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Sherwood 2017
Sherwood 2017
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Department of Anthropology and Center for the Advanced Study of Human Paleobiology,
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https://doi.org/10.1146/annurev-anthro-102215- Abstract
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Human behavior is shaped by social learning to an extent that is unrivaled in
Copyright c 2017 by Annual Reviews. the natural world. What neurobiological changes have occurred in human
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evolutionary history that have enabled this remarkable cultural capacity?
Human brain anatomy and function have evolved to be highly responsive
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REVIEWS Further to experience from the environment, especially the milieu of social inter-
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specialization leading to increased plasticity. These include the timing of
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tionary changes in human brain plasticity are also evident in fossil hominins
and from analyses of ancient DNA.
399
AN46CH23_Sherwood ARI 8 September 2017 10:23
ment (Han & Ma 2015). What neurobiological changes have occurred in our species’ evolutionary
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others, and utilize language, depends on early-life experiences with social partners (McLaughlin
et al. 2017). Studies have shown that variation in early-life rearing experience impacts the devel-
opment of cognitive performance in other primates as well (e.g., Dettmer et al. 2016); for example,
chimpanzees and bonobos raised in settings characterized by frequent sociocommunicative inter-
actions with humans performed better on social and physical cognition tasks than did apes reared
in standard laboratory or zoo conditions (Russell et al. 2011). Additionally, great ape populations
in nature exhibit local traditions in behavior that are thought to be maintained through social
transmission (Whiten et al. 1999, van Schaik et al. 2003, Robbins et al. 2016). Thus, social expe-
rience plays an essential role in shaping neural circuits of the primate brain (Platt et al. 2016), a
process that has been further amplified in human evolution.
Brain plasticity refers to the way synaptic connections, axon fiber pathways, and the mapping of
the cerebral cortex can change during the lifespan in response to the environment and experience
(Bufill et al. 2011). This capacity for neuroplasticity can also serve as the basis for recovery of
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function after events such as stroke or traumatic brain injury. Notably, the brain is especially open
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to modification by the environment through learning during early stages of development, which
include critical periods for the onset of a variety of cognitive functions and language acquisition
(McLaughlin et al. 2017). Brain development in mammals proceeds with an initial overproduction
of neurons and synaptic connections during fetal and early postnatal periods. Some of these con-
nections are pruned later in postnatal development to refine circuits based on activity-dependent
mechanisms (Edelman 1987, Workman et al. 2013). Within this neurodevelopmental framework,
there are multiple avenues to increase brain plasticity within a lineage. Shifts in the timing between
neurodevelopmental events and birth may alter the window of opportunity for environmental and
social factors to influence the establishment of circuitry (Halley 2017). Additionally, modifications
in the timing or expression level of molecular signals underlying neuron proliferation and migra-
tion, axon pathfinding, myelination, and synaptic formation and turnover may also contribute to
species-specific variation in neuroplasticity (Somel et al. 2013, Finlay & Uchiyama 2015). There
might also be evolutionary changes in epigenetic interactions through DNA methylation that alter
the degree to which experience can modify gene expression patterns (Zeng et al. 2012, Mendizabal
et al. 2016). In this article, we review various lines of evidence that support the conclusion that
brain plasticity has increased throughout human evolution.
Table 1 Variation in neonatal and adult brain and body weight in apesa
Neonatal Neonatal Neonatal/ Neonatal/
Gestation brain weight body weight Adult brain Adult body adult brain adult body
Species time (days) (g) (g) weight (g) weight (g) weight weight
Hylobates lar 210 65 400 102 5500 0.637 0.073
Pongo pygmaeus 270 129 1500 343 36900 0.376 0.041
Gorilla gorilla 265 227 1750 406 140000 0.559 0.013
Pan troglodytes 230 128 1560 360 45000 0.356 0.035
Homo sapiens 270 335 3660 1300 65000 0.258 0.056
a
Data from Sacher & Staffeldt (1974).
1.2% in gorillas, and 4.1% in orangutans, following data in Sacher & Staffeldt (1974). In contrast,
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neonatal brain size in humans represents only one-quarter of adult brain size, whereas neonatal
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brain size in chimpanzees and orangutans is approximately one-third of adult brain size and that
of gorillas is approximately half of adult brain volume (Table 1). Thus, human altriciality arises
because a significantly greater proportion of brain growth and maturation is offset to the postnatal
period as compared with great apes and other primates (Figure 1).
Why is such a large fraction of human brain size growth deferred to occur after birth? During
the fetal period of neurogenesis, there is minimal variation among eutherian mammals, including
humans, in the overall pattern of volumetric growth acceleration of the brain (Halley 2017). Thus,
it is not a change in the shape of the human brain’s intrinsic growth curve that accounts for the
emergence of altriciality. Rather, two major constraints on the overall length of gestation might
be at play: obstetrical (Rosenberg 1992) and metabolic (Dunsworth et al. 2012). Both types of
constraints are related to the evolution of a progressively larger brain, which, in combination
with the narrow birth canal that is functionally required for bipedalism in hominins, poses spatial
limitations during parturition (Rosenberg 1992) or which requires large amounts of energy that
cannot be supplied by the mother (Dunsworth et al. 2012). These constraints are thought to have
prohibited gestation from lengthening to the extent that would be expected for a species with such
a large brain size. Therefore, a more altricial pattern of development came to characterize humans
as brain size increased in our evolutionary history.
Because mammalian peak brain growth velocity curves are relatively invariant (Halley 2017),
after birth in modern humans, brain volume continues to increase at an extremely rapid fetal-
like rate for more than a year, which is not observed in other primates (Leigh 2006). Based
on the predictable sequence of neurodevelopmental events (Workman et al. 2013), it can be
modeled that certain aspects of brain maturation, such as the onset of myelination of limbic,
striatal, and neocortical structures, were transposed from the prenatal period to the postnatal
period over the course of human evolution as brain size expanded (Gómez-Robles et al. 2017).
Indeed, comparative study of longitudinal samples of human, chimpanzee, and rhesus macaque
magnetic resonance imaging (MRI) scans shows that humans are characterized by a much more
rapid increase in cerebral white matter volume during early infancy (Sakai et al. 2012). The growth
of white matter underlying the neocortex is the major basis of overall brain volume expansion in
the first 18 months of infant development in humans. The secondarily altricial nature of human
brain development means that greater exposure to social and environmental variability during
postnatal development has the capacity to exert a strong influence during the early establishment
of connectivity. This may be especially important in boosting brain plasticity, which enables the
achievement of developmental milestones that typically occur in the first year of life, such as the
onset of joint attention and the appearance of first words (Fjell et al. 2015).
