& Plotsky,P. (2001). Early adverse expe­
Tomasello, M.,&. Call, J. (2008). Assessing the validity of ape­
rience as a developmental risk factor for later psychopathol­
human comparisons: A reply to Boesch (2007). journal of
ogy: Evidence from rodent and primate models. Development
and Psychopathology, 13, 419---449.
Schaller,G. B. (1972). The Serengeti lion. Chicago: University of
Chicago Press.
Comparative Psychology, 122,449---452.
Tomasello, M., Carpenter, M., Call, J., Behne,T., & Moll, H.
(2005). Understanding and sharing intentions: The origins
of cultural cognition. Behavioral and Brain Sciences, 28,
S chino,G.,& Aureli,F. (2009). Reciprocal altruism in primates:
Partner choice, cognition and emotions. Advances in the
Study ofBehavior, 39,45-69.
Schino,G.,& Aureli,F. (2010). The relative roles of kinship and
reciprocity in explaining primate altruism. Ecology Letters,
13,45-50.
675-691.
Trivers, R. L. (1971). The evolution of reciprocal altruism.
Quarterly Review ofBiology, 46, 35-57.
(1985). Social evolution. Menlo Park, CA:
Trivers, R. L.
Benjamin/Cummings Publishing Company.
van Sch'aik, C. (1996). Social evolution in primates: The role
Sch reier, A., & Swedell, L. (2009). The fourth level of social
structure in a multi-level society: Ecological and social func­
tions of clans in Hamadryas baboons. American journal of
Primatology, 71,948-955.
of ecological factors and male behaviour. Proceeding of the
British Aetulemy, 88, 9-31.
van Schaik, C., & Kappeler, P. (1997). Infanticide risk and the
evolution of male-female association in primates. Proceeding
Shettleworth, S. (1998). Cognition, evolution and behavior. New
York: Oxford University Press.
of the Royal Society London, Series B, 264,1687-1694.
Vonk, J., Brosnan, S., Silk, J., Henrich, J., Richardson,
Silk, J., Alberts, S., & Altmann, J. (2006a). Social relation­
A., Lambeth, S., Schapiro, S., & Povinelli, D. (2008).
ships among adult female baboons (Papio cynocephalus) I.
Chimpanzees do not rake advantage of very low cost oppor­
Variation in the strength of social bonds. Behavioral Ecology
tunities to deliver food to unrelated group members. Animal
and Sociobiofogy, 61,183-195.
Behaviour, 75,1757-1770.
Silk, J., Alberrs, S.,& Alrmann, J. (2006b). Social relationships
Warneken, F., Hare, B., Melis, A., Hanus, D., & Tomasello, M.
among adult female baboons (Papio cynocephalus) I I. Variation
(2007). Spontaneous altruism by chimpanzees and young
in rhe quality and stability of social bonds. Behavioral Ecology
children. PLoS Biology, 5, e184.
and Sociobiology, 61,197-204.
Warneken, F., & Tomasello, M. (2006). Altruistic helping
Silk, J., Brosnan, S., Vonk, J., Henrich, J., Povinelli, D.,
Richardson, A., Lambeth, S., Mascaro, J., & Schapiro, S.
(2005). Chimpanzees are indifferent to the welfare of unre­
lated group members. Nature 437,1357-1359.
in human infants and young chimpanzees. Science, 311,
1301-1303.
Watts, D., & Mirani,J. (200 1). Boundary patrols and intergroup
encounters in wild chimpanzees. Behaviour, 138, 299-327.
Smyke, A., Zeanah, C., Fox, N., Nelson, C., & Guthrie,
D. (2010). Placement in foster care enhances quality of
Warts, D., & Mitani, J. (2002). Hunting and meat sharing by
chimpanzees ofNgogo, Kibale National Park,Uganda. In C.
attachment an1ong young institutionalized children. Child
Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural
Development, 81, 212-223.
diversity in chimpanzees
Srander, P. E. (1992). Cooperative hunting in lions: The role
of the individual. Behavioral Ecology and Sociobiology, 29,
445---454.
(pp.
244-255).
Watts, D., Muller, M., Amsler, S., Mbabazi, G., & Mitani, ].
(2006). Lethal intergroup aggression by chimpanzees in
Srander, P. E.,& Albon, S. D. (1993). Hunting success of lions
in a semi-arid environment. Symposium of the Zoological
Society, London, 65, 127-143.
the Kibale National Park, Uganda. American journal of
Primatology, 68, 161-180.
West,S.,& Gardner, A. (2010). Altruism,spite and greenbeard.
Srevens, J., & Hauser, M. (2004). Why be nice? Psychological
constraints on the evolution of cooperation.
and bonobos
Cambridge,England: Cambridge University Press.
Trends in
Cognitive Sciences, 8, 60-65.
Strum, S. (1981). Processes and products of change: Baboon
predatory behavior at Gilgil, Kenya. In R. S. 0. Harding &
G. Teleki (Eds.), Omnivorous primates: Gathering and hunt­
Science, 327,1341-1344.
West, S., Griffin, A., & Gardiner, A. (2007). Social seman­
tics: Altruism, cooperation, mutualism, strong reciprocity
and group selection. Journal of Evolutionary Biology, 20,
415---432.
Williams,J.,Pusey,A.,Carlis,J.,Farm,B.,& Goodali,J. (2002).
ing in human evolution (pp. 255-302). New York: Columbia
Female competition and male territorial behaviour influence
University Press.
female chimpanzees' ranging panerns. Animal Behaviour, 63,
Suddendorf,T., & Corballis, M. (2007). The evolution of fore­
sight: What is mental travel and is it unique to humans?
Behavorial and Brain Sciences, 30, 299-351.
Thierry, B.,& Anderson, J. (1987). Adoption in anthropoid pri­
mates. lnterntttional journal of Primatology, 7, 191-216.
Tomasello, M., &. Call, J. (1997). Primate cognition. Oxford,
England: Oxford University Press.
347-360.
Wolpert, L. (2007). Causal beliefmakes human. In C. Pasternak,
(Ed.), What makes us human? (pp. 164-181). Oxford,
England: Oneworld Publications.
Y amamoto, S., & Tanaka, M. (2010). The influence of kin
relationship and reciprocal context on chimpanzee's other­
regarding preferences. Animal Behaviour, 79, 595-602.
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