The Role of Ontogeny in the Evolution of Human Cooperation

Abstract

To explain the evolutionary emergence of uniquely human skills and motivations for cooperation Tomasello et al. (2012) proposed the interdependence hypothesis. The key adaptive context in this account was the obligate collaborative foraging of early human adults. Hawkes (2014), following Hrdy (2009), provided an alternative account for the emergence of uniquely human cooperative skills in which the key was early human infants’ attempts to solicit care and attention from adults in a cooperative breeding context. Here we attempt to reconcile these two accounts. Our composite account accepts Hawkes’ contention that the extremely early emergence of human infants’ cooperative skills suggests an important role for cooperative breeding as adaptive context, perhaps in early Homo. But our account also insists that human cooperation goes well beyond these nascent skills to include such things as the communicative and cultural conventions, norms, and institutions created by later Homo and early modern humans to deal with adult problems of social coordination. As part of this account we hypothesize how each of the main stages of human ontogeny (infancy, childhood, adolescence) was transformed during evolution both by infants’ cooperative skills “migrating up” in age and by adults’ cooperative skills “migrating down” in age.

Full text

The Role of Ontogeny in the Evolution
of Human Cooperation
Michael Tomasello
1,2
&Ivan Gonzalez-Cabrera
1,3
Published online: 18 May 2017
#The Author(s) 2017. This article is an open access publication
Abstract To explain the evolutionary emergence of uniquely human skills and motiva-
tions for cooperation, Tomasello et al. (2012,inCurrent Anthropology 53(6):673–92)
proposed the interdependence hypothesis. The key adaptive context in this account was
the obligate collaborative foraging of early human adults. Hawkes (2014,inHuman
Nature 25(1):28–48), following Hrdy (Mothers and Others, Harvard University Press,
2009), provided an alternative account for the emergence of uniquely human cooperative
skills in which the key was early human infants’attempts to solicit care and attention from
adults in a cooperative breeding context. Here we attempt to reconcile these two accounts.
Our composite account accepts Hrdy’s and Hawkes’s contention that the extremely early
emergence of human infants’cooperative skills suggests an important role for cooperative
breeding as adaptive context, perhaps in early Homo. But our account also insists that
human cooperation goes well beyond these nascent skills to include such things as the
communicative and cultural conventions, norms, and institutions created by later Homo
and early modern humans to deal with adult problems of social coordination. As part of
this account we hypothesize how each of the main stages of human ontogeny (infancy,
childhood, adolescence) was transformed during evolution both by infants’cooperative
skills “migrating up”in age and by adults’cooperative skills “migrating down”in age.
Keywords Human cooperation .Shared intent ionality.Coop erative breeding .Evolution
of human ontogeny .Collaborative foraging
Many of the most distinctive cognitive and social differences between humans and their
nearest primate relatives derive from humans’unique skills and motivations for
Hum Nat (2017) 28:274–288
DOI 10.1007/s12110-017-9291-1
*Michael Tomasello
tomas@eva.mpg.de
1
Max Planck Institute for Evolutionary Anthropology, 04105 Leipzig, Germany
2
Department of Psychology and Neuroscience, Duke University, Durham, NC, USA
3
Konrad Lorenz Institute for Evolution and Cognition Research, Klosterneuburg, Austria
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

cooperation. Tomasello et al. (2012) summarize these differences and hypothesize a
two-step evolutionary sequence—from small-scale collaboration to culture-level coop-
eration—to explain their emergence in the human lineage. Hawkes (2014)doesnot
dispute this general account, but, following Hrdy (2009), she emphasizes a subset of
humans’unique skills and motivations for cooperation and so hypothesizes an
alternative evolutionary scenario focusing on the role of cooperative breeding,
especially the unique demands it places on infants. Our attempt here is to synthesize
these two evolutionary scenarios into one account that is more accurate and
comprehensive than either alone.
The Interdependence Hypothesis
To account for the emergence of uniquely human forms of cooperation, Tomasello et al.
(2012) propose the interdependence hypothesis. Following Roberts (2005), the evolu-
tionary logic of the hypothesis is that in highly social species individuals depend on one
another for various aspects of their fitness. A primate individual’smostimportant
mating partner, coalition partner, or, in some cases, foraging partner, are important to
their fitness. Following the same logic as kin selection, there is thus an evolutionary
benefit for helping these partners, and so the individual should invest, to some degree,
in their fitness. There is obviously a mathematics to this investment determining the
maximally beneficial level, just as there is in kin selection. And just as there is in kin
selection, there is potentially a motivation to free ride—to let others help my kin or my
valued partners—but often an incentive to do the helping oneself to make sure it gets
done. Thus, interdependence means that individuals in social groups are constantly, to
some degree, investing in the fitness of their group mates.
For the first step in the account, the proposal is that species-unique forms of
human cooperation, and the underlying psychology supporting them, first emerged
in the context of early humans’shift to obligate collaborative foraging. The
process very likely began around 2 million years ago with the emergence of the
genus Homo and was consolidated by around 400,000 years ago with the emer-
gence of Homo heidelbergensis (Stiner 2013). In terms of cognition, the interde-
pendence hypothesis holds that humans’unique cognitive skills first emerged to
solve problems of social coordination in the context of mutualistic collaboration
(Tomasello 2014). Much evidence suggests that humans collaborate with a partner
in unique ways; for example, they form together a joint goal, which then creates
two interrelated roles aimed at the same end (Fletcher et al. 2012; Hamann et al.
2012). Unique forms of human cooperative communication—initially the uniquely
human communicative gestures of pointing and pantomiming—arose as means for
coordinating such mutualistic activities (Tomasello 2008). Such cooperative com-
munication depends on joint attention to external referents and the ability to
recursively “read”the intentional states of others. In terms of sociality, early
humans engaged in a kind of cooperativization of competition resulting in a sense
of fairness in dividing the spoils of collaborative efforts in mutually satisfactory
ways (excluding underserving free riders in the process). An important dimension
of this process was partner choice and control (and the resulting social selection):
individuals who could not peaceably divide the spoils of a collaborative effort
Hum Nat (2017) 28:274–288 275
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

with a partner (or otherwise cooperate) would not be selected as a partner in the
future. Early human collaborative partners knew that each of them had to play
their role in mutually known ways for their joint success, leading to processes of
social evaluation and, eventually, moral judgment.