1,500
1,000
Total brain
volume (cm3)
500
Homo
0 sapiens
800
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Gorilla
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beringei
600
200 Macaca
mulatta
0
Sapajus
800 apella
600
White matter
volume (cm3) 400
200
0
0 2 4 6 8 10
Age (years)
Figure 1
Variation in total brain volume, cerebral gray matter, and white matter volume during postnatal development in humans, mountain
gorillas, chimpanzees, rhesus macaques, and tufted capuchins. Data have been obtained from relevant references (Cofran & DeSilva
2015, McFarlin et al. 2013, Phillips & Sherwood 2008, Sakai et al. 2012). Growth curves were fitted according to best models described
in original publications.
folding, which are the result of regional patterns of cortical expansion, continue in the early
postnatal period (Hill et al. 2010, White et al. 2010). At the microstructural level, most cortical
neurogenesis and migration are complete at birth, such that the laminar structure of the cerebral
cortex is established at term (Kostović et al. 2002, de Graaf-Peters & Hadders-Algra 2006). The
earliest synaptic connections are formed during the first trimester of prenatal development, but
these are transient connections with preplate neurons that will later give rise to the more stable
connections that are part of mature circuits (Tau & Peterson 2009).
At the time of birth, dendritic arborization and synaptogenesis are occurring at peak rate,
which will extend well into the first few years of postnatal life (Huttenlocher & Dabholkar 1997).
The excess of neurons and synaptic connections formed during early development is pruned later
through a process regulated by synaptic activity, cell-cell contact, and various trophic factors that
are produced by neurons and glia (Huttenlocher 1984, Lossi & Merighi 2003).
This process of activity-dependent refinement is essential in the establishment of local and
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association circuitry that facilitates the integration of information across cortical domains (Levitt
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2003). The timing of synaptic pruning in the human brain differs among cortical regions, as has
been shown through direct measures of synaptic densities (Huttenlocher & Dabholkar 1997) and
indirect measures of cortical gray matter thinning (Sotiras et al. 2017). These data demonstrate a
more extended period of maturation in heteromodal association regions compared with primary
sensory and motor areas. Notably, human neuroimaging studies show that there is a relationship
between protracted developmental changes in cortical morphology and cognitive performance
later in life (Shaw et al. 2006, Schnack et al. 2015). For example, using a longitudinal sample,
Shaw et al. (2006) found that children who scored the highest on an intelligence test had brains
that were characterized by an especially prolonged phase of initial increase in prefrontal cortical
thickness prior to the period of thinning.
Comparison of developmental changes in cortical synaptic densities and pyramidal neuron
dendritic arborization between humans and other primates shows variation that may be related
to plasticity (Figure 2). In macaques, the process of synaptogenesis, whereby new synapses are
formed, peaks during infancy at approximately three months of age, and pruning of excess synapses
is completed by the end of the juvenile period (Rakic et al. 1986). By contrast, in humans and chim-
panzees, peak synapse density occurs later during the juvenile period, with pruning of synapses
extending into early adulthood (Huttenlocher & Dabholkar 1997, Petanjek et al. 2011, Bianchi
et al. 2013). Interspecific differences also occur in the timing of maturation among different cortical
regions. In macaque monkeys, densities of spines located on the dendrites of prefrontal pyramidal
neurons are higher than other areas from the time of birth and throughout postnatal development
(Elston et al. 2006). In humans and chimpanzees, however, dendritic arbors of prefrontal cortex
pyramidal neurons reach adult-like morphological complexity and spine density later in develop-
ment than do dendritic arbors in sensory and motor cortices (Travis et al. 2005, Bianchi et al.
2013). Thus, the overall pattern of development of cortical connections appears to be extended in
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 2
Variation in synapse density and myelination during development in rhesus macaques (top), chimpanzees (middle) and humans (bottom).
Data were obtained from different published papers (Bianchi et al. 2013, Huttenlocher & Dabholkar 1997, Huttenlocher et al. 1982,
Miller et al. 2012, Rakic et al. 1986). X-axes represent the proportion of time to adulthood at each age. Adult life for each species was
calculated as the age of first reproduction in females plus 8% of the maximum lifespan for each species as reported in Mitani et al.
(2012). Adult ages calculated in this way are 8 years in rhesus macaques, 18 years in chimpanzees, and 28 years in humans. For synaptic
density, bi- and tri-exponential curves were fitted to data in all species because growth curves were not provided in the original
publications for rhesus macaques and humans. For myelination, best-fit curves described in the original publication are shown.
both humans and chimpanzees relative to macaques. What is further remarkable in the evolution
of human brain development is that this protracted synaptic refinement occurs in a neocortex that
is concomitantly also growing to be more than threefold the size of the cortex in chimpanzees and
other great apes, meaning that a much greater diversity of connectional networks has the potential
to be impacted by developmental plasticity (Buckner & Krienen 2013).
40
Brodmann’s area
Synapses per 100 μm2
Prefrontal 9 10 10
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Macaca 10 Visual 17 18 18
mulatta
Limbic 34 – –
1.6 4.8 8
years years years
0
0 20 40 60 80 100
Proportion of adult life (%)
20
0.08
Myelinated fiber length
Synapses per 100 μm3
15
density (μm/μm3)
0.06
10 0.04
Pan 5 0.02
troglodytes
3.6 10.8 18 3.6 10.8 18
years years years years years years
0 0
0 20 40 60 80 100 0 20 40 60 80 100
Proportion of adult life (%) Proportion of adult life (%)
70
60 0.08
Myelinated fiber length
Synapses per 100 μm3
density (μm/μm3)
50
0.06
40
30 0.04
Homo 20
sapiens 0.02
10
5.6 16.8 28 5.6 16.8 28
years years years years years years
0 0
0 20 40 60 80 100 0 20 40 60 80 100
Proportion of adult life (%) Proportion of adult life (%)
SYNAPTOGENESIS MYELINATION
perspective-taking, which characterize the transition from adolescence to early adulthood (Sotiras
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et al. 2017). Although major changes in decision making and emotional regulation are well known
to occur during this life-history period in humans, we do not have comparable data to determine
whether other primates undergo similar developmental changes in cognition after the transition
to adulthood.
Taken together, the extended period of neural development observed in humans offers an
additional opportunity for environment-dependent brain maturation in adolescence and early
adulthood, during which important processes, such as myelination (Miller et al. 2012) and con-
tinued developmental pruning of synaptic spines on pyramidal neurons in the prefrontal cortex
(Petanjek et al. 2011), are known to occur. This prolonged period of brain maturation is expected
to play a less critical role in increasing plasticity than does the initial postnatal period, during
which major brain size growth and patterning are under way. However, the adolescent period
is important in the acquisition of social skills and in the establishment of adult forms of lan-
guage and communication (Locke & Bogin 2006), as well as in the acquisition of foraging skills
(Schuppli et al. 2012).
