Emerging Trends in The Social and Behavioral Sciences

Behavioral Heterochrony

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Behavioral Heterochrony

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Behavioral Heterochrony
VICTORIA WOBBER and BRIAN HARE

Abstract
Behavioral heterochrony is the study of the timing and speed of development
of behavior from an evolutionary perspective. Key to studies of behavioral heterochrony is the comparison of development across different species. Such studies
can illuminate whether a trait thought to be unique to a given species might in
fact have its precursors in the early development of a closely related species. They
can inform our understanding of how behavioral development is constrained by
elements of somatic or reproductive maturation. Studies of behavioral heterochrony
can also elucidate mechanisms by which behavior evolves, by targeting evolutionary
shifts in developmental pathways. Finally, such studies can enrich our knowledge
of human evolution, in contextualizing the vast shifts in human life history patterns
relative to other primates in terms of corresponding changes in behavioral and
cognitive development. On the whole then, research in behavioral heterochrony
can advance our understanding of behavior through forging interdisciplinary links
between anthropology, biology, and psychology.

INTRODUCTION
Social and life scientists have used a variety of methodologies to understand
behavioral traits—whether investigating a behavior’s ontogenetic origins, its
proximate determinants, its phylogenetic distribution, or its potential adaptive value. The majority of these studies have focused on quantifying either a
behavior’s proximate determinants (how that behavior arises in the moment
or across development), or the behavior’s ultimate functions (why that behavior arises in certain species, and how it might function adaptively)—in line
with the framework outlined by Niko Tinbergen nearly 50 years ago (Tinbergen, 1963). However, the adherence to this framework may have led studies
of behavior to fall behind other areas of biology—where in fact, studies integrating both proximate and ultimate perspectives to investigate the evolution
of development can provide the strongest means by which to understand a
given trait. Here, therefore, we argue that studies of behavior should build
on the insights gained from evolutionary developmental biology to investigate the evolution of behavioral development, or behavioral heterochrony.
Emerging Trends in the Social and Behavioral Sciences. Edited by Robert Scott and Stephen Kosslyn.
© 2015 John Wiley & Sons, Inc. ISBN 978-1-118-90077-2.

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In essence, understanding changes in behavioral development across species
may, in fact, facilitate conclusions that would be lost by comparing adults
alone.
Studies of behavioral heterochrony are particularly relevant given the
increasing evidence from the field of evolutionary developmental biology
that evolutionary change frequently occurs via shifts in developmental
trajectories. We argue, therefore, that studies of comparative behavioral and
cognitive development can improve our understanding of how behavior
and cognition evolve. Such studies can illuminate how aspects of behavioral
development scale with (or shift independently of) somatic and reproductive maturation. These studies may also reveal that behaviors previously
assumed to be novel in a given species or population, in fact, have roots
in the early development of a closely related group. Finally, in the case of
human origins, studies of comparative behavioral development will clarify
the links between the well-known changes in human life history patterns
and changes in our behavioral development.
We provide support for this argument by first discussing foundational
research on the evolution of development. We then review recent studies in
the area of behavioral heterochrony. We conclude by outlining key questions
and debates that can be addressed by studies of behavioral heterochrony.
FOUNDATIONAL RESEARCH—SKELETAL HETEROCHRONY
The concept of heterochrony, or the evolution of development, has a long
history in the study of skeletal morphology. Charles Darwin noted the importance of studying developmental pathways in The Descent of Man (Darwin,
1871), while Ernst Haeckel went so far as to assert that “ontogeny recapitulates phylogeny” in his study of embryology (Haeckel, 1866; ontongeny
being the study of development). While Haeckel’s argument may have been
too simplistic, studies of biology and human evolution have continued to
underscore the central role of development in generating variation between
individuals and species (Carroll, 2003; Gould, 1977).
In the case of human evolution, in particular, studies of heterochrony
have advanced our understanding of the changes occurring in the human
skeleton throughout our recent evolutionary past. Comparisons of development between humans and other apes have revealed that humans are
born with underdeveloped crania, yet develop more rapidly during infancy
and juvenility to eventually exceed other apes in cranial capacity (Robson
& Wood, 2008). Compounded with the evidence that humans also show a
prolonged juvenile period relative to other primates, these findings suggest
striking alterations in developmental trajectories in hominoid evolution

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(Charnov & Berrigan, 1993). But how could such broad-scale changes in
development have occurred?
Recent studies have identified a critical role of gene expression in mediating
sweeping developmental change between individuals and species (Albert
et al., 2012; Atchley, 1987; King & Wilson, 1975). These studies have revealed
that in addition to changes in genomic sequence, which can alter the specific
proteins coded for by a given gene, changes in gene expression can influence
the degree and timing of protein production, with significant effects on phenotype (Carroll, 2003). The field of evolutionary developmental biology has
now extensively documented the ways in which developmental variation in
gene expression can underlie evolutionary change in species ranging from
plants to humans.
Findings from the field of “evo-devo” therefore suggest that minor alterations in development can lead to major differences in adult phenotype. We
propose that, similarly, minor alterations in behavioral development can lead
to significant differences in adult behavior, whether between individuals or
species. Although this assertion is intuitive, that development should influence an adult state, the role of development in behavioral evolution is vastly
understudied.
One example that illustrates this point comes from the study of helping
behavior in communally breeding birds. In these communally breeding
species, where juvenile individuals help to feed nestlings, it had been argued
that this helping behavior arose de novo as an adaptive correlate of a species
adapting a communal breeding strategy (Emlen, 1982). However, an alternative hypothesis proposes that this helping behavior arose as an unselected
by-product of a shift in life history strategy. Specifically, with changes in
ecology that made breeding dispersal less effective and heightened the
tolerance of juvenile individuals by a breeding pair, juveniles were provided
with an opportunity to exhibit helping behaviors that previously would
only have been displayed in adulthood. Therefore, a shift in life history
could have led to heightened helping by juveniles via “predisplacement”
of helping behavior. Importantly then, a behavior argued to have evolved
for its function in juveniles may instead have arisen as an unexpected
by-product of larger selection pressures acting via shifts in life history
(Hatchwell, 2009; Jamieson, 1989) This critical alternative could not have
been revealed without the study of comparative development.
This example also illustrates one potential difficulty in studying behavioral
heterochrony, in that developmental trajectories of behavior are not as
predictable as those of morphological traits. Extensive work in the skeletal
heterochrony literature has quantified the precise relationships in changes
of the size and shape of a trait over time during growth, specifying precise
terms for the varying combinations of shifts in these parameters (Gould,