The second evolutionary step of the interdependence hypothesis proposes that
all of this got scaled up as modern humans began forming cultural groups
beginning some 150,000 years ago. All the members of a modern human cultural
group understood themselves to be interdependent with their group mates for
survival, including in the context of competition with other groups, and indeed
members of other groups were thought of as free riders or competitors not
deserving of any of the fruits of their collective labor. In this context, modern
humans evolved, cognitively, the ability to create collective, group-minded cul-
tural structures such as linguistic conventions, social norms, and cultural
institutions to coordinate and regulate their group life.
Much of the evidence that Tomasello et al. (2012) cite for this account derives
from experimental studies comparing the behavior of great apes and human
children of various ages. Many of the important aspects of human uniqueness
emerge during human infancy and early childhood, especially the uniquely human
versions of collaboration, joint attention, cooperative communication, and
resource sharing. Hawkes (2012,2014) adopts the perspective of human life
history theory and asks why these uniquely human cognitive and social abilities
should emerge at such a young age. If it’s all about collaborative foraging and
intergroup competition, why do infants need unique skills? In their response,
Tomasello et al. (2012) merely point out that many skills important for adults
begin their ontogenetic trajectories earlier in development because they require
time for maturation, learning, and other forms of preparation. But further consid-
eration deems this an inadequate response, as children develop the skills many
years before they would be needed for their adult functions, with a long period of
early and middle childhood in between. To date, then, the question of early
ontogenetic emergence has not been answered from the point of view of the
interdependence hypothesis.
The Cooperative Breeding Hypothesis
For other extant apes, childcare is provided almost exclusively by the mother, and
mother and infant are in almost constant bodily contact. But for humans, childcare is
also provided by fathers, grandparents, and others in the social group, on average across
many different cultures in the contemporary world at the rate of about 50% after early
infancy. Hrdy (1999,2005,2009) identified this pattern as an instance of cooperative
breeding—broadly defined to include all systems in which alloparents as well as parent
help care for and protect offspring—which has a number of somewhat different
manifestations across species. Prototypically, many bird species—and among primates
the callitrichidae (marmosets and tamarins)—practice cooperative breeding, with
helpers doing such things as provisioning and transporting infants. The evolutionary
bases of cooperative breeding systems often involve kin selection, and sometimes
individuals are punished by others in the group if they do not help (so-called pay to
276 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

stay).
1
Human mothers benefit from childrearing help in many ways, not least of which
is the ability to care for more offspring.
Hrdy (1999,2009) notes that in cooperative breeding species helpers must have at least
some kind of prosocial motivation, even if their goal to help others is grounded evolu-
tionarily in kin selection or proximately in a desire to avoid punishment. In the human
case, kin selection is clearly not the whole story, as helpers are often other unrelated adults,
and punishing non-helpers does not seem to play an important role. In this case, then,
helpers should evolve especially strong prosocial motivations. Burkart and van Schaik
(2010) surveyed observational and experimental data on cooperative breeding species
across a variety of different taxa and concluded that indeed cooperative breeding leads to,
among other things, more prosocial motivations. Hawkes (2014) proposes some addi-
tional hypotheses. Following Hrdy, she focuses on the implications of a human-like
cooperative breeding system not just for the helpers but for the infants themselves (what
might be called the “development plus social selection model”for the effects of the human
cooperative breeding system on ontogeny; Hrdy 2016). Human infants face a new
challenge as they grow up with a mother who, unlike other primate mothers, leaves them
for some periods of time with other adults. The infants must then compete with siblings
and other infants and young children for the attention and care of their mother, and, in
addition, the attention and care of less-familiar caregivers. Because cooperative breeding
enables human mothers to have more closely spaced offspring, there is, presumably,
heightened sibling competition.
The human cooperative breeding system thus sets up a selective context in which those
infants do best who can discern the thoughts and moods of caregivers and solicit help and
care best through various kinds of emotional and referential communication. The outcome
is that not only have humans been selected to be especially prosocial as helpers in a
cooperative breeding system, the human infancy period has come under special selection
pressures for various skills of social cognition and communication. Both Hrdy and
Hawkes single out for special attention various skills of shared intentionality, which have
been shown to be unique to the human species and of special importance in the evolution
of cooperation and culture (e.g., Tomasello et al. 2005,2012). The foundational skills,
which emerge in human infancy and early childhood, concern such things as joint
attention (the intersubjective sharing of experience) and cooperative communication via
gestures such as pointing and, ultimately, language. The infant adaptations are special in
this account because they are seen as ontogenetic adaptations for the infancy period, not as
deferred adaptations whose original function was to promote the fitness of adults. This is
clearly a different hypothesis from that of Tomasello et al. (2012), who have posited that
humans’unique skills and motivations of shared intentionality are adaptations mainly for
1
The evolution of cooperative breeding in the human lineage is estimated to have happened around 2.0–1.8
million years ago with Homo erectus (see Burkart and van Schaik 2010). In other cooperative breeding
species, pressures that lead to cooperative breeding include predation risk, environmental unpredictability, and
those associated with the colonization of new habitats (Clutton-Brock 2006; Hrdy 2005,2009;Islerandvan
Schaik 2012). These selective pressures likely played some role in the evolution of cooperative breeding in the
human lineage. For example, predation risk is expected to intensify with shifts toward more open habitats
(Hart and Sussman 2005), and the most significant shift toward open landscapes occurred after 2.0 million
years ago (Lee-Thorp, Sponheimer, and Luyt 2007). Moreover, conditions of increasing seasonality during the
Pleistocene also led to environmental unpredictability (Potts 1998). Finally, early Homo is known to have
colonized large areas outside Africa around the same period, which has been traditionally linked to the
emergence of cooperative breeding (Burkart and van Schaik 2010; Hrdy 2005,2009).
Hum Nat (2017) 28:274–288 277
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

adults’uniquely cooperative forms of social life, especially as manifested in cooperative
foraging and other cultural lifeways.