Comparisons of population variability in the cerebral morphology of adult humans and chim-
panzees are congruent with the microstructural evidence for the evolutionary enhancement of
neurodevelopmental plasticity in humans. Analyses of large samples of MRI scans have shown
that human brains exhibit substantially more fluctuating asymmetry than do chimpanzee brains
(Figure 3) (Gómez-Robles et al. 2013). Fluctuating asymmetry differs from directional asym-
metry, which has a genetic origin and is related to the lateralization of functions, such as hand
preference and language. By contrast, fluctuating asymmetry is the result of environmental influ-
ences during development (Dongen 2006). Although fluctuating asymmetry is usually considered
to be indicative of developmental instability, it may also be the outcome of increased develop-
mental plasticity (Palmer & Strobeck 2003). The observation of very high levels of fluctuating
asymmetry in healthy human populations supports this interpretation. In addition, heritability for
cortical organization in humans is relatively low, whereas in chimpanzees it is high and similar to
the heritability level for brain size; the latter points to the greater level of environmental influence
in cortical organization in humans (Gómez-Robles et al. 2015). The lowest heritability values are
observed in association areas of the human cerebral cortex, which also show the greatest expansion
from birth to adulthood and during primate evolution (Hill et al. 2010) as well as the highest de-
gree of interindividual variation among humans (Mars et al. 2017). In addition, the general level of
fluctuating asymmetry has significant heritability in several brain areas in both chimpanzees and
humans, which indicates that plasticity—as inferred from fluctuating asymmetry—is an evolvable
trait (Gómez-Robles et al. 2016).
Size Symmetry
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75.3% 56.4%
h 2 = 0.53 h 2 = 0.83
SP SF SP
SF
IP IP
Lobe Directional
proportions O IF O IF asymmetry
T T
1.9% 8.1%
CS CS
PCS SyF
SyF POS PCS Fluctuating
Sulci FOS
LS LOS asymmetry
STS STS
19.1% 26.6%
Figure 3
Differences in heritability (h2 ) and asymmetric variation between chimpanzees and humans. Left: Heritability for brain volume and
general lobe proportions is high in both species, whereas heritability for sulcal anatomy is also high in chimpanzees but generally low in
humans (with the exception of the central sulcus and the Sylvian fissure). Right: Percentages indicate the proportion of total variance
corresponding to the different types of symmetric and asymmetric variation. Asymmetric variation is substantially greater in humans
than in chimpanzees, both for directional and for fluctuating asymmetry. Both types of asymmetric variation are preferentially located
in inferior parietal areas in humans, whereas in chimpanzees only directional asymmetry is preferentially localized in this region. Data
are from Gómez-Robles et al. (2013, 2015). Abbreviations for lobe proportions: IF, inferior frontal length; IP, inferior parietal length;
O, occipital length; SF, superior frontal length; SP, superior parietal length; T, temporal length. Abbreviations for sulci: CS, central
sulcus; FOS, fronto-orbital sulcus; LOS, latero-orbital sulcus; LS, lunate sulcus; PCS, precentral sulcus; POS, parieto-occipital sulcus;
STS, superior temporal sulcus; SyF, Sylvian fissure.
Changes in the sequence of particular genetic regions, such as FOXP2 (Forkhead Box P2) and
SRGAP2 (SLIT-ROBO Rho GTPase Activating Protein 2), show evidence of human-specific
effects on synaptic growth and plasticity (Enard 2011, Charrier et al. 2012, Dennis et al. 2012).
Humans carry four duplicates of the SRGAP2 gene, whereas other primates carry only one (Sud-
mant et al. 2010). This gene underwent two duplications after chimpanzees and humans diverged
(Dennis et al. 2012). One of these duplications, designated as SRGAP2C, is expressed in the de-
veloping human brain, where it dimerizes with ancestral SRGAP2A, silencing its function. This
inhibition underlies certain human-specific neural developmental changes that are related to brain
plasticity (Charrier et al. 2012). Studies of cells containing SRGAP2C from genetically modified
mice and human brain tissue show that the gene slows down the process of neuronal migration
and dendritic spine development, leading to a greater total number of synapses that mature over
a longer period of time (Charrier et al. 2012).
The FOXP2 gene encodes a transcription factor that is crucial to the development of speech
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
motor control in humans (Enard 2011). Research has demonstrated human-specific changes in
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FOXP2 that are associated with the development and function of corticostriatal circuits that are
involved in speech and language (Fisher & Scharff 2009). Experiments using mice engineered to
express the human variant of FOXP2 reveal particularly remarkable effects in the striatum, includ-
ing extending neurite outgrowth of medium spiny neurons and affecting synaptic strength and
dopaminergic neurotransmission, supporting the conclusion that the FOXP2 changes in human
evolution might have altered mechanisms of brain plasticity that are important for vocal learning
(Enard et al. 2009).
Profiling mRNA (messenger RNA) and protein expression changes across postnatal develop-
ment has also been employed as a strategy to examine differences between human brains and those
of other primates. The human neocortex is known to be an especially dynamic site of developmen-
tal change at the molecular level. For example, interindividual variation in mRNA expression is
higher in children than in adults (Sterner et al. 2012). Over the lifespan, 50–70% of brain-expressed
genes show changes in mRNA abundance; the most rapid changes take place in newborns (Somel
et al. 2009). In general, the human brain shows a conserved pattern in the trajectory of devel-
opmental changes in transcriptome, metabolome, and lipidome levels, with similar increases and
decreases in expression level as those observed in chimpanzees and macaque monkeys (Somel et
al. 2009). What differs most, however, is the timing of these molecular expression trajectories,
suggesting that heterochrony (i.e., delay or acceleration of developmental events across species)
might be a powerful mechanism at play in human brain evolution. The most striking developmen-
tal shift observed is an extension of gene expression patterns associated with synapse formation
and elimination in the human prefrontal cortex (Liu et al. 2012). These processes might reflect
neoteny, a mechanism of heterochrony where traits are retained from earlier stages of develop-
ment into later phases of life by slowing the pace of ontogenetic changes (Gould 1977, Bufill et al.
2011). In the same data set, however, it is notable that no human-specific prolongation of synaptic
gene expression is evident in the cerebellum, nor is there a delay in the prefrontal cortex for other
important neurodevelopmental processes such as myelination or axonogenesis.
Molecular evidence indicates that the human brain maintains a high level of plasticity into
adulthood as well. Many studies have now examined mRNA and protein expression in brain tissue
from adult humans and other primates. Several studies have shown that among the genes that are
differentially expressed in the human neocortex, a greater number show an increase in expression
than show a decrease (Preuss et al. 2004, Khaitovich et al. 2005, Vallender et al. 2008; but see Uddin
et al. 2004, Babbitt et al. 2010). This research has consistently found that the human neocortex
is characterized by upregulation of transcripts associated with synapse formation, glutamatergic
excitatory neurotransmission, and aerobic energy metabolism (Cáceres et al. 2003, 2007; Uddin
et al. 2004; Muntané et al. 2015). Measurements of metabolites and other proteins from mass
spectrometry similarly show an acceleration of metabolic changes in the human prefrontal cortex
compared with other primates (Fu et al. 2011, Bauernfeind et al. 2015), which suggests a higher
level of neuronal and synaptic activity than in our closest relatives (Preuss 2011).
