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Toward a life history of the Hominidae

Article  in  Annual Review of Anthropology · January 1995

DOI: 10.1146/annurev.anthro.24.1.257

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Annu. Rev. Anthropol. 1995. 24:257-79

Copyright © 1995 by Annual Review.s Inc. All rights reserved

TOWARD A LIFE HISTORY OF THE

HOMINIDAE
B. Holly Smith and Robert L. Tompkins
Museum of Anthropology, University of Michigan, Ann Arbor, MI 48109 and Depart-
ment of Anthropology, University of New Mexico, Albuquerque, New Mexico 87131
KEY WORDS; dental development, human growth and development, primates

ABSTRACT
Two new developments promise to greatly improve our ability to reconstruct
the evolution of the human life cycle: 1. the introduction of the comparative
methodology of life history into anthropology and 2. research on bone and
dental development that reveals a world of life history preserved in the fossil
record. Comparative study suggests that the human strategy depends on rich
energy sources and low mortality and that our general rate of growth and aging
evolved in parallel with brain size. It now appears that the australopithecines
were a substantially primitive grade of hominid with life histories more like
apes than humans. The life cycle of early Homo erectus was probably unlike
any living hominoid: Evidence suggests that it grew up somewhat faster than
living humans, it lacked an adolescent growth spurt, and H. erectus infants
were more helpless than those of chimpanzees (but conceivably of more ma-
ture body proportion and motor advancement than our own). The appearance
of fully modern life histories is still not fully resolved: Early Pleistocene/fomo
probably did not share them, and late Pleistocene hominids probably did, but
life history is still little documented in the intervening million years. Although
many details remain to be uncovered, the combination of advancing method
and theory should soon lead to more robust models of human origins.

INTRODUCTION
Life history might be defined as the allocation of an organism's energy toward
growth, maintenance, reproduction, raising offspring to independence, and
avoiding death. For a mammal, it is the strategy of when to be born, when to be

0084-6570/95/1015-0257$05.00 257
258 HOMINID LIFE HISTORY
weaned, when to stop growing, when to reproduce, and when to die (135).
Organisms on earth have greatly different life plans, and understanding what
shapes these histories is one of the most interesting areas in whole-organism
biology.
As anthropologists, we are interested in explaining the significance of our
own life strategy and how it evolved, but it can also be argued that human life
history presents a special challenge for general theory. Humans live on a vastly
extended time scale compared to most other mammals. Life-history theory
needs to explain how humans evolved long gestation and large neonates for
body weight, few young, an extended period of offspring dependency, slow
growth, delayed reproduction, the maximum life span of the terrestrial mam-
mals, helpless young, an unusually high rate of postnatal brain growth, a brief
duration of breast feeding, an adolescent growth spurt, intense maternal care,
paternal care, concealed ovulation, and menopause. Are life histories a pack-
age or a mosaic? Humans and primates have historical importance when this
question is addressed (20, 50, 90,114,130).
Anthropologists have written many essays on the significance of life his-
tory for human origins, especially concerning infancy and mating patterns.
The resulting "origins literature" has been criticized on many fronts: as the
shuffling and reshuffling of a few stereotyped narrative elements (72), as ecologi-
cally unsound (73, 151), as "fossil free" (73), and as a political battle for
the right to define human nature (39, 159). Nevertheless, not even the latter
charge is likely to stop attempts to model human origins. After all, without
modeling or theory, human evolution remains a dry list of inexplicable events.
A specific criticism that could be made of anthropological models of human
origins is that the life-history pattems they envision are often unrealistic.
Consider the following post-1970 reconstructions:
(a) Small-brained, small-bodied Australopithecus species matured as slowly
as modern humans but died by age 35 or 40 (80, 85, 92,157).
(b) Early hominids matured by age 12 but became "feeble" in their mid-twen-
ties (9).
(c) Newborn early Homo were as altricial (i.e. as less-developed at birth) as
modern infants (143,154).
The last of these reconstructions may be debatable, but the first two contrast
sharply with what we know about life-history patterns in living mammals.l
The lives of mammals offer an enormous amount of information that anthro-
Criticisms of a: Rates of maturation are nearly in lock step with brain size (113, 130), and life
expectancies are much greater than twice the ages of sexual maturity (98); b: species whose
members are feeble in their twenties mature at age 2 or 3 years, not 12 (50); and c: gestation and
ahriciality may be extremely conservative life-history parameters (91).