Tomasello et al. (2012) acknowledged a role for cooperative breeding in the evolution
of humans’lesser aggression and dominance relative to other apes, and greater tolerance
around food. But they did not agree with Hrdy and Hawkes that shared intentionality—at
least in its foundational aspects—is an ontogenetic adaptation enabling infants to better
navigate the special social world created by a cooperative breeding system. In particular,
they argued that cooperative breeding would not seem to create the kinds of cognitive
challenges that would lead beyond the relatively simple kinds of things that infants do to
capture attention and solicit care to such cognitively complex things as social conventions,
norms, and institutions (including conventional languages). For the evolution of these
things we need the kinds of cognitive challenges that adults face, perhaps in the context of
obligate collaborative foraging and, later, cultural life.
The result of all of these considerations is that the interdependence hypothesis has a
weakness in that it has no ready explanation for the early ontogenetic emergence of
skills of shared intentionality, and the cooperative breeding hypothesis has a weakness
in that it has no ready explanation for how humans go beyond joint attention and
gestural communication to the complex cognition underlying human cultural life.
A Composite Account
Our proposal here is that a comprehensive account of the evolution of human cooper-
ation—and the psychological skills and motivations of shared intentionality that go
with it—requires insights from both the interdependence and the cooperative breeding
hypotheses. Following Hrdy and Hawkes, what we need is an evolutionary scenario
that takes into account human life history, that is, the adaptations that have emerged to
deal with the challenges of each ontogenetic period on its own terms. In addition, we
need a scenario in which adaptations originally associated with one ontogenetic period
may be extended to different ontogenetic periods, with cascading effects as they interact
with existing developmental pathways in novel ways.
We focus here on Tomasello et al.’s(2012) first step in the evolution of uniquely
human cooperation, a period during which early humans (from Homo erectus to Homo
heidelbergensis) began cooperating in new ways but did not yet have cultural organiza-
tion. (Later we speculate briefly about the ontogeny of modern humans, Homo sapiens,
after the emergence of culture.) The proposal is that these new ways of cooperating
involved both collaborative foraging and cooperative breeding, which would have been
complementary components in an overall more cooperative lifestyle. We leave open the
original selective context for cooperative breeding—which presumably went along with
the emergence of human pair bonding (Chapais 2008)—but only claim that at some point
these two forms of ultra-cooperative interaction were mutually supportive.
Evolution and Ontogeny
A central insight of evolutionary developmental biology (evo-devo; e.g., West-
Eberhard 2003) is that many, if not most, significant evolutionary changes result from
changes in ontogenetic timing. That is, if an adaptation emerges earlier or later in
278 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

ontogeny, or takes shorter or longer to develop, in a modern population as compared
with an ancestral population, the result can be huge changes in the phenotype because
of the interaction of this change with existing developmental pathways. For example,
when over evolutionary time juvenile characteristics come to be extended into adult-
hood in a pattern of neoteny, the effects may extend well beyond that characteristic
itself (e.g., childhood curiosity combines with adult cognitive and social skills to result
in science). Or if it were the case that running was originally an adaptation for adults
stalking prey, if it extended to an earlier period in ontogeny, it might now be adaptive
for children outrunning predators.
The way such changes happen are strictly Darwinian, but in a developmental context.
Thus, many changes in developmental timing are a simple result of the fact that because of
random variation an adaptation emerges in some individuals a bit earlier or a bit later than
the norm, or the adaptation takes shorter or longer to develop than is typical. If there is a
fitness benefit for individuals at the extreme—those in whom the adaptation emerges
earliest or latest—then a change in timing should occur. The fitness benefit is first and
foremost about the particular developmental periods involved, but it may extend to later
developmental periods if, for example, skills developed at one period are especially good
preparation for challenges to be faced at some later period. Any time there is a potential
change in developmental timing, there are “developmental constraints”that must be
overcome, in the sense that the change in timing of one system cannot disrupt already
existing systems inordinately. Organisms must be fit at each step in ontogeny indepen-
dently—and this cannot be disrupted—if they are to live to pass on their genes, with the
greatest fitness benefits going to those who live long and fecund lives.
In this context, the interdependence hypothesis can be recast as follows:
adaptations for shared intentionality that were beneficial in adult activities
(i.e., collaborative foraging) “migrated down”in ontogeny because they benefit-
ed immature individuals in their activities as well. This migration process, in
turn, also benefited affected adults because developing skills earlier enabled
extra preparation and practice for collaborative activities in adulthood. In the
same spirit, the cooperative breeding hypothesis can be recast as follows:
adaptations for shared intentionality that were beneficial to infants and young
children in a cooperative breeding context “migrated up”in ontogeny because
they benefited these children in their later collaborative and communicative
activities as well. These individuals were then better adapted, in some sense
by chance, for adult activities relying on collaboration and communication.
Our proposal is that in fact both of these processes occurred. That is, we propose that
human cooperative breeding and collaborative forms of subsistence coevolved because
mothers who received help rearing their young could be much more productive in
collaborative foraging (and the helpers would share in the fruits of her labor). This
combined hypothesis would explain both why skills of shared intentionality first emerge
in contemporary human ontogeny in infants and young children—that is, as ontogenetic
adaptations for infancy in a human-like cooperative breeding situation—and why con-
temporary humans have the complex cognitive skills for social and cultural coordination
that they have—that is, as these ontogenetic adaptations extended to older children and
adults and interacted with other systems for solving adult problems of social and cultural
coordination (and perhaps set the stage for new adaptations for these older individuals as
well) in ways that increased adult fitness.
Hum Nat (2017) 28:274–288 279
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Our composite account thus consists of both bottom-up and top-down processes of
natural selection operating within ontogeny. Bottom-up processes are those in which an
ontogenetic adaptation migrates up and—by chance, as it were—increases the fitness of
the adult individuals who possess it, a kind of ontogenetic preadaptation for adulthood.
But, of course, if there is a fitness benefit for adults who possess the competency, then this
creates a kind of ontogenetic top-down selective pressure as well for younger individuals
to develop the competency as a deferred adaptation (assuming that a longer ontogeny,
beginning earlier, is somehow advantageous for adults as preparation for the “real thing”).
With this background, of special importance in the current account are three relatively
distinct periods of ontogeny, each with its own set of adaptive challenges: (i) infancy and
toddlerhood (before weaning, approximately 0–3 years); (ii) early and middle childhood
(weaning to sexual maturity, approximately 4–12 years); and (iii) adolescence and
adulthood (sexual maturity, approximately 13 years and beyond).