Regulation of gene expression may be influenced by several factors, including stochastic, ge-
netic, and environmental effects. Importantly, the environment can impact gene expression via
epigenetic mechanisms such as DNA methylation and histone modification. DNA methylation is a
chemical alteration that affects chromatin regulation and gene expression, which occurs by adding
a methyl group to nucleotide bases, predominantly at cytosines followed by guanines (CpGs).
DNA methylation of gene promoters can silence mRNA transcription. Hundreds of genes show
lower levels of promoter methylation in the human prefrontal cortex than in chimpanzees and
rhesus macaques, which indicates that the epigenomic landscape has been significantly modified in
human brain evolution (Zeng et al. 2012, Mendizabal et al. 2016). Consequently, these methylomic
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
differences suggest that gene regulation in human brain tissue may have an increased capacity to
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Table 2 Variation in estimated neonatal and observed adult cranial capacity in homininsa,b
Estimated neonatal Adult endocranial Neonatal/adult endocranial
Species endocranial volume (cc) volume (cc) volume
Ardipithecus ramidus 126.5 300.0 0.422
Australopithecus afarensis 170.2 455.6 0.374
Australopithecus africanus 172.5 463.3 0.372
Paranthropus boisei 181.8 498.4 0.365
Paranthropus robustus 190.1 530.0 0.359
Homo habilis 210.6 612.2 0.344
Homo erectus 274.2 886.0 0.310
Homo neanderthalensis 397.3 1424.8 0.279
Homo sapiens 373.8 1336.1 0.280
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a
Data from DeSilva (2011).
b
Note, data for Homo sapiens differ moderately between Sacher & Staffeldt (1974) and DeSilva (2011).
For species with a brain size intermediate between that of modern humans and that of great apes,
such as Homo erectus, determining their developmental pattern has been especially challenging.
Whereas some researchers have estimated the pattern of postnatal brain size growth of Homo
erectus to be midway between that of chimpanzees and of modern humans (Coqueugniot et al.
2004, O’Connell & DeSilva 2013, Hublin et al. 2015), others have suggested that its developmental
pattern was within the range of variation of Homo sapiens (Leigh 2006). Favoring one or the other
position is not straightforward because they both have similar drawbacks. First, most inferences
concerning Homo erectus ontogeny are based on the study of one single infant, the Mojokerto
child (Antón 1997). Because brain growth rate is estimated from the proportion of adult brain size
reached by this child at death, inferences critically depend on his/her age, which has been estimated
to be as young as less than 1 year old and as old as 8 years old (Antón 1997, Coqueugniot et al.
2004). Second, developmental patterns are often calculated from comparisons of infant and adult
endocranial size, which provides a crude estimate of the rate and duration of brain size growth and
cannot provide insight into the cellular and molecular mechanisms of neurodevelopment (Webb et
al. 2001). Third, another source of discrepancy derives from uncertainty regarding the geological
age of the Mojokerto child, which is estimated to be 1.2–1.8 Ma (Swisher et al. 1994, Morwood et
al. 2003, Huffman et al. 2006, O’Connell & DeSilva 2013). Although this variation is substantial
and has important implications for developmental inferences, it certainly corresponds to an early
representative of H. erectus, whose temporal range is estimated to be 1.8 Ma to less than 100 ka
(Antón 2003). Because a temporal trend to increase brain size exists from earlier to later Homo
erectus (Antón 2002), we cannot rule out a gradual modification of development within the Homo
erectus lineage.
Insights into the evolution of hominin brain plasticity can also be gleaned from the study
of ancient DNA through the comparison of the genome of modern humans, Neanderthals, and
Denisovans (Figure 4) (Meyer et al. 2012, Prüfer et al. 2014). Mitochondrial and nuclear DNA
has also been obtained from earlier Middle Pleistocene hominins (Meyer et al. 2014, 2016), but
information on these specimens is too limited to be included in this comparison. Among those
genes that show human-specific changes, several are involved in brain growth and development
(O’Bleness et al. 2012). In particular, the modern human version of FOXP2 has also been found in
Neanderthals and Denisovans (Krause et al. 2007, Reich et al. 2010), which indicates that the forms
Denisovans
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Figure 4
Evolution of plasticity-related genes as inferred from ancient DNA. FOXP2 coding changes typical of modern humans are also found in
Denisovans and Neanderthals, whereas regulatory changes appear to be unique to modern humans. Changes in SRGAP2 paralogs are
shared by the three species. Data are from Dennis et al. (2012), Krause et al. (2007), and Maricic et al. (2013). Parts of the figure have
been adapted from Birney & Pritchard (2014), Gunz et al. (2012), Sawyer et al. (2015).
of brain plasticity associated with the FOXP2 mutation in modern humans may be shared by several
late hominin species. However, researchers have also suggested that, although coding changes in
the FOXP2 sequence may have evolved before the divergence of the [(Neanderthal–Denisovan)-
modern human] clade, they may have been later followed by regulatory changes unique to modern
humans (Maricic et al. 2013).
The human-specific duplication giving rise to SRGAP2C is estimated to have occurred at 2–
3 Ma (Dennis et al. 2012), corresponding roughly with the emergence of the genus Homo (Vill-
moare et al. 2015). This stage in hominin evolution is associated with continued brain size expan-
sion and intensification of widespread manufacture of stone tools (although recent reports have
shown that an earlier technology may predate the emergence of the genus Homo) (Harmand et al.
2015). Consistent with this date, evidence shows that both Neanderthals and Denisovans carried
the human-specific duplication, SRGAP2C (Dennis et al. 2012). Thus, as is the case for FOXP2
evolution, specific aspects of brain plasticity related to the evolution of SRGAP2 paralogs may
have been shared by several species within the genus Homo.
Finally, a new approach that offers a promising window to evaluate the evolution of brain
plasticity is the study of the ancient epigenome. DNA methylation is one of the best known epi-
genetic markers, and it can impact gene expression through several different mechanisms ( Jones
2012). Recent studies have used the natural degradation process of methylated and unmethylated
cytosines to infer methylation maps in Denisovans and Neanderthals (Gokhman et al. 2014), for
which high-coverage genome sequences are available (Meyer et al. 2012, Prüfer et al. 2014). Com-
parison of the Neanderthal, Denisovan, and modern human epigenomes has shown differentially
methylated regions that are especially common in brain-related genes (Gokhman et al. 2014).
This observation may initially appear to support the conclusion that there are differences in brain
plasticity between the three species. However, there are difficulties studying epigenetic variation
in a paleoanthropological context. Because methylation maps in Neanderthals and Denisovans
come from bone tissue in adult individuals, it remains uncertain how the observed epigenetic
signature can be extrapolated to developing brain tissue (Orlando & Willerslev 2014, Schneider
et al. 2014). Nevertheless, methylomes from various tissues and cell types show a high degree of
similarity for the majority of CpG sites (Ziller et al. 2013). Thus, ancient methylomes from fossils
may hold the promise of allowing us to glimpse human-specific changes that are relevant to the
evolution of brain plasticity.
prolonged myelination, and molecular mechanisms that enhance the formation and refinement of
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synapses. Altricial development, an enlarged and high energy–consuming neocortex, and increased
synaptic activity are all metabolically expensive traits. Estimates of daily total energy expenditure
in adult humans compared with great apes indicate that humans consume between 400 and 820
kcal per day more than close relatives do, in part owing to an elevated resting metabolic rate
(RMR) to support organ functions (Pontzer et al. 2016). A significant contributor to these costs
is the brain. Calculation of the percent of RMR required to support the brain shows that in males
and females the adult brain comprises 19.1% and 24.0%, respectively, of the body’s total energetic
budget; the relative cost is even higher in newborns (52.5% in males and 59.8% in females) and
children (66.3% in males and 65.0% in females) (Kuzawa et al. 2014).
