Evolving the neuroendocrine physiology of human and primate cooperation and collective action

Abstract

While many hormones play vital roles in facilitating or reinforcing cooperative behaviour, the neurohormones underlying competitive and cooperative behaviours are largely conserved across all mammals. This raises the question of how endocrine mechanisms have been shaped by selection to produce different levels of cooperation in different species. Multiple components of endocrine physiology—from baseline hormone concentrations, to binding proteins, to the receptor sensitivity and specificity—can evolve independently and be impacted by current socio-ecological conditions or individual status, thus potentially generating a wide range of variation within and between species. Here, we highlight several neurohormones and variation in hormone receptor genes associated with cooperation, focus-ing on the role of oxytocin and testosterone in contexts ranging from parenting and pair-bonding to reciprocity and territorial defence. While the studies reviewed herein describe the current state of the literature with regard to hormonal modulators of cooperation and collective action, there is still a paucity of research on hormonal mechanisms that help facilitate large-scale collective action. We end by discussing several potential areas for future research.

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Review
Cite this article: Trumble BC, Jaeggi AV,
Gurven M. 2015 Evolving the neuroendocrine
physiology of human and primate cooperation
and collective action. Phil. Trans. R. Soc. B 370:
20150014.
http://dx.doi.org/10.1098/rstb.2015.0014
Accepted: 8 September 2015
One contribution of 13 to a theme issue
‘Solving the puzzle of collective action through
inter-individual differences: evidence from
primates and humans’.
Subject Areas:
behaviour
Keywords:
testosterone, oxytocin, cooperation
Author for correspondence:
Benjamin C. Trumble
e-mail: ben.trumble@gmail.com
†
Present address: Center for Evolution and
Medicine, and School of Human Evolution and
Social Change, Arizona State University, Tempe,
AZ 85287, USA.
‡
Present address: Department of Anthropology,
Emory University, Atlanta, GA 30322, USA.
Evolving the neuroendocrine physiology
of human and primate cooperation
and collective action
Benjamin C. Trumble†, Adrian V. Jaeggi‡and Michael Gurven
Department of Anthropology, University of California Santa Barbara, Santa Barbara, CA 93106, USA
While many hormones play vital roles in facilitating or reinforcing coopera-
tive behaviour, the neurohormones underlying competitive and cooperative
behaviours are largely conserved across all mammals. This raises the ques-
tion of how endocrine mechanisms have been shaped by selection to
produce different levels of cooperation in different species. Multiple com-
ponents of endocrine physiology—from baseline hormone concentrations,
to binding proteins, to the receptor sensitivity and specificity—can evolve
independently and be impacted by current socio-ecological conditions or
individual status, thus potentially generating a wide range of variation
within and between species. Here, we highlight several neurohormones
and variation in hormone receptor genes associated with cooperation, focus-
ing on the role of oxytocin and testosterone in contexts ranging from
parenting and pair-bonding to reciprocity and territorial defence. While
the studies reviewed herein describe the current state of the literature with
regard to hormonal modulators of cooperation and collective action, there
is still a paucity of research on hormonal mechanisms that help facilitate
large-scale collective action. We end by discussing several potential areas
for future research.
1. Introduction
Humans and to some extent other primates engage in various forms of
cooperation and collective action ranging from parenting and pair-bonding
to cooperative food production and sharing, territorial defence and warfare
[1–3], with some of these behaviours going beyond the reaction norm of
many mammals in terms of scale and coordination. Yet, the neurohormones
underlying competitive and cooperative behaviours in vertebrates are largely
conserved [4], raising the question of how endocrine mechanisms are shaped
by selection to help modulate these extensive cooperative behaviours.
Multiple components of endocrine physiology can evolve independently
and be impacted by current socio-ecological conditions or individual status
(figure 1), thus potentially generating a wide range of variation within and
between species. This variation can inform ultimate function as individual or
species differences in baseline hormone levels, acute reactivity or receptor dis-
tributions may reflect exaptations, different adaptive strategies, trade-offs or
constraints [5,6], all of which could lead to individual differences in cooperation
and collective action.
To illustrate how endocrine mechanisms evolved to facilitate human and
primate cooperation, we focus on the contexts of cooperation typical of the
‘human adaptive complex’, i.e. the evolved human life history and social organ-
ization [7,8], and their primate analogues: parenting, pair-bonding, reciprocity
and collective action. We focus our discussion on the role of two hormones in
these contexts in depth, oxytocin (OT) and testosterone. We also highlight other
neurohormones and variation in hormone receptor genes that have been associ-
ated with cooperation. In doing so, we aim to provide a roadmap for
identifying shared and derived mechanisms underlying human and primate
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cooperation that can give insights into the ecological and
social selection pressures that produced them [6] (figure 1).