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1977; McKinney & McNamara, 1991). Skeletal traits typically begin at a
smaller size, with an underdeveloped form, and eventually grow to reach
the adult state, which is then fixed. For behavioral traits, however, development does not always happen steadily, nor is the adult state always fixed.
In addition, there may be cases where a behavior is absent in adults, rather
than fully grown—for example, in the case of play behaviors, which are
typically prevalent among juveniles but minimal in adulthood. This means
that studies of behavioral heterochrony may not fit the precise definitions
set forth by studies of skeletal heterochrony, and that instead we must
term such studies “comparative ontogenetic allometry” (Lieberman, 2012).
Nonetheless, the critical advances that have been made in morphology
and genetics by incorporating the study of development, particularly
comparative development, are too notable for behavioral scientists to pass
by. In the next section, we review some of the insights that have been gained
from existing studies of behavioral heterochrony, before moving onto the
key directions for future research.
CUTTING-EDGE RESEARCH—BEHAVIORAL HETEROCHRONY
There are a number of fields in which studies of behavioral heterochrony
have enriched our understanding of behavioral traits. Here we discuss four
main areas where behavioral heterochrony studies have made a significant
contribution, reviewing studies that examine: (i) the genetic basis for changes
in behavioral development; (ii) the correlation between behavioral development and the developmental trajectories of nonbehavioral traits; (iii) the
effects of selection on developmental trajectories; and (iv) behavioral heterochrony during hominoid evolution.
GENETIC UNDERPINNINGS OF CHANGES IN BEHAVIORAL DEVELOPMENT
As mentioned, methodological advances allowing the study of gene expression have greatly expanded our understanding of how genetic changes can
be expressed as changes in phenotypic development. For behavioral traits,
connecting genotype to phenotype can often be extremely complex given
that typically behavioral traits are polygenic and genetic changes are relayed
through the brain in affecting behavioral outcomes. Nonetheless, studies of
the mechanisms underlying behavioral development in model organisms
have made significant gains in recent years.
One line of research where mechanisms have been particularly well elucidated comes from studies of social insects. Recent research has identified specific genes that can readily lead to the spread of ultra-sociality, also known as

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eusociality, through shifts in development (Linksvayer & Wade, 2005). Specifically, shifts in genes that regulate the expression of maternal care behaviors
allowing them to be expressed earlier on in development would facilitate
“maternal-care”-type behaviors between siblings, rather than only between
mother and offspring (Toth et al., 2007). These findings provide a mechanism
by which alterations in behavioral development, through changes in gene
expression, might underlie the evolution of eusociality in promoting greater
social behaviors throughout life (Linksvayer & Wade, 2005; Toth et al., 2007).
These findings underscore the point that developmental changes can serve as
a mechanism by which to produce species differences, with studies of model
organisms allowing us to identify the specific genetic changes that accompany changes in phenotype.
These findings also align with a large body of literature in rodents cataloguing mechanisms by which early development can shape ultimate behavioral
outcomes. This work has shown that early exposure to stress (particularly
low levels of care by one’s mother) can alter gene expression and ultimately
constrain patterns of stress reactivity. In turn, these patterns of stress reactivity can constrain an individual’s expression of appropriate maternal behaviors as an adult (Meaney, 2001). On the whole then, these studies highlight
the importance of studying development to contextualize adult phenotypes,
including a better understanding of the mechanisms that influence behavior
and how they vary across individuals and species.
CORRELATIONS BETWEEN BEHAVIORAL DEVELOPMENT AND OTHER ASPECTS OF MATURATION
A second area in which studies of behavioral heterochrony have contributed
valuable insight is in linking behavioral development with its broader
maturational context. This perspective is increasingly important in our
understanding of human health, given the recent argument that human
developmental disorders can arise via a “mismatch” of psychological and
physiological developmental trajectories (e.g., in the case of early sexual
maturity precipitating precocious sexual behavior and greater risk-taking
(Forbes & Dahl, 2010)).
Studies showing a strong correlation between behavioral development and
somatic maturation have come from investigations of locomotor behavior,
for example the ontogeny of flight behavior in birds. Researchers in this area
have shown how changes in the ontogeny of feather microstructure directly
influence birds’ capacities to generate aerodynamic force during flight (Dial,
Heers, & Tobalske, 2012). Moreover, the developmental trajectories of flight
behavior have been found to differ between species in line with the varying uses of flight behavior among adults. In species where flight is used for

