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Growth, Development, and Life History throughout the Evolution of Homo

Author(s): Gary T. Schwartz

Source: Current Anthropology, Vol. 53, No. S6, Human Biology and the Origins of Homo
(December 2012), pp. S395-S408
Published by: The University of Chicago Press on behalf of Wenner-Gren Foundation for
Anthropological Research

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Current Anthropology Volume 53, Supplement 6, December 2012


Growth, Development, and Life History

throughout the Evolution of Homo
by Gary T. Schwartz
For over a century, paleoanthropologists have listed the presence of prolonged periods of gestation, growth, and
maturation, extremely short interbirth intervals, and early weaning among the key features that distinguish modern
humans from our extant ape cousins. Exactly when and how this particular scheduling of important developmental
milestonestermed a life history profilecame to characterize Homo sapiens is not entirely clear. Researchers
have suggested that the modern human life history profile appeared either at the base of the hominin radiation (ca.
6 Ma), with the origins of the genus Homo (ca. 2.5 Ma), or much later in time, perhaps only with H. sapiens (ca.
200100 Ka). In this short review, evidence of the pace of growth and maturation in fossil australopiths and early
members of Homo is detailed to evaluate the merits of each of these scenarios. New data on the relationship between
dental development and life history in extant apes are synthesized within the context of life history theory and
developmental variation across modern human groups. Future directions, including new analytical tools for extracting
more refined life history parameters as well as integrative biomechanical and developmental models of facial growth
are also discussed.

Compared with our closest living relativesthe extant great
apesthe sole surviving member of the genus Homo possesses
a suite of features that make us quite distinct, including unusually large brains, obligate bipedality, a reliance on the production and use of tools, and a strikingly different life history.
Generally, patterns of mammalian growth, development, and
life history are thought of as lying along a spectrum somewhere between two end points that are colloquially referred
to as live fast, die young and live slow, die old. Modern
human life history incorporates elements of both schedules:
long gestation periods, altricial offspring, enlarged brains,
slow maturation rates, increased life span, and protracted periods of offspring dependence are suggestive of a live slow
strategy, whereas relatively early weaning, short interbirth intervals, and the ability to overlap births (resulting in the presence of multiple offspring) are suggestive of a live fast schedule. Of interest to paleoanthropologists is whether this
modern human life history package evolved as a single developmental module or accumulated in a mosaic fashion
(with different attributes appearing at different points in
time). Furthermore, it is of great interest to understand when
Gary T. Schwartz is Associate Professor of Anthropology at the
Institute of Human Origins at Arizona State University (900 South
Cady Mall, Tempe, Arizona 85287-2402, U.S.A. []).
This paper was submitted 12 XII 11, accepted 28 VI 12, and
electronically published 20 XI 12.

this transition occurred and thus determine whether the human life history package appeared as part of a suite of fundamental adaptations at the base of the hominin clade;
whether it evolved somewhat later, perhaps tied to the reorganization of the cranium and postcranium that characterized the earliest members of the genus Homo; or whether
it appeared even later still, perhaps in the last hundred thousand years or so.
The last decade has been marked by a tremendous amount
of research into reconstructing the pattern of growth, development, and life history of extant great apes, australopiths,
and early to later members of the genus Homo. Novel analytical techniques, imaging modalities, and hard-fought observational data from naturalistic studies of great apes can
now be synthesized to paint a broad view of the evolution of
life history throughout the course of the human story. The
goal of this paper is to review the current state of knowledge
of the evolution of human life history within the comparative
context of what we know about these attributes in populations
of extant hominoids and fossil hominins. These data will be
evaluated within the light of what is known about primate
life history, ecology, diet, and so forth, and will be used to
help suggest future avenues of inquiry into studies of hominin
life history.

What Is Life History?

By marrying the principles of organic evolution with those
of theoretical population ecology, life history theory seeks to
understand the general rules that account for the tremendous

2012 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2012/53S6-0011$10.00. DOI: 10.1086/667591

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Current Anthropology Volume 53, Supplement 6, December 2012

variation in life cycles across all organisms (Stearns 1992). In

short, life history theory views variation in the pattern, sequence, and pace of growth as the outcome of how natural
selection operates on a series of trade-offs in the allocation
of an organisms energetic budget. Smith and Tompkins
(1995:257) emphasized the importance of these trade-offs in
defining life history as the allotment of an organisms energy
towards, growth, maintenance, reproduction, raising offspring to independence, and avoiding death. Bogin (1988:
154) suggested that the life history of a species can be viewed
as a strategy that determines when to be born, when to be
weaned, how many and what type of prereproductive stages
of development to pass through, when to reproduce, and
when to die. Central to these and other definitions is the
notion that energy is a limiting commodity that is distributed
toward growth, maintenance (of tissues), and/or reproduction
throughout the lives of individuals (Bogin and Smith 2000;
Roff 2002; Stearns 1992). In a strict Darwinian sense, selection
should favor an apportionment of energy in ways that reduce
mortality and maximize fecundity. Thus, the application of
life history theory to ontogenetic studies seeks to understand
how the scheduling of key events in an organisms life cycle
(including but not limited to gestation length, age at weaning,
interbirth interval, timing of maturation, age at first reproduction, frequency of reproduction, fecundity, and life span)
better enable some individuals of a species to minimize mortality risks more effectively and thus increase overall fitness.
This scheduling or sequence of events can be thought of as
a life history profile and is, effectively, the product of how
developmental variables (e.g., growth rates, age at skeletal
maturation) interact with demographic variables (e.g., survival, reproduction, population growth) to influence individual survival (Godfrey, Petto, and Sutherland 2002; Ross 1998).
Aside from being viewed as an energetic trade-off, a species
life history profile is directly linked to rates of extrinsic mortality, which is defined as the risk of death as a result of
environmental conditions such as predation, disease, accidents, and so forth (Stearns 1992). High extrinsic mortality
should favor shorter life spans, while lower extrinsic mortality
results in a larger proportion of the population surviving to
older ages. Compared with great apes, human populations
are able to ramp up reproductive success because our life
history profile is characterized by lower mortality rates, which
has the effect of slowing down rates of maturation, delaying
reproduction, and thus spreading it out across later years. For
a large primate, a strategy including a prolongation of growth
and development comes with some risk, as evidenced by recent data on the inability of orangutan populations (with late
ages of reproductive maturity and interbirth intervals of 7
years) to recover from even slight reductions in population
density (Knott, Thompson, and Wich 2009). At a finer scale
of comparison (i.e., across populations of modern Homo sapiens), differences in subsistence strategies, environments, and
mortality rates comingle to produce tremendous variation in
patterns of human ontogeny (e.g., Migliano and Guillon

2012). For instance, in a survey of 22 small-scale societies,

Walker et al. (2006) found that populations experiencing low
survivorship (i.e., high mortality) during the subadult years
were characterized by an overall pattern of accelerated development and thus reached the important developmental
milestones of puberty, menarche, and first reproduction at
relatively earlier ages. Interestingly, new evidence suggests that
adverse early life conditions in humans, ranging from the
biological (low birth weight for gestational age, breast-feeding
duration) to the psychosocial (separation anxiety, family residential relocation, degree of parental involvement) mediate
reproductive scheduling by accelerating the age at first pregnancy (Nettle, Coall, and Dickins 2010 and references
therein). A more detailed understanding of exactly how such
environmental constraints, broadly speaking, shape life history variation across human populations would be extremely
informative. Similarly, uncovering the role developmental
plasticity (the capacity of an individual to modify its ontogeny
in response to shifting environmental conditions on a fairly
rapid timescaledays, months, or a few years) plays in generating novel phenotypes that enhance the evolutionary potential, or evolvability, of developmental systems may help
illuminate the process(es) whereby selection assembled the
total package of modern human life history attributes over a
period of several hundred thousand years (e.g., see Kuzawa
and Bragg 2012; West-Eberhard 2003).

Reconstructing Hominin Life History Profiles

When viewed in the light of life history theory, it might seem
impossible to infer such reproductive, physiological, demographic, environmental, and behavioral parameters from fossilized remains. However, the vast majority of the hominin
fossil record comprises isolated teeth and dentognathic remains, and many of the important life history variables discussed above are tightly linked with aspects of developing
dentitions. As a result, studies on the timing of particular
dental developmental events figure prominently in paleoanthropological investigations that aim to reconstruct the life
history profiles of fossil primates and hominins (e.g., Beynon
et al. 1998; Bromage and Dean 1985; Conroy and Kuykendall
1995; Conroy and Vannier 1991a, 1991b; Dean et al. 1993,
2001; Godfrey et al. 2001; Mann 1975; Robson and Wood
2008; Schwartz et al. 2005; Smith 1989, 1993; Smith, Crummett, and Brandt 1994; Smith, Gannon, and Smith 1995;
Smith et al. 2010a, 2010b; Zihlman, Bolter, and Boesch 2004).
Ever since the pioneering studies on primate growth by
Schultz (1935, 1940, 1960) and Sacher (1959, 1975, 1978;
Sacher and Staffeldt 1974), evolutionary biologists and paleoanthropologists have linked aspects of somatic and neural
growth rates to reproduction, metabolism, and life span in
an attempt to reconstruct aspects of early hominin maturation. The first study to flesh out the relationship between the
sequence and pace of dental development and aspects of life
history was by Schultz (1949), who observed that the per-