(a) Hormones and behaviour
In order for a hormone to directly impact behaviour, it must
bind to receptors in critical regions in the brain (or other
target tissues). Thus, while measuring circulating hormone
levels is an excellent first step, it is crucial to also consider the
hormonal receptors that turn chemical messages into electrical
signals [4]. While most hormones are measured peripherally
(outside of the brain), concentrations of hormones vary within
the brain, and not all circulating hormones can enter brain
tissue. The brain is protected by a selectively permeable set
of capillary tissues called the blood– brain barrier, which pro-
tects cerebral tissue by only allowing certain substances in
circulating blood to pass. Behaviour can only be directly influ-
enced by hormones small enough to cross the blood– brain
barrier (e.g. steroids), or that are produced locally in the brain
(peptides like OT), or hormones that interact with others that
can be active within the brain. Neurohormones like OT and tes-
tosterone are known to impact the reward (e.g. dopagenic
neurons) and fear centres of the brain (e.g. amygdala), and
thus have the ability to reinforce or discourage behaviour. Neu-
roimaging studies indeed find strong effects of OT and
testosterone on behavioural and neural responses to social
stimuli [9,10], thus highlighting their neuromodulatory effects.
Cooperative behaviour, whether food sharing or resource
defence, is context and condition dependent; behaviours
towards other individuals may differ based on their related-
ness, social proximity or the actor’s physical condition.
This means that individuals need to adjust behaviours
based on their social setting and local ecology. For example,
group-living primates may tolerate relatives at the same feed-
ing patch, while simultaneously protecting their patch
against out-group members. Hormones and neurotransmit-
ters can change rapidly in response to different social and
environmental cues, enhancing tolerance of others in one
social situation, intensifying the potential for aggression in
another. Thus, hormones can exert the kind of flexible
and rapid control needed to adjust behaviour to varying
socio-ecological contexts.
(b) Studying hormonal mechanisms can inform
ultimate function
Understanding the physiology and biology of hormone–
behaviour interactions can provide insight into adaptations,
exaptations, trade-offs and constraints in the evolution of
these behaviours [5,6]. Selection may favour mutations for
higher levels of a hormone that impacts physiology and social
behaviour, resulting in higher baseline hormones. As baseline
hormone levels affect many target tissues, such evolutionary
changes may modulate many traits, some of which are not
O
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Figure 1. Critical areas to examine for the evolution of hormonal– behaviour interactions associated with cooperation. Evolution could result in higher circulating
hormone levels to saturate receptors through: (a) higher baseline levels of hormones, (b) lower levels of binding proteins resulting in higher ‘free’ hormone levels
and/or (c) larger acute increases in hormone levels. Neural responses to circulating hormones could be impacted by (d) greater hormone receptor density, (e) greater
sensitivity of receptors to a hormone, ( f) higher specificity of receptors for a specific hormone and (g) location and connectivity of the receptors to critical brain
areas. (Online version in colour.)
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the original target of the selective pressure; these by-products
are commonly referred to as exaptations, and artificial selection
experiments may quantify the linkage between traits, resulting
in trade-offs and constraints on adaptation [6]. Changes in the
acute reactivity of specific target tissues, such as mutations in
receptor density or function, are more likely to be the original
target of selection, and therefore reflect adaptations. A classic
example often used to describe hormonal adaptations and
exaptations is the female spotted hyaena; female hyaenas
have relatively high levels of testosterone which probably
evolved as an adaptation to facilitate female–female compe-
tition and aggression [6]. As a systemic by-product of high
testosterone, female hyaenas are masculinized and develop
penile-like clitorises which are used in greetings and rank-dis-
play between adult females [11]. In this case, the adaptation is
higher baseline testosterone to facilitate competition, and the
exaptation is the co-option of the pseudo-penis in social behav-
iour [6]. Generally speaking, evolutionary changes in acute
reactivity and responsiveness of specific target tissue, e.g.
through changes in hormone receptor genes, probably reflect
selection for specific hormone–trait interactions and therefore
represent adaptations, whereas evolutionary changes in base-
line hormone levels are more likely to produce exaptations or
trade-offs [9] (figure 1).
Phylogenetic analysis can be a useful way to examine
when, and under what socio-ecological conditions a behaviour-
al change occurred, and whether these behavioural changes
were associated with any endocrine changes. However, in
order to appreciate the adaptive importance of any evolu-
tionary change in behaviour, the hormonal mechanisms must
be understood (cf. figure 1); thus, evolutionary history, current
utility and mechanism are critical for understanding the ulti-
mate function of complex behaviours such as cooperation and
collective action.
2. The role of oxytocin in the establishment and
maintenance of cooperative relationships
Cooperation requires investment in a social relationship that
generates direct or indirect fitness benefits, oftentimes by
paying a short-term cost to reap a long-term gain. This creates
several adaptive problems. First, ancestral mammalian asocial
preferences need to be overcome to increase tolerance of others
and shift behaviour in more prosocial directions. Second, suit-
able partners have to be identified, recruited and remembered,
with the level of investment in each relationship adjusted to the
expected fitness gains. Finally, benefits from cooperation
generated within the relationship have to be protected from
outside threats.
OT is fundamentally linked to each of these adaptive
problems, in cooperative relationships of all levels [4,12,13]
(table 1). OT achieves these functions by (i) decreasing social
anxiety, (ii) enhancing social cognition and social memory,
(iii) tracking the valence of social partners and regulating
prosocial motivation and (iv) enhancing the social salience of
outside threats. In the following sections, we discuss these
functions in the various relational contexts that OT is involved
in, ranging from the mother–infant bond to large-scale collec-
tive action. In each of these contexts, the function of OT is likely
to be parochial, regulating cooperative investment within
the relationship, but increasing xenophobia and protective
aggression against out-groups [13].