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predation avoidance and flight development is correspondingly fast or “precocial,” individuals become competent in flight behavior early on in development but improve gradually toward adult levels of aerodynamic proficiency. In contrast, among species where flight is used for migration and its
development is slow or “altricial,” individuals only develop flight capacities upon reaching adult mass (Dial et al., 2012; Jackson, Segre, & Dial, 2009).
Future studies in this area can reveal the degree to which developmental
trajectories of flight behavior shift in line with ecological pressures impacting the function of flight behavior among adults (even across populations
within-species), providing new insight into the relationship between morphology and behavior through the study of their correlated development.
Morphological and behavioral traits are not always this tightly coupled,
however. For example, certain species ranging from newts to orangutans
show “facultative paedomorphosis,” where individuals can “choose” to
retain juvenile morphological characteristics into adulthood rather than fully
develop into the adult form. Intriguingly, these subadult morphs have been
shown to possess full reproductive capacity despite their skeletal juvenility
(Denoel, 2002; Maggioncalda, Sapolsky, & Czekala, 1999). These results
therefore indicate that there may be certain correlations in developmental
trajectories across traits, for example, in the area of locomotor behavior,
where the behavior itself is strongly constrained by morphology. However,
in other areas, even those where physiological maturation plays a significant
role, such as in reproductive behavior, these findings imply that we cannot
assume that behavioral ontogeny will scale precisely with the concurrent
maturational processes.
EFFECTS OF SELECTION ON DEVELOPMENTAL TRAJECTORIES
Recent studies using experimental selection in model organisms reveal that
developmental shifts play a critical role in generating differences in phenotype between individuals and species. Some of the most notable research
examining the effects of artificial selection on behavioral development comes
from populations of mice selected differentially for their rates of aggression
as adults. In two series of experiments (Cairns, MacComble, & Hood, 1983;
Gariepy, Bauer, & Cairns, 2001), researchers found that in selecting for
adult differences in aggressive behavior, the mechanism underlying these
differences was a shift in behavioral development. While the unselected
or high-aggression lines developed aggressive behaviors as they aged, the
low-aggression line did not increase in aggressive behavior at maturity
(Cairns et al., 1983). Gariepy et al. (2001) illustrated this phenomenon particularly precisely by documenting the ontogenetic patterns of aggressive
behavior across selected and unselected lines. This study revealed that while

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all of the mouse lines showed some increase in aggression from infancy to
adulthood, the magnitude of increase at all ages was much less in the line
selected for low aggression relative to either the control or high-aggression
lines. Moreover, these differences in developmental trajectories became
more extreme with more generations selected. These findings provide direct
evidence that selective pressures can influence shifts in development, even
in the case of a behavioral trait.
The findings from these mouse studies conform to other studies looking
at the effects of selection against aggression, both within experimental populations (Belayev’s foxes (Belyaev, 1979; Trut, 1999)) and studies comparing naturally domesticated species to their wild forebears (particularly work
on guinea pigs, (Kunzl, Kaiser, Meier, & Sachser, 2003)). Across numerous
taxa, selection against aggression has been found to produce individuals that
retain juvenile characteristics into adulthood in features of their morphology, physiology, behavior, and cognition (Hare, Wobber, & Wrangham, 2012).
These findings suggest the compelling possibility that common underlying
mechanisms might govern the ontogeny of multiple traits, and that these
mechanisms in turn may have been impacted by selection for any one of
the traits—implying some genetic link, or pleiotropic effect, on the others.
Continued studies in this area can therefore test the effects of selection on
developmental trajectories, testing hypotheses about the origins of species
differences through comparative study of the proximate mechanisms that
facilitate these differences.
USING BEHAVIORAL HETEROCHRONY TO UNDERSTAND HUMAN EVOLUTION
A final area where studies of behavioral heterochrony have contributed
recent insight is in our understanding of human origins. For years researchers
have extensively documented the differences in human life history relative
to other primates—including our prolonged juvenile period, extended
overall lifespan, and heightened reproductive rate relative to other primates.
While patterns of somatic and reproductive maturation have been well
studied in humans and comparative models, studies of behavioral and
cognitive ontogeny in a comparative perspective have lagged behind in
comparison.
Our recent work has therefore focused on behavioral and cognitive development in chimpanzees and bonobos, in using studies of heterochrony to
understand the differences between these two apes but also to shed light on
evolutionary mechanisms that may have been at play in recent human evolution. We first examined a behavior that is well known to differ between
adult bonobos and chimpanzees—food sharing. Bonobos have been found
to share food more readily than chimpanzees both in the wild and in experimental contexts (de Waal, 1989; Fruth & Hohmann, 2002; Hare, Melis, Woods,

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Hastings, & Wrangham, 2007), and their greater tolerance in food sharing
allows them to cooperate in experimental situations where chimpanzee cooperation breaks down (Hare et al., 2007). We examined whether the difference
in sharing and tolerance between adults of the two species might be due to
shifts in the development of these traits. We found that while the two species
share food at similar, high rates as juveniles, chimpanzees develop intolerance in food sharing with age, while bonobos maintain these juvenile levels
of tolerance in sharing into adulthood (Wobber, Wrangham, & Hare, 2010b).
These results support the argument that shifts in behavioral development can
underlie species differences in adult behavior (Wobber, Wrangham, & Hare,
2010a).
In addition, taken together with findings that bonobos also maintain several
juvenile skeletal (Durrleman, Pennec, Trouve, Ayache, & Braga, 2012; Lieberman, Carlo, Ponce de Leon, & Zollikofer, 2007), endocrine (Wobber, Lipson,
Hare, Wrangham, & Ellison, 2013), and cognitive (Wobber et al., 2010a, 2010b)
characteristics into adulthood, these findings suggest potential broad-scale
shifts in development between bonobos and chimpanzees. In fact, these differences might be tied to selection against aggression in bonobos, given the
strong evidence that this type of selection facilitates retention of juvenile characteristics into adulthood among domesticated and experimentally selected
populations (Hare et al., 2012). With the evidence that, in fact, bonobos are
markedly less aggressive than chimpanzees (Kano, 1992; Muller, 2002), these
findings begin to make testable a prediction from the ecology of the two
species regarding their selection history and the mechanisms by which the
differences between the two species arose. Further work in this area is needed
to examine the degree to which patterns of human behavioral and cognitive
ontogeny can be characterized as shifts in development, potentially owing to
convergent selection pressures.
KEY ISSUES FOR FUTURE RESEARCH
Having reviewed recent findings in the area of behavioral heterochrony, we
now turn to areas that can be addressed by future research. Given the broad
spectrum of studies outlined, we believe that in fact there are a number of literatures and existing debates that can be enriched by greater study of behavioral heterochrony. We list just a few open questions, in the four areas that
we have discussed:
MECHANISMS OF DEVELOPMENT
To what degree are our adult behaviors shaped by early life or even prenatal
factors? How can mechanisms of gene expression account for differing adult
behavioral outcomes between individuals and species?

