Modern humans live in an "exploded" network
with unusually large circles of trust that form
due to prosociality toward unfamiliar people
(i.e. xenophilia). In a set of experiments we
demonstrate that semi-free ranging bonobos (Pan
paniscus), both juveniles and young adults ,
also show spontaneous responses consistent with
xenophilia. Bonobos voluntarily aided an
unfamiliar, non-group member in obtaining food
even when he/she did not make overt requests for
help. Bonobos also showed evidence for
involuntary, contagious yawning in response to
videos of yawning conspecifics who were complete
strangers. These experiments reveal that
xenophilia in bonobos can be unselfish,
proactive and automatic. They support the first
impression hypothesis that suggests xenophilia
can evolve through individual selection in
social species whenever the benefits of building
new bonds outweigh the costs. Xenophilia likely
evolved in bonobos as the risk of intergroup
aggression dissipated and the benefits of
bonding between immigrating members increased.
Our findings also mean the human potential for
xenophilia is either evolutionarily shared or
convergent with bonobos and not unique to our
species as previously proposed.
Résumé
La famille de nos contemporains est le plus
souvent dispersée et le cercle de vie
sociale est élargi à de nombreux
individus étrangers à la famille.
Dans un ensemble d'expériences, les
auteurs démontrent que les bonobos
semi-libres (Pan paniscus), deux jeunes et deux
jeunes adultes, montrent également des
réponses spontanées compatibles
avec la xénophilie.
Par exemple, un Bonobo a volontairement
aidé un autre, non membre de sa famille
(et n'appartenant pas à un groupe)
à obtenir de la nourriture alors
même qu'une demande d'aide n'était
pas manifeste. Un Bonobo a également
montré des preuves de bâillements
involontaires et contagieux en réponse
à des vidéos de
conspécifiques bâillant qui
étaient de parfaits inconnus.
Ces expériences
révèlent que la xénophilie
chez les bonobos peut être
désintéressée, proactive et
automatique. Elles valident l'hypothèse
initiale, ce qui suggère que la
xénophilie peut évoluer au travers
de la sélection individuelle dans les
espèces sociales chaque fois que les
avantages de la construction de nouvelles
relations l'emportent sur les coûts.
La xénophilie a probablement
évolué chez les bonobos à
mesure que le risque d'agression intergroupe
s'est dissipé et que les avantages de la
relation entre les membres immigrants ont
augmenté.
Ces résultats signifient
également que le potentiel humain pour la
xénophilie est soit une
conséquence d'une évolution
partagée ou convergente avec celle des
bonobos et qu'elle n'est pas unique à
notre espèce comme cela était
précédemment proposé.
Introduction
Trust is fundamental to social life. One
hallmark of human societies is that they have an
unusually wide circle of trust. This includes
unfamiliar individuals that can be anything from
distant acquaintances to anonymous strangers.
Conflicts occur between rival groups, but modern
humans manage to live in a global social network
connected by trusting relationships between
unrelated strangers. Contemporary
hunter-gatherers commonly engage in cooperative
interactions among unfamiliar individuals, so
did early Homo sapiens (e.g. flexible dispersal,
high social fluidity, intergroup alliance and
long-distance trade). This extensive circle of
trust provides enormous benefits by creating an
interconnected and ever-growing market for
information, goods and support. Such
interconnectedness has been suggested to allow
for cumulative culture and large-scale
cooperation, two cornerstones of humanity.
The human potential for xenophilia or
prosociality toward unfamiliar individuals seems
critical then to our species success in
encouraging cooperation and cultural exchange.
In absence of past experience with strangers,
humans rely on signals of positivity in
establishing trust. When encountering a stranger
of unknown group membership humans are capable
of making these positive signals with a
prosocial first move. This is in contrast to a
negative or xenophobic response, and it does not
require a prosocial preference for the
unfamiliar over the familiar, although such a
preference can be considered the extreme
expression of xenophilia. A pattern of human
xenophilia is observed across cultures and early
in development. It can occur even when the
xenophilic actors obtain no selfish benefits,
have limited cognitive control and receive no
signals for help from the recipient. This
profile suggests that human xenophilia is in
part driven by unselfish motivations and
automatic processes. However, it remains unclear
to what extent this kind of xenophilia evolved
once our lineage split with other apes.
One hypothesis proposes that human
xenophilia was derived in our lineage, which is
supported by the larger pattern of xenophobia in
most primates - including chimpanzees. It has
been suggested that human xenophilia evolved
from the conserved fear of strangers seen across
primates as a result of unique human bonding
mechanisms such as intermarriage and cultural
institutions. Others suggest human xenophilia
evolved due to ultra-strong prosocial motivation
produced by group selection or cooperative
breeding.