Infancy and Toddlerhood (Pre-Weaning; 0–3years)
Hrdy’s(2005,2009) basic proposal is that in a cooperative breeding context, in which
mothers had much help, they had babies at more closely spaced birth intervals than did
other apes. Mothers were thus forced to divide their care and attention to offspring more
than other apes, and indeed to relinquish physical contact and responsibility to other
adults to care for their offspring (in a way that other apes do not systematically do). In
her “development and social selection”corollary hypothesis, children of all ages would
then have had to compete more strenuously for adult care and attention, and they would
have had to learn to deal with different adults more flexibly (see Sulloway 1996 on the
important role of sibling competition in human development).
Neither Hrdy nor Hawkes goes into much detail about the uniquely human skills and
motivations of shared intentionality involved, but there are several. First, at around six
weeks of age infants begin smiling at others engagingly and from a distance, followed
some weeks later by laughing at others engagingly and from a distance. Although one
may identify some precursor behaviors in infant chimpanzees when they interact with
humans (e.g., Bard 2012), they do not smile and laugh at others from a distance in their
natural social development with mothers or other conspecifics. From around 2 months of
age, human infants begin to engage in the kinds of positive-emotion-sharing interactions
with adults made possible by these unique social behaviors in turn-taking sequences that
some researchers have dubbed “protoconversations”(e.g., Trevarthen 1979;seealso
Reddy 2015; Rochat 2009). The adaptive function of these kinds of infant behaviors is
not attachment; attachment has its own mechanisms with their own evolutionary history,
presumably functioning mainly to ensure protection, reaching back well before the
emergence of primates (Bowlby 1969). Rather, the adaptive function of these unique
infant behaviors is, plausibly, to secure adult care, feeding, and other forms of attention by
sharing positive emotional states, which are reinforcing to both parties.
Tomasello et al. (2005) propose that human infants’skills and motivations for
emotion sharing in protoconversation are transformed, beginning at around 9 months
of age, into a suite of uniquely human skills and motivations for shared intentionality.
At around 9 months of age, human infants are beginning to understand others as
intentional agents (with goals and perceptions that guide their behavior) in the same
basic way as do other great apes, although, interestingly, human infants seem to
280 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

develop these skills at a somewhat earlier age (Wobber et al. 2013). What happens,
then, is that the sharing of emotions extends to the sharing of attention and interest in
external objects and events—behaviors in which great ape infants never engage (see
Tomasello and Carpenter 2005; Tomonaga et al. 2004)—via a synergistic combination
of uniquely human emotion sharing and great ape–wide cognitive skills for under-
standing the intentionality of others. These joint attentional behaviors are not just
following the gaze direction of others—which great apes do from an early age as well
(e.g., Tomasello et al. 2001)—rather they involve more active acts such as showing and
offering objects to others, with an expectation that this will lead to a positive sharing of
emotions about these objects and/or their associated events. In the analysis of Bruner
(1983; see also Tomasello 1995), these unique forms of social interaction involve a
recursive cognitive process in which each expects the other to expect them to expect . . .
(and so on). Importantly, Bakeman and Adamson (1984) found that infants engage in
joint attention much more readily with adults than with infant peers, suggesting adults
as special targets. And in an experimental study with adults, Wolf et al. (2015)found
that subjects showed more signs of social bonding with a partner after they had engaged
with him in joint attention.
An especially important outgrowth of infants’joint attentional behaviors is
cooperative communication as expressed prelinguistically in the uniquely human
gestures of pointing and pantomiming. Whereas great apes will sometimes point
for humans (not conspecifics) imperatively, for things they want (e.g., Leavens
and Hopkins 1998), from around their first birthday human infants point expres-
sively to simply share with an adult their enthusiasm for some object or event (see
Tomasello et al. 2007 for a review). They typically do this dozens of times per day
every day (Matthews et al. 2012), and they do it beginning at about the same age
in all human cultures investigated (Callaghan et al. 2011; Salomo and Liszkowski
2013). In what has been called the nine-month revolution, then, human infants
begin to be highly motivated to share attention to and interest in things with
adults—indeed,toinitiatesuchsharedattention and interest by offering, showing,
and pointing referentially to external events and entities. Their motive is not just
to get the other to look at the object or event, but rather that the adult share a sense
of interest and enthusiasm for it (Liszkowski et al. 2006). They also, and also
uniquely, use the pointing gesture to inform adults of things to help them—for
example, indicating the location of a sought-for object (Liszkowski et al. 2008).
Importantly, Ninio (2016) found that contemporary human infants use their com-
municative skills much more readily and often with adult partners rather than with
peers (see also Stoeber et al. 2017).
The motive to help others is already present in great apes (e.g., Warneken
et al. 2007; Melis et al. 2011). But human infants help others, especially adults,
in some unique ways. In addition to helping them by informing them of things
with the pointing gesture, young human children seem to take the perspective
of the other when engaging in such helping—for example, by providing extra
help to those who have previously been harmed (Vaish et al. 2009), which apes
do not do (Liebal et al. 2014). And, once again, although a properly controlled
experimental study has not been done, comparing across studies one can infer
that human infants help adults at a significantly higher rate than they help other
infants (Warneken and Tomasello 2006; Hepach et al. 2016).
Hum Nat (2017) 28:274–288 281
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

The proposal is thus, following Hrdy (2005,2009), that these uniquely human infant
behaviors evolved in the context of sibling and peer competition for adult care and
attention. Adults are rewarded by sharing emotions, interest in, and attention to objects
and events with infants, and so infants compete to provide adults with these rewards.
Adults thus engage in a process of social selection (West-Eberhard 1979)inwhichthe
infants that are best able to engage them get the most attention. Following Hrdy (2005,
2009,2016), as elaborated by Hawkes (2012,2014), then, we may see the earliest
ontogenetic emergence of skills and motivations for shared intentionality as adaptations
for sibling/peer competition for securing adult attention. Note that in this hypothesis, it
must be infants who lead the way in skills and motivations for joint attention. In the early
evolutionary steps, they must have used joint attentional skills to “hijack”already existing
adult emotional and bonding mechanisms for their own ends. Adult skills and motivations
for shared intentionality would have then followed as these skills and motivations also
provided fitness benefits to individuals at older ages (see Table 1for a summary).