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Are there behaviors that appear to be similar across species and therefore
assumed to be shared via inheritance, but in fact develop via differing means,
instead suggesting that they are independently derived?
LINKS BETWEEN BEHAVIORAL DEVELOPMENT AND MATURATION
To what degree are aspects of behavioral development constrained or facilitated by aspects of somatic and reproductive maturation?
How can we recognize potential mismatches between developmental trajectories, including potentially treating these mismatches if they result in
pathologies?
EFFECTS OF SELECTION ON DEVELOPMENT
How do differences in ecology shape behavioral development in closely
related populations/species? Are there behaviors assumed to be novel
responses to environmental circumstances that in fact have their roots in the
early development of ancestral species?
If aspects of development across numerous traits (morphology, physiology,
behavior) are linked, how can selective pressures lead to pleiotropic effects on
multiple developmental trajectories with selection on only one target trait?
DEVELOPMENT AND HUMAN EVOLUTION
What selection pressures existed in human evolutionary history, and how
might these have altered our patterns of development and adult phenotypes?
Does the prolonged juvenile period in humans correlate with prolonged
behavioral and cognitive development, facilitating greater acquisition of
skills in the domains of foraging and social interaction?
On the whole, it is an exciting time for studies of behavioral heterochrony.
Novel methodologies, greater access to comparative models, and better
cross-talk across disciplines can generate scientific advances that were
unavailable to previous generations. Through studies of comparative behavioral development that target ontogenetic differences between individuals,
populations, and species, we can grasp heretofore underappreciated insights
into how behavior evolves and what it means to be human.
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FURTHER READING
Carroll, S. B. (2005). Endless forms most beautiful: The new science of evo devo. New York,
NY: W.W. Norton & Company.
Hare, B., Wobber, V., & Wrangham, R. (2012). The self-domestication hypothesis:
Bonobo psychology evolved due to selection against aggression. Animal Behaviour,
83(3), 573–585.
Mitteroecker, P., & Gunz, P. (2012). Human EvoDevo. Evolutionary Biology, 39(4),
443–446.
Toth, A., & Robinson, G. (2007). Evo-devo and the evolution of social behavior. Trends
in Genetics, 23(7), 334–341.
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D’Alessio, A. C., Sharma, S., Seckl,
J.R. … Meaney, M. J. (2004). Epigenetic programming by maternal behavior.
Nature Neuroscience, 7(8), 847–854.

Dr. VICTORIA WOBBER SHORT BIOGRAPHY
Dr. Victoria Wobber is a post-doctoral fellow in the Department of
Psychology at Harvard University and a member of the Laboratory for
Developmental Studies (https://software.rc.fas.harvard.edu/lds/). She
received her PhD in Human Evolutionary Biology from Harvard in 2012,
and her AB in Anthropology from Harvard in 2006. Her work focuses on
the evolutionary origins of human behavior, cognition, and endocrinology,
primarily through studies of humans’ closest living relatives, chimpanzees
and bonobos. More information about her research can be found on her
website (www.people.fas.harvard.edu/∼wobber).
Dr. BRIAN HARE SHORT BIOGRAPHY
Dr. Brian Hare is associate professor of evolutionary anthropology at
Duke University in North Carolina and a member of the Center for Cognitive Neuroscience, which is a division of the Duke Institute for Brain
Sciences (http://www.dibs.duke.edu/research/profiles/88-brian-hare). He

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received his PhD from Harvard University in 2004, founded the Hominoid
Psychology Research Group in 2004 while at the Max Planck Institute for
Evolutionary Anthropology in Leipzig, Germany, and subsequently founded
the Duke Canine Cognition Center when arriving at Duke University in 2007
(http://evolutionaryanthropology.duke.edu/research/dogs). He recently
published The New York Times Bestselling book The Genius of Dogs with his
wife Vanessa Woods. He is also the founder and Chief Scientific Officer of
the citizen science company Dognition.com (https://www.dognition.com).
RELATED ESSAYS
Telomeres (Psychology), Nancy Adler and Aoife O’Donovan
Learning Across the Life Course (Sociology), Jutta Allmendinger and Marcel
Helbig
Intersectionality and the Development of Self and Identity (Psychology),
Margarita Azmitia and Virginia Thomas
The impact of Bilingualism on Cognition (Psychology), Ellen Bialystok
Four Psychological Perspectives on Creativity (Psychology), Rodica Ioana
Damian and Dean Keith Simonton
Insight (Psychology), Brian Erickson and John Kounios
Patterns of Attachment across the Lifespan (Psychology), Robyn Fivush and
Theodore E. A. Waters
Gender and the Transition to Adulthood: A Diverse Pathways View (Sociology), Ingrid Schoon
Language and Thought (Psychology), Susan Goldin-Meadow
Family Relationships and Development (Psychology), Joan E. Grusec
An Evolutionary Perspective on Developmental Plasticity (Psychology),
Sarah Hartman and Jay Belsky
Grandmothers and the Evolution of Human Sociality (Anthropology), Kristen
Hawkes and James Coxworth
Biology and Culture (Psychology), Robert Peter Hobson
The Development of Social Trust (Psychology), Vikram K. Jaswal and Marissa
B. Drell
Social Change and Entry to Adulthood (Sociology), Jeylan T. Mortimer
Childhood (Anthropology), Karen L. Kramer
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Media and the development of Identity (Psychology), Adriana M. Manago
Evolutionary Perspectives on Animal and Human Personality (Anthropology), Joseph H. Manson and Lynn A. Fairbanks