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Schwartz Life History Evolution in Homo

manent replacement molars emerge into the oral cavity before

the shedding of deciduous teeth in faster-growing primates.
This phenomenon has since been dubbed Schultzs rule
(Smith 2000) and accurately relates dental emergence sequences to maturation rates across primates as a whole, especially anthropoids (see Godfrey et al. 2005). It also allowed
paleoanthropologists an opportunity to evaluate when the
modern human developmental pattern (i.e., tooth crown development and emergence sequence) first appeared during
the course of human evolution as it could be used to assess
the relative developmental status of juvenile hominins (Smith
1986). Along with other studies examining the sequence of
dental development and emergence in hominins (e.g., Conroy
and Kuykendall 1995; Conroy and Vannier 1991a, 1991b), it
became increasingly clear that the earliest hominins, and indeed even fossil species of the genus Homo, were characterized
by dental developmental patterns, and thus maturational profiles, more similar to extant apes (at the time, meaning predominantly Pan troglodytes). This work was extremely important because the prevailing paradigm held that all
hominins, including the earliest australopiths, possessed a
modern humanlike maturation profile with the attendant prolonged infant and childhood dependency that was so fundamental to producing the social, cognitive, and cultural complexity that serves as the hallmark of our species (Mann 1975).
Given the intimate relationship between brain size, life
span, and rates of maturation and the plasticity of certain
reproductive parameters, Smith (1989) reasoned that the dentition should be one of the more stable markers of growth
given its high heritability and resistance to environmental
perturbations. She conducted a broad, interspecific comparison of dental maturation with various life history variables
and revealed the extremely high correlation between brain
size and the age at first molar (M1) emergence on the one
hand and between M1 emergence age and various life history
variables related to reproduction (gestation length, ages at
weaning and first breeding, life span) on the other. This seminal study laid the groundwork for linking aspects of the
timing or pace of dental development to critical components
of a species life history and, equally importantly, provided a
chronological marker for probing the maturation rates of fossils if information on the timing of key dental development
events (i.e., M1 emergence) could somehow be retrieved from
the fossil record.
At around the same time, a group of paleoanthropologists
began to mine the rich vein of growth data contained within
teeth. Based on some foundational work in dental hard tissue
biology (Boyde 1963, 1964), a series of investigations began
to appear that documented how to retrieve information on
the absolute timing of dental development utilizing the
growth record contained within enamel and dentine. The cells
that secrete the dental tissues enamel and dentine (for reasons
of brevity, cementum is not discussed here) leave a record of
their activity in the form of short- and long-period incremental growth lines. These include, respectively, daily cross


striations and Retzius lines in the enamel and the corresponding von Ebner and Andresen lines in dentine (Dean 1987,
2006; Schwartz and Dean 2000; Smith 2006, 2008). Careful
counts of these lines reveal the time taken to form a tooth,
including the tooth crown and however much root had
formed at the time of death, thereby providing a detailed
chronology of dental development that can, under the right
circumstances, also yield precise ages for key events such as
molar emergence (e.g., Beynon, Dean, and Reid 1991; Dean
et al. 2001; Dirks 1998; Kelley and Schwartz 2010; Smith,
Reid, and Sirianni 2006; Smith et al. 2010a, 2010b).
Data on molar emergence ages in hominins, while rare, are
becoming more accessible, especially with the application of
new, noninvasive imaging modalities that allow access to the
internal dental growth record (e.g., Smith et al. 2007b, 2007c,
2010b). While it is critically important to establish a growing
database on molar emergence ages in key hominin taxa, it is
also necessary to chart more fully dental developmental variation in extant hominoids and to interpret that variation in
light of a particular species population ecology, demography,
and life history. For now, good population data on molar
emergence ages exist only for P. troglodytes (Anemone, Mooney, and Siegel 1996; Conroy and Mahoney 1991; Kuykendall,
Mahoney, and Conroy 1992; Nissen and Reisen 1945, 1964;
Reid et al. 1998; Schultz 1940; Smith et al. 2007a, 2010a;
Zihlman, Bolter, and Boesch 2004; though see Dirks 2003 and
Dirks and Bowman 2007 for individual hylobatids; and Beynon, Dean, and Reid 1991; Winkler, Schwartz, and Swindler
1991; and Kelley and Schwartz 2010; and Willoughby 1978
for individual gorillas and orangutans). There is also a growing awareness that emergence ages for captive primate populations may be slightly advanced compared with wild populations (e.g., Kelley and Schwartz 2010; Smith and Boesch
2011; Zihlman, Bolter, and Boesch 2004), suggesting at the
very least some caution in relying on databases derived exclusively from captive colonies. Expanding our knowledge of
dental developmental variation across natural fertility populations of modern humans is another key element (e.g., Liversidge 2003) and will ultimately allow more fine-scale tests
of how population-level variation in aspects of dental development (e.g., M1 emergence age) relates to that for various
life history attributes.
Early Homo
It has generally been viewed that the origin of the genus Homo
was characterized by a trend away from bipedal apelike forms
to obligate terrestrial bipeds who were endowed with much
larger brains and the capacity to manufacture and use stone
tool technology and who also exhibited a shift in dietary and
foraging adaptations. Fossil representatives of the genus Homo
were first described by Leakey, Tobias, and Napier (1964) from
material derived from Bed I, Olduvai Gorge, Tanzania, and
were dated to 1.81.7 Ma. These authors viewed the material
as distinct from australopith material given its possession of

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Current Anthropology Volume 53, Supplement 6, December 2012

a larger, more globular and gracile cranium with a cranial

capacity 1600 cm3 and a concomitant reliance on the habitual
production and use of lithic technology. Fossil evidence for
even earlier representatives of Homo includes mostly isolated
specimens from South Africa (Sterkfontein, ca. 2.6 Ma),
Kenya (Chemeron, 2.4 Ma), and Malawi (Uraha, 2.51.9
Ma), with a maxilla from Hadar, Ethiopia (A.L. 666-1, 2.3
Ma) being the best candidate for the earliest Homo (Kimbel,
Johanson, and Rak 1997; see recent review in Kimbel 2009),
thereby extending the origin of Homo further back in time
to at least 2.5 Ma, to a time when Africa was undergoing a
transition toward cooler, drier conditions with an increase in
more open habitats (see also Potts 2012). Regardless of the
precise time and location of the origins of our own genus
though it is generally held to be within the critical interval
of 32.0 Mamany paleoanthropologists support the usage
of Leakey, Tobias, and Napiers morphological-behavioral
complex (increased brain size, stone tool production) as the
sole criterion for inclusion within the genus and would therefore recognize three securely attributed representative species
of premodern early Homo in Africa: Homo habilis (1.91.4
Ma), Homo rudolfensis (1.91.8 Ma), and Homo ergaster and
Homo erectus (1.90.9 Ma; see Anton 2012; Kimbel 2009; and
Wood and Lonergan 2008 for recent reviews of the fossil
evidence of Homo).
Not everyone would include the transitional species of
H. habilis and H. rudolfensis within the genus Homo. Wood
and Collard (1999) maintained that all members of a genus
should occupy the same adaptive zone (and thus possess a
similar adaptive strategy) and proposed a set of criteria for
the inclusion of any species into the genus Homo. Based on
its large body size, body proportions, reduced dentition, and
commitment to long-range bipedality, they recommend that
H. ergaster be the earliest hominin to satisfy their adaptive
criteria, thereby relegating both of the earlier Homo species
to the genus Australopithecus. Recent metric analyses, however, demonstrate similarities in some of these anatomical
complexes (limb lengths and proportions) and suggest that
reassigning these species may be unwarranted (Holliday
Regardless of generic assignations, many of the hominins
before 2.5 Ma can be broadly characterized as relatively smallbrained, large-toothed, nonstone tool producing human ancestors (though recent work suggests that some australopith
taxa may have been using stone tools; McPherron et al. 2010).
As such, it may seem reasonable to postulate some sort of
grade shift in life history during this critical interval. Alternatively, species of early Homo (and Australopithecus for that
matter) might each possess slightly different life histories, as
these profiles are closely calibrated to local environment and
ecologies, and the critical time interval for the evolution of
Homo (32.0 Ma) is characterized by magnified climate variability and thus variable adaptive settings (deMenocal 1995;
Potts 1996, 2012).

What Do We Know about Life History in Early Homo?

In short, not as much as we would like to know. This is in
part because an organisms strategy for parsing out energy
for purposes of growth, maintenance, and/or reproduction
(i.e., their gestation length, age at weaning, interbirth interval,
timing of maturation, frequency of reproduction, fecundity,
and life span) is not a durable part of the fossil record. Importantly, there are now some good attempts at deriving gestation length, interbirth intervals, and weaning age from hard
tissue remains for certain primate taxa (see Dirks et al. 2010;
Humphrey et al. 2008a, 2008b; Schwartz et al. 2002), though
how fruitful they will be if applied to fossil human taxa is
currently unknown.
For several decades, paleoanthropologists have viewed the
evolution of modern human growth, development, and life
history through the lens of a comparative dichotomy between
modern Pan on the one hand and modern humans on the
other. This is not unreasonable given that recent DNA analyses
support a Pan-Homo clade to the exclusion of all other hominoids (e.g., Bradley 2008; Ruvolo 1994). It is interesting,
however, that several early hominin specimens exhibit striking
anatomical similarities with extant gorillas (Dean 2010). For
instance, certain aspects of scapular morphology in the recently discovered Dikika skeleton and the mandibular morphology of other Australopithecus afarensis specimens bear a
close resemblance to the condition in extant Gorilla (Alemseged et al. 2006; Rak, Ginzburg, and Geffen 2007). Unfortunately, not enough is currently known about development
in Gorilla, or developmental variation among Gorilla spp., to
speculate on the importance of this for understanding how
best to model the mosaic pattern of great ape morphology/
dental development evident within australopiths and perhaps
early Homo (Dean 2010).
What we have been able to reconstruct about life history
in early Homo, and indeed for several earlier and later hominins, is based on estimates of the pattern and pace of dental
development or on the tight association between brain size
and life history (or some skeletal correlate of life history).
Thus, a series of key questions related to understanding the
ontogeny of early Homo can now be asked. Is there evidence
that the earliest hominins (including the earliest members of
the genus Homo) matured in a wayhad a chronology of
dental developmentthat was similar to extant chimpanzees
(and moreover, do all extant apes mature, dentally, in an
identical manner)? Do the early hominins differ in the chronology of tooth emergence in ways that might suggest developmental heterogeneity in their reconstructed life history
profiles? Do the earliest representatives of the genus Homo
exhibit dental developmental chronologies that align them
more closely with the penecontemporaneous australopiths or
with geologically younger Neanderthals and archaic Homo
sapiens populations?
Inferences from extant ape development. We know more about
chimpanzee growth, development, diet, and ecology than we

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Schwartz Life History Evolution in Homo