Childhood (Weaning to Sexual Maturity; 4–12 years)
Human infants wean a year or two younger than other apes, at around three years of
age, but then they, unlike other apes, depend on adults for provisioning, protection, and
other care well into adolescence. During the still-dependent periods of early and middle
childhood, then, human children are still engaged in a process of sibling/peer compe-
tition for adult care and attention. In addition, children in this age range are dependent
on adults for learning many necessary things about their shared world and how best to
accomplish things in it. One way children gain the needed adult care and attention is by
making themselves especially useful to adults (ingratiating themselves with adults) by
helping them with various tasks. Kramer (2005) has thus emphasized that human
children often help their parents and caregivers in various ways, and so cooperative
breeding actually fosters a two-way interdependence between adults and youngsters.
But, in addition, early and middle childhood also ushers in a whole new social world
for children: the world of peers. Interactions with adults are inherently asymmetrical
because adults possess all of the power, competence, and knowledge, which infants and
young children respect and defer to. But interactions with peers are more symmetrical
Tab le 1 Species-unique behaviors of human infants evolved to solicit care and attention (and/or bonding)
from distracted adults in cooperative breeding context
Uniquely Human
Infant Behavior
Function in Cooperative
Breeding Context
Relevant Reference(s)
to Apes and Human Infants
Intentional crying and imperative
gestures
Requesting help from adults Tomasello (2008) for a review
Helping and informative gestures Offering help and information
to adults
Bullinger et al. (2014);
Liszkowski et al. (2008)
Social smiling and laughing
at a distance
Recognition of and affiliation
to recipient
Trevarthen (1979); Bard (2012)
Expressive gestures (e.g., pointing
to share interest)
Aligning psychological states (joint
attention) as way of bonding
Tomasello and Carpenter (2005);
Wolf et al. (2015)
282 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

since peers have no special power, competence, or knowledge; they must be dealt with
on an equal footing. The child cannot rely on or defer to a peer partner as she can an
adult partner, and so things must be worked out. On the one hand, being too shy and
unassertive will result in being taken advantage of, but, on the other hand, attempting to
be too dominant might very well end up in ostracism. With specific reference to moral
development—as uniquely human internalized cooperative tendencies—Piaget (1932)
describes childhood as inhabiting two distinct social worlds, one based on authority
(with adults) and the other based on reciprocity (with peers).
The peer world is the world the individual will inhabit as an adult. This is a world in
which things must be worked out among more-or-less equal partners. In this sense,
children’s adaptations for interacting with peers during early and middle childhood are
very likely deferred adaptations, whose adaptive significance lies in the ways in which
they prepare children for adulthood. During early and middle childhood children learn
to make decisions with others—for example, about where to go or what to play
(Köymen et al. 2014). They learn to treat others fairly—for example, by sharing
resources in a mutually satisfactory manner (Hamann et al. 2011). They learn to make
and keep joint commitments, as they commit to doing something in the future and must
keep it or risk reprisals (Gräfenhain et al. 2009).Allofthisiscementedinhuman
development by a unique tendency (i.e., unique among apes): young children, but not
other apes, are concerned about others’evaluations of their cooperative tendencies, and
they adjust their behavior based on their prediction of how others will assess it, so-
called impression management (Engelmann et al. 2012). And thus children do not have
to try out things and get feedback on how others view them; rather they self-regulate
their own behavior by anticipating how others will assess it.
The proposal is that early human children who developed more and better skills of
shared intentionality fared better in this new world of peer interaction. Hence the
infants’ontogenetic adaptation for shared intentionality in joint attentional and com-
municative interactions with adults “migrated up.”As a crucial part of the process, in
early and middle childhood a new process emerged of social selection involving not
adults but peers. Perhaps often in the protected context of play, but sometimes in more
serious contexts as well, young children must cooperate with others or suffer the
consequences. They know this, and so they develop a kind of cooperative identity—
simultaneously a social persona and an internalized sense of self—for social interac-
tions with peers. Arguably, this does not and cannot develop out of interactions with
adults, who do not cooperate but rather legislate. If these kinds of childhood interac-
tions are conceived as preparations for adulthood, two consequences ensue. On the one
hand, one’s interactions with same-gender peers are crucial in developing a cooperative
identity for engaging in various collaborative tasks. And, on the other hand, despite the
pronounced gender segregation of the social interactions during middle childhood, this
will very likely have effects on the judgments of individuals of the opposite gender as
well and thus, in a community of mostly familiar peers, will have effects for one’s
sexual prospects in adulthood.
The outcome is the two social worlds of childhood. During early and middle
childhood, there is social selection from three sources: (i) adults selectively dispense
attention and resources to children whom they like and who help them; (ii)same-
gender peers prefer and selectively interact with good cooperators; and (iii)opposite-
gender peers begin selecting for mates with good prospects and status in the social
Hum Nat (2017) 28:274–288 283
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

group. But, as Tomasello (2016) has argued, it is not just that children of this age are
being controlled by “them,”but rather they have internalized the collaborative role
standards used by everyone as coming from “us,”and so they develop a genuine sense
of cooperative identity that guides everything they do. Skills and motivations of shared
intentionality fostered during infancy give individuals an adaptive advantage in these
interactions, and once that advantage is established, a top-down process ensues in
which the ontogeny of infants’skills can also have deferred adaptive benefits at the later
stage of childhood.
Adolescence/Adulthood (Sexual Maturity; 13+ Years)
During adolescence, things begin to get real. Whereas many of the cooperative
interactions of childhood take place in playful contexts, during adolescence and
adulthood one must collaborate with one’s peers for basic subsistence (and, again, with
ramifications for one’s attractiveness as a sexual partner).