These energetic costs must be subsidized through means that allow for high-quality dietary
resources to be delivered to growing humans during a time when they are too young to procure
their food independently (Aiello & Wheeler 1995, Isler & van Schaik 2009, Leonard & Robertson
1994). Consequently, human infants and children are especially dependent on not only their
mothers, but also other allomaternal caregivers such as grandparents, fathers, older siblings, and
other nonkin community members (Konner 2011, Isler & Van Schaik 2014). In humans, the
coevolution of more intensive cooperative behavior with allomaternal care might be an extension
of a more general pattern observed across primates, where such a cooperative breeding strategy
is correlated with proactive prosociality (Burkart et al. 2014). Such an extreme dependence on an
extended network of caregivers during early life is a distinctive aspect of human sociality and is
associated with an increased frequency and quality of social interactions that take place between
the infant and a range of social partners (Hrdy 2011). Because human infants receive attention
from a diversity of allomaternal caregivers at the time when plastic neural networks are being
actively constructed, these social relationships may serve as a critical scaffold for the understanding
of others’ intentions, setting the foundation for the developmental emergence of language and
culture.
According to this model, several interrelated life-history factors would be associated with
the evolution of large, altricial, and plastic brains in humans (Figure 5). For one, the demands
of relatively helpless infants might have acted as a selective force to increase longevity because
postreproductive kin, especially grandmothers, would be vital to providing additional support to
mothers (Hawkes 2003). Accordingly, the combination of such a high energy–consuming brain and
an extended lifespan may account for our species’ more pronounced brain structure deterioration in
old age and our heightened vulnerability to certain neurodegenerative illnesses, such as Alzheimer’s
disease (Bufill et al. 2013). Notably, even in the absence of disease, normal human brain aging
is characterized by overt volumetric shrinkage of cerebral gray matter, white matter, and the
Brain enlargement
Energetic costs
Dietary shift
Obstetrical and
metabolic constraints
Elongated lifespan
illness
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Social learning
Figure 5
A model of the evolution of human brain plasticity and its interactions with life history and cognition.
hippocampus after 50 years of age, whereas the brains of chimpanzees and macaques do not
show such profound decline (Sherwood et al. 2011). Additional neurodevelopmental illnesses
might also be associated with the evolution of our human-specific life history and brain plasticity,
including schizophrenia and bipolar disorder, which have an onset in the late adolescent/early-
adult period of cortical development. This life-history stage is characterized by uniquely human
prolonged myelination (Miller et al. 2012). Notably, autism spectrum disorder disrupts novel
molecular pathways involved in human-specific delayed synaptic gene expression (Liu et al. 2016).
Thus, some brain disorders of humans may be, in part, by-products of neoteny, causing shifts in
ontogenetic timing to retain juvenile characteristics into later stages of life.
Although plasticity may come with certain evolutionary costs (Pigliucci 2005), these aspects of
modern human development and neurobiology are related to fitness benefits as our species has
become dependent on cultural learning as a key adaptation (Tomasello 2009, Boyd et al. 2011).
Such an increase in the flexibility of the human brain allows for the incorporation of culturally
specific behaviors into the behavioral toolkit. Learning of languages, attitudes, belief systems,
and technologies all may serve to mark social group identity and facilitate cooperative sharing
of resources and skills (Richerson et al. 2016). According to this perspective, neural plasticity is
an essential component of human brain evolution, which, together with brain size enlargement
and neuroanatomical reorganization, transformed populations of human ancestors into a highly
intelligent and culture-dependent species.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We are grateful to Chris Kuzawa, Soojin Yi, Drew Halley, and an anonymous reviewer for pro-
viding thoughtful comments that helped to improve this manuscript.
LITERATURE CITED
Aiello LC, Wheeler P. 1995. The expensive-tissue hypothesis: the brain and the digestive system in human
and primate evolution. Curr. Anthropol. 36(2):199–221
Antón SC. 1997. Developmental age and taxonomic affinity of the Mojokerto child, Java, Indonesia. Am. J.
Phys. Anthropol. 102(4):497–514
Antón SC. 2002. Evolutionary significance of cranial variation in Asian Homo erectus. Am. J. Phys. Anthropol.
118(4):301–23
Antón SC. 2003. Natural history of Homo erectus. Am. J. Phys. Anthropol. 122(S37):126–70
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Babbitt CC, Fedrigo O, Pfefferle AD, Boyle AP, Horvath JE, et al. 2010. Both noncoding and protein-coding
Access provided by University of Reading on 10/23/17. For personal use only.
RNAs contribute to gene expression evolution in the primate brain. Genome Biol. Evol. 2:67–79
Balsters JH, Cussans E, Diedrichsen J, Phillips KA, Preuss TM, et al. 2010. Evolution of the cerebellar cortex:
the selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage 49(3):2045–52
Barton RA, Venditti C. 2013. Human frontal lobes are not relatively large. PNAS 110(22):9001–6
Bauernfeind AL, de Sousa AA, Avasthi T, Dobson SD, Raghanti MA, et al. 2013. A volumetric comparison
of the insular cortex and its subregions in primates. J. Hum. Evol. 64(4):263–79
Bauernfeind AL, Reyzer ML, Caprioli RM, Ely JJ, Babbitt CC, et al. 2015. High spatial resolution proteomic
comparison of the brain in humans and chimpanzees. J. Comp. Neurol. 523(14):2043–61
Bianchi S, Stimpson CD, Duka T, Larsen MD, Janssen WGM, et al. 2013. Synaptogenesis and develop-
ment of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans. PNAS
110(Suppl. 2):10395–401
Birney E, Pritchard JK. 2014. Archaic humans: Four makes a party. Nature 505(7481):32–34
Boyd R, Richerson PJ, Henrich J. 2011. The cultural niche: why social learning is essential for human adap-
tation. PNAS 108(Suppl. 2):10918–25
Bruner E, De La Cuétara JM, Holloway R. 2011. A bivariate approach to the variation of the parietal curvature
in the genus Homo. Anat. Rec. 294:1548–56
Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, et al. 2002. A new hominid from the Upper Miocene
of Chad, Central Africa. Nature 418(6894):145–51
Buckner RL, Krienen FM. 2013. The evolution of distributed association networks in the human brain. Trends
Cogn. Sci. 17:648–65
Bufill E, Agustı́ J, Blesa R. 2011. Human neoteny revisited: the case of synaptic plasticity. Am. J. Hum. Biol.