Table 1. Comparative life history and M1 emergence age (years) in extant great apes and humans
Age at first reproduction
Interbirth interval
Age at M1 emergence
Cranial capacity (cm3)





10.1a (51.3)
20.6f (38.1)
3.8 (65.5)

14.3b (72.6)
29.7 (54.9)
4.0b (69.0)

15.7c (79.7)
43.0 (79.5)
4.6c (79.3)


Note. Numbers in parentheses indicate the percentage relative to the values in modern humans. References for life
history, survivorship, and M1 emergence data are reported in Kelley and Schwartz (2010).
Value for mountain gorilla Gorilla gorilla beringei, which is likely to be earlier than in Gorilla gorilla gorilla.
Values for Pan troglodytes verus only (Ta Forest, Ivory Coast).
Values for Pongo pygmaeus pygmaeus (i.e., orangutans from Borneo) only.
Interbirth interval is anomalously low in modern humans compared with other anthropoid species. This life
history variable is included for between-ape comparisons only, and percentages of human values were not calculated.
Expected age at death at age 15 years based on empirically derived survivorship curves.
Average of female (24.8 years, or 45.8%) and male (16.4 years, or 30.3%) values. Courtesy of Anne Bronikowski
and the Dian Fossey Gorilla Fund International.

do for any other ape, and with the exception of baboons,

perhaps for any other primate. Dean (2010) recently synthesized all that is known about dental development in Pan,
revealing some interesting similarities with and differences
from modern humans. Overall, chimpanzee dental development occurs along an accelerated schedule, taking 12 years
compared with 18 years in modern humans. This acceleration
is reflected in advanced median molar emergence ages that
occur well before those of humans. The first mean gingival
emergence ages for chimp M1s were reported to be 3.3 years
(range of 2.63.8 years; Nissen and Reisen 1964). After three
more decades of studies on captive chimps, median emergence
ages for M1s are reconstructed as quite close to that original
estimate, at 3.2 years (M1 range, 2.264.38 years; M1 range,
2.143.99 years; Kuykendal, Mahoney, and Conroy 1992).
Thus, for several decades, it was generally taken that M1
emergence in Pan, and thus for African apes as a whole,
occurred somewhere in the range of 3.03.5 years. By comparison, the range for modern humans calculated across
global populations averages 4.77.0 years (Liversidge 2003).
Given the presence of the so-called wild effect (sensu
Smith and Boesch 2011; see also Hamada et al. 1996; Kimura
and Hamada 1996), it became critical to evaluate gingival
emergence ages in wild populations. To date, the only reliable
estimate for age at M1 emergence in noncaptive apes is a
single individual of Pan troglodytes verus at approximately 4.1
years for the maxillary M1. The likely age of emergence for
the mandibular M1 in this individual was approximately 3.8
3.9 years, resulting in a combined age of M1 emergence of
approximately 4.0 years (Smith et al. 2010a; Zihlman, Bolter,
and Boesch 2004). Interestingly, a recent analysis by Dean
(2010) using data from the histological growth record of
crowns and roots found that the predicted mean age of attainment for molar emergence in Pan M1 is 4.1 years, nearly
coincident with that reported in the wild P. troglodytes verus
To date, no reliable gingival emergence data exist for any

great ape species other than the common chimpanzee. This

deficiency may limit the accuracy and reliability of life history
reconstructions for fossil hominins, and so it is critical to
obtain M1 emergence data for both African and Asian apes
and to obtain these data from noncaptive animals. Recently,
reliable ages at M1 emergence were reported for orangutan
(Pongo pygmaeus pygmaeus, 4.6 years) and gorilla (Gorilla
gorilla gorilla, 3.8 years) obtained from wild-shot individuals
in museum osteology collections (Kelley and Schwartz 2010).
These data offer support for the likelihood of a later average
age at M1 emergence in free-living chimpanzees than in captive animals. Although limited, they also suggest that the average age at M1 emergence in noncaptive extant great apes
ranges from just younger than 4 years to just older than 4.5
years, or approximately 1 year later than the conventional
range reported as 3.03.5 years.
These new comparative data allow an evaluation of just
how consistent M1 emergence data are with the comparative
life histories of extant Asian and African apes and modern
humans. As can be seen from table 1, the new ape emergence
data fit well with expectations based on the comparative life
histories of living hominoids both in relation to one another
and in comparison with that of modern humans. Ages at M1
emergence between 3.8 and 4.6 years for great apes represent
65%80% of modern human emergence at 6 years
(6.2 0.8 years, mean 1 SD), signaling a close fit between
ages at attainment (or duration) of some key life history events
in great apes, as these life history attributes are also 60%
80% of the modern human value. As a side note, and by
comparison, gingival emergence ages of 3.03.5 in extant apes
would represent only 50%60% of the average modern human value. These new data reinforce earlier studies (Smith
1989) that identified dental eruption as a reliable means by
which to reconstruct life history profiles in extinct hominins.
Unfortunately, reliable ages at M1 emergence are available
for a very small number of fossils. It is difficult to extract
these data given the relatively few specimens that died during

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Current Anthropology Volume 53, Supplement 6, December 2012

the eruptive process of M1 and the difficulty in arranging for

these specimens to be subjected to the latest in noninvasive
imaging technology. Rather, utilizing the incremental growth
record contained within dental hard tissues, estimates of the
age at death for juveniles with mixed dentitions (both deciduous and permanent teeth present) near or subsequent to M1
gingival emergence do exist for a handful of australopiths and
early and later species of the genus Homo. These age-at-death
estimates can thus be used as the basis for estimating ages at
M1 emergence (table 2; Kelley and Schwartz 2012). All of the
australopith emergence age estimates resemble extant African
apes more than they do modern humans, and this also holds
for the earliest members of the genus Homo (H. erectus, H.
ergaster) for which there are reliable data.
An important way to evaluate these calculated ages at M1
emergence is in the context of its relationship with cranial
capacity. As mentioned earlier, cranial capacity and age at M1
emergence are strongly correlated in extant anthropoids
(Godfrey et al. 2001; Smith 1989), and both exhibit a high
correlation with aspects of life history. As is evident in figure
1, all of the great apes fall on or above the regression line,
with Gorilla having the relatively earliest age at M1 emergence,
as might be expected given its more folivorous diet (see Godfrey et al. 2001). Humans fall well below the regression line,
but it is most reasonable to attribute this to the tremendous
increase in cranial capacity in human populations during the
later Pleistocene, which has seemingly forced a partial dissociation between cranial capacity and age at M1 emergence.
Without this dissociation, M1 emergence (with a predicted
mean age of 7.1 years using the regression model versus the
actual modern human interpopulation mean of 5.8 years)
as well as the subsequent emergence of the more posterior

molars would be delayed perhaps beyond ages that are fully

compatible with weaning and the food-processing requirements of adolescent growth. All of the australopith and early
Homo specimens (and thus, perhaps, species) also fall below
the regression line, indicating that these species were also
characterized by a relatively advanced age at M1 emergence
for their brain size.
The total range of variation in modern human M1 emergence age is quite large, spanning almost 2.5 years (reviewed
in Liversidge 2003). Despite that, reconstructed emergence
ages for some of the early Homo species do not extend into
the range for modern humans. Importantly, we do not yet
know exactly how, if at all, certain life history attributes covary
with dental development within and among modern human
peoples or how to integrate these sorts of important intraspecific data with the interspecific trends discussed here.

The earliest species of Homo: the transitional hominins H.

habilis and H. rudolfensis. Based on detailed reconstructions
of dental chronologies, it seems that australopiths fall well
within the range of emergence ages known for captive and
wild chimps, and none falls within the ranges known for
modern humans. Thus, it is reasonable to conclude that early
hominins possessed a life history profile more similar to modern African apes than to modern humans. Dental maturation
data for the earliest members of Homo, however, are much
more limited. To date, dental maturational data for H. habilis
and H. rudolfensis consist of either reconstructed root formation times (OH 16, H. habilis) or crown formation times
(KNM-ER 1805E, H. habilis; KNM-ER 1590, KNM-ER 1802,
KNM-ER 1482B, H. rudolfensis; but see Anton 2012 as to

Table 2. Estimated ages (years) at death and M1 emergence in great apes, australopiths,
and Homo
Species (specimen)
Great apes:
Pongo pygmaeus pygmaeus
Gorilla gorilla beringei
Pan troglodytes verus
Australopithecus afarensis (LH 2)
Australopithecus africanus (Sts 24)
A. africanus (Taung 1)
Paranthropus robustus (SK 62)
P. robustus (SK 63)
Paranthropus boisei (KNM-ER 1820)
Homo erectus (Sangiran S7-37)
Homo ergaster (KNM-WT 15000)
Homo neanderthalensis (La Chaise)
Homo sapiens (Global)

Estimated age at death

Age at M1 emergence



5.8 (4.77.1)

Note. An asterisk indicates estimated values.

Sources. Data for australopiths compiled from Dean et al. (1993); Bromage and Dean (1985); Dean (1987);
Beynon and Dean (1988); Conroy and Vannier (1991a, 1991b); Lacruz, Ramirez Rozzi, and Bromage (2005);
and Kelley and Schwartz (2012). Data for species of Homo are combined from Dean et al. (2001); Liversidge
(2003); and Macchierelli et al. (2006).