The first impression hypothesis suggests
that xenophilia evolves in response to the
benefits of new social partners. This hypothesis
predicts that prosocial responses to strangers
can evolve in any social species where the
selfish benefits of bonding with new partners
outweigh the costs. For example, xenophilia can
be favored when there is limited risk of
xenophobic aggression. In this case positive
encounters with strangers can develop into
repeated interactions. Strangers will become
attractive social partners since social networks
can be expanded through the formation of low
risk and low cost "weak ties". A core prediction
of the first impression hypothesis is that
social preferences for positive interactions
with non-group members (e.g. xenophilia) and
cognition should evolve to support the network
expansion of individuals when it enhances
inclusive fitness49.
Bonobos (Pan paniscus) provide a powerful
test of this prediction of the first impression
hypothesis. Bonobos have been proposed as a
product of selection against aggression or
"self-domestication" that was driven by reduced
feeding competition. Bonobos not only possess a
syndrome of morphological and physiological
traits associated with domestication, but also
show less severe forms of aggression than
chimpanzees. Territorial patrols, infanticide,
and lethal intergroup aggression have never been
observed in bonobos. Tension can rise during
intergroup encounters, but escalation into
physical aggression with injuries is uncommon.
Instead, affiliative behaviors such as grooming,
traveling together and socio-sexual behaviors
have often been seen during interactions between
immigrants or neighboring groups.
Unlike chimpanzees in captivity, there are
no reports of bonobos killing adults or infants
as a result of transfers between groups
(although male immigrants without mothers can
become targets of female aggression). Most
importantly, while both bonobos and chimpanzees
are patrilocal, only bonobo immigrants are
attractive social partners for resident males
and females. Unrelated, immigrating members in
bonobo groups even form alliances, gain priority
of access to food and achieve high social
status
Experiments have demonstrated that physical
interactions with unfamiliar conspecifics can be
rewarding for bonobos. Instead of monopolizing
food in their possession, bonobos unlocked a
one-way door in order to physically interact and
co-feed for the first time with an unfamiliar
neighbor (but not with a familiar recipient).
They often opened a second door for another
non-group member even if it meant being
outnumbered by non-group members - something
chimpanzees actively avoid68. In another
experimental context bonobos also released an
unfamiliar conspecific into a room with food
that they themselves could not access. This
meant bonobos helped non-group members even when
they received no social reward.
However, it is still unclear how similar the
xenophilic tendencies of bonobos are to that
seen in humans - which can be unselfish,
proactive and automatic toward complete
strangers. While proactive or unsolicited
prosociality toward group members has been
experimentally demonstrated in some contexts in
chimpanzees and other primates, proactive food
provisioning of unfamiliar individuals from
other groups remains little studied. Previous
tests with bonobos have demonstrated their
tendency to share with unfamiliar recipients
from a different social group when using
explicit measures of prosociality. This work
even suggests the potential for proactive
sharing in bonobos since help was not contingent
on gestures made by recipients. However, we
remain without a strong test of (1) proactive
sharing, (2) with completely novel conspecifics
and (3) involuntary or implicit measures of
social preferences commonly used in human
research. We conducted a series of experiments
to test the first impression hypothesis that
meet these methodological challenges.
We first examined whether bonobos
voluntarily provisioned an unfamiliar
conspecific from a neighboring group who was
unable to use overt signals to indicate their
desire for help (i.e. since overt requests for
help were prevented, aid was considered
proactive). We then tested whether bonobos had
an involuntary contagious yawning response to
complete strangers. Contagious yawning has been
used by many as an implicit measure of social
preference in various primates and non-primate
species since it is under involuntary control,
although see. Regardless of its exact proximate
mechanism, contagious yawning has been
positively associated with social rapport in a
variety of animals including humans and bonobos.
This includes work showing that yawn contagion
in xenophobic chimpanzees is made in response to
in-group but not out-group conspecifics. These
findings make contagious yawning a useful
implicit measure of positive social preference.
We therefore tested the first impression
hypothesis by examining how bonobos help and
contagiously yawn in response to unfamiliar
conspecifics. The first impression hypothesis
predicts that bonobos will proactively provision
food to unfamiliar, non-group members and will
contagiously yawn in response to complete
strangers.
Discussion
In strong support of the first impression
hypothesis bonobos proactively provisioned
out-of-reach food to an unfamiliar non-group
member and showed involuntary, contagious
responses to the yawns of complete strangers.
The aid that bonobos explicitly provided the
unfamiliar recipient in obtaining food is
consistent with common definitions of proactive
prosociality, while contagious yawning suggests
their xenophilia is not completely under
voluntary control and is present even when there
is zero familiarity. This bonobo pattern of
xenophilia resembles contagious yawning and
unconscious mimicry seen in humans more than
chimpanzees, as well as the heuristic-like
response that drives human sharing with
strangers in controlled experiments. Like
humans, bonobos proactively help unfamiliar
conspecifics and their positive response is at
least in part automatic.