SMITH & TOMPKINS 259
pologists must use to make more realistic models, information that will surely
give new insight into human life.
New developments hold some promise that models can become more
ecologically sound and more scientific. First, life-history method and theory
have made real advances in recent years; second, recent work suggests that we
have greatly underestimated the amount of life history that is preserved in the
mammalian fossil record. Many models of human origins depend on a particu-
lar order of appearance of developmental, morphological, behavioral, and
technological adaptations. If evidence may lead us to reject some models, or at
least parts of them, models qualify as hypotheses rather than stories. The
combination of a fossil record of human life history and an enlarged under-
standing of life-history evolution must eventually lead to more robust models
of human origins.
HISTORY
Life History and Human Nature
Life history holds a place in centuries of literary, philosophical, and scientific
explanations of human nature. Philosophers and poets like Locke and Pope
(78,105) and moralists like Fiske and Spencer (41,142) considered prolonged
infant dependency and slow maturation as the foundation of our social ties and
family life (48, 79). The importance deeded maturation in anthropological
theory probably stems most directly from the critical importance of the work
of a series of developmental anatomists to physical anthropology. From Bolk
(12), to Le Gros Clark (74), Dart (27), Keith (63), Montagu (95), and Wash-
burn (155), anatomists saw the slow pace of human development and altricial-
ity of our young as by-products of selection for large brains and intelligence.
The human life cycle has been incorporated into nearly all models of human
origins, sometimes as cause, sometimes effect. Before 1970, models often set
up technology, family structure, and residence pattems as causes of life-his-
tory evolution. Etkin (37), for example, suggested that helpless young and
delayed development could only appear after permanent domiciles and mo-
nogamy; Washburn's "man the hunter" (155, 156) promoted hunting as the
behavior that brought about selection for greater intelligence, which in turn
affected life-history evolution.
In 1968, Mann (82) interpreted fossil evidence to mean that the human life
cycle was ancient (see below), and this widely discussed work had an impact
on theory. After 1970, with few exceptions, cause and effect switched: Basic
parameters of the human life cycle were now taken as given, and life cycle
shaped behavior. Thus, extreme infant helplessness, short birth spacing, and/or
prolonged juvenile dependency were viewed as pressures that brought about
260 HOMINID LIFE HISTORY
the evolution of a home base, food sharing, and an elaborate division of labor
by sex (58, 70, 80); the evolution of mating patterns and family structure (80,
127); or all of the above (127, 159). Thus Lancaster's "carrying and sharing"
(70) and Tanner & Zihlman's "woman the gatherer" (148, 159) were not
simply responses to "man the hunter." Like Lovejoy's "provisioning monoga-
mist" essay (80), they were written at a time when many paleoanthropologists
had come to think that human life history preceded almost all other aspects of
humanness.
Lovejoy and others encountered intense criticism (39, 59, 127), but they
opened a dialogue on life-history thinking, altriciality, monogamy, hunting,
and social organization of early hominids that has greatly improved the quality
of the discussion (43, 54, 64). Recently our view of the evolutionary grade of
Australopithecus has changed profoundly (see below) and life history is once
again something to be explained in early hominid evolution (1,55, 71,143).
Fossil and Skeletal Evidence
Almost from the start, teeth were considered the most promising source of
evidence on the rate at which species mature. When the first real data about
great apes in captivity became available, Keith (62), Krogman (68), Schultz
(120), and Zuckerman (160) pursued every anecdote about ape tooth eruption,
seeking to establish whether humans actually were the slowest maturing pri-
mate (140). Eventually it was established that humans take about twice as long
to erupt teeth, twice as long to reach adulthood, and live about twice as long as
great apes. Clearly, human growth and development had an evolutionary his-
tory since the last common ancestor of apes and humans, but when did the
human pattern appear—in the Miocene, Pliocene, or Pleistocene? Opinions on
that question spanned the full range. Bolk (12), for instance, had claimed that
not even the Pleistocene Neanderthals grew up in the human fashion. Le Gros
Clark (74) suggested the opposite: that gradients of molar wear observable on
australopithecine cheek teeth indicated slow maturation, an idea Dart (27)
promoted.