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Schwartz Life History Evolution in Homo

Figure 1. Bivariate plot of ln M1 emergence age in months (y)

versus ln cranial capacity in cubic centimeters (x) for a sample
of anthropoids (taxa include Callithrix jacchus, Saguinas fuscicollis, Saguinas nigricollis, Cebus albifrons, Cebus apella, Saimiri
sciureus, Aotus trivirgatus, Trachypithecus cristata, Chlorocebus aethiops, Macaca fascicularis, Macaca mulatta, Macaca nemestrina,
Macaca fuscata, Papio cynocephalus, Papio anubis, Pan troglodytes,
Pongo pygmaeus, Gorilla gorilla, and Homo sapiens and are derived
primarily from Smith [1989] with supplemental data from recent
analyses, especially on great ape molar emergence; see references).
Summary statistics for the ordinary least squares regression are
as follows: y p 0.630x 0.072, 95% confidence interval (CI;
slope): 0.5550.704, R2 p 0.949 (P ! .001), and the 95% prediction intervals are indicated by the shaded region. Reduced major
axis regression: y p 0.646x 0.144, 95% CI (slope): 0.5720.721.
Ceboids are indicated by x, cercopithecoids are filled circles, great
apes are filled squares, and H. sapiens is the open diamond.
Australopith species are represented by triangles (from top left,
clockwise: SK 48, DIK-1-1, Taung 1, OH 5) and Homo erectus
(KNM-WT 15000 and Sangiran S7-37) by open squares.

species groups). Taken together, they suggest a dental developmental profile that was more modern apelike than modern
humanlike, providing some tantalizing evidence that neither
species likely possessed an extended period of childhood dependence (Dean 1995; Dean et al. 2001).
Later species of Homo. Given the extraordinarily complete and
well-preserved juvenile specimen KNM-WT 15000, we perhaps know more about overall growth and development, and
thus life history, in African H. erectus than any other early
hominin taxon. Based on the lack of fusion of the distal elbow
joint and the acetabulum in particular, KNM-WT 15000 was
given an age of death at ca. 13 years, or the early part of the
adolescent stage of growth (i.e., postpubertal; Ruff and Walker
1993). Interestingly, the mostly completed dentition (26 permanent teeth had emerged, all but the M3s and maxillary
canines) suggested an age at death of 10.2 years. This discord
of almost 3 years suggests a somewhat unique developmental
trajectory for H. erectus (Smith 2004). Equally interesting is
that based on a chimpanzee developmental standard, the state


of somatic development suggests an age at death of 77.5

years, while the state of dental development suggests an age
estimate of 7 years (Smith 1993). Each scenario carries vastly
different implications for the life history profile of H. erectus,
and dental developmental data hold the potential to resolve
the discrepancy.
Data on the pace of development derived from the histology
of enamel and dentine originally yielded an age-at-death estimate of closer to 8 than to 12 years of age (Dean et al. 2001).
A more extensive analysis, informed by several more years of
data on crown and root development in larger samples of
humans and fossil hominins and thus based on clearer estimates of certain dental growth parameters, has confirmed this
by suggesting that an age-at-death interval of 7.68.8 years is
most appropriate (Dean and Smith 2009). Furthermore, the
reconstructed age at M1 emergence based on inferences from
incremental growth data is 4.5 years, just slightly outside the
known ranges for extant captive (2.14.0 years) and wild (3.8
3.9 years) Pan and slightly earlier than that for modern humans (4.77.0 years). Given the relationship between brain
size and dental development (see fig. 1), a brain size estimate
for KNM-WT 15000 (810 cm3) generates a point prediction
for M1 emergence age of 5.2 years (95% prediction interval:
3.28.7 years), suggesting that H. erectus likely possessed rapid
maturation and was more modern apelike in overall growth
and development and certainly closer to the expectation for
an ape of comparable dental and skeletal maturity (ca. 7.5)
than for a human (ca. 1015) (Dean and Smith 2009:114).
Taken together, these data make it unlikely that all or even
some of the distinctive features of modern human life history
were present ca. 2.01.5 Ma.
Slower maturation translates into later ages for achieving
certain developmental milestones, such as the onset of puberty, adolescence, and so forth, and is intricately linked to
the ability of mothers to wean offspring earlier and shorten
interbirth intervals, thereby increasing fertility by having multiple, overlapping offspring. This stacking phenomenon is
only possible because of the lower energetic requirements for
fueling growth in slower maturing organisms compared with
the tremendous energetic burden mothers would face having
to subsidize the growth of fast-growing, multiple offspring
(Dean and Smith 2009; Gurven and Walker 2006). Available
data from modern hunter-gatherers suggest that humans follow the ecological risk aversion model (Janson and van Schaik
1993) that posits slow growth and the maintenance of small
sizes for longer periods of time, reduces feeding competition,
and translates into significant energetic savings. This energetic
savings is offset by a period of accelerated growth, known as
the adolescent growth spurt, which could be subsidized by
older individuals, highlighting the importance of older individuals in contributing to the care and feeding of children
(i.e., paternal care, grandmothering, etc.; e.g., Hawkes 2003;
Hawkes et al. 1998; Kaplan et al. 2000). Thus, the human
strategy can be seen as one where higher fertility is achieved
by emphasizing more slow-growing children with a later

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Current Anthropology Volume 53, Supplement 6, December 2012

growth spurt than few faster-growing ones (e.g., Bogin 1988,

1997; Gurven and Walker 2006; Leigh 2001; Leigh and Park
1998). The combined lack of evidence for protracted growth
and for an adolescent growth spurt (Anton and Leigh 2003;
Smith 1993; Smith and Tompkins 1995) in H. erectus and H.
ergaster supports the assertion that fully modern human life
histories had yet to evolve by 1.5 Ma.
Recently, several investigations have been launched to ascertain whether the modern human pattern of growth, development, and life history characterized Neanderthal (Homo
sapiens neanderthalensis) populations (e.g., Bayle et al. 2009a,
2009b, 2010; Coqueugniot and Hublin 2007; Guatelli-Steinberg 2009; Guatelli-Steinberg et al. 2005; Macchiarelli et al.
2006; Ponce de Leon et al. 2008; Ramirez-Rozzi and Bermudez
de Castro 2004; Smith et al. 2007b, 2007c, 2010b). A convincing argument is mounting that dentally, Neanderthals
may have experienced accelerated growth, which would in
turn suggest that a growth profile that included prolonged
dental development, and one that may have included most
or all of the other human life history attributes, did not evolve
until the appearance of H. sapiens. Unfortunately, very little
is known about dental development in taxa postdating H.
erectus and predating Neanderthals, but it would seem parsimonious to reconstruct dental development as being at least
as accelerated in middle Pleistocene taxa such as Homo antecessor and Homo heidelbergensis. Limited data are not inconsistent with this hypothesis: certain growth parameters of
anterior teeth in these species seem more similar to Neanderthals than to modern humans (Ramirez-Rozzi and Bermudez de Castro 2004).
Reconstructing life history in early Homo. Given the available
data, the full suite of modern human life history characteristics was most certainly not present at the base of the hominin
lineage, nor was it present at the emergence of the genus
Homo, but it likely occurred at some time during the middle
to late Pleistocene. That does not mean, however, that all
hominins before the appearance of H. sapiens possessed a life
history that was completely modern apelike despite the fact
that all of the included species of early Homo seem quite
accelerated dentally. There are several possible interpretations
of the relatively early M1 emergence ages of the hominins
(reviewed in detail in Kelley and Schwartz 2012). Aside from
scenarios regarding the manner in which these age estimates
were generated or how incremental growth is charted, there
are several ways to interpret these data.
Perhaps the ages at M1 emergence indicate the presence of
relatively rapid life histories in australopiths and early Homo
and thus are more similar to Gorilla than to Pan. This could
be related to dietary differences: lower-quality food such as
that preferred by primary folivores such as Gorilla gorilla beringei display more accelerated life history schedules and relatively precocious dental development than similar-size frugivores (Breuer et al. 2009; McFarlin et al. 2009).
While diet type and nutritional quality are still debated for

many hominin taxa, it is clear that members of early Homo

were committed terrestrial bipeds. Across primates, highly
terrestrial species possess more accelerated life history schedules than nonterrestrial species (Deaner, Barton, and van
Schaik 2003; Ross 1992, 1998), likely as a result of increased
extrinsic mortality in the form of predation. Early hominins
clearly succumbed to predation with some regularity, and the
signal of relatively rapid life history profiles in australopiths
and early Homo may be a direct outcome of selection operating on low survivorship by accelerating overall development
to reach sexual maturity at an earlier age. In that context,
dental development may be linked, perhaps through a mechanism such as pleiotropy, to overall somatic development and
is therefore similarly accelerated.
Scenarios to explain early Homo life history need not rely
on inferences based on diet or inferred mortality profiles
alone. The combination of low nutritive value of ingested
food with high rates of extrinsic mortality would have the
result of selecting for individuals within populations that
would grow at a slow rate and mature early, producing adults
of small stature such as those found within contemporary
hunter-gatherers of the rainforests (Kuzawa and Bragg 2012).
High mortality on its own would also select for faster growth
and early maturation, though at normal adult sizes. In this
context, it is interesting to speculate that populations experiencing increases in nutritional quality along with high extrinsic mortality should grow faster to reach maturation earlier at larger adult sizes compared with ancestral populations
with low nutritional quality and high mortality. As shown by
McHenry (1992, 1994), Holliday (2012), and Pontzer (2012),
there is good evidence for a general trend of an increase in
body mass from Australopithecus to Homo (also see Ruff 2002
and references therein). If rates of extrinsic mortality were
held constant, this could imply a transition from hominin
populations with low nutritional quality to those with higher
nutritional quality. This is not inconsistent with recent dietary
reconstructions of early Homo, wherein H. erectus diets were
reconstructed as far more varied than in preceding H. habilis
(Ungar 2012; Ungar et al. 2011), perhaps suggesting that a
broadening of the resource base was an important contributing factor to the evolution of larger body sizes and perhaps
ultimately to shifts in life history. Interestingly, researchers
have speculated on whether similar conditions may have led
to selection for accelerated growth in Neanderthals and include scenarios where they experienced serious nutritional
stress linked with elevated rates of young adult mortality (Oglivie, Curran, and Trinkaus 1989; Pettitt 2000; Trinkaus 1995;
Trinkaus and Tompkins 1990). According to life history theory, both of these factors in combination would have the
effect of selecting for rapid and early maturation.
A second possible interpretation is that reconstructions of
the pace of life history are indeed more accurately reflected
by brain size, and so the scheduling of at least some life history
attributes occurred at a slower pace than would be inferred
from simply evaluating M1 emergence ages alone. In other