23:729–39
Bufill E, Blesa R, Augustı́ J. 2013. Alzheimer’s disease: an evolutionary approach. J. Anthropol. Sci. 91:135–57
Burkart JM, Allon O, Amici F, Fichtel C, Finkenwirth C, et al. 2014. The evolutionary origin of human
hyper-cooperation. Nat. Commun. 5:4747
Cáceres M, Lachuer J, Zapala MA, Redmond JC, Kudo L, et al. 2003. Elevated gene expression levels distin-
guish human from non-human primate brains. PNAS 100:13030–35
Cáceres M, Suwyn C, Maddox M, Thomas JW, Preuss TM. 2007. Increased cortical expression of two
synaptogenic thrombospondins in human brain evolution. Cereb. Cortex 17:2312–21
Charrier C, Joshi K, Coutinho-Budd J, Kim J-E, Lambert N, et al. 2012. Inhibition of SRGAP2 function by
its human-specific paralogs induces neoteny during spine maturation. Cell 149(4):923–35
Charvet CJ, Hof PR, Raghanti MA, Van Der Kouwe AJ, Sherwood CC, Takahashi E. 2017. Combining
diffusion magnetic resonance tractography with stereology highlights increased cross-cortical integration
in primates. J. Comp. Neurol. 525(5):1075–93
Cofran Z, DeSilva JM. 2015. A neonatal perspective on Homo erectus brain growth. J. Hum. Evol. 81:41–47
Coqueugniot H, Hublin J-J, Veillon F, Houët F, Jacob T. 2004. Early brain growth in Homo erectus and
implications for cognitive ability. Nature 431(7006):299–302
de Graaf-Peters VB, Hadders-Algra M. 2006. Ontogeny of the human central nervous system: What is hap-
pening when? Early Hum. Dev. 82(4):257–66
Deacon TW. 1997. The Symbolic Species: The Co-Evolution of Language and the Brain. New York: Norton
Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA, et al. 2012. Evolution of human-specific neural
SRGAP2 genes by incomplete segmental duplication. Cell 149:912–22
DeSilva JM. 2011. A shift toward birthing relatively large infants early in human evolution. PNAS 108(3):1022–
27
Dettmer AM, Kaburu SS, Simpson EA, Paukner A, Sclafani V, et al. 2016. Neonatal face-to-face interactions
promote later social behaviour in infant rhesus monkeys. Nat. Commun. 7:11940
Dongen SV. 2006. Fluctuating asymmetry and developmental instability in evolutionary biology: past, present
and future. J. Evol. Biol. 19:1727–43
Dubois J, Benders M, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, et al. 2008. Mapping the early cortical
folding process in the preterm newborn brain. Cereb. Cortex 18(6):1444–54
Dunsworth HM, Warrener AG, Deacon T, Ellison PT, Pontzer H. 2012. Metabolic hypothesis for human
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Edelman G. 1987. Neural Darwinism. The Theory of Neuronal Group Selection. New York: Basic Books
Elston GN, Benavides-Piccione R, Elston A, Zietsch B, Defelipe J, et al. 2006. Specializations of the granular
prefrontal cortex of primates: implications for cognitive processing. Anat. Rec. A. Discov. Mol. Cell. Evol.
Biol. 288A(1):26–35
Enard W. 2011. FOXP2 and the role of cortico-basal ganglia circuits in speech and language evolution. Curr.
Opin. Neurobiol. 21:415–24
Enard W, Gehre S, Hammerschmidt K, Hölter SM, Blass T, et al. 2009. A humanized version of Foxp2 affects
cortico-basal ganglia circuits in mice. Cell 137:961–71
Fields RD. 2015. A new mechanism of nervous system plasticity: activity-dependent myelination. Nat. Rev.
Neurosci. 16(12):756–67
Finlay BL, Uchiyama R. 2015. Developmental mechanisms channeling cortical evolution. Trends Neurosci.
38:69–76
Fisher SE, Scharff C. 2009. FOXP2 as a molecular window into speech and language. Trends Genet. 25(4):166–
77
Fjell AM, Westlye LT, Amlien I, Tamnes CK, Grydeland H, et al. 2015. High-expanding cortical regions in
human development and evolution are related to higher intellectual abilities. Cereb. Cortex 25(1):26–34
Fu X, Giavalisco P, Liu X, Catchpole G, Fu N, et al. 2011. Rapid metabolic evolution in human prefrontal
cortex. PNAS 108:6181–86
Gokhman D, Lavi E, Prüfer K, Fraga MF, Riancho JA, et al. 2014. Reconstructing the DNA methylation
maps of the Neandertal and the Denisovan. Science 344(6183):523–27
Gómez-Robles A, Hopkins WD, Schapiro SJ, Sherwood CC. 2015. Relaxed genetic control of cortical orga-
nization in human brains compared with chimpanzees. PNAS 112(48):14799–804
Gómez-Robles A, Hopkins WD, Sherwood CC. 2013. Increased morphological asymmetry, evolvability and
plasticity in human brain evolution. Proc. R. Soc. B 280(1761):20130575
Gómez-Robles A, Hopkins WD, Sherwood CC. 2014. Modular structure facilitates mosaic evolution of the
brain in chimpanzees and humans. Nat. Commun. 5:4469
Gómez-Robles A, Hopkins WD, Schapiro SJ, Sherwood CC. 2016. The heritability of chimpanzee and human
brain asymmetry. Proc. R. Soc. B 283(1845):20161319
Gómez-Robles A, Smaers JB, Sherwood CC. 2017. The evolution of human altriciality and brain plasticity in
comparative context. Am. J. Phys. Anthropol. 161:197
Gould SJ. 1977. Ontogeny and Phylogeny. Cambridge, MA: Harvard Univ. Press
Gunz P, Neubauer S, Golovanova L, Doronichev V, Maureille B, Hublin J-J. 2012. A uniquely modern
human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal
newborn from Mezmaiskaya. J. Hum. Evol. 62(2):300–313
Gunz P, Neubauer S, Maureille B, Hublin J-J. 2010. Brain development after birth differs between Nean-
derthals and modern humans. Curr. Biol. 20(21):R921–22
Halley AC. 2017. Minimal variation in eutherian brain growth rates during fetal neurogenesis. Proc. Biol. Sci.