(a) Origins of oxytocin in mother –infant bonds
For placental mammals, internal gestation and lactation are
expensive for mothers both in terms of time and energy.
Above and beyond the ancestral mammalian patterns of
investment, extended human altriciality with multiple depen-
dents escalates these costs [7]. Hormones that help facilitate
bonding between mother and infant, particularly those that
lead to higher levels of maternal investment by stimulating
neural reward systems probably had a selective advantage
by increasing offspring survival, and thus enhancing female
reproductive success.
OT is stronglyassociated with smooth muscle contraction in
the context of parturition (and OT analogues with egg-laying in
non-mammals), as well as the milk let down response, which
begins with infant stimulation (either suckling or crying) pro-
moting a surge of OT that facilitates milk ejection [13,41]. The
neuroendocrine physiology of OT was co-opted for numerous
behaviours associated with maternal care including the regu-
lation of the amount of care given by mothers and demanded
Table 1. Examples of social contexts associated with OT and testosterone for humans and primates. Note that review articles were cited when possible; blank
cells indicate that more research is needed, shaded cells are not applicable contexts.
hormone social context primates human males human females
OT maternal care all primates [13] [14]
paternal care marmosets [15] [16]
pair bond marmosets [17] [18,19]
friendships chimpanzees [20,21], macaques [22], marmosets [23] [9,13,24,25]
intergroup interactions [26,27]
testosterone paternal care marmosets [28], not titi monkeys [29] [16]
pair bond [16]
in-group [30] [31]
out-group chimpanzees [32] [33] no effect [34]
intrasexual competition chimpanzees [35], baboons [36], colobus monkeys [37],
not bonobos [38]
[39,40] [31]
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by infants [13,42] (table 1). While OT has similar impacts on lac-
tation and behaviour across many mammals, human and great
ape altriciality coupled with relatively high dependency loads
may have placed additional selective pressures on proximate
mechanisms that modulated maternal behaviour, in particular
tolerance to a long period of offspring contact and (multiple)
dependence. These selective pressures may have resulted in
higher baseline levels of OT, larger acute increases in OT when
exposed to offspring, greater densities or sensitivities of OT
receptors in the brain, or greater neural connections between
OT receptors and reward centres in the brain (figure 1), though
little is currently known about thephylogeny of OT in primates.
Similar changes probably resulted in the co-option of OT path-
ways for various other relational contexts as highlighted below.
It is important to reiterate that OT not only has
socio-positive effects, it is also expected to affect protective
aggression and to modulate trade-offs between current and
future reproduction (in addition to being an important modu-
lator of cognitive trade-offs [9]). Experimental evidence in mice
demonstrates that maternal OT mediates defence of offspring
against potential threats [43]. Studies in primates have yet to
examine offspring defence but do find evidence that OT
mediated in-group bias and defence at the level of larger
social groups in marmosets and humans [23,26,27] (see also
below). While OT is associated with increased maternal invest-
ment, there are conditions under which trade-offs between
current and future offspring should lead to downregulation
or even termination of investment. Studies have yet to test
whether low-quality infants induce a smaller OT response in
mothers or fathers, a hypothesis worth testing. Thus to sum-
marize this section, OT evolved in placental mammals as a
part of the milk let-down reflex, but then was later co-opted
to help modulate maternal behaviour and mediate trade-offs
between current and future reproduction.
(b) Oxytocin and male parental investment
Maternal careof offspring is universal among mammals, but less
than 5% of male mammals (and no great apes) engage in any
paternal care [44]. Many human fathers invest heavily in their
offspring [16,44], making the paternal–infant bond a derived
trait in humans. The human feeding niche requires extensive
bi-parental care, as well as additional multi-generational sup-
port, all of which would benefit from extensive tolerance by
human males of both their offspring and other family members
[45]. The anxiolytic and bonding aspects of increased OT may be
a critical proximate mechanism that keeps human males
engaged in familial provisioning [46].
Human males may not provide milk for their children, but
both baseline OT and acute increases in OT have been impli-
cated with increased levels of paternal care [14,16,47]. Fathers
who more intently play with their children show larger actuate
increases in OT [48,49]. Additionally, fathers given exogenous
OT engage in more physical contact, social reciprocity, eye
gazing and object manipulation with their infants than males
given a placebo [47]. Co-optionof OT in paternal care is not lim-
ited to humans; in other primates with relatively high levels of
paternal investment such as marmosets and tamarins, exogen-
ous and endogenous changes in OT facilitate paternal care [15].
In sum, while males do not lactate, OT appears to have poten-
tially beneficial impacts on male parental investment in the
few primate species that do engage in paternal care.
(c) Oxytocin and pair-bonds
From a female perspective, OT modulation of pair-bonding
behaviour can be seen as an extension of the female’s reproduc-
tive context [13], but there is growing evidence that OT also
facilitates pair-bonding in male primates including humans.