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Schwartz Life History Evolution in Homo

words, different life history parameters could be dissociated

from one another so that selection could act on them individually or as smaller developmental subsets. It is critical to
bear in mind that dissociations among developmental systemsthe scheduling of dental events versus that of reproductive events, for instancemay not be as tightly linked
across closely related species as they appear to be across hominoid genera. In fact, the clear associations between dental
development and life history variables as well as among life
history variables that exist when examined across primates as
a whole are known to break down when examined across
closely related species. The general trend for primates holds
that larger species take longer to grow and reach sexual maturity; however, data on hylobatids suggest that it is the
smaller-bodied Hylobates, not the larger Syndactylus that possesses a later age at sexual maturity and a longer life span
(Dirks and Bowman 2007). That same study also demonstrated that the age at molar emergence is not correlated with
age at menarche or the age at first reproduction in exactly
the same way in both cercopithecoids and hylobatids. On an
even broader scale, certain strepsirrhines buck the primate
trend as a means of solving the problem of how to cope with
highly seasonal and unpredictable environments. Compared
with lemurids, large-bodied indriids exhibit extreme dental
precocity while maintaining slower rates of somatic growth,
thus allowing for relatively earlier weaning as a strategy to
help reduce the metabolic burden on mothers (e.g., Godfrey
et al. 2001). These are just a few examples of how an understanding of developmental dissociations, or modularity
(sensu Leigh and Blomquist 2007), urges some caution in
directly linking dental development and the scheduling of life
history. An exciting avenue of future study would be to document the extent to which dental developmental profiles are
correlated with life history attributes within populations of
modern humans, an endeavor made easier these days by the
ever-expanding data on the chronology of developing teeth
in worldwide populations (see Liversidge 2003). This may
ultimately yield clearer and more refined insights into the
finer details of life history evolution across hominin species
and especially within more closely related and even conspecific
hominin populations. At the same time, these analyses may
unveil the extent to which the human life history package is
dissociable and allow us to begin to develop models of how
shifting patterns of ecology, subsistence, demography, diet,
and so forth, throughout the Homo lineage may have resulted
in a more piecemeal acquisition of the fully modern human
life history profile. Some new data suggest that this may be
an interesting way forward. Very recently, DeSilva (2011) posited that infant : mother mass ratios of 5% (generally 6%
in modern humans; cf. 3% in extant chimpanzees) were already present in early australopiths. That author suggests that
more modern humanlike birthing strategies, the adoption of
alloparenting behavior, and so forth, may have been present
13 Ma, well before the origin of Homo. On the other hand,
other aspects of the human life history package such as life


span, for example, may be a more recent acquisition. New

data on adult mortality patterns suggest similar population
demographics for late archaic (Neanderthals) and early modern (Middle and earlier Upper Paleolithic) humans, an observation that weakens support for some sort of demographic
advantage related to enhanced longevity for early modern
humans (Trinkaus 2011).

Future Directions
Discoveries of new infant and subadult fossils along with
advances in noninvasive imaging and analytical methods are
providing opportunities to probe further the fossil record of
human growth and development. For instance, it is likely that
the age at which important life history events, such as weaning, will be assessable directly from the fossil record. The
timing of weaning is a key life event for both mother and
offspring, and analyses of life history variation as it relates to
weaning across Primates provide one example of the selective
basis of these sorts of developmental dissociations. Within
Malagasy prosimians, selection has acted to accelerate weaning
and dental development but has delayed the age at first reproduction (Godfrey et al. 2001; Richard et al. 2002; Schwartz
et al. 2002). It has been suggested that some australopiths
show rapid deciduous tooth wear, which was taken as evidence
suggestive of relatively early weaning (Aiello, Montgomery,
and Dean 1991; Dean 2006, 2010). It may now be possible
to retrieve direct evidence for reconstructing weaning age and
shifts in energy provisioning for offspring through the evolution of Homo. Across Primates, weaning is closely tied in
time to the emergence of M1. However, human life history
is characterized by relatively early weaning followed by a prolonged period of postweaning dependency. The advancement
of weaning age throughout human evolution coupled with
rapid and early brain growth implies a shift in how the rising
energetic demands of offspring are met: initially, energetic
costs are subsidized completely by the mother but then by
members of the social group through the provisioning of
weanlings (Humphrey 2010). This pattern of high maternal
investment and alloparenting behavior is important because
it is a clear determinant of birth spacing. Such a stratagem
has also been suggested to characterize the earliest members
of Homo (Aiello and Wells 2002). Recently, models have been
proposed to establish the precise age at which organisms were
weaned by accessing the isotopic record, in particular, strontium : calcium ratios (Sr/Ca) preserved within dental hard
tissues (e.g., Humphrey et al. 2008a, 2008b). Charting shifts
in this ratio throughout the developmental period associated
with early tooth tissue formation is one exciting way of reconstructing infant diet as well as tracking dietary transitions
throughout early life. If early Homo and later-occurring archaic Homo populations were indeed characterized by relatively early weaning, then analyses of the isotopic chemistry
throughout enamel development hold the potential to verify

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Current Anthropology Volume 53, Supplement 6, December 2012

Figure 2. Bivariate plot of bite point positions for all teeth and masticatory muscle positions relative to the temporomandibular
joint (TMJ; y-axis) versus age (x-axis) in a cross-sectional ontogenetic series of modern humans (Nubian archaeological sample
housed at University of Colorado, Boulder). Bite points are measured as the distance of each tooth from the TMJ, measured in the
occlusal plane, and are illustrated by the two vertical arrows (left) indicating bite points for the dm1 and dm2. Masticatory muscle
position (for the superficial and deep masseters, temporalis, and medial pterygoid muscles) is defined as the point where each
muscles resultant force crosses the occlusal plane relative to the position of the TMJ. Primary masticatory adductor position and
orientation are based on a series of 2-D and 3-D linear and angular measurements and, taken together, capture what has been
termed masticatory system configuration (see Spencer 1995, 1999). Note the consistent position of the dm2 (small white sphere)
and the permanent M1, M2, and M3 (large white spheres) anterior to the masticatory muscles (i.e., above the white dotted line) at
the time of emergence. Also note the differing rates of anterior growth of the dental arcade and masticatory muscles (as indicated
by the slopes of second-order polynomials); space for emerging molars is a product of these different growth rates. A color version
of this figure appears in the online edition of Current Anthropology.

this with direct evidence for the age at weaning from the fossil
record itself.
While continued probing of the fossil record to establish
more precise demographic and maturational profiles holds
the potential to yield key details in the evolution of human
life history, another interesting way forward is to attempt to
understand the processes that lie behind the slightly dissimilar
patterns in dental development, and thus inferred life history
profiles, among hominins. A host of studies have advanced
our understanding of how dental developmental variation
intersects with primate life history variation, but surprisingly
little is known about the precise mechanism that governs,
modulates, regulates, constrains, and so forth, the timing of
molar eruption and as such the underlying processes that
regulate these temporal events are largely unknown.
Recently, it was postulated that a set of biomechanical constraints regulates masticatory system configuration throughout ontogeny and therefore modulates the position and ultimately the timing of emerging molars within developing
faces (Spencer and Schwartz 2008). Based on an ontogenetic
sample of modern human crania, it seems that successive

molar emergence events are predominantly a function of rates

of facial growth such that successive molars (deciduous and
permanent) emerge at a consistent position relative to the
masticatory musculature (fig. 2). Moreover, there appears to
be a consistent position of newly erupted molars (deciduous
and permanent) relative to the temporomandibular joint
(TMJ) that in an archaeological sample of modern humans
is 40 mm (fig. 3). This ontogenetic arrangement ensures
that there is a biomechanically optimal location for molar
eruption anterior to the net vector of masticatory muscle
effort (note position of white dots relative to dotted white
line, fig. 2) and that each successive molar erupts into this
optimal position only at a point during ontogeny when it is
vacated as a result of facial growth. This all suggests covariation in rates of facial growth (indicated by the slope of the
first part of the curve for each molar, fig. 2), the position of
the masticatory musculature, the spatial position of an erupting molar, and the timing of molar emergence.
The validity of this biomechanical model for modulating
the timing of molar emergence has not been fully established.
Indeed, whether this constraint operates across hominoids is

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Schwartz Life History Evolution in Homo

Figure 3. Consistent position of newly erupted molars relative

to the temporomandibular joint (TMJ) as indicated by the length
of the horizontal white line. The dot on the left of the line marks
the position of the TMJ in lateral view, while the dot on the right
marks the position of the newly emerged molar. Note that the
line is the same length for individual human crania at the time
of M1 emergence (top), M2 emergence (middle), and M3 emergence (bottom). This is illustrated graphically by the consistent
width of the shaded rectangle. While the absolute distance is
different, the same pattern of spatial consistency in molar position holds for an ontogenetic sample of wild-living Pan (see
text). A color version of this figure appears in the online edition.

not yet clear, but preliminary data on an ontogenetic series

of western African chimpanzees (Pan troglodytes verus; n p
37) are striking: like the modern human sample, no significant
differences are present between the position of each successively emerging molar and the TMJ (Kruskal-Wallis, df p 2,
P p .6215) despite the fact that, unsurprisingly, the absolute
distance is slightly greater in this sample (48 mm).
A fuller mapping of the influence of these biomechanical
constraints onto variation in the ontogeny of masticatory
muscle position and explicitly testing hypotheses that integrate craniofacial architecture, muscle function, facial growth,
and molar emergence across hominoids is currently underway. These are critical comparative data because selection for
accelerated molar eruption, as seems to characterize early
Homo relative to modern humans, should require a similar
acceleration in facial growth. The delay in molar emergence


ages in modern humans may therefore result from reduced

rates of facial growth and extreme orthognathy, perhaps in
combination with a developmental delay in facial growth. A
later initiation of facial growth would result in a delay in
clearance of a biomechanically appropriate space available
for molar emergence.
In the absence of good ontogenetic data on craniofacial
growth in early Homo, it is useful to evaluate how well this
biomechanical model integrates craniofacial morphology with
data on developmental rates within other members of the
Homo lineage. This model predicts the advanced molar emergence schedules of Neanderthals to be related to a combination of their higher degree of midfacial prognathism and
accelerated cranial growth trajectories. Some evidence in support of faster rates of craniofacial growth (Ponce de Leon and
Zollikofer 2001; Ponce de Leon et al. 2008) and dental development (Smith et al. 2007c, 2010b) exist. Thus, selection
may have accelerated age at weaning and thus ecological independence by advancing rates of cranial growth in a manner
that permitted a more accelerated molar development/eruption schedule, which would represent an effective life history
strategy under conditions of high extrinsic mortality. More
thorough explorations of how the timing of molar development and emergence may result from the complex spatial
interplay between growing faces and expanding neurocrania
hold tremendous potential for illuminating the underlying
mechanism that regulates molar emergence and, ultimately,
for unlocking the linkages between dental development and
life history events.
Finally, it is generally agreed that the earliest species of
Homo evolved from Australopithecus, either in East or South
Africa. The cranium from Bouri, Ethiopia, at 2.5 Ma attributed to Australopithecus garhi (Asfaw et al. 1999) and the
associated cranial and postcranial material for the newly announced Australopithecus sediba from Malapa, South Africa,
at 1.9 Ma (Berger et al. 2010) may therefore provide important
clues for helping to better understand the complex interplay
among morphological, ecological, reproductive, and behavioral adaptations that underlies the transition to and ultimate
success of the genus Homo.