Mann (82, 85) became the first to undertake an organized approach to the
time depth of human growth and development. He agreed that wear gradients
might reflect maturation but thought better evidence would be found in the
pattern of events in tooth crown and root formation. With this idea, he exam-
ined a sample of australopithecines. The fossils were difficult to radiograph,
however, and in the end, only four juvenile Australopithecus robustus from
Swartkrans could be studied. In the four, pattems of development appeared to
resemble humans rather than chimpanzees, Australopithecines, Mann con-
cluded, matured slowly and were of an advanced grade of evolution, deserving
of the term "human" (83, 85).
SMITH & TOMPKINS 261
At the time of Mann's work (in the late 1960s and early 1970s), paleoan-
thropologists thought that human ancestry could be traced back to the Mio-
cene, and if so, it was credible that the human life cycle might characterize
Pliocene hominids (83). Simons & Pilbcam (124) were quick to suggest that
Ramapithecus, which also showed steep wear gradients, might have matured
slowly, although they realized that gradients could be formed by heavy wear
alone.
Although Mann's work was influential in paleoanthropology (103, 157),
the field was never without dissent. About the same time as Mann's early
work, Biggerstaff (8) assembled data on age of tooth eruption in five anthro-
poid species. He suggested that the small size of australopithecines made
likely rapid growth and short maturation times. Although Mann (85) brushed
aside Biggerstaff's suggestion as one without supporting evidence, outside of
anthropology, zoologists had gathered a great deal of evidence on this very
point. Sacher and colleagues had shown that brain weight is highly related to
gestation length and life .span in mammals (113, 115). As early as 1975, both
Cutler (25) and Sacher (114) pointed out that australopithecine brains were too
small to expect human-like rates of growth and aging.
By the 1980s, anthropologists were reevaluating australopithecines on all
counts. Molecular analyses and new fossil finds had halved the apparent time
depth of human origins (19). The advent of firm dating chronologies in Africa
(24) together with the discovery of Australopithecus afarensis (60) finally
made it clear that australopithecines appeared millions of years before stone
tools. Comparative studies (90, 114) were difficult to reconcile with a view
that the genus was advanced in grade of evolution (104). In 1984, Trinkaus
(152) revived the question of whether Neanderthals had fully modem life
histories. Soon after, Bromage (13) interpreted bone remodeling on the face of
the Taung child under an assumption of a short ape-like period of growth and
development. It was only a matter of time before the question of life history
would be reexamined in the entire hominid fossil record.
LIVE SLOW, DIE OLD: THE HUMAN STRATEGY
Life History Correlates
Outside anthropology, comparative studies made great strides in elucidating
the correlates of slow maturation and long life in mammals. Both charac-
teristics proved to be linked to enlarged brains, large body size, enhanced
learning and sociality, and increased parental investment (77, 102, 113-115).
For primates, Harvey & Clutton-Brock (50) detailed the strong positive rela-
tionships between size (e.g. brain, body, and neonatal weights) and time inter-
262 HOMINID LIFE HISTORY
vals in life histories (e.g. gestation length, age of weaning, age of sexual
maturity, life span).
Contemporary life-history studies, already well grounded in empirical data,
have moved into an exciting era of theoretical advance. Size is understood to
be strongly associated with life history (17, 50, 117), but as Harvey & Read
(52) point out, "size" as a causal factor ultimately begs the question. Instead,
one might regard time and size as equally important vectors in animal life (51,
135), realizing that change in either alters access to strategies and energetic
costs.
Large brains can be looked at as an energetic problem (89). Large brains are
costly investments: in humans, about 20% of resting metabolism supports
energetic demands of our brains, compared to 9% in a chimpanzee, and about
2% in an average marsupial (56). Moreover, larger brains have lower toler-
ances for temperature extremes, maternal blood pressure, and oxygenation (38,
131) and may increase obstetric risks or compromise locomotion (155). The
costs are high, but what is the pay-off? One explanation is that a large brain is
an investment that only pays off on a long time scale (131; see also 36). An
organism recoups its energetic "investment" in a large brain through complex
behavior, which is itself the combined product of large brains, slow develop-
ment, extended parental care, and enhanced learning, among other influences.
Moreover, benefits of large brains probably accrue slowly over a long life. For
primates, much of life history may act in support of a substantial investment in
brains.