OT levels were highly correlated among marmoset pairs, and
pairs with higher OT levels were more affiliative, though
females showed increases in OT when engaged in grooming,
while males only showed increases in OT when engaging in
sexual activity [50]. OT administration in marmosets led to
more huddling with reproductive partners, while OT antagon-
ists resulted in reduced proximity [17]. OT administration in
marmosets also decreased socio-sexual contact with strangers,
thus increasing fidelity within the pair bond [51]. In humans,
males display acute increases in OT when shown pictures
of their girlfriends, but not when shown pictures of other
women [52], suggesting the importance of context and connec-
tion, and not just sexual behaviour [18]. Indeed, men and
women who rate their relationships as stronger have higher
basal levels of OT [19]. However, as a mediator of investment
in pair-bonding, OT is subject to trade-offs in relationship
investment based on relationship quality. For example, in
aggressive individuals, OT administration increases jealousy
[53], as well as the propensity for intimate partner violence, a
potential tactic to limit a mate’s access to members of the oppo-
site sex [54]. In sum, OT is associated with the regulation and
maintenance of pair-bonds, above and beyond sexual behav-
iour, with studies indicating both positive and negative
impacts of OT on relationships depending on the social context.
(d) Oxytocin and friendships
Beyond parental care and pair-bonding, humans and some
primates engage in cooperative relationships among both
related and unrelated individuals, i.e. friendships [55– 57].
Friendships involve the reciprocal exchange of various social
behaviours such as grooming, food sharing and coalitionary
support [2,58–60], and appear to be regulated by OT. For
example, a greater number and intensity in female friendships
in macaques is associated with higher levels of baseline OT,
though the same effect was not found among male macaques
[22]. In chimpanzees, acute increases in OT occur following
food sharing, leading to an intensification of reciprocal invest-
ment in the relationship [21]. Grooming also results in acute
increases in OT, with greater increases after grooming by kin
or friends [20]; short-term endogenous changes in OT thus
track the valence of social relationships, which is crucial
for adjusting cooperative behaviour to partner value. As
such, OT provides a mechanism for regulating investment in
reciprocal relationships.
The extensive reciprocal cooperation with changing
partners required by the human foraging niche and fission–
fusion sociality [8] was probably facilitated by a further co-
option of OT to increase prosocial disposition and motivate
the establishment and regulation of cooperative relationships
with new partners. Indeed, prosociality increases following
OT administration in a variety of economic games mimicking
resource-sharing contexts [24,61]. Additionally, experimental
evidence suggests that both endogenous release of OT [62]
and exogenously administered OT make individuals more will-
ing to trust their partners in economic games [25]. In this
context, the fact that the appropriate level of investment in the
relationship, exemplified by trust (i.e. the belief that a social
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partner will cooperate), can be increased by endogenous OT or
artificial OT administration (and reduced by testosterone; see
below) highlights OT’s role in adjusting cooperation to expected
fitness gains. To conclude, OT has been co-opted beyond just
parental care and pair-bonding to influence many aspects of
prosocial behaviour, and species differences in reciprocal
cooperation should be reflected in evolutionary changes in
OT physiology ( figure 1).
(e) Oxytocin and intergroup interactions
As mentioned before, the formation of an in-group at every
relational level (parent–infant, pair-bonds, friendships) also
creates an out-group which could threaten the benefits gener-
ated by cooperation and result in a parochial psychology
probably mediated by OT. In some species, interactions with
out-groups can be a context of large-scale collective action;
males in several non-human primate species from capuchins to
chimpanzees engage in coalitional aggression against out-
groups [63,64]. Little is currently known about hormonal
mechanisms underlying such coalitional aggression in other pri-
mates, though testosterone is involved in border patrols among
chimpanzees (see below) [32]. In humans, OT administration
increases in-group conformity [65], increases ethnocentrism
and decreases trust of out-group members [66], as well as
increasing willingness to lie to out-group members [67]. Thus,
while OT mediates aspects of bonding with in-group members,
it also fosters an out-group psychology.
Internal and external warfare among small-scale hunter–
gatherer groups arguably resembles coalitionary aggression in
chimpanzees [1] and to the extent that this indicates an ancestral
adaptive problem, the OT mediated in-group/out-group psy-
chology described above [68] might reflect shared adaptations
for coalitional aggression among humans and chimpanzees.
However, in the past 8000 years shifts to more defensible
resources such as livestock or agricultural land have led to
increases in the frequency, scale and intensity of warfare [8].
In this context, culturally evolving mechanisms for co-opting
the parochial effects of OT could have been crucial for success
in warfare [69– 71]; for instance, the creation of stable coopera-
tive units with fictive kinship categories (‘brothers in arms’)
could perhaps amplify in-group loyalty and xenophobia,
while the rigid hierarchies and systems of reward and punish-
ment typical of successful armies might be partly based on
hormonal mechanisms for dominance and subordination
shared with other hierarchical primates. In summary, there is
good evidence that OT modulates parochial psychology in
humans, though little research has examined its effects in real
intergroup interactions in any species. It is an open question
whether the large-scale collective action seen in human warfare
is mediated by derived mechanisms or ones shared with
other primates.