I would like to thank Leslie Aiello and Susan Anton for their
invitation to participate in the Wenner-Gren workshop, all of
the conference participants for their stimulating and thoughtful discussions throughout the conference, and the two anonymous reviewers for their input and constructive comments
on this manuscript. The ideas and work laid out here are the
results of many discussions and ongoing collaborations, especially with Chris Dean, Jay Kelley, Tanya Smith, Debbie
Guatelli-Steinberg, Laurie Godfrey, Wendy Dirks, Bill Kimbel,
Mark Spencer, Terry Ritzman, Kierstin Catlett, and Halszka

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Current Anthropology Volume 53, Supplement 6, December 2012

Glowacka. I am grateful to the Institute of Human Origins

at Arizona State University for their generous support.

References Cited
Aiello, Leslie C., Carey Montgomery, and M. Christopher Dean. 1991. The
natural history of deciduous tooth attrition in hominoids. Journal of Human
Evolution 21:397412.
Aiello, Leslie C., and Jonathan C. K. Wells. 2002. Energetics and the evolution
of the genus Homo. Annual Review of Anthropology 31:323338.
Alemseged, Zeresenay, Fred Spoor, William H. Kimbel, Rene Bobe, Denis
Geraads, Denne Reed, and Jonathan G. Wynn. 2006. A juvenile early hominin skeleton from Dikika, Ethiopia. Nature 443:296301.
Anemone, Robert L., Mark P. Mooney, and Michael I. Siegel. 1996. Longitudinal study of dental development in chimpanzees of known chronological age: implications for understanding the age at death of Plio-Pleistocene
hominids. American Journal of Physical Anthropology 99:119133.
Anton, Susan C. 2012. Early Homo: who, when, and where. Current Anthropology 53(suppl. 6):S278S298.
Anton, Susan C., and Steven R. Leigh. 2003. Growth and life history in Homo
erectus. In Patterns of growth and development in the genus Homo. Jennifer
L. Thompson, Gail E. Krovitz, and Andrew J. Nelson, eds. Pp. 219245.
Cambridge: Cambridge University Press.
Asfaw, Berhane, Tim White, C. Owen Lovejoy, Bruce Latimer, Scott Simpson,
and Gen Suwa. 1999. Australopithecus garhi: a new species of early hominin
from Ethiopia. Science 284:629635.
Bayle, Priscilla, Jose Braga, Arnaud Mazurier, and Roberto Macchiarelli. 2009a.
Brief communication: high-resolution assessment of the dental developmental pattern and characterization of tooth tissue proportions in the late
Upper Paleolithic child from La Madeleine, France. American Journal of
Physical Anthropology 138:493498.
. 2009b. Dental developmental pattern of the Neanderthal child from
Roc de Marsal: a high resolution 3D analysis. Journal of Human Evolution
Bayle, Priscilla, Roberto Macchiarelli, Erik Trinkaus, Cidalia Duarte, Arnaud
Mazurier, and Joao Zilhao. 2010. Dental maturational sequence and dental
tissue proportions in the early Upper Paleolithic child from Abrigo do Lagar
Velho, Portugal. Proceedings of the National Academy of Sciences of the USA
Berger, Lee R., Darryl J. de Ruiter, Steven E. Churchill, Peter Schmid, Kristian
J. Carlson, Paul H. G. M. Dirks, and Job M. Kibii. 2010. Australopithecus
sediba: a new species of Homo-like australopith from South Africa. Science
Beynon, A. David, C. Barry Clayton, Fernando V. Ramirez Rozzi, and Donald
J. Reid. 1998. Radiographic and histological methodologies in estimating
the chronology of crown development in some modern humans and great
apes: a review with some applications for studies on juvenile hominids.
Journal of Human Evolution 35:351370.
Beynon, A. David, and M. Christopher Dean. 1988. Distinct dental development patterns in early fossil hominids. Nature 335:509514.
Beynon, A. David, M. Christopher Dean, and Donald J. Reid. 1991. Histological study on the chronology of the developing dentition in gorilla and
orangutan. American Journal of Physical Anthropology 86:189203.
Bogin, Barry. 1988. Patterns of human growth. Cambridge: Cambridge University Press.
. 1997. Evolutionary hypotheses for human childhood. Yearbook of
Physical Anthropology 104:6390.
Bogin, Barry, and B. Holly Smith. 2000. Evolution of the human life cycle.
In Human biology: an evolutionary and biocultural perspective. Sarah Stinson,
Barry Bogin, Rebecca Huss-Ashmore, and Dennis ORourke, eds. Pp. 377
424. New York: Wiley-Liss.
Boyde, Alan. 1963. Estimation of age at death of young human skeletal remains
from incremental lines in dental enamel. In Third international meeting in
forensic immunology, medicine, pathology and toxicology (London, April 16
24th, 1963): plenary session 2A. Pp. 3646. Amsterdam: Exerpta Medica.
. 1964. The structure and development of mammalian enamel. PhD
thesis, University of London.
Bradley, Brenda J. 2008. Reconstructing phylogenies and phenotypes: a molecular view of human evolution. Journal of Anatomy 212:337353.
Breuer, Thomas, Mireille B. Hockemba, Claudia Olejniczak, Richard J. Parnell,
and Emma J. Stokes. 2009. Physical maturation, life-history classes and age

estimates of free-ranging western gorillas: insights from Mbeli Bai, Republic

of Congo. American Journal of Primatology 71:106119.
Bromage, Timothy G., and M. Christopher Dean. 1985. Re-evaluation of the
age at death of immature fossil hominids. Nature 317:525527.
Conroy, Glenn C., and Kevin L. Kuykendall. 1995. Paleopediatrics: or when
did human infants really become human? American Journal of Physical
Anthropology 98:121131.
Conroy, Glenn C., and C. James Mahoney. 1991. Mixed longitudinal study
of dental emergence in the chimpanzee, Pan troglodytes (Primates, Pongidae). American Journal of Physical Anthropology 86:243254
Conroy, Glenn C., and Michael W. Vannier. 1991a. Dental development in
South African australopithecines. 1. Problems of pattern and chronology.
American Journal of Physical Anthropology 86:121136.
. 1991b. Dental development in South African australopithecines. 2.
Dental stage assessment. American Journal of Physical Anthropology 86:137
Coqueugniot, Hele`ne, and Jean-Jacques Hublin. 2007. Endocranial volume
and brain growth in immature Neanderthals. Periodicum Biologorum 109:
Dean, M. Christopher. 1987. The dental developmental status of six East
African juvenile fossil hominids. Journal of Human Evolution 16:197213.
. 1995. The nature and periodicity of incremental lines in the primate
dentition and their relationship to periradicular bands in OH 16 (Homo
habilis). In Aspects of dental biology: paleontology, anthropology, and evolution.
Jacopo Moggi-Cecchi, ed. Pp. 239265. Florence: International Institute for
the Study of Man.
. 2006. Tooth microstructure tracks the pace of human life history.
Proceedings of the Royal Society B: Biological Sciences 273:27992802.
. 2010. Retrieving chronological age from dental remains of early fossil
hominins to reconstruct human growth in the past. Philosophical Transactions of the Royal Society B: Biological Sciences 365:33973410.
Dean, M. Christopher, A. David Beynon, J. Francis Thackeray, and Gabriele
A. Macho. 1993. Histological reconstruction of dental developmental and
age at death of a juvenile Paranthropus robustus specimen, SK 63, from
Swartkrans, South Africa. American Journal of Physical Anthropology 91:
Dean, M. Christopher, Meave G. Leakey, Donald J. Reid, Friedemann Schrenk,
Gary T. Schwartz, Christopher Stringer, and Alan C. Walker. 2001. Growth
processes in teeth distinguish modern humans from Homo erectus and
earlier hominins. Nature 414:628631.
Dean, M. Christopher, and B. Holly Smith. 2009. Growth and development
of the Nariokotome youth, KNM-WT 15000. In The first humans: origins
and evolution of the genus Homo. Frederick E. Grine, John C. Fleagle, and
Richard E. Leakey, eds. Pp. 101120. New York: Springer.
Deaner, Robert O., Robert A. Barton, and Carel P. van Schaik. 2003. Primate
brains and life history: renewing the connection. In Primate life histories
and socioecology. Peter M. Kappeler and Michael E. Pereira, eds. Pp. 233
265. Chicago: University of Chicago Press.
deMenocal, Peter B. 1995. Plio-Pleistocene African climate. Science 270:53
DeSilva, Jeremy M. 2011. A shift toward birthing relatively large infants early
in human evolution. Proceedings of the National Academy of Sciences of the
USA 108:10221027.
Dirks, Wendy. 1998. Histological reconstruction of dental development and
age of death in a juvenile gibbon (Hylobates lar). Journal of Human Evolution
. 2003. Effect of diet on dental development in four catarrhine primates. American Journal of Primatology 61:2940.
Dirks, Wendy, and Jacqui E. Bowman. 2007. Life history theory and dental
development in four species of catarrhine primates. Journal of Human Evolution 53:309320.
Dirks, Wendy, Louise T. Humphrey, M. Christopher Dean, and Teresa E.
Jeffries. 2010. The relationship of accentuated lines in enamel to weaning
stress in juvenile baboons (Papio hamadryas anubis). Folia Primatologica
Godfrey, Laurie R., Andrew J. Petto, and Michael R. Sutherland. 2002. Dental
ontogeny and life-history strategies: the case of the giant extinct indrioids
of Madagascar. In Reconstructing behavior in the primate fossil record. J.
Michael Plavcan, Richard F. Kay, William L. Jungers, and Carel P. van Schaik,
eds. Pp. 113157. New York: Kluwer.
Godfrey, Laurie R., Karen E. Samonds, William L. Jungers, and Michael R.
Sutherland. 2001. Teeth, brains, and primate life histories. American Journal
of Physical Anthropology 114:192214.