In the scenario for early humans that we are envisioning here, there would
have been an initial period in which they were mostly individual foragers, like
all apes, but with a few pockets of collaboration. Like chimpanzees and
bonobos, perhaps, they would have hunted in small groups for monkeys and
other small mammals. If there were now selective pressures for collaborative
foraging—Tomase llo et al. (2012) point out a period during the early Pleisto-
cene in which there was a rapid radiation of terrestrial monkeys, who might
have outcompeted early humans for their preferred fruits—then those individ-
uals who were best able to collaborate with their peers would have had an
adaptive advantage. It is in this context that we may speculate that those
individuals who had already developed especially powerful skills and motiva-
tions of shared intentionality, beginning in infancy and continuing throughout
childhood, would already have a special stock of skills needed for new forms
of collaborative foraging. The outcome is an ontogenetic preadaptation: an
ontogenetic adaptation selected for at an early developmental period that turns
out to be useful for a later development period, including especially adulthood
during which individuals actually pass on their genes.
We may thus picture a kind of pincer movement of bottom-up and top-down
selective pressures. There are pressures for infants’ontogenetic adaptations for
joint attention, cooperative communication, and helping, to “migrate up”be-
cause they are useful to children and adults in the context of ecological
pressures for collaboration and collaborative foraging. And these ecological
pressures for collaborative adults could easily begin to “migrate down,”at least
into early and middle childhood when children are learning to collaborate with
peers in various simple, sometimes playful contexts, which prepares them for
adult collaboration in serious contexts. We may thus imagine early humans
gradually evolving a more cooperative lifestyle in general based mainly on
cooperative breeding and cooperative foraging, which fit together like hand in
glove. Each of these new and unique ways of surviving made for an especially
cooperative ape, each with its primary focus at a different ontogenetic period
but with possibilities for “migration”either up or down, initiating all kinds of
synergistic effects.
284 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Some Notes about Modern Humans and Culture
As just a brief note: with the emergence of modern humans and culture, some new
forces come into play. These are not our focus here because they come rather late in the
process. But we may at least note two extremely important new developments in the
current context: (1) active adult instruction of children in the ways of the culture, often
embodied in explicit cultural norms, and (2) child conformity to instruction and norms
based not just on prudence but on a kind of group-mindedness in which the good of the
group is a basic concern alongside other basic concerns. Indeed, we think that the
increase in behavioral and cultural complexity from anatomically modern humans to
behaviorally and culturally modern humans several tens of thousands of years later is
explained by the emergence of human group-mindedness as a new layer of “top-down”
influences on human ontogeny.
Complex social groups rely on economic specialization, division of labor, and social
norms and conventions. Norms and conventions require not only increased common
cultural ground but also extending trust to all in the group. As economic and demographic
complexity increases, cooperation gets more challenging and reliant on delayed returns in
a different currency, often through a third party (Sterelny 2012). As a result, in large and
culturally complex societies, successful cooperation and coordination rely heavily upon
trusting strangers (Seabright 2004), based not just on individual experience but also on
cultural norms and values, especially those that signal group identity. The key point is that
modern human adults began to construct a wide variety of cultural conventions, norms,
and institutions to solve adult problems of cooperation and coordination, which were
transmitted to young children as injunctions to conform. These may just be seen as a new
layer of “top-down”influences on human ontogeny, in the sense that these cultural
creations are adapted to adult concerns, and they trickle down to children as they prepare
to become adults (i.e., following these norms is adaptive not only during childhood, but
also as preparation for adulthood). This new group-mindedness also manifests in a new
concern with distinguishing in-group members from out-group members in the context of
group competition and cultural group selection (Henrich 2015).
By the time of modern humans, then, we have a hyper-cooperative lifestyle based on
cooperative breeding, cooperative foraging, and cooperative sharing of cultural infor-
mation (Sterelny 2012), with ontogenetic adaptations migrating both up and down. In
modern humans, there were additional and special “top-down”selective pressures in
which adults expected children to conform the culture’s way of doing things in order to
further the interests of the group.
Conclusion
The study of human life history has focused almost exclusively on such things as
weaning age, reproductive age, longevity, and other basic processes of survival and
reproduction. The study of human psychological development, in contrast, has focused
very little on the evolutionary bases of different periods of ontogeny. A full under-
standing of how human beings have come to be as they are requires an understanding
of both human evolution and human ontogeny with regard to a variety of life history
variables and psychological competencies as well.
Hum Nat (2017) 28:274–288 285
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Our specific conclusion here is that to explain the many and various unique forms of
human cooperation requires both the cooperative breeding hypothesis, positing a unique
selective environment for fostering the most basic skills and motivations of shared
intentionality during infancy, and the interdependence hypothesis, positing a critical role
for the obligate collaborative foraging of adults as a selective environment favoring
individuals who could engage in various forms of complex social coordination and
communication. The cooperative breeding hypothesis by itself cannot account for the
many complex cognitive developments associated with human cooperation, but the
interdependence hypothesis by itself cannot account for the early emergence of skills
and motivations for shared intentionality during human infancy. A composite account is
needed, and our attempt here has been to provide the beginnings of such an account.
Empirical support for our composite account is of course not straightforward. But we have
provided at least some evidence here—and would hope to be able to provide more in the
future—that (i) human infants’initial skills of shared intentionality are mostly adapted for
interaction not with peers but with adults; (ii)infants’engaging with adults in acts of
shared intentionality is inherently pleasurable for both parties and so, presumably, serves
to enhance their relationship; and (iii) older children begin to develop further skills and
motivations for engaging in acts of shared intentionality with peers.
Although in some sense implicit in evo-devo accounts, our analysis here has also
highlighted in a new way the process by which ontogenetic adaptations geared toward a
particular developmental period may be extended either up or down in age as a natural
consequence of random variation in age of onset and selective pressures present during
adjacent developmental periods. Cooperative breeding thus generates during infancy
ontogenetic preadaptations for cooperation that later prove useful for older children and
adults, and interdependent collaboration during adulthood creates pressure for ever-
younger children to begin acquiring and practicing their collaborative skills. For the full
story we need both phylogeny and ontogeny and how they relate.
Acknowledgments Open access funding provided by Max Planck Society.
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International
License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and repro-
duction in any medium, provided you give appropriate credit to the original author(s) andthe source, provide a
link to the Creative Commons license, and indicate if changes were made.
References
Bakeman, R., & Adamson, L. (1984). Coordinating attention to people and objects in mother-infant and peer-
infant interactions. Child Development, 55,1278–1289.
Bard, K. A. (2012). Emotional engagement: How chimpanzee minds develop. In F. De Waal & P. Ferrari (Eds.),
The primate mind: Built to engage with other minds (pp. 224–245). Cambridge: Harvard University Press.