3. Testosterone, competition and paternal
investment
While we have thus far focused on OT, there are a number of
other endocrine mechanisms associated with social behaviour
(tables 1 and 2); when it comes to conflict and competition,
either in human or animal models, most hormonal research
has focused on testosterone. Testosterone is related to many
male reproductive trade-offs; higher levels of testosterone
have anabolic effects on muscle tissue which, while beneficial
for male–male physical confrontations, can force energetic
trade-offs between costly muscle mass and immune function
[83]. The evolution of testosterone in vertebrates probably
began with male – male competition over access to mates.
Muscle tissue is calorically costly to maintain, as muscle
mass uses approximately 20% of daily basal metabolic rate
in adult human males [84], and testosterone is also lipolytic,
burning off fat reserves that could be vital during lean times
[85]. Males in better condition can afford higher levels of
testosterone and the associated physiological costs; thus
there is a wide range of testosterone levels within and between
individuals [86,87].
Males in poor condition cannot maintain high levels of
testosterone; illness and injury lead to rapid decreases in tes-
tosterone [88– 90], as does short and longer term fasting
[91,92], and extensive energetic expenditure [93]. While
some human and chimpanzee populations show no seasonal
variation in testosterone [94,95], large studies of subsistence
human and wild baboon populations report decreases in tes-
tosterone during leaner times [96,97]. Despite population
variation in baseline testosterone, even populations with
low baseline testosterone express acute increases in testoster-
one of the same relative magnitude as those reported in
energetically replete populations [98]. Because maintaining
consistently high levels of testosterone can be energetically
expensive (among other costs to parenting and potential
immunosuppression), many seasonally breeding species
avoid these costs by only producing high levels of testosterone
during the mating season [87].
(a) Testosterone, parenting and pair-bonding
While OT tends to increase during parenting, many species,
including humans, show decreases in testosterone [16,99].
Higher levels of testosterone are correlated with mating
effort in seasonally breeding [100,101] and non-seasonally
Table 2. Examples of other potential hormonal mechanisms associated with human and non-human primate cooperative behaviour. Review papers cited where
possible, blank cells indicate that more research is needed.
hormone context primates human males human female
serotonin in-group macaques [72] [73–75]
prolactin paternal behaviour/pair-bonding marmosets [76], tamarins [77] [16]
oestrogen in-group no effect [34]
cortisol in-group marmosets [78], baboons [79],
bonobos [38], macaques [53]
[80–82]
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breeding primates [16,35]. Engaging in mate competition,
mate guarding and courtship takes a significant amount of
time and energy. For primates that engage in paternal behav-
iour, the energetic costs of investing in new reproductive
opportunities trades off against investment in paternal care
of current offspring. Thus, it is not surprising that males in
species with paternal care tend to have lower levels of testos-
terone while engaging in paternal behaviour [102]. For
monogamous species, reproductive effort not only trades
off against parenting, but also with investment in a single
mate versus other mates [16,29,103]. Thus, high testosterone
levels are associated with short-term mating strategies, and
low testosterone levels with long-term mating strategies.
(b) Testosterone and dyadic competition
Acute increases in testosterone during male–male compe-
tition permit short-term benefits such as increased sugar
uptake by muscle cells during physical confrontations while
avoiding the energetic costs of a continually high testosterone
phenotype [104,105]. The dynamics of acute and longer term
(e.g. seasonal) testosterone change have been well studied
using a life-history theory framework with a theoretical
model called the challenge hypothesis (CH) [99]. The CH
has been applied to dyadic encounters in many vertebrates
from fish [106] to birds [99], and mammals including
primates [35,107,108]. The acute male– male competition por-
tion of the CH, which has since been expanded upon by
Wingfield and co-workers [109], has also been applied to
human male sports competitions among unrelated men,
resulting in increased testosterone during and following com-
petition [39]. It should be noted that while in humans this
research is usually conducted among young, college-age
males who are in the peak age range for testosterone, acute
increases in testosterone occur across a wide range of ages
[98], and even among women [31].
While engaging in physical competition often results in
acute increases in testosterone in both competitors, the
winners of male–male competition appear to have larger
increases in testosterone across many taxa [107], includ-
ing many, though not all, studies in humans [39]; this
phenomenon is often called the ‘Winner Effect’ or ‘Winner-
Challenge Effect’. In humans and animal models, repeated
acute increases in testosterone during physical activity have
the potential to benefit muscle physiology [104,105,110]
(though see [111,112], and the rebuttal [113]). In animal
models, repeated winning during conflict can result in more
aggressive strategies and the increased probability of winning
future fights [107,114]. The mechanism responsible for acute
increases in testosterone during competition or even physical
activity has yet to be elucidated, and indeed some types of
non-competitive physical activity result in greater increases
in testosterone than direct male– male competition [115]. It
is therefore difficult to test whether acute increases in testos-
terone during physical activity are an adaptation, or
exaptation. That said, it is important to note that acute
increases in testosterone also occur during competition in
the absence of physical activity (e.g. chess, dominoes and
video games) [30,116,117]. Acute increases in testosterone
during even non-physical interactions help prepare the com-
petitor, by activating receptors in the amygdala that increase
the salience of violent threat [10], and also via acute benefits
to muscle physiology in the event that the confrontation
escalates to violence [105]. Additionally, there appears to be
an anticipatory rise in testosterone prior to sports compe-
tition, even before any physical activity has taken place,
perhaps preparing the body both physically and mentally
[118]. Thus it seems likely that acute increases in testosterone
during competitive non-physical activity, or in preparation
for physical competition, are indeed adaptations to prepare
the competitor both mentally and physically, while avoiding
the costs (e.g. energetic, potentially immunosuppressive,
parenting) of consistently elevated testosterone.