Life-History Theory
We can identify a strategy of larger brains, slow maturation, and complex
behavior in primates and hominids, but what controls the evolution of this
strategy versus one that features small brains, quick maturation, and a more
rigid behavioral repertoire? Ultimate determinants must lie elsewhere. The
most influential theory about strategies is MacArthur & Wilson's theory of r
and K selection (81). The theory took its name from equations about popula-
tion growth in which r is the maximum intrinsic rate of increase and K, the
carrying capacity of the environment. MacArthur & Wilson postulated two
polar reproductive strategies that emerge from selection in contrasting set-
tings: Unstable environments produced r-selected species, which are oppor-
tunistic, gaining advantage through their ability to reproduce rapidly; these
species grow up quickly and keep investment in offspring low. Stable environ-
ments produced AT-selected species, on the other hand, which live near the
carrying capacity of the environment and gain advantage by increasing com-
petitive ability; these species grow up slowly, have fewer offspring, and invest
more in each (see 42).
SMITH & TOMPKINS 263
Elements of r and K theory continue to be useful, although current theorists
suggest that there is a more complex relation between environments and
outcomes (144). Since 1990, a series of studies argues that a better model of
ultimate determinants is provided by age-specific mortality—the probability
an individual of a given age has of living to next month, next season, or next
year (20, 21, 51, 108). A critical spectrum of life history stretches from "live
fast, die young" to "live slow, die old" (much the same as the r and K
spectrum, but without suppositions about population density or environmental
stability). High juvenile mortality selects for a strategy of "live fast, die
young." On the other hand, intraspecific competition selects for "live slow, die
old," because that strategy produces higher quality, more competitive off-
spring. "Slow" life histories, however, entail the constant risk of death before
offspring reach independence and can only be sustained when juvenile mortal-
ity is low.
Life-history theory is ultimately based on the general principles of thermo-
dynamics, that energy used for one purpose cannot be used for another, and
thus, rates of energy harvest impinge on outcomes (55). Diet is directly rele-
vant to energy harvest. At a given body size, the species that extracts higher
quality foods from the environment—e.g. fruit or animals instead of
leaves—has increased life-history options. Body size is also inextricably inter-
twined with life history because it is critical to energy budget. Increasing body
size, for example, requires more total energy, but it also improves heat reten-
tion and lessens energy needed per gram of tissue (17, 66, 91,117). Increasing
body size may also function to decrease mortalhy, because there are always
fewer predators for large mammals than for small ones. We would expect that
age-specific mortality, energy budget, and intraspecific competition all deter-
mine a species' position on the slow-fast continuum of life history.
Human hunter-gatherers have vastly lower infant and juvenile mortality
than do apes and monkeys (55, 71), and one of the first and most crucial
adaptations for early Pleistocene hominids may have been one that lowered
juvenile mortality—whether brought about by a change in grouping, group
transfer, foraging, parenting, or technology. We know that hominid body size,
brain size, and dietary quality increased in the Pleistocene, and theory gives us
every reason to expect that life histories adapted hand in hand.
Predictions
For a paleontologist, life-history characteristics can seem ephemeral. Smith
(130) turned to something that can be reconstructed from the fossil record
much more easily—age of tooth eruption. Because a juvenile mammal's sur-
vival depends on a having a working dentition, tooth eruption is also a life-his-
tory variable. A correlative study across 21 primate species found age of first
molar (Mi) eruption to be highly associated with brain weight (r = 0.98) and a
264 HOMINID LIFE HISTORY SMITH & TOMPKINS 265
host of other life-history variables. The strength of the correlations seemed weekly, and daily rhythms, giving rise to incremental lines of growth in tree
best explained by the robusticity of tooth development to environmental per- trunks, shells, and skeletons (97). Other metabolic upsets may also disturb
turbations, especially when compared to such life-history variables as age of growth rhythms. A brief interruption of tissue formation at birth can be recorded
sexual maturation or first birth. The study concluded that the mean age of tooth permanently in tooth crowns by the so-called neonatal line, a striation visible in
eruption is a good overall measure of the maturation rate of a species—a first histological sections of dentin and enamel observed in humans and some other
proxy of a species' position on the fast-slow continuum of life history. For mammals (112, 118, 146). Morbidity after weaning is thought to cause many
example, chimpanzees erupt Mi at about 3.1 years of age, whereas humans do enamel defects observed in humans (47). Use of incremental lines preserved in
not until 5-6 years (see Table 1). teeth to estimate individual age is well established in wildlife biology (57, 65,
Relationships observed in the living can be used to make predictions about 116). Microanatomical research has discovered evidence of birth, age of death,
the past. A regression of eruption on brain size in living anthropoids season of death, and other life events in teeth and tusks of fossil and living
predicts that the mean age of M^ emergence in gracile australopithecines was mammals (40, 65, 67).