B 284(1854):20170219
Han S, Ma Y. 2015. A culture-behavior-brain loop model of human development. Trends Cogn. Sci. 19:666–76
Hare B. 2011. From hominoid to hominid mind: What changed and why? Annu. Rev. Anthropol. 40:293–309
Harmand S, Lewis JE, Feibel CS, Lepre CJ, Prat S, et al. 2015. 3.3-million-year-old stone tools from Lomekwi
3, West Turkana, Kenya. Nature 521(7552):310–15
Hawkes K. 2003. Grandmothers and the evolution of human longevity. Am. J. Hum. Biol. 15:380–400
Hecht EE, Gutman DA, Bradley BA, Preuss TM, Stout D. 2015. Virtual dissection and comparative connec-
tivity of the superior longitudinal fasciculus in chimpanzees and humans. Neuroimage 108:124–37
Herculano-Houzel S. 2012. The remarkable, yet not extraordinary, human brain as a scaled-up primate brain
and its associated cost. PNAS 109(Suppl. 1):10661–68
Hill J, Inder T, Neil J, Dierker D, Harwell J, Van Essen D. 2010. Similar patterns of cortical expansion during
human development and evolution. PNAS 107(29):13135–40
Holloway RL. 1968. The evolution of the primate brain: some aspects of quantitative relations. Brain Res.
7(2):121–72
Holloway RL, Broadfield DC, Yuan MS. 2004. The Human Fossil Record. Vol. 3: Brain Endocasts: The Paleoneu-
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Hrdy SB. 2011. Mother and Others: The Evolutionary Origins of Mutual Understanding. Cambridge, MA: Belknap
Press
Hrvoj-Mihic B, Bienvenu T, Stefanacci L, Muotri AR, Semendeferi K. 2013. Evolution, development, and
plasticity of the human brain: from molecules to bones. Front. Hum. Neurosci. 7:707
Hublin J-J, Neubauer S, Gunz P. 2015. Brain ontogeny and life history in Pleistocene hominins. Philos. Trans.
R. Soc. B 370(1663):20140062
Huffman OF, Zaim Y, Kappelman J, Ruez DR Jr., de Vos J, et al. 2006. Relocation of the 1936 Mojokerto
skull discovery site near Perning, East Java. J. Hum. Evol. 50(4):431–51
Hüppi PS, Warfield S, Kikinis R, Barnes PD, Zientara GP, et al. 1998. Quantitative magnetic resonance
imaging of brain development in premature and mature newborns. Ann. Neurol. 43(2):224–35
Huttenlocher PR. 1984. Synapse elimination and plasticity in developing human cerebral cortex. Am. J. Ment.
Defic. 88(5):488–96
Huttenlocher PR, Dabholkar AS. 1997. Regional differences in synaptogenesis in human cerebral cortex.
J. Comp. Neurol. 387(2):167–78
Huttenlocher PR, de Courten C, Garey LJ, Van der Loos H. 1982. Synaptogenesis in human visual cortex—
evidence for synapse elimination during normal development. Neurosci. Lett. 33(3):247–52
Isler K, van Schaik CP. 2009. The expensive brain: a framework for explaining evolutionary changes in brain
size. J. Hum. Evol. 57(4):392–400
Isler K, Van Schaik CP. 2014. How humans evolved large brains: comparative evidence. Evol. Anthropol.
23:65–75
Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet.
13:484–92
Khaitovich P, Hellmann I, Enard W, Nowick K, Leinweber M, et al. 2005. Parallel patterns of evolution in
the genomes and transcriptomes of humans and chimpanzees. Science 309:1850–54
Konner M. 2011. The Evolution of Childhood: Relationships, Emotion, Mind. Cambridge, MA: Belknap Press
Kostović I, Judaš M, Radoš M, Hrabač P. 2002. Laminar organization of the human fetal cerebrum revealed
by histochemical markers and magnetic resonance imaging. Cereb. Cortex 12(5):536–44
Krause J, Lalueza-Fox C, Orlando L, Enard W, Green RE, et al. 2007. The derived FOXP2 variant of modern
humans was shared with Neandertals. Curr. Biol. 17:1908–12
Kuzawa CW, Chugani HT, Grossman LI, Lipovich L, Muzik O, et al. 2014. Metabolic costs and evolutionary
implications of human brain development. PNAS 111:13010–15
Leigh SR. 2006. Brain ontogeny and life history in Homo erectus. J. Hum. Evol. 50(1):104–8
Leonard WR, Robertson ML. 1994. Evolutionary perspectives on human nutrition: the influence of brain and
body size on diet and metabolism. Am. J. Hum. Biol. 6(1):77–88
Levitt P. 2003. Structural and functional maturation of the developing primate brain. J. Pediatr. 143(4
Suppl.):35–45
Liu X, Han D, Somel M, Jiang X, Hu H, et al. 2016. Disruption of an evolutionarily novel synaptic expression
pattern in autism. PLOS Biol. 14:e1002558
Liu X, Somel M, Tang L, Yan Z, Jiang X, et al. 2012. Extension of cortical synaptic development distinguishes
humans from chimpanzees and macaques. Genome Res. 22:611–22
Locke JL, Bogin B. 2006. Language and life history: a new perspective on the development and evolution of
human language. Behav. Brain Sci. 29(3):259–80; discussion 280–325
Lossi L, Merighi A. 2003. In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian
CNS. Prog. Neurobiol. 69(5):287–312
Maricic T, Günther V, Georgiev O, Gehre S, Ćurlin M, et al. 2013. A recent evolutionary change affects a
regulatory element in the human FOXP2 gene. Mol. Biol. Evol. 30(4):844–52
Marques-Bonet T, Ryder OA, Eichler EE. 2009. Sequencing primate genomes: What have we learned? Annu.
Rev. Genom. Hum. Genet. 10:355–86
Mars RB, Passingham RE, Neubert F-X, Verhagen L, Sallet J. 2017. Evolutionary specializations of human
association cortex. In Evolution of Nervous Systems, ed. J Kaas, TM Preuss, pp. 185–205. Cambridge, MA:
Acad. Press/Elsevier. 2nd ed.
McFarlin SC, Barks SK, Tocheri MW, Massey JS, Eriksen AB, et al. 2013. Early brain growth cessation in
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
wild Virunga mountain gorillas (Gorilla beringei beringei). Am. J. Primatol. 75:450–63
Access provided by University of Reading on 10/23/17. For personal use only.
McLaughlin KA, Sheridan MA, Nelson CA. 2017. Neglect as a violation of species-expectant experience:
neurodevelopmental consequences. Biol. Psychiatry https://doi.org/10.1016/j.biopsych.2017.02.1096
Mendizabal I, Shi L, Keller TE, Konopka G, Preuss TM, et al. 2016. Comparative methylome analyses identify
epigenetic regulatory loci of human brain evolution. Mol. Biol. Evol. 33:2947–59
Meyer M, Fu Q, Aximu-Petri A, Glocke I, Nickel B, et al. 2014. A mitochondrial genome sequence of a
hominin from Sima de los Huesos. Nature 505:403–6
Meyer M, Kircher M, Gansauge M-T, Li H, Racimo F, et al. 2012. A high-coverage genome sequence from
an archaic Denisovan individual. Science 338(6104):222–26
Meyer M, Arsuaga J-L, de Filippo C, Nagel S, Aximu-Petri A, et al. 2016. Nuclear DNA sequences from the
Middle Pleistocene Sima de los Huesos hominins. Nature 531:504–7
Miller DJ, Duka T, Stimpson CD, Schapiro SJ, Baze WB, et al. 2012. Prolonged myelination in human
neocortical evolution. PNAS 109:16480–85
Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB. 2012. The Evolution of Primate Societies. Chicago: Univ.