(c) Testosterone and intergroup competition
While many mammalian competitions are dyadic with a
single winner and a single loser, human and other primate
competitions often involve large groups of related or unre-
lated individuals. Consistent with the parochial psychology
described above (e.g. [65,66]), men and women engaging in
competition against another team show larger increases in
testosterone than when they are scrimmaging with their
own teammates [30,31]. Interactions between testosterone
and OT may reinforce each other to produce these parochial
effects (see below). Additional evidence with more salient in-
groups come from Dominica, where men playing dominoes
against competitors from neighbouring villages tended to
have larger increases in testosterone than individuals playing
against competitors from their home community [117].
A recent study found that acute increases in testosterone can
increase cooperation within an in-group via increased paro-
chial altruism when facing a potential out-group [119].
Interestingly, research conducted among Tsimane
´,where
community membership is fluid and community-based com-
petitions often pit men against their kin, show no evidence of
a team-based winner effect [98].
Competition between sports teams often allow individuals
to show their prowess regardless of their team’s success;
indeed, studies find that males who outperform their team-
mates show larger increases in testosterone, regardless of
whether their team won or lost [98]. In chimpanzees, certain
‘impact’ males increase the likelihood of a border patrol
[120,121], and some of these impact patrollers also went on to
become alpha male and achieve high reproductive success. It
is not known whether these impact patrollers show acute
spikes in testosterone beyond that of other chimpanzees on
the same patrol, but such a study would be an interesting com-
parison given that high impact human soccer players have
larger acute increases in testosterone than others on the same
team [98]. Thus, individual differences in performance
or motivation are probably related to differences in endocrine
physiology, with substantial effects for collective action.
4. Synthesis and future directions
While the above studies describe some of the current state of
the literature in regards to two potential hormonal modu-
lators of cooperation at various relational levels, there is still
a paucity of research on hormonal mechanisms that help
facilitate large-scale collective action. Three potential areas
for future research are discussed below; (a) interactions
between hormonal systems, (b) genetics and sensitivity of
hormone receptors and (c) phylogenetic analyses.
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(a) Interactions between hormonal systems
Most studies of hormone– behaviour interactions focus on a
single behaviour and a single hormone, but not interactions
between endocrine systems. Interactions are important
because considerations of adaptive value or exaptation for a
particular hormone requires knowledge of the average effects
of that hormone across all conditions, even when those
conditions may vary across levels of other hormones. A few
papers have addressed the possibility of interactions between
a limited number of hormones. For example, the ‘Dual
Hormone Hypothesis’ examines interactions between cortisol
and testosterone with respect to dominance [122]; in particu-
lar, when male social status is under threat, high testosterone
men become aggressive, though only when cortisol is low
[123]. Another line of evidence examines the ‘Steroid/Peptide
Theory of Social Bonds’ focusing on the inter-related roles of
testosterone, OT, vasopressin and social bonding [103]. Other
studies have examined the impact of cortisol on testosterone
following fatherhood [124]. These are excellent first steps, as
individual hormones do not exist in isolation. There are
many examples of hormonal systems that overlap in their
response to a stimulus; during mammalian stress response,
rapid increases in catecholamines (epinephrine and norepi-
nephrine) have acute impacts on heart rate and blood
pressure, and release glucose stored in the liver to increase
energy necessary to fight or flee from the stressor. Catechol-
amines also release enzymes that speed up the ability of the
body to release cortisol. Thus, there are networks of synergis-
tic and antagonistic hormones that reinforce and feedback
into other hormonal systems. With the advent of new imag-
ing techniques like multiplex technology, it is now possible
to measure multiple hormones simultaneously, and to
explore interactions not only between baseline hormone
levels, but also among levels during acute changes in these
hormones, in relation to different treatment conditions.
How do OT and testosterone interact to produce
cooperation at the various relational levels discussed here?
While testosterone and OT are usually considered diametri-
cally opposed forces, with testosterone promoting aggression
and OT promoting bonding (e.g. [13,103]), there is evidence
in mouse models that higher levels of testosterone can promote
OT binding [125] and receptor transcription [126]. OT can also
augment Leydig cell testosterone production [127,128]. Studies
in humans show that both testosterone and OT increase simul-
taneously in a range of activities from sexual activity [18], to
hunting [46], to in-group/out-group competition [26,33], and
that exogenous OT administration increased salivary testoster-
one levels and enjoyment from parenting in fathers [47]
(though note that not all OT administration studies find con-
current increases in testosterone [129]). Taken at face value,
this evidence may suggest the potential for OT and testosterone
to work in concert to promote cooperative or coalitional beha-
viours. For example, high levels of OT could increase tolerance
within an in-group and simultaneously facilitate negative
interactions with out-group members [26,67,68], while a con-
current rise in testosterone could prepare both body [105]
and mind [10] for potential violent interactions. Thus, testoster-
one and OT could be working in a coordinated fashion to
facilitate investment in cooperative relationships (mostly low
testosterone, high OT), but also protective aggression against
out-group threats at any relational level (high testosterone,
high OT). Beyond parenting and mating contexts [103], studies
examining interactions between testosterone and OT in terms
of baseline levels and acute changes in relation to cooperative
behaviour have yet to be conducted [47].