14

EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES

A Bio-Social-Cultural Approach to Early Cognitive Development: Entering
the Community of Minds (Psychology), Katherine Nelson
Modeling Life Course Structure: The Triple Helix (Sociology), Tom Schuller
Becoming Adult: Meanings of Markers to Adulthood (Sociology), Richard A.
Settersten, Jr. et al.
Social Neuroendocrine Approaches to Relationships (Anthropology), Sari M.
van Anders and Peter B. Gray
The Intrinsic Dynamics of Development (Psychology), Paul van Geert and
Marijn van Dijk
Understanding Biological Motion (Psychology), Jeroen J. A. Van Boxtel and
Hongjing Lu
Theory of Mind (Psychology), Henry Wellman



Behavioral Heterochrony
VICTORIA WOBBER and BRIAN HARE

Abstract
Behavioral heterochrony is the study of the timing and speed of development
of behavior from an evolutionary perspective. Key to studies of behavioral heterochrony is the comparison of development across different species. Such studies
can illuminate whether a trait thought to be unique to a given species might in
fact have its precursors in the early development of a closely related species. They
can inform our understanding of how behavioral development is constrained by
elements of somatic or reproductive maturation. Studies of behavioral heterochrony
can also elucidate mechanisms by which behavior evolves, by targeting evolutionary
shifts in developmental pathways. Finally, such studies can enrich our knowledge
of human evolution, in contextualizing the vast shifts in human life history patterns
relative to other primates in terms of corresponding changes in behavioral and
cognitive development. On the whole then, research in behavioral heterochrony
can advance our understanding of behavior through forging interdisciplinary links
between anthropology, biology, and psychology.

INTRODUCTION
Social and life scientists have used a variety of methodologies to understand
behavioral traits—whether investigating a behavior’s ontogenetic origins, its
proximate determinants, its phylogenetic distribution, or its potential adaptive value. The majority of these studies have focused on quantifying either a
behavior’s proximate determinants (how that behavior arises in the moment
or across development), or the behavior’s ultimate functions (why that behavior arises in certain species, and how it might function adaptively)—in line
with the framework outlined by Niko Tinbergen nearly 50 years ago (Tinbergen, 1963). However, the adherence to this framework may have led studies
of behavior to fall behind other areas of biology—where in fact, studies integrating both proximate and ultimate perspectives to investigate the evolution
of development can provide the strongest means by which to understand a
given trait. Here, therefore, we argue that studies of behavior should build
on the insights gained from evolutionary developmental biology to investigate the evolution of behavioral development, or behavioral heterochrony.
Emerging Trends in the Social and Behavioral Sciences. Edited by Robert Scott and Stephen Kosslyn.
© 2015 John Wiley & Sons, Inc. ISBN 978-1-118-90077-2.

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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES

In essence, understanding changes in behavioral development across species
may, in fact, facilitate conclusions that would be lost by comparing adults
alone.
Studies of behavioral heterochrony are particularly relevant given the
increasing evidence from the field of evolutionary developmental biology
that evolutionary change frequently occurs via shifts in developmental
trajectories. We argue, therefore, that studies of comparative behavioral and
cognitive development can improve our understanding of how behavior
and cognition evolve. Such studies can illuminate how aspects of behavioral
development scale with (or shift independently of) somatic and reproductive maturation. These studies may also reveal that behaviors previously
assumed to be novel in a given species or population, in fact, have roots
in the early development of a closely related group. Finally, in the case of
human origins, studies of comparative behavioral development will clarify
the links between the well-known changes in human life history patterns
and changes in our behavioral development.
We provide support for this argument by first discussing foundational
research on the evolution of development. We then review recent studies in
the area of behavioral heterochrony. We conclude by outlining key questions
and debates that can be addressed by studies of behavioral heterochrony.
FOUNDATIONAL RESEARCH—SKELETAL HETEROCHRONY
The concept of heterochrony, or the evolution of development, has a long
history in the study of skeletal morphology. Charles Darwin noted the importance of studying developmental pathways in The Descent of Man (Darwin,
1871), while Ernst Haeckel went so far as to assert that “ontogeny recapitulates phylogeny” in his study of embryology (Haeckel, 1866; ontongeny
being the study of development). While Haeckel’s argument may have been
too simplistic, studies of biology and human evolution have continued to
underscore the central role of development in generating variation between
individuals and species (Carroll, 2003; Gould, 1977).
In the case of human evolution, in particular, studies of heterochrony
have advanced our understanding of the changes occurring in the human
skeleton throughout our recent evolutionary past. Comparisons of development between humans and other apes have revealed that humans are
born with underdeveloped crania, yet develop more rapidly during infancy
and juvenility to eventually exceed other apes in cranial capacity (Robson
& Wood, 2008). Compounded with the evidence that humans also show a
prolonged juvenile period relative to other primates, these findings suggest
striking alterations in developmental trajectories in hominoid evolution