This content downloaded from on Tue, 18 Nov 2014 10:01:21 AM

All use subject to JSTOR Terms and Conditions

Schwartz Life History Evolution in Homo

Godfrey, Laurie R., Karen E. Samonds, Patricia C. Wright, and Stephen J.
King. 2005. Schultzs unruly rule: dental developmental sequences and
schedules in small-bodied, folivorous lemurs. Folia Primatologica 6:7799.
Guatelli-Steinberg, Debbie. 2009. Recent studies of dental development in
Neanderthals: implications for Neanderthal life histories. Evolutionary Anthropology 18:920.
Guatelli-Steinberg, Debbie, Donald J. Reid, Thomas A. Bishop, and Clark
Spencer Larsen. 2005. Anterior tooth growth periods in Neanderthals were
comparable to those of modern humans. Proceedings of the National Academy of Sciences of the USA 102:1419714202.
Gurven, Michael, and Robert Walker. 2006. Energetic demands of multiple
dependents and the evolution of slow human growth. Proceedings of the
Royal Society B: Biological Sciences 273:835841.
Hamada, Yuzuru, Toshifumi Udono, Migaku Teramoto, and Tsutomu Sugawara. 1996. The growth pattern of chimpanzees: somatic growth and reproductive maturation in Pan troglodytes. Primates 37:279295.
Hawkes, Kristen. 2003. Grandmothers and the evolution of human longevity.
American Journal of Human Biology 15:380400.
Hawkes, Kristen, James F. OConnell, Nicholas G. Blurton Jones, Helen Alvarez, and Eric L. Charnov. 1998. Grandmothering, menopause, and the
evolution of human life histories. Proceedings of the National Academy of
Sciences of the USA 95:13361339.
Holliday, Trenton W. 2012. Body size, body shape, and the circumscription
of the genus Homo. Current Anthropology 53(suppl. 6):S330S345.
Humphrey, Louise T. 2010. Weaning behavior in human evolution. Seminars
in Cellular and Developmental Biology 21:453461.
Humphrey, Louise T., M. Christopher Dean, Teresa E. Jeffries, and Malcom
Penn. 2008a. Unlocking evidence of early diet from tooth enamel. Proceedings of the National Academy of Sciences of the USA 105:68346839.
Humphrey, Louise T., Wendy Dirks, M. Christopher Dean, and Teresa E.
Jeffries. 2008b. Tracking dietary transitions in weanling baboons using strontium/calcium ratios in enamel. Folia Primatologica 79:197212.
Janson, Charles H., and Carel P. van Schaik. 1993. Ecological risk aversion in
juvenile primates: slow and steady wins the race. In Juvenile primates: life
history, development and behavior. Michael Pereira and Lynn Fairbanks, eds.
Pp. 5776. New York: Oxford University Press.
Kaplan, Hillard, Kim Hill, Jane Lancaster, and Ana Magdalena Hurtado. 2000.
A theory of human life history evolution: diet, intelligence, and longevity.
Evolutionary Anthropology 9:156184.
Kelley, Jay, and Gary T. Schwartz. 2010. Dental development and life history
in living African and Asian apes. Proceedings of the National Academy of
Sciences of the USA 107:10351040.
. 2012. Life-history inference in the early hominins Australopithecus
and Paranthropus. International Journal of Primatology 33:13321363.
Kimbel, William H. 2009. The origin of Homo. In The first humans: origin
and early evolution of the genus Homo. Frederick E. Grine, John G. Fleagle,
and Richard E. Leakey, eds. Pp. 3137. New York: Springer.
Kimbel, William H., Don C. Johanson, and Yoel Rak. 1997. Systematic assessment of a maxilla of Homo from Hadar, Ethiopia. American Journal of
Physical Anthropology 103:235262.
Kimura, Tasuku, and Yuzuru Hamada. 1996. Growth of wild and laboratory
born chimpanzees. Primates 37:237251.
Knott, Cheryl D., Melissa Emery Thompson, and Serge A. Wich. 2009. The
ecology of reproduction in wild orangutans. In Orangutans: geographic variation in behavioral ecology and conservation. Serge A. Wich, S. Suci UtamiAtmoko, Tatang Mitra Setia, and Carel P. van Schaik, eds. Pp. 171188.
Oxford: Oxford University Press.
Kuykendall, Kevin L., C. James Mahoney, and Glenn C. Conroy. 1992. Probit
and survival analysis of tooth emergence ages in a mixed-longitudinal sample of chimpanzees (Pan troglodytes). American Journal of Physical Anthropology 89:379399.
Kuzawa, Christopher W., and Jared M. Bragg. 2012. Plasticity in human life
history strategy: implications for contemporary human variation and the
evolution of genus Homo. Current Anthropology 53(suppl. 6):S369S382.
Lacruz, Rodrigo S., Fernando Ramirez Rozzi, and Timothy G. Bromage. 2005.
Dental enamel hypoplasia, age at death, and weaning in the Taung child.
South African Journal of Science 101:567569.
Leakey, Louis S. B., Phillip V. Tobias, and John Napier. 1964. A new species
of the genus Homo from Olduvai Gorge. Nature 202:79.
Leigh, Steven R. 2001. Evolution of human growth. Evolutionary Anthropology
Leigh, Steven R., and Gregory E. Blomquist. 2007. Life history. In Primates
in perspective. Christina J. Campbell, Agustn Fuentes, Katherine C.

MacKinnon, Melissa Panger, and Simon K. Bearder, eds. Pp. 396407. New
York: Oxford University Press.
Leigh, Steven R., and Paul B. Park. 1998. Evolution of human growth prolongation. American Journal of Physical Anthropology 107:331350.
Liversidge, Helen. 2003. Variation in modern human dental development. In
Patterns of growth and development in the genus Homo. Jennifer L. Thompson, Gail E. Krovitz, and Andrew J. Nelson, eds. Pp. 73113. Cambridge:
Cambridge University Press.
Macchiarelli, Roberto, Luca Bondioli, Andre Debenath, Arnaud Mazurier,
Jean-Francois Tournepiche, Wendy Birch, and M. Christopher Dean. 2006.
How Neanderthal molar teeth grew. Nature 444:748751.
Mann, Alan E. 1975. Some paleodemographic aspects of the South African Australopithecines. Philadelphia: University of Pennsylvania Press.
McFarlin, Shannon C., Timothy G. Bromage, Alecia A. Lilly, Michael R. Cranfield, Stephen P. Nawrocki, Amandine Eriksen, David Hunt, Albert
Ndacyayisenga, Celestin Kanimba Misago, and Anthony Mudakikwa. 2009.
Recovery and preservation of a mountain gorilla skeletal resource in
Rwanda. American Journal of Physical Anthropology 138(suppl.):257258.
McHenry, Henry M. 1992. Body size and proportions in early hominids.
American Journal of Physical Anthropology 87:407431.
. 1994. Behavioral ecological implications of early hominid body size.
Journal of Human Evolution 27:7787.
McPherron, Shannon P., Zeresenay Alemseged, Curtis W. Marean, Jonathan
G. Wynn, Denne Reed, Denis Geraads, Rene Bobe, and Hamdallah A.
Bearat. 2010. Evidence for stone-tool-assisted consumption of animal tissues
before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857860.
Migliano, Andrea Bamberg, and Myrtille Guillon. 2012. The effects of mortality, subsistence, and ecology on human adult height and implications for
Homo evolution. Current Anthropology 53(suppl. 6):S359S368.
Nettle, Daniel, David A. Coall, and Thomas E. Dickins. 2010. Early-life conditions and age at first pregnancy in British women. Proceedings of the Royal
Society B: Biological Sciences 278:17211727.
Nissen, Henry W., and Austin H. Riesen. 1945. The deciduous dentition of
chimpanzee. Growth 9:265274.
. 1964. The eruption of the permanent dentition of chimpanzee. American Journal of Physical Anthropology 22:285294.
Ogilvie, Marsha D., Bryan K. Curran, and Erik Trinkaus. 1989. Prevalence
and patterning of dental enamel hypoplasia among the Neanderthals. American Journal of Physical Anthropology 79:2541.
Pettitt, Paul B. 2000. Neanderthal lifecycles: developmental and social phases
in the lives of the last archaics. World Archaeology 31:351366.
Ponce de Leon, Marcia S., Lubov Golovanova, Vladimir Doronichev, Galina
Romanova, Takeru Akazawa, Osamu Kondo, Hajime Ishida, and Christoph
P. E. Zollikofer. 2008. Neanderthal brain size at birth provides insights into
the evolution of human life history. Proceedings of the National Academy of
Sciences of the USA 105:1376413768.
Ponce de Leon, Marcia S., and Christoph P. Zollikofer. 2001. Neanderthal
cranial ontogeny and its implications for late hominid diversity. Nature 412:
Pontzer, Herman. 2012. Ecological energetics in early Homo. Current Anthropology 53(suppl. 6):S346S358.
Potts, Richard. 1996. Evolution and climate variability. Science 273:922923.
. 2012. Environmental and behavioral evidence pertaining to the evolution of early Homo. Current Anthropology 53(suppl. 6):S299S317.
Rak, Yoel, Avishag Ginzburg, and Eli Geffen. 2007. Gorilla-like anatomy on
Australopithecus afarensis mandibles suggests Au. afarensis links to robust
australopiths. Proceedings of the National Academy of Sciences of the USA
Ramirez-Rozzi, Fernando V., and Jose Maria Bermudez de Castro. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936939.
Reid, Donald J., Gary T. Schwartz, Malkanthi S. Chandrasekera, and M. Christopher Dean. 1998. A histological reconstruction of dental development in
the common chimpanzee, Pan troglodytes. Journal of Human Evolution 35:
Richard, Alison F., Robert E. Dewar, Marion Schwartz, and Joelisoa Ratsirarson. 2002. Life in the slow lane? demography and life histories of male
and female sifaka (Propithecus verreauxi verreauxi). Journal of Zoology 256:
Robson, Shannen L., and Bernard A. Wood. 2008. Hominin life history: reconstruction and evolution. Journal of Anatomy 212:394425.
Roff, Derek A. 2002. Life history evolution. Sunderland, MA: Sinauer.
Ross, Caroline. 1992. Environmental correlates of the intrinsic rate of natural
increase in primates. Oecologia 90:383390.