(b) Beyond hormone concentrations: genetics and
sensitivity of hormone receptors
Most studies examining hormone– behaviour interactions have
focused on measuring baseline and/or acute changes in circu-
lating hormones, or the behavioural changes induced by an
exogenous administration of a hormone; yet circulating hor-
mone levels comprise only one component of a broader
biological communication network that facilitates different be-
havioural responses (figure 1). A classic example of the role of
hormone receptors, above and beyond circulating hormone
levels, comes from monogamous prairie voles and polygynous
montane voles, both of which have the same circulating levels
of OT but differ in receptor distribution in the brain [130]. As
the effects of these changes are highly localized (as opposed
to the systemic effects of changes in baseline levels), they prob-
ably represent adaptations resulting from selection on specific
behaviours, in this case pair-bonding and parenting [7].
For a hormone to have an impact on behaviour then, it must
activate receptors in critical brain regions. Most hormone
receptors are laid down during sensitive organizational
periods, such as perinatally and during puberty [131– 133].
Most experimental work on receptors is with murine models,
where exposure to androgens is critical for the development
of androgen receptors and the organization of brain physi-
ology. Male mice gonadectomized prior to puberty never
develop the level of androgen receptors required for activa-
tion of male behaviours, even when exposed to high levels of
testosterone during adulthood [131]. This may explain some
sex differences in male and female response to exogenous tes-
tosterone (table 1); studies in humans find that males given
testosterone supplementation show changes in behaviour on
economic games [33], while women show no behavioural
change [34]. Interestingly, female hyaenas are one of relatively
few species where testosterone regulates female aggression,
and females have relatively high levels of circulating androgens
in utero and during the peri-pubertal period; female hyaenas
thus develop androgen receptors and behaviour typically
associated with male mammals [6,11].
It is difficult to measure receptor densities in living ani-
mals. Most studies that directly measure receptor densities
sacrifice the animal, and then stain brain tissue. Another,
less invasive method to examine individual or species differ-
ences in receptors is through variation in the genetics of
hormone receptors (table 3). With regards to androgens, the
number of CAG codon repeats on the androgen receptor
modulates the impact of circulating androgens; fewer CAG
repeats result in greater androgen receptor protein expression
and transcriptional activity, which result in greater impact
per unit of circulating androgen [150]. In non-human pri-
mates, macaques and marmosets have no variation in CAG
repeats (monomorphic), while baboons and chimpanzees
show polymorphic variation [151]. Several studies have
reported that human males with fewer CAG repeats have
higher levels of upper body strength, self-reported competi-
tiveness and greater testosterone response to potential mate
exposure [150,152], though not all studies find associations
between strength and CAG repeat length [153,154].
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Though the genetics of androgen receptors may be a prom-
ising avenue, the evidence for impacts of several candidate
single nucleotide polymorphisms (SNPs) associated with the
OT receptor gene OXTR appears less conclusive, as indicated
by a recent meta-analysis finding no significant overall effects
of OXTR variation on social behaviour [147] (though another
meta-analysis vindicated an association with autism [145]).
Furthermore, bonobos and chimpanzees do not exhibit these
candidate SNPs despite differences in social behaviour [143],
and variation in OXTR as well as prolactin and vasopressin
receptor genes across primates more broadly do not easily
map onto social and mating systems [148,149,155]. Finally, sug-
gestive results have been found for various other receptor
genes, as summarized in table 3. For example, chimpanzees
with a deleted DupB region of the vasopressin receptor have
impaired social cognition and fewer allies [142]; in human
males, deletion of a portion of the same region (RS3) is associ-
ated with higher divorce rates [144]. In summary, there is a
limited, but growing body of evidence that variation in the gen-
etics of hormone receptors may impact social behaviour above
and beyond circulating hormone levels (e.g. figure 1), thus
providing more direct evidence for adaptation [9].
In sum, hormonal reinforcement of behaviour need not just
result from increased hormone levels, but also increased recep-
tor sensitivity or density, or even increased neural transport of
hormonal signals to critical brain regions. When considering
the evolution of mechanisms that could reinforce behaviour,
it is therefore essential to focus not just on hormones, but
also their binding proteins (which modulate the bioavailability
of circulating hormones), receptor sensitivity and specificity,
and the location of those receptors in critical brain regions
(figure 1). For example, most circulating testosterone in
humans is bound to carrier proteins (sex hormone-binding
globulin (SHBG) and albumin), with only about 2% of circulat-
ing testosterone unbound or ‘free’. Testosterone bound to
SHBG is unavailable for use in target tissues, so species level
variation in SHBG could influence the bioavailability of testos-
terone even for two species with the same total levels of
testosterone. Advances in endocrinology, receptor genetics
and neuroimaging will make it possible to examine how
changes in hormones impact brain physiology in ways that
impact changes in behaviour [10,156].