somewhere between 3.0 and 3.4 years (133, 141), on par with that of living Microanatomy could lead us to unravel our own life-history evolution, but
chimpanzees. Interestingly, Homo habilis and early H. erectus are predicted to this technique usually requires sectioning a tooth to observe dentin (an internal
resemble nothing alive today—occupying a life-history niche between living tissue), something few curators of fossil hominids allow. Bromage & Dean
great apes and humans. On a gross scale, life histories near those of living (16) were the first to see their way around the problem of destructive research.
humans would be expected to arise as hominid brain size crested 1000 As they explained (16, 29, 30), a series of experiments dating from 1931 to
cc—something that occurred in middle Pleistocene H. erectus (Table 1). As 1959 (44, 93, 99, 119), some in sources obscure to western researchers,
Smith et al (141) point out, if we assume that human life history was fully showed that microscopic bands crossing enamel prisms (cross striations) were
formed in australopithecines, then we must imagine that humans increased best explained as the result of circadian rhythms in enamel-depositing cells.
their brain volume by another 900 ml with no concomitant change in life Groups of seven or eight cross striations, representing approximately one week
history. in time, formed larger-scale bands known as striae of Retzius, and this phe-
nomenon appeared to hold true across Old World monkeys and apes. Bromage
Evidence & Dean pointed out that the majority of striae of Retzius emerge on incisor
surfaces in clearly marked bands known as perikymata. These surface periky-
MICROANATOMY All terrestrial organisms are affected by astronomical cycles. mata could be counted to estimate the number of days involved in tooth crown
Tissue formation, in particular, may wax and wane in seasonal, monthly. formation. Individuals who died while still forming an incisor crown could be
Table 1 Increase in brain size and predicted increase in age of first permanent molar eruption
assigned a fairly accurate age of death by adding in an estimate of time lapsed
in the Hominidae and Pan^ between birth and initiation of crown formation (a few months for mandibular
incisors of great apes and humans).
Taxon Mean cranial capacity Actual or predicted (*) mean Bromage & Dean (16) used perikymata to date events in maturation for a
(ml) age of Mi eruption (yr)
Living H. sapiens, range of lOS-^-lSSl 5,0-6.3?
series of Pliocene hominids that had died as juveniles. Whereas Mann (85) had
means proposed that australopithecines that died about the time Mj erupted were all
"Early modern" H. Sapiens 1567 6.5* about 6 years of age, microanatomical study could only account for 3.3 years,
H. sapiens neanderthalensis 1519 6.4* an age that would be expected in a great ape, not a human (see Table 1).
Asian H. erectus 983 5.0' Bromage & Dean's findings suggested that australopithecines grew up nearly
African H. erectus 826 4.5* twice as fast as modern humans—which agrees with predictions based on
H. habilis 610 3.8* brain size (133).
A. africanus 440 3.1* Use of microanatomy to age fossil hominids has not gone unchallenged.
A. afarensis 404 3.0* Mann and colleagues argue that such techniques are unreliable, offering objec-
P. trof;lodytes 383 3.1
'Data from References: 3, 140, 141,153.
tions at every level: from suggesting that cross striations might be "knife-chat-
*Predicted from regression of In (eruption) on In (cranial capacity) across living anthropoid ter" from sectioning (87), to claiming extreme ranges for human perikymata
primates species (141). numbers and crown formation times (88). Many of these objections, however.
266 HOMINID LIFE HISTORY
are poorly grounded. Mann and colleagues (69, 86-88) regularly appeal to
Nolla (97a) for tooth formation data, although it is now thought that NoUa's
"backwards" solution of her equations combined with other statistical oddities
resulted in notably poor estimates of the timing of events (129, 134). In
addition, the high end of the ranges Mann et al (88) give for perikymata and
crown formation times are theoretical estimates they have derived from pecu-
liar extrapolations. Likewise, Dean & Beynon (31) regard some of Mann's
counterclaims for perikymata counts as unlikely to stand up to histological
scrutiny.