This content downloaded from on Tue, 18 Nov 2014 10:01:21 AM

All use subject to JSTOR Terms and Conditions


Current Anthropology Volume 53, Supplement 6, December 2012

. 1998. Primate life histories. Evolutionary Anthropology 6:5463.

Ruff, Christopher B. 2002. Variation in human body size and shape. Annual
Review of Anthropology 31:211232.
Ruff, Christopher B., and Alan C. Walker. 1993. Body size and body shape.
In The Nariokotome Homo erectus skeleton. Richard E. F. Leakey and Alan
C. Walker, eds. Pp. 234265. Cambridge, MA: Harvard University Press.
Ruvolo, Maryellen. 1994. Molecular evolutionary processes and conflicting
gene trees: the hominoid case. American Journal of Physical Anthropology
Sacher, George A. 1959. Relationship of lifespan to brain weight and body
weight in mammals. In The lifespan of animals. G. E. W. Wolstenholme and
Meave OConnor, eds. Pp. 115133. CIBA Foundation Colloquia on Aging,
vol. 5. London: Churchill.
. 1975. Maturation and longevity in relation to cranial capacity in
hominid evolution. In Primate functional morphology and evolution. Russell
H. Tuttle, ed. Pp. 417441. The Hague: Mouton.
. 1978. Longevity, aging, and death: an evolutionary perspective. Gerontology 18:112119.
Sacher, George A., and Everett F. Staffeldt. 1974. Relation of gestation time
to brain weight for placental mammals: implications for the theory of
vertebrate growth. American Naturalist 108:593616.
Schultz, Adolph H. 1935. Eruption and decay of the permanent teeth in
primates. American Journal of Physical Anthropology 19:489581.
. 1940. Growth and development of the chimpanzee. Contributions to
Embryology 28:163.
. 1949. Ontogenetic specializations of man. Archiv der Julius KlausStiftung fur Vererbungsforschung, Sozialanthropologie und Rassenhygiene 24:
. 1960. Age changes in primates and their modification in man. In
Human growth. James M. Tanner, ed. Pp. 120. Oxford: Pergamon.
Schwartz, Gary T., and M. Christopher Dean. 2000. Interpreting the hominid
dentition: ontogenetic and phylogenetic aspects. In Development, growth
and evolution: implications for the study of the hominid skeleton. Paul
OHiggins and Martin J. Cohen, eds. Pp. 207233. London: Academic Press.
Schwartz, Gary T., Patrick Mahoney, Laurie R. Godfrey, Frank P. Cuozzo,
William L. Jungers, and Gise`le F. N. Randria. 2005. Dental development in
Megaladapis edwardsi (Primates, Lemuriformes): implications for understanding life history variation in subfossil lemurs. Journal of Human Evolution 49:702721.
Schwartz, Gary T., Karen E. Samonds, Laurie R. Godfrey, William L. Jungers,
and Elwyn L. Simons. 2002. Dental microstructure and life history in subfossil Malagasy lemurs. Proceedings of the National Academy of Sciences of
the USA 99:61246129.
Smith, B. Holly. 1986. Dental development in Australopithecus and early Homo.
Nature 323:327330.
. 1989. Dental development as a measure of life history variation in
primates. Evolution 43:683688.
. 1993. The physiological age of KNM-WT 15000. In The Nariokotome
Homo erectus skeleton. Richard E. F. Leakey and Alan C. Walker, eds. Pp.
195220. Cambridge, MA: Harvard University Press.
. 2000. Schultzs rule and the evolution of tooth emergence and
replacement patterns in primates and ungulates. In Development, function
and evolution of teeth. Mark F. Teaford, Moya Meredith Smith, and Mark
W. J. Ferguson, eds. Pp. 212227. Cambridge: Cambridge University Press.
Smith, B. Holly, and Christophe Boesch. 2011. Mortality and the magnitude
of the wild effect in chimpanzee tooth emergence. Journal of Human
Evolution 60:3446.
Smith, B. Holly, Tracey L. Crummett, and Kari L. Brandt. 1994. Ages of
eruption of primate teeth: a compendium for aging individuals and comparing life histories. Yearbook of Physical Anthropology 37:177231.
Smith, B. Holly, and Robert L. Tompkins. 1995. Toward a life history of the
Hominidae. Annual Review of Anthropology 24:257279.
Smith, Richard J., Patrick J. Gannon, and B. Holly Smith. 1995. Ontogeny of
australopithecines and early Homo: evidence from cranial capacity and dental eruption. Journal of Human Evolution 29:155168.
Smith, Shelley. 2004. Skeletal age, dental age, and the maturation of KNMWT 15000. American Journal of Physical Anthropology 125:105120.
Smith, Tanya M. 2006. Experimental determination of the periodicity of incremental features in enamel. Journal of Anatomy 208:99114.

. 2008. Incremental dental development: methods and applications in

hominoid evolutionary studies. Journal of Human Evolution 54:205224.
Smith, Tanya M., Donald J. Reid, M. Christopher Dean, Anthony J. Olejniczak,
and Lawrence B. Martin. 2007a. Molar development in common chimpanzees (Pan troglodytes). Journal of Human Evolution 52:201216.
Smith, Tanya M., Donald J. Reid, and Joyce E. Sirianni. 2006. The accuracy
of histological assessments of dental development and age at death. Journal
of Anatomy 208:125138.
Smith, Tanya M., B. Holly Smith, Donald J. Reid, Heike Siedel, Linda Vigilant,
Jean-Jacques Hublin, and Christophe Boesch. 2010a. Dental development
of the Ta Forest chimpanzees revisited. Journal of Human Evolution 58:
Smith, Tanya M., Paul Tafforeau, Donald J. Reid, Rainer Grun, Stephen Eggins,
Mohamed Boutakiout, and Jean-Jacques Hublin. 2007b. Earliest evidence
of modern human life history in North African early Homo sapiens. Proceedings of the National Academy of Sciences of the USA 104:61286133.
Smith, Tanya M., Paul Tafforeau, Donald J. Reid, Joane Pouech, Vincent
Lazzari, John P. Zermeno, Debbie Guatelli-Steinberg, et al. 2010b. Dental
evidence for ontogenetic differences between modern humans and Neanderthals. Proceedings of the National Academy of Sciences of the USA 107:
Smith, Tanya M., Michel Toussaint, Donald J. Reid, Anthony J. Olejniczak,
and Jean-Jacques Hublin. 2007c. Rapid dental development in a Middle
Paleolithic Belgian Neanderthal. Proceedings of the National Academy of
Sciences of the USA 104:2022020225.
Spencer, Mark A. 1995. Masticatory system configuration and diet in anthropoid primates. PhD dissertation, State University of New York, Stony
. 1999. Constraints on masticatory system evolution in anthropoid
primates. American Journal of Physical Anthropology 108:483506.
Spencer, Mark A., and Gary T. Schwartz. 2008. The ontogeny of masticatory
system configuration in humans and its influence on the timing of molar
eruption. American Journal of Physical Anthropology 135(suppl.):299.
Stearns, Stephen. 1992. The evolution of life histories. Oxford: Oxford University
Trinkaus, Erik. 1995. Neanderthal mortality patterns. Journal of Archaeological
Science 22:121142.
. 2011. Late Pleistocene adult mortality patterns and modern human
establishment. Proceedings of the National Academy of Sciences of the USA
Trinkaus, Erik, and Robert L. Tompkins. 1990. The Neanderthal life cycle: the
possibility, probability, and perceptibility of contrasts with recent humans.
In Primate life history and evolution. C. Jean De Rousseau, ed. Pp. 153180.
New York: Wiley-Liss.
Ungar, Peter S. 2012. Dental evidence for the reconstruction of diet in African
early Homo. Current Anthropology 53(suppl. 6):S318S329.
Ungar, Peter S., Frederick E. Grine, Mark F. Teaford, and Sireen El Zaatari.
2011. Dental microwear and diets of African early Homo. Journal of Human
Evolution 50:7895.
Walker, Robert S., Michael Gurven, Kim Hill, Andrea Migliano, Napolean
Chagnon, Roberta De Souza, Gradimir Djurovic, et al. 2006. Growth rates
and life histories in twenty-two small-scale societies. American Journal of
Human Biology 18:295311.
West-Eberhard, Mary Jane. 2003. Developmental plasticity and evolution. New
York: Oxford University Press.
Willoughby, David P. 1978. All about gorillas. South Brunswick, NJ: Barnes.
Winkler, Linda A., Jeffrey H. Schwartz, and Daris R. Swindler. 1991. Aspects
of dental development in the orangutan prior to the eruption of the permanent dentition. American Journal of Physical Anthropology 86:255272.
Wood, Bernard A., and Mark Collard. 1999. The human genus. Science 284:
Wood, Bernard A., and Nicholas Lonergan. 2008. The hominin fossil record:
taxa, grades and clades. Journal of Anatomy 212:354376.
Zihlman, Adrienne, Debra Bolter, and Christophe Boesch. 2004. Wild chimpanzee dentition and its implications for assessing life history in immature
hominin fossils. Proceedings of the National Academy of Sciences of the USA

This content downloaded from on Tue, 18 Nov 2014 10:01:21 AM

All use subject to JSTOR Terms and Conditions