(c) Phylogenetic approaches to hormonal mechanisms
Examining the evolutionary history of the mechanisms that
mediate hormonal physiology is a vital step for disentangling
adaptations from exaptations, trade-offs or constraints [6]. Phy-
logenetic analyses of more than 100 avian species suggest that
environmental constraints shape reproductive behaviour and
mediate both baseline and peak levels of androgens [157].
However, phylogenetic analyses examining differences in
Table 3. Examples of receptor genetics associated with cooperative behaviours for humans and primates. Review articles cited when possible, blank cells
indicate more research is needed.
receptor genetics context primates human males human females
androgen receptor short CAG repeats !less prosocial in Chinese, but
not Israeli men
[134]
no effect [134]
oestrogen receptor
(ER-b)
shorter allele (suggesting more oestrogenic
activity) linked to lower minimal
acceptable offer
[134]
serotonin
transporter (5-HTT)
longer allele more prosocial, shorter allele
more anxious
macaques [135–137] [138]
dopamine receptor
(DRD4)
DRD4 allele increase in fairness no effect in macaques [135] [139]
vasopressin receptor vasopressin receptor AVPR1A-RS3 carriers
less fair in dictator games
[140,141]
double deletion of DupB region (which
includes RS3) decreases social cognition,
competence
chimpanzees [142]
no deletion in bonobos [143]
vasopressin receptor AVPR1A-RS3 more
likely to divorce
[144]
OT receptor OXTR SNPs (rs53576 and rs2254298)
increase prosociality
no variation in chimpanzees and
bonobos [143]
mixed results [145,146], but some
meta-analyses show no significant
effect [147]
OXTR and pair-bonding receptor differences in primates
do not map onto mating
system [148]
prolactin receptor pair-bonding receptor differences do not map onto paternal care [149]
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hormone– behaviour interactions, particularly those related to
cooperation, competition and collective action in primates,
have yet to be conducted. One of the few studies looking at
closely related primate species with different social ecologies
found substantial differences in chimpanzee and bonobo
hormonal responses to competition [38]. An integrated phylo-
genetic approach, examining both baseline and acute changes
in neurohormones and receptor densities, binding proteins
and other potential hormonal mechanisms across primate
species, is needed to advance our understanding of evolved
human behavioural endocrinology.
5. Conclusion
While most of the hormone–behaviour interactions discussed
here were species typical (e.g. the role of OT in marmoset
paternal care), individuals within many species vary in their
degree and willingness to cooperate, reflecting different adap-
tive strategies. The rich literature on animal and human
personality, or ‘behavioural syndromes’, is similarly focused
on the adaptive logic of relatively stable, individual differences
[158]. Hormones may play a proximate role in modulating
certain aspects of personality variation. For example, testoster-
one has been linked to behaviours conceptually related to
dispositional dominance [159]. Basal levels of hormones like
testosterone may serve as biomarkers of individual difference,
given its relative temporal stability. A recent study among
high fertility Senegalese men showed that higher testosterone
was associated with greater extraversion [160], lower parenting
effort and greater tendency to be married polygynously [161],
whereas in a US sample high testosterone men also had larger
testes, engaged in less parenting and showed weaker neuronal
activation in response to pictures of their babies [102]. Thus, one
potential underlying proximate cause for individual differences
is that both baseline and acute changes in neurohormones like
testosterone or OT vary within and between individuals. As
mentioned above, it is likely that such hormonally mediated
personality differences play a substantial role in shaping
cooperation and collective action [121].
Despite sharing the same conserved components of the
endocrine architecture with other primates and mammals,
humans cooperate in more contexts and at larger scales
[1–3]. A critical question for future research is whether
high levels of cooperation in humans differ mechanistically
from other species, and in particular whether they are
driven by changes in circulating hormone levels that
impact various behaviours, e.g. through selection for
reduced dominance (testosterone) and increased tolerance
(OT), or whether selection for specific behaviours has chan-
ged endocrine physiology in more targeted ways (e.g.
differences in receptor density or selectivity, binding pro-
teins, etc.; cf. figure 1) [7]. Answering these questions has
potential implications for various theories of human and
primate cooperation such as the cooperative breeding
hypothesis [3] (which posits a general increase in social tol-
erance and cognition, e.g. through higher OT levels) or the
self-domestication hypothesis [162] ( general decrease in
aggression, e.g. through lower testosterone). It is likely
that with a better understanding of interactions between
hormones, a stronger focus on hormone receptors and
better tools to examine neuronal function, we will have a
better understanding of the hormonal modulation that facili-
tated the evolution of large-scale human and primate
coalitional behaviour.
Authors’ contributions. B.C.T. designed and drafted the review, A.V.J. and
M.G. contributed substantially to the design, interpretation and criti-
cally reviewed the document; all authors approved the final version.
Competing interests. We have no competing interests.
Funding. This work was funded by NIA R01AG024119-01,
R56AG024119-06, R01AG024119-07.
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