Since their first studies, additional investigations by Bromage, Dean,
Beynon, and colleagues describe both range (6-10) and mean number
(7.7-8.2) of cross striations within striae of Retzius in individual humans (6,
30) and the beginning of detailed work on great apes (5). Their newer work
(32,145) often provides ranges for age estimates of early hominids rather than
the single values originally published (16). New studies, however, also offer
evidence of consistent results between teeth in the same individual (5, 31) and
verify periodicity in controlled experiments with higher primates (15). Tech-
niques have been tested on historical skeletal material of known age (145) and
actual number of cross striations within striae of Retzius counted in sectioned
and broken australopithecine teeth (7, 32). Even attributing highest reasonable
estimates of time to incisor crown formation in australopithecines does not
double age estimates—and doubling would be necessary to bring these esti-
mates in line with human schedules of maturation.
Study of surface enamel (16) has opened up a new world of research for
paleoanthropology, but the dictates of nondestructive research still produce
difficuhies. Calculating age from surface perikymata rather than from a sec-
tion showing actual striae of Retzius adds two layers of estimation (without
sectioning, the number of cross striations within striae and the number of
perikymata that do not reach the surface must both be estimated). Without
sectioning, human age estimates are most accurate within a short window of
time during the three or four years after birth, during which time mandibular
incisor crowns form. Older children with complete crowns and forming roots
are problematic. Dean, Beynon, and colleagues are working on ways to esti-
mate root extension rates (5, 28, 31, 32). Even restricting work to tooth
crowns, maxillary central incisors are apparently less reliable in expressing
striae of Retzius on their surface than are mandibular incisors and canines (5),
and the complexity of molar and premolar crowns still requires sectioning or
study of naturally broken teeth (7, 110). Sectioning of some teeth, especially
from older hominid juveniles, would greatly speed progress. Even so, section-
ing can be kept to a minimum: Knowledge gained from occasional sectioning,
naturally broken teeth, perikymata counts, and relative stages of crown-root
development can be combined to build a chronology of dental development for
SMITH & TOMPKINS 267
hominid species that may be used to assign ages of death to other juveniles (4,
7,23,110).
Only time will tell whether the studies of surface enamel must be pursued
or whether more curators will allow selected sectioning of fossil teeth, but
regardless, microanatomy is here to stay. Despite some initial resistance within
anthropology, what is at stake—all that we might learn about life history—is
far too interesting not to pursue these techniques.
PATTERNS OF DEVELOPMENT Patterns and rates of development are not the
same, of course, but the two probably covary in the real world because no life
strategy can work at all scales (135). Schultz (120, 122) originally suggested
that sequence of tooth eruption in primates is adapted to the rapidity of postnatal
growth—that patterns covary with rates. Mann (85) developed the argument at
length, suggesting that patterns of root-crown development were likely to be
strongly linked to rate of development. Although not all agree (125), evidence
supports Schultz's and Mann's theoretical position.
Smith (135), using techniques of allometry, showed that mammals adapt
several sequences of events in maturation to the time scale at which they
occur. It has also been shown (136) that tooth emergence in primates and
ungulates follows a simple progression: The later that tooth emergence begins,
the earlier anterior teeth (I1-P4) appear in sequence (probably because the
deciduous teeth they replace wear out). The sequence of mandibular tooth
eruption reconstructed for Australopithecus africanus (Ml II 12 M2 P3 P4 C
M3) matches that of the rapidly developing genera Pan and Macaca (139).
Modern humans, it appears, adapted to slower development by shifting C, P3,
and P4 forward in the sequence to M l II12 C P3 P4 M2 M3 (120, 139).
Patterns of crown-root development are more complex than simple se-
quences of tooth eruption, but the same hypothesis applies—that rate and
pattern covary. Mann (82) took a descriptive approach to the problem, but by
the 1980s, data had become available on great apes (34) and more than a dozen
fossil hominids, and it was time for a numerical approach. Smith (128) as-
signed two sets of dental ages to 15 fossil hominids under conflicting hypothe-
ses: (a) that maturation mirrored that of humans or {b) that it mirrored great
apes. For many hominids, dental ages of individual teeth were more in syn-
chrony when assigned under the great ape model of development. Interest-
ingly, patterns of development seemed similar within species but different
between them. At first, the few data available for H. erectus suggested that
patterns might have resembled apes (128), but additional data subsequently
placed it closer to modern humans (133, 138). The few data available on
Neanderthals suggested nearly modern dental development. Patterns were not,
however, easy to understand in robust australopithecines, which appeared to
share some features of human development. Most importantly, clear evidence
268 HOMINID LIFE HISTORY
existed for evolution of growth and development within Plio-Pleistocene
Hominidae.