Bowlby, J. (1969). Attachment and loss.NewYork:BasicBooks.
Bruner, J. (1983). Child’s talk.NewYork:Norton.
Bullinger, A., Melis, A., & Tomasello, M. (2014). Chimpanzees instrumentally help but do not communicate
in a mutualistic cooperative task. Journal of Comparative Psychology, 128,251–260.
Burkart, J. M., & van Schaik, C. P. (2010). Cognitive consequences of cooperative breeding in primates?
Animal Cognition, 13(1), 1–19.
Callaghan, T., Moll, H., Rakoczy, H., Warneken, F., Liszkowski, U., Behne, T., & Tomasello, M. (2011). Early
social cognition in three cultural contexts. Monographs of the Society for Research in Child Development,
76(2), 1–142.
286 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Chapais, B. (2008). Primeval kinship: How pair-bonding gave birth to human society. Cambridge: Harvard
University Press.
Clutton-Brock, T. H. (2006). Cooperative breeding in mammals. In P. M. Kappeler & C. P. van Schaik (Eds.),
Cooperation in primates and humans: Mechanisms and evolution (pp. 172–190). Berlin/New York:
Springer.
Engelmann, J. M., Herrmann, E., & Tomasello, M. (2012). Five-year olds, but not chimpanzees, attempt to
manage their reputations. PloS One, 7(10), e48433.
Fletcher, G., Warneken, F., & Tomasello, M. (2012). Differences in cognitive processes underlying the
collaborative activities of children and chimpanzees. Cognitive Development, 27, 136–153.
Gräfenhain, M., Behne, T., Carpenter, M., & Tomasello, M. (2009). Young children’s understanding of joint
commitments. Developmental Psychology, 45,1430–1443.
Hamann, K., Warneken, F., Greenberg, J., & Tomasello, M. (2011). Collaboration encourages equal sharing in
children but not chimpanzees. Nature, 476, 328–331.
Hamann, K., Warneken, F., & Tomasello, M. (2012). Children’s developing commitments to joint goals. Child
Development, 83,137–145.
Hart,D.,&Sussman,R.W.(2005).Man the hunted: Primates, predators, and human evolution. New York:
Westview Press.
Hawkes K. (2012). Stag hunts or rearing environments? Comment on M Tomasello et al., “Two key steps in the
evolution of human cooperation: The interdependence hypothesis.”Current Anthropology 53(6), 687–88.
Hawkes, K. (2014). Primate sociality to human cooperation: Why us and not them? Human Nature, 25(1), 28–48.
Henrich, J. (2015). The secret of our success. Princeton: Princeton University Press.
Hepach, R., Vaish, A., Grossmann, T., & Tomasello, M. (2016). Young children want to see others get the help
they need. Child Development, 87,1703–1714.
Hrdy, S. (1999). Mother Nature: A history of mothers, infants and natural selection. New York: Pantheon Press.
Hrdy, S. (2005). Evolutionary context of human development: The cooperative breeding model. In C. S.
Carter & L. Ahnert (Eds.), Attachment and bonding: A new synthesis (pp. 9–32). Dahlem Workshop No.
92. Cambridge: MIT Press.
Hrdy, S. (2009). Mothers and others: The evolutionary origins of mutual understanding. Cambridge: Harvard
University Press.
Hrdy, S. (2016). Development plus social selection in the emergence of “emotionally modern humans.”In L.
Meehan & A. Crittenden (Eds.), Childhood: Origins, evolution, and implications. Albuquerque:
University of New Mexico Press and School for Advanced Research Press.
Isler, K., & van Schaik, C. P. (2012). How our ancestors broke through the gray ceiling: Comparative evidence
for cooperative breeding in early Homo.Current Anthropology, 53,S453–S465.
Köymen, B., Schmerse, D., Lieven, E., & Tomasello, M. (2014). Young children create partner-specific
referential pacts with peers. Developmental Psychology, 50(10), 2334–2342.
Kramer, K. (2005). Children’s help and the pace of reproduction: Cooperative breeding in humans.
Evolutionary Anthropology, 14(6), 224–237.
Leavens, D. A., & Hopkins, W. D. (1998). Intentional communication by chimpanzees: A cross-sectional
study of the use of referential gestures. Developmental Psychology, 34,813–822.
Lee-Thorp, J. A., Sponheimer, M., & Luyt, J. (2007). Tracking changing environments using stable carbon
isotopes in fossil tooth enamel: An example from the South African hominin sites. Journal of Human
Evolution, 53(5), 595–601.
Liebal, K., Vaish, A., Haun, D., & Tomasello, M. (2014). Does sympathy motivate prosocial behavior in great
apes? PloS One, 9(1), e84299.
Liszkowski, U., Carpenter, M., Striano, T., & Tomasello, M. (2006). 12- and 18-month-olds point to provide
information for others. Journal of Cognition and Development, 7,173–187.
Liszkowski, U., Carpenter, M., & Tomasello, M. (2008). Twelve-month-olds communicate helpfully and
appropriately for knowledgeable and ignorant partners. Cognition, 108,732–739.
Matthews, D., Behne, T., Lieven, E., & Tomasello, M. (2012). Origins of the human pointing gesture: A
training study. Developmental Science, 15,817–829.
Melis, A. P., Warneken, F., Jensen, K., Schneider, A.-C., Call, J., & Tomasello, M. (2011). Chimpanzees help
conspecifics to obtain food and non-food items. Proceedings of the Royal Society of London, B,
278(1710), 1405–1413.
Ninio, A. (2016). Bids for joint attention by parent-child dyads and by dyads of young peers in interaction.
Journal of Child Language, 43(1), 135–156.
Piaget, J. (1932/1997). The moral judgment of the child. New York: The Free Press.
Potts, R. (1998). Variability selection in hominid evolution. Evolutionary Anthropology, 7(3), 81–96.
Reddy, V. (2015). Joint intentions in infancy. Journal of Consciousness Studies, 22,24–44.
Hum Nat (2017) 28:274–288 287
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Roberts, G. (2005). Cooperation through interdependence. Animal Behaviour, 70(4), 901–908.
Rochat, P. (2009). Others in mind: Social origins of self-consciousness. New York Cambridge University
Press.