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(Charnov & Berrigan, 1993). But how could such broad-scale changes in
development have occurred?
Recent studies have identified a critical role of gene expression in mediating
sweeping developmental change between individuals and species (Albert
et al., 2012; Atchley, 1987; King & Wilson, 1975). These studies have revealed
that in addition to changes in genomic sequence, which can alter the specific
proteins coded for by a given gene, changes in gene expression can influence
the degree and timing of protein production, with significant effects on phenotype (Carroll, 2003). The field of evolutionary developmental biology has
now extensively documented the ways in which developmental variation in
gene expression can underlie evolutionary change in species ranging from
plants to humans.
Findings from the field of “evo-devo” therefore suggest that minor alterations in development can lead to major differences in adult phenotype. We
propose that, similarly, minor alterations in behavioral development can lead
to significant differences in adult behavior, whether between individuals or
species. Although this assertion is intuitive, that development should influence an adult state, the role of development in behavioral evolution is vastly
understudied.
One example that illustrates this point comes from the study of helping
behavior in communally breeding birds. In these communally breeding
species, where juvenile individuals help to feed nestlings, it had been argued
that this helping behavior arose de novo as an adaptive correlate of a species
adapting a communal breeding strategy (Emlen, 1982). However, an alternative hypothesis proposes that this helping behavior arose as an unselected
by-product of a shift in life history strategy. Specifically, with changes in
ecology that made breeding dispersal less effective and heightened the
tolerance of juvenile individuals by a breeding pair, juveniles were provided
with an opportunity to exhibit helping behaviors that previously would
only have been displayed in adulthood. Therefore, a shift in life history
could have led to heightened helping by juveniles via “predisplacement”
of helping behavior. Importantly then, a behavior argued to have evolved
for its function in juveniles may instead have arisen as an unexpected
by-product of larger selection pressures acting via shifts in life history
(Hatchwell, 2009; Jamieson, 1989) This critical alternative could not have
been revealed without the study of comparative development.
This example also illustrates one potential difficulty in studying behavioral
heterochrony, in that developmental trajectories of behavior are not as
predictable as those of morphological traits. Extensive work in the skeletal
heterochrony literature has quantified the precise relationships in changes
of the size and shape of a trait over time during growth, specifying precise
terms for the varying combinations of shifts in these parameters (Gould,

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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES

1977; McKinney & McNamara, 1991). Skeletal traits typically begin at a
smaller size, with an underdeveloped form, and eventually grow to reach
the adult state, which is then fixed. For behavioral traits, however, development does not always happen steadily, nor is the adult state always fixed.
In addition, there may be cases where a behavior is absent in adults, rather
than fully grown—for example, in the case of play behaviors, which are
typically prevalent among juveniles but minimal in adulthood. This means
that studies of behavioral heterochrony may not fit the precise definitions
set forth by studies of skeletal heterochrony, and that instead we must
term such studies “comparative ontogenetic allometry” (Lieberman, 2012).
Nonetheless, the critical advances that have been made in morphology
and genetics by incorporating the study of development, particularly
comparative development, are too notable for behavioral scientists to pass
by. In the next section, we review some of the insights that have been gained
from existing studies of behavioral heterochrony, before moving onto the
key directions for future research.
CUTTING-EDGE RESEARCH—BEHAVIORAL HETEROCHRONY
There are a number of fields in which studies of behavioral heterochrony
have enriched our understanding of behavioral traits. Here we discuss four
main areas where behavioral heterochrony studies have made a significant
contribution, reviewing studies that examine: (i) the genetic basis for changes
in behavioral development; (ii) the correlation between behavioral development and the developmental trajectories of nonbehavioral traits; (iii) the
effects of selection on developmental trajectories; and (iv) behavioral heterochrony during hominoid evolution.
GENETIC UNDERPINNINGS OF CHANGES IN BEHAVIORAL DEVELOPMENT
As mentioned, methodological advances allowing the study of gene expression have greatly expanded our understanding of how genetic changes can
be expressed as changes in phenotypic development. For behavioral traits,
connecting genotype to phenotype can often be extremely complex given
that typically behavioral traits are polygenic and genetic changes are relayed
through the brain in affecting behavioral outcomes. Nonetheless, studies of
the mechanisms underlying behavioral development in model organisms
have made significant gains in recent years.
One line of research where mechanisms have been particularly well elucidated comes from studies of social insects. Recent research has identified specific genes that can readily lead to the spread of ultra-sociality, also known as

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eusociality, through shifts in development (Linksvayer & Wade, 2005). Specifically, shifts in genes that regulate the expression of maternal care behaviors
allowing them to be expressed earlier on in development would facilitate
“maternal-care”-type behaviors between siblings, rather than only between
mother and offspring (Toth et al., 2007). These findings provide a mechanism
by which alterations in behavioral development, through changes in gene
expression, might underlie the evolution of eusociality in promoting greater
social behaviors throughout life (Linksvayer & Wade, 2005; Toth et al., 2007).
These findings underscore the point that developmental changes can serve as
a mechanism by which to produce species differences, with studies of model
organisms allowing us to identify the specific genetic changes that accompany changes in phenotype.
These findings also align with a large body of literature in rodents cataloguing mechanisms by which early development can shape ultimate behavioral
outcomes. This work has shown that early exposure to stress (particularly
low levels of care by one’s mother) can alter gene expression and ultimately
constrain patterns of stress reactivity. In turn, these patterns of stress reactivity can constrain an individual’s expression of appropriate maternal behaviors as an adult (Meaney, 2001). On the whole then, these studies highlight
the importance of studying development to contextualize adult phenotypes,
including a better understanding of the mechanisms that influence behavior
and how they vary across individuals and species.
CORRELATIONS BETWEEN BEHAVIORAL DEVELOPMENT AND OTHER ASPECTS OF MATURATION
A second area in which studies of behavioral heterochrony have contributed
valuable insight is in linking behavioral development with its broader
maturational context. This perspective is increasingly important in our
understanding of human health, given the recent argument that human
developmental disorders can arise via a “mismatch” of psychological and
physiological developmental trajectories (e.g., in the case of early sexual
maturity precipitating precocious sexual behavior and greater risk-taking
(Forbes & Dahl, 2010)).
Studies showing a strong correlation between behavioral development and
somatic maturation have come from investigations of locomotor behavior,
for example the ontogeny of flight behavior in birds. Researchers in this area
have shown how changes in the ontogeny of feather microstructure directly
influence birds’ capacities to generate aerodynamic force during flight (Dial,
Heers, & Tobalske, 2012). Moreover, the developmental trajectories of flight
behavior have been found to differ between species in line with the varying uses of flight behavior among adults. In species where flight is used for