Chicago Press
Morwood MJ, O’Sullivan P, Susanto EE, Aziz F. 2003. Revised age for Mojokerto 1, an early Homo erectus
cranium from East Java, Indonesia. Aust. Archaeol. 57:1–4
Muntané G, Horvath JE, Hof PR, Ely JJ, Hopkins WD, et al. 2015. Analysis of synaptic gene expression in
the neocortex of primates reveals evolutionary changes in glutamatergic neurotransmission. Cereb. Cortex
25:1596–607
O’Bleness M, Searles VB, Varki A, Gagneux P, Sikela JM. 2012. Evolution of genetic and genomic features
unique to the human lineage. Nat. Rev. Genet. 13(12):853–66
O’Connell CA, DeSilva JM. 2013. Mojokerto revisited: evidence for an intermediate pattern of brain growth
in Homo erectus. J. Hum. Evol. 65(2):156–61
Orlando L, Willerslev E. 2014. An epigenetic window into the past? Science 345(6196):511–12
Palmer AR, Strobeck C. 2003. Fluctuating asymmetry analyses revisited. In Developmental Instability. Causes
and Consequences, ed. M Polak, pp. 279–319. Oxford, UK: Oxford Univ. Press
Passingham RE, Smaers JB. 2014. Is the prefrontal cortex especially enlarged in the human brain? Allometric
relations and remapping factors. Brain Behav. Evol. 84(2):156–66
Petanjek Z, Judaš M, Šimić G, Rašin MR, Uylings HBM, et al. 2011. Extraordinary neoteny of synaptic spines
in the human prefrontal cortex. PNAS 108(32):13281–86
Phillips KA, Sherwood CC. 2008. Cortical development in brown capuchin monkeys: a structural MRI study.
Neuroimage 43(4):657–64
Pigliucci M. 2005. Evolution of phenotypic plasticity: Where are we going now? Trends Ecol. Evol. 20(9):481–86
Platt ML, Seyfarth RM, Cheney DL. 2016. Adaptations for social cognition in the primate brain. Philos. Trans.
R. Soc. B 371(1687):20150096
Ponce de León MS, Bienvenu T, Akazawa T, Zollikofer CPE. 2016. Brain development is similar in Nean-
derthals and modern humans. Curr. Biol. 26(14):R665–66
Pontzer H, Brown MH, Raichlen DA, Dunsworth H, Hare B, et al. 2016. Metabolic acceleration and the
evolution of human brain size and life history. Nature 533:390–92
Portmann A. 1969. Biologische Fragmente Zu Einer Lehre Vom Menschen. Basel, Switz.: Benno Schwabe
Preuss TM. 2011. The human brain: rewired and running hot. Ann. N. Y. Acad. Sci. 1225(Suppl. 1): E182–91
Preuss TM, Cáceres M, Oldham MC, Geschwind DH. 2004. Human brain evolution: insights from microar-
rays. Nat. Rev. Genet. 5:850–60
Prüfer K, Racimo F, Patterson N, Jay F, Sankararaman S, et al. 2014. The complete genome sequence of a
Neanderthal from the Altai Mountains. Nature 505(7481):43–49
Rakic P, Bourgeois J, Eckenhoff M, Zecevic N, Goldman-Rakic P. 1986. Concurrent overproduction of
synapses in diverse regions of the primate cerebral cortex. Science 232(4747):232–35
Reich D, Green RE, Kircher M, Krause J, Patterson N, et al. 2010. Genetic history of an archaic hominin
group from Denisova Cave in Siberia. Nature 468(7327):1053–60
Richerson P, Baldini R, Bell AV, Demps K, Frost K, et al. 2016. Cultural group selection plays an essential
role in explaining human cooperation: a sketch of the evidence. Behav. Brain Sci. 39:e30
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Rilling JK. 2006. Human and nonhuman primate brains: Are they allometrically scaled versions of the same
Access provided by University of Reading on 10/23/17. For personal use only.
Sherwood CC, Subiaul F, Zawidzki TW. 2008. A natural history of the human mind: tracing evolutionary
changes in brain and cognition. J. Anat. 212(4):426–54
Smaers JB, Gómez-Robles A, Parks AN, Sherwood CC. 2017. Exceptional evolutionary expansion of prefrontal
cortex in great apes and humans. Curr. Biol. 27(5):714–20
Smith TM, Tafforeau P, Reid DJ, Pouech J, Lazzari V, et al. 2010. Dental evidence for ontogenetic differences
between modern humans and Neanderthals. PNAS 107(49):20923–28
Somel M, Franz H, Yan Z, Lorenc A, Guo S, et al. 2009. Transcriptional neoteny in the human brain. PNAS
106:5743–48
Somel M, Liu X, Khaitovich P. 2013. Human brain evolution: transcripts, metabolites and their regulators.
Nat. Rev. Neurosci. 14:112–27
Sotiras A, Toledo JB, Gur RE, Gur RC, Satterthwaite TD, Davatzikos C. 2017. Patterns of coordinated cortical
remodeling during adolescence and their associations with functional specialization and evolutionary
expansion. PNAS 114:3527–32
Sterner KN, Weckle A, Chugani HT, Tarca AL, Sherwood CC, et al. 2012. Dynamic gene expression in the
human cerebral cortex distinguishes children from adults. PLOS ONE 7:e37714
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
Sudmant PH, Kitzman JO, Antonacci F, Alkan C, Malig M, et al. 2010. Diversity of human copy number
Access provided by University of Reading on 10/23/17. For personal use only.
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Rock Art and Ontology
Andrew Meirion Jones p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 167
Collective Action Theory and the Dynamics of Complex Societies
Elizabeth DeMarrais and Timothy Earle p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 183
Archaeologies of the Contemporary World
Rodney Harrison and Esther Breithoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 203
The Archaeological Study of Sacrifice
Glenn M. Schwartz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 223
Archaeology and Human–Animal Relations: Thinking Through
Anthropocentrism
Brian Boyd p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 299
Social Network Analysis in Archaeology
Barbara J. Mills p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 379
Biological Anthropology
Late Australopiths and the Emergence of Homo
Darryl J. de Ruiter, S.E. Churchill, J. Hawks, and L.R. Berger p p p p p p p p p p p p p p p p p p p p p p p p p p p99
Primate Positional Behavior Development and Evolution
Michelle Bezanson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 279
The Monkeying of the Americas: Primate Biogeography in the
Neotropics
Jessica Lynch Alfaro p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Brain Plasticity and Human Evolution
Chet C. Sherwood and Aida Gómez-Robles p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 399
vii
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Sociocultural Anthropology
Annu. Rev. Anthropol. 2017.46:399-419. Downloaded from www.annualreviews.org
viii Contents
AN46_FrontMatter ARI 7 September 2017 20:51
Human–Animal Communication
Access provided by University of Reading on 10/23/17. For personal use only.
Indexes
Errata
Contents ix