Xenophilia in the current experiments was
directed to conspecifics with various levels of
familiarity, from neighbors with whom the
subjects had never shared an enclosure to
completely novel individuals. The xenophilia
observed in this sanctuary sample is consistent
with reports from a wide range of field sites
and captive facilities showing that bonobos
display affiliative behaviors toward
acquaintances and new immigrants. Our findings
together with these observations do not support
the alternative that our subjects have become
xenophilic due to repeated testing, due to their
rearing history, or due to the sanctuary
environment that allowed visual and vocal
contacts across group barriers. Given that
sanctuary bonobos are relatively risk-averse and
indifferent to novel stimuli in non-social
contexts, a general attraction to novelty
clearly cannot explain our findings. Finally,
the social context at the sanctuary is highly
similar to the experience of most wild primates
that often see or hear neighboring groups but
rarely physically interact with them due to the
potential cost of aggression. Despite this, and
unlike chimpanzees, bonobos in the wild and in
our experiments appear to have evolved a
xenophilic preference for this same type of
stranger.
It is difficult to explain the prosociality
observed here as a result of harassment,
reciprocity or a lack of inhibition since
subjects could not physically interact with
recipients, they had never been in the same
group and pretests demonstrated subjects
understood the experimental set-up (i.e. they
passed self-regard pretests). The physical setup
and presence of a conspecific in the controls
rule out mechanisms such as local enhancement or
social facilitation. We are unaware of any
evidence that bonobos can solicit the novel form
of help tested here through non-gestural cues
(e.g. subtle vocalizations, facial expressions
or even situational cues1). This might be an
interesting topic for future research, given
bonobos are relatively sensitive to human social
cues. Moreover, based on our control the
contagious yawning results cannot be attributed
to an inability of subjects to discriminate
strangers from groupmates in the videos.
According to the first impression
hypothesis, xenophilia evolves when the benefits
of bonding with new partners outweigh the costs.
In the case of bonobos, strong female alliances
and sexual selection against male aggression
likely removed the threat of lethal intergroup
aggression that drives chimpanzee
xenophobia44,116. This might have turned a
costly interaction into a highly beneficial one.
Xenophilia was increasingly favored as strangers
became more likely to turn into valuable
long-term social partners. It is important for
future studies to test other predictions of the
first impression hypothesis. Future research
will need to examine the role of age and sex as
it relates to the strength of xenophilia in
bonobos. For example, our subjects were
relatively young (4-18 years old), and within
the age range (6-14 years old) that bonobos
typically leave their natal groups in the wild.
Bonobos may show a different preference once
they are past this age. Or the preferences of
older adults may vary depending on the sex of
the stranger. The first impression hypothesis
predicts that, unfamiliar adult females will be
preferred over adult males and that unfamiliar
adult males may illicit xenophobic responses in
some contexts (i.e. interactions between two
strange adult males). It will be exciting to
take this next step and understand which kind of
strangers bonobos respond with xenophilia.
Another powerful test of this hypothesis
will be quantitative comparisons between
spontaneous responses toward strangers in
bonobos and chimpanzees1. Despite a growing
literature documenting bonobo xenophilia and
chimpanzee xenophobia, most studies, including
the current one, have focused on one species.
This creates methodological variations across
paradigms that prevent a more precise comparison
between the two species. Although in one current
experiment (experiment 2) we made the design and
the analysis as comparable to the chimpanzee
study by Campbell et al. as possible, our
comparison is still qualitative. Methods that
allow for direct quantitative comparisons of
both species are still needed. This comparison
would be particularly powerful if it used eye
tracking techniques to examine attention as it
relates to yawning rates. It might be important
to correct for higher levels of attention given
to the yawns of strangers than those of
groupmates.
While there is consensus that contagious
yawning is involuntary, the nature of the
mechanism driving this automatic response is
still unclear. Future research will be needed to
understand if bonobo contagious yawning is an
expression of some basic form of empathy, a
'social heuristic', or an oxytocin-vasopressin
mediated response. Regardless of the exact
mechanism, our results suggest that bonobos have
an involuntary positive response to complete
strangers. As described for humans, bonobos seem
predisposed to making a good "first impression"
when interacting with a new social partner. For
both humans and bonobos, many strong bonds
likely start from positive encounters between
unfamiliar adults catalyzed by xenophilia.
However, our results also suggest how xenophilia
is constrained in both species in different
ways. For example, the strong xenophobic
reaction that humans display toward strangers
from different cultural mediated outgroups
severely limits human intergroup prosociality.
Likewise, while bonobos potentially even prefer
an unfamiliar conspecific from another group
over their own groupmate, they are probably much
less flexible in terms of the contexts and the
consistency with which they will provide aid
(e.g. food-provisioning to strangers did not
occur when the cost became considerably
high).
The most exciting puzzle for the future will
be determining why humans evolved the potential
for trusting relationships with strangers in a
wider variety of contexts - allowing rapid
diffusion of information and reciprocal
between-group cooperation. This will require
uncovering whether some forms of xenophilia are
shared or convergent between humans and bonobos.
Regardless of the answer, bonobo networking has
much to teach us about the origins of the human
network we all rely upon.