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predation avoidance and flight development is correspondingly fast or “precocial,” individuals become competent in flight behavior early on in development but improve gradually toward adult levels of aerodynamic proficiency. In contrast, among species where flight is used for migration and its
development is slow or “altricial,” individuals only develop flight capacities upon reaching adult mass (Dial et al., 2012; Jackson, Segre, & Dial, 2009).
Future studies in this area can reveal the degree to which developmental
trajectories of flight behavior shift in line with ecological pressures impacting the function of flight behavior among adults (even across populations
within-species), providing new insight into the relationship between morphology and behavior through the study of their correlated development.
Morphological and behavioral traits are not always this tightly coupled,
however. For example, certain species ranging from newts to orangutans
show “facultative paedomorphosis,” where individuals can “choose” to
retain juvenile morphological characteristics into adulthood rather than fully
develop into the adult form. Intriguingly, these subadult morphs have been
shown to possess full reproductive capacity despite their skeletal juvenility
(Denoel, 2002; Maggioncalda, Sapolsky, & Czekala, 1999). These results
therefore indicate that there may be certain correlations in developmental
trajectories across traits, for example, in the area of locomotor behavior,
where the behavior itself is strongly constrained by morphology. However,
in other areas, even those where physiological maturation plays a significant
role, such as in reproductive behavior, these findings imply that we cannot
assume that behavioral ontogeny will scale precisely with the concurrent
maturational processes.
EFFECTS OF SELECTION ON DEVELOPMENTAL TRAJECTORIES
Recent studies using experimental selection in model organisms reveal that
developmental shifts play a critical role in generating differences in phenotype between individuals and species. Some of the most notable research
examining the effects of artificial selection on behavioral development comes
from populations of mice selected differentially for their rates of aggression
as adults. In two series of experiments (Cairns, MacComble, & Hood, 1983;
Gariepy, Bauer, & Cairns, 2001), researchers found that in selecting for
adult differences in aggressive behavior, the mechanism underlying these
differences was a shift in behavioral development. While the unselected
or high-aggression lines developed aggressive behaviors as they aged, the
low-aggression line did not increase in aggressive behavior at maturity
(Cairns et al., 1983). Gariepy et al. (2001) illustrated this phenomenon particularly precisely by documenting the ontogenetic patterns of aggressive
behavior across selected and unselected lines. This study revealed that while

Behavioral Heterochrony

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all of the mouse lines showed some increase in aggression from infancy to
adulthood, the magnitude of increase at all ages was much less in the line
selected for low aggression relative to either the control or high-aggression
lines. Moreover, these differences in developmental trajectories became
more extreme with more generations selected. These findings provide direct
evidence that selective pressures can influence shifts in development, even
in the case of a behavioral trait.
The findings from these mouse studies conform to other studies looking
at the effects of selection against aggression, both within experimental populations (Belayev’s foxes (Belyaev, 1979; Trut, 1999)) and studies comparing naturally domesticated species to their wild forebears (particularly work
on guinea pigs, (Kunzl, Kaiser, Meier, & Sachser, 2003)). Across numerous
taxa, selection against aggression has been found to produce individuals that
retain juvenile characteristics into adulthood in features of their morphology, physiology, behavior, and cognition (Hare, Wobber, & Wrangham, 2012).
These findings suggest the compelling possibility that common underlying
mechanisms might govern the ontogeny of multiple traits, and that these
mechanisms in turn may have been impacted by selection for any one of
the traits—implying some genetic link, or pleiotropic effect, on the others.
Continued studies in this area can therefore test the effects of selection on
developmental trajectories, testing hypotheses about the origins of species
differences through comparative study of the proximate mechanisms that
facilitate these differences.
USING BEHAVIORAL HETEROCHRONY TO UNDERSTAND HUMAN EVOLUTION
A final area where studies of behavioral heterochrony have contributed
recent insight is in our understanding of human origins. For years researchers
have extensively documented the differences in human life history relative
to other primates—including our prolonged juvenile period, extended
overall lifespan, and heightened reproductive rate relative to other primates.
While patterns of somatic and reproductive maturation have been well
studied in humans and comparative models, studies of behavioral and
cognitive ontogeny in a comparative perspective have lagged behind in
comparison.
Our recent work has therefore focused on behavioral and cognitive development in chimpanzees and bonobos, in using studies of heterochrony to
understand the differences between these two apes but also to shed light on
evolutionary mechanisms that may have been at play in recent human evolution. We first examined a behavior that is well known to differ between
adult bonobos and chimpanzees—food sharing. Bonobos have been found
to share food more readily than chimpanzees both in the wild and in experimental contexts (de Waal, 1989; Fruth & Hohmann, 2002; Hare, Melis, Woods,

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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES

Hastings, & Wrangham, 2007), and their greater tolerance in food sharing
allows them to cooperate in experimental situations where chimpanzee cooperation breaks down (Hare et al., 2007). We examined whether the difference
in sharing and tolerance between adults of the two species might be due to
shifts in the development of these traits. We found that while the two species
share food at similar, high rates as juveniles, chimpanzees develop intolerance in food sharing with age, while bonobos maintain these juvenile levels
of tolerance in sharing into adulthood (Wobber, Wrangham, & Hare, 2010b).
These results support the argument that shifts in behavioral development can
underlie species differences in adult behavior (Wobber, Wrangham, & Hare,
2010a).
In addition, taken together with findings that bonobos also maintain several
juvenile skeletal (Durrleman, Pennec, Trouve, Ayache, & Braga, 2012; Lieberman, Carlo, Ponce de Leon, & Zollikofer, 2007), endocrine (Wobber, Lipson,
Hare, Wrangham, & Ellison, 2013), and cognitive (Wobber et al., 2010a, 2010b)
characteristics into adulthood, these findings suggest potential broad-scale
shifts in development between bonobos and chimpanzees. In fact, these differences might be tied to selection against aggression in bonobos, given the
strong evidence that this type of selection facilitates retention of juvenile characteristics into adulthood among domesticated and experimentally selected
populations (Hare et al., 2012). With the evidence that, in fact, bonobos are
markedly less aggressive than chimpanzees (Kano, 1992; Muller, 2002), these
findings begin to make testable a prediction from the ecology of the two
species regarding their selection history and the mechanisms by which the
differences between the two species arose. Further work in this area is needed
to examine the degree to which patterns of human behavioral and cognitive
ontogeny can be characterized as shifts in development, potentially owing to
convergent selection pressures.
KEY ISSUES FOR FUTURE RESEARCH
Having reviewed recent findings in the area of behavioral heterochrony, we
now turn to areas that can be addressed by future research. Given the broad
spectrum of studies outlined, we believe that in fact there are a number of literatures and existing debates that can be enriched by greater study of behavioral heterochrony. We list just a few open questions, in the four areas that
we have discussed:
MECHANISMS OF DEVELOPMENT
To what degree are our adult behaviors shaped by early life or even prenatal
factors? How can mechanisms of gene expression account for differing adult
behavioral outcomes between individuals and species?