Salomo, D., & Liszkowski, U. (2013). Sociocultural settings influence the emergence of prelinguistic deictic
gestures. Child Development, 84(4), 1296–1307.
Seabright, P. (2004). The company of strangers: A natural history of economic life. Princeton, NJ: Princeton
University Press.
Sterelny, K. (2012). The evolved apprentice.Cambridge:MITPress.
Stiner, M. (2013). An unshakable middle Paleolithic? Trends versus conservatism in the predatory niche and
their social ramifications. Current Anthropology, 54(S8), 288–304.
Stoeber, G., Moore, R., & Tomasello, M. (2017). Differences in the way infants communicate with adults and
other infants. Ms. in preparation.
Sulloway, F. (1996). Born to rebel: Birth order, family dynamics, and creative lives. New York: Pantheon
Books.
Tomasello, M. (1995). Joint attention as social cognition. In C. Moore & P. J. Dunham (Eds.), Joint attention:
Its origin and role in development (pp. 103–130). Hillsdale: Lawrence Erlbaum.
Tomasello, M. (2008). Origins of human communication. Cambridge: MIT Press.
Tomasello, M. (2014). A natural history of human thinking. Cambridge: Harvard University Press.
Tomasello, M. (2016). A natural history of human morality. Cambridge: Harvard University Press.
Tomasello, M., & Carpenter, M. (2005). The emergence of social cognition in three young chimpanzees.
Monographs of the Society for Research in Child Development, 70(279).
Tomasello, M., Hare, B., & Fogleman, T. (2001). The ontogeny of gaze following in chimpanzees (Pan
troglodytes) and rhesus macaques (Macaca mulatta). Animal Behaviour, 61, 335–343.
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, 675–735.
Tomasello, M., Hare, B.,Lehmann, H., & Call, J. (2007). Reliance on head versus eyes in the gaze following of great
apes and human infants: The cooperative eye hypothesis. Journal of Human Evolution, 52,314–320.
Tomasello, M., Melis, A. P., Tennie, C., Wyman, E., & Herrmann, E. (2012). Two key steps in the evolution of
cooperation: The interdependence hypothesis. Current Anthropology, 53(6), 673–692.
Tomonaga, M., Tanaka, M., Matsuzawa, T., Myowa-Yamakoshi, M., Kosugi, D., Mizuno, Y., Okamoto, S.,
Yamaguchi, M. K., & Bard, K. A. (2004). Development of social cognition in infant chimpanzees (Pan
troglodytes): Face recognition, smiling, gaze, and the lack of triadic interactions. Japanese Psychological
Research, 46(3), 227–235.
Trevarthen, C. (1979). Instincts for human understanding and for cultural cooperation: Their development in
infancy. In M. von Cranach, K. Foppa, W. Lepenies, & D. Ploog (Eds.), Human ethology: Claims and
limits of a new discipline (pp. 530–571). Cambridge: Cambridge University Press.
Vaish, A., Carpenter, M., & Tomasello, M. (2009). Sympathy through affective perspective-taking and its
relation to prosocial behavior in toddlers. Developmental Psychology, 45(2), 534–543.
Warneken, F., & Tomasello, M. (2006). Altruistic helping in human infants and young chimpanzees. Science,
31, 1301–1303.
Warneken, F., Hare, B., Melis, A., Hanus, D., & Tomasello, M. (2007). Spontaneous altruism by chimpanzees
and young children. PLoS Biology, 5(7), e184.
West-Eberhard, M. J. (1979). Sexualselection, social competition, andevolution. Proceedings of the American
Philosophical Society, 51(4), 222–234.
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.
Wobber, V., Herrmann, E., Hare, B., Wrangham, R., & Tomasello, M. (2013). Differences in the early
cognitive development of children and great apes. Developmental Psychobiology, 56(3), 547–573.
Wolf, W., Launey, J., & Dunbar, R. (2015). Joint attention, shared goals, and social bonding. British Journal of
Psychology, 107(2), 322–337.
Michael Tomasello is co-director of the Max Planck Institute for Evolutionary Anthropology, Leipzig,
Germany, and professor of psychology and neuroscience at Duke University, Durham, North Carolina.
Ivan Dario Gonzalez-Cabrera is a PhD student in the School of Philosophy at the Australian National
University and a visiting fellow at the Department of Comparative and Developmental Psychology at the Max
Planck Institute for Evolutionary Anthropology in Leipzig. He currently has a fellowship at the Konrad Lorenz
Institute in Vienna.
288 Hum Nat (2017) 28:274–288
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center
GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers
and authorised users (“Users”), for small-scale personal, non-commercial use provided that all
copyright, trade and service marks and other proprietary notices are maintained. By accessing,
sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of
use (“Terms”). For these purposes, Springer Nature considers academic use (by researchers and
students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and
conditions, a relevant site licence or a personal subscription. These Terms will prevail over any
conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription (to
the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of
the Creative Commons license used will apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may
also use these personal data internally within ResearchGate and Springer Nature and as agreed share
it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not otherwise
disclose your personal data outside the ResearchGate or the Springer Nature group of companies
unless we have your permission as detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial
use, it is important to note that Users may not:
use such content for the purpose of providing other users with access on a regular or large scale
basis or as a means to circumvent access control;
use such content where to do so would be considered a criminal or statutory offence in any
jurisdiction, or gives rise to civil liability, or is otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association
unless explicitly agreed to by Springer Nature in writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a
systematic database of Springer Nature journal content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a
product or service that creates revenue, royalties, rent or income from our content or its inclusion as
part of a paid for service or for other commercial gain. Springer Nature journal content cannot be
used for inter-library loans and librarians may not upload Springer Nature journal content on a large
scale into their, or any other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not
obligated to publish any information or content on this website and may remove it or features or
functionality at our sole discretion, at any time with or without notice. Springer Nature may revoke
this licence to you at any time and remove access to any copies of the Springer Nature journal content
which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or
guarantees to Users, either express or implied with respect to the Springer nature journal content and
all parties disclaim and waive any implied warranties or warranties imposed by law, including
merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published
by Springer Nature that may be licensed from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a
regular basis or in any other manner not expressly permitted by these Terms, please contact Springer
Nature at
onlineservice@springernature.com