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Are there behaviors that appear to be similar across species and therefore
assumed to be shared via inheritance, but in fact develop via differing means,
instead suggesting that they are independently derived?
LINKS BETWEEN BEHAVIORAL DEVELOPMENT AND MATURATION
To what degree are aspects of behavioral development constrained or facilitated by aspects of somatic and reproductive maturation?
How can we recognize potential mismatches between developmental trajectories, including potentially treating these mismatches if they result in
pathologies?
EFFECTS OF SELECTION ON DEVELOPMENT
How do differences in ecology shape behavioral development in closely
related populations/species? Are there behaviors assumed to be novel
responses to environmental circumstances that in fact have their roots in the
early development of ancestral species?
If aspects of development across numerous traits (morphology, physiology,
behavior) are linked, how can selective pressures lead to pleiotropic effects on
multiple developmental trajectories with selection on only one target trait?
DEVELOPMENT AND HUMAN EVOLUTION
What selection pressures existed in human evolutionary history, and how
might these have altered our patterns of development and adult phenotypes?
Does the prolonged juvenile period in humans correlate with prolonged
behavioral and cognitive development, facilitating greater acquisition of
skills in the domains of foraging and social interaction?
On the whole, it is an exciting time for studies of behavioral heterochrony.
Novel methodologies, greater access to comparative models, and better
cross-talk across disciplines can generate scientific advances that were
unavailable to previous generations. Through studies of comparative behavioral development that target ontogenetic differences between individuals,
populations, and species, we can grasp heretofore underappreciated insights
into how behavior evolves and what it means to be human.
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D. A., … Robinson, G. E. (2007). Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science, 318(5849), 441–444.
doi:10.1126/science.1146647
Trut, L. (1999). Early canid domestication: The farm-fox experiment. American Scientist, 87, 160–169.

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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES

Wobber, V., Lipson, S., Hare, B., Wrangham, R., & Ellison, P. (2013). Different ontogenetic patterns of testoterone production reflect divergent male reproductive strategies in chimpanzees and bonobos. Physiology and Behavior, 116, 44–53.
Wobber, V., Wrangham, R., & Hare, B. (2010a). Application of the heterochrony
framework to the study of behavior and cognition. Communicative and Integrative
Biology, 3, 1–3.
Wobber, V., Wrangham, R., & Hare, B. (2010b). Bonobos exhibit delayed development
of social behavior and cognition relative to chimpanzees. Current Biology, 20(3),
226–230.

FURTHER READING
Carroll, S. B. (2005). Endless forms most beautiful: The new science of evo devo. New York,
NY: W.W. Norton & Company.
Hare, B., Wobber, V., & Wrangham, R. (2012). The self-domestication hypothesis:
Bonobo psychology evolved due to selection against aggression. Animal Behaviour,
83(3), 573–585.
Mitteroecker, P., & Gunz, P. (2012). Human EvoDevo. Evolutionary Biology, 39(4),
443–446.
Toth, A., & Robinson, G. (2007). Evo-devo and the evolution of social behavior. Trends
in Genetics, 23(7), 334–341.
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D’Alessio, A. C., Sharma, S., Seckl,
J.R. … Meaney, M. J. (2004). Epigenetic programming by maternal behavior.
Nature Neuroscience, 7(8), 847–854.

Dr. VICTORIA WOBBER SHORT BIOGRAPHY
Dr. Victoria Wobber is a post-doctoral fellow in the Department of
Psychology at Harvard University and a member of the Laboratory for
Developmental Studies (https://software.rc.fas.harvard.edu/lds/). She
received her PhD in Human Evolutionary Biology from Harvard in 2012,
and her AB in Anthropology from Harvard in 2006. Her work focuses on
the evolutionary origins of human behavior, cognition, and endocrinology,
primarily through studies of humans’ closest living relatives, chimpanzees
and bonobos. More information about her research can be found on her
website (www.people.fas.harvard.edu/∼wobber).
Dr. BRIAN HARE SHORT BIOGRAPHY
Dr. Brian Hare is associate professor of evolutionary anthropology at
Duke University in North Carolina and a member of the Center for Cognitive Neuroscience, which is a division of the Duke Institute for Brain
Sciences (http://www.dibs.duke.edu/research/profiles/88-brian-hare). He

Behavioral Heterochrony

13

received his PhD from Harvard University in 2004, founded the Hominoid
Psychology Research Group in 2004 while at the Max Planck Institute for
Evolutionary Anthropology in Leipzig, Germany, and subsequently founded
the Duke Canine Cognition Center when arriving at Duke University in 2007
(http://evolutionaryanthropology.duke.edu/research/dogs). He recently
published The New York Times Bestselling book The Genius of Dogs with his
wife Vanessa Woods. He is also the founder and Chief Scientific Officer of
the citizen science company Dognition.com (https://www.dognition.com).
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