Debate soon crystallized over the age of the Taung infant, the type speci-
men of A. africanus. Tooth development had been ignored in Taung because
its face is unbroken (hiding crown-root development) and teeth erupted are
nondiagnostic. Conroy & Vannier (22, 23) used CT scanning to observe devel-
oping teeth within the face, and they agreed that patterns of development were
more ape- than human-like. Their work renewed the debate over the age of the
Taung infant (86, 135, 158), at issue since Dart's original description (26,
160). As always, the issue was not the age of a single dead child, but the rate of
maturation in human ancestors.
Several lines of evidence suggest that australopithecines were substantially
primitive in growth and development. Mann and colleagues, however, con-
tinue to object on all fronts, arguing for faults in evidence of life-history
correlation, statistical patterns, developmental sequences, microanatomy, and
gross anatomy (69, 86-88, 158). They go so far as to reject future approaches
that might be devised (69): "biological diversity in pattern and age known to
characterize modern human dental development are not amenable to simple
statistical analytic models" (p. 125). A universe so constructed holds little
possibility for rejecting an old hypothesis. Although highly critical of new
methodologies, these authors offer no new evidence that australopithecines
matured on a human schedule, an argument that was always based on slim
evidence (14).
WITHIN HOMO It is now fairly certain that the outline of human life history took
shape within the evolution of Homo and not before. Indeed, australopithecines
probably lived at a pace nearly twice as fast as modern humans—fast enough to
be reflected even in gross developmental sequences such as tooth emergence.
Little is known of H. habilis, and this may be one of the most interesting species
for future studies, but in many ways the most difficult case to interpret involves
late Pleistocene Homo (Neanderthals and early modern Homo sapiens).
Dental microanatomy remains in the exploratory stage for late Pleistocene
hominids, but both indirect and direct evidence suggests that developmental
timing is not far from that of modern humans. First, late Pleistocene hominids
are close relatives of living humans, falling within modern limits in brain size
(see Table 1). Second, whereas australopithecine dental ages were halved
under microanatomical study, only small discrepancies characterize recent
Homo. For example, stages of tooth formation in the Gibraltar 2 Neanderthal
infant approximate those of a 4-year-old human (128), and the I' perikymata
count suggests an age of 3.1/-3.9 years (145)—a small difference given that I'
perikymata may underestimate age slightly. Patterns of development are like-
wise close. In study of a substantial sample, Tompkins (149, 150) found late
SMITH & TOMPKINS 269
Pleistocene dental development to be fairly homogeneous. The fossil sample
(Neanderthals plus early modern H. sapiens) differed only slightly from a
worldwide sampling of modern humans (black Africans, white French-Cana-
dians, and Amerindians). The fossils, however, tend toward the more primitive
pattern of anterior tooth delay relative to molars (149), a tendency associated
with a slightly early age of M^ emergence in living humans (139).
Two studies (33, 145) suggested that some juvenile Neanderthals, particu-
larly the Gibraltar 2 infant, had large cranial size for their dental age. Trinkaus
& Tompkins (153), however, concluded that such a distinction did not hold
when a sample of five Neanderthal juveniles was compared to modern chil-
dren of comparable dental age. Other researchers have found only minor
differences in maturation of the Neanderthal cranium compared to modern
humans (94,126).
We are on less stable ground in predicting precisely how late Pleistocene
life history differed from that of modern humans. Brain size predicts that
life-history parameters might be on the high side of modern human values, but
interspecific regressions are poor predictors of small sub-specific differences.
Although evidence is far from complete, most investigators have argued that
Neanderthals in particular would have been less able to tolerate risks and the
expense of long, slow maturation than living humans and might have experi-
enced more stresses and matured more quickly (33, 53, 100, 145, 153). If
Neanderthals and living humans differed only subtly in life histories, study of
large samples will be necessary to show it. We may hope that the richer, more
complete fossil record for late Pleistocene hominids will eventually balance
the difficulties.
NOVELTIES AND TRADE-OFFS
Not all elements of human life history fit intuitively on a fast-slow continuum.
Real life histories seem to contain trade-offs and other novelties that are not
easily predictable from the simple general theories developed to date (144).
Among aspects not readily brushed into the "slow" category are helplessness
of human newborns (106), absolutely and relatively early weaning (132),
absolutely and relatively short birth spacing (80), the adolescent growth spurt
(137), concealed ovulation (2), and menopause (101). At present, we limit our
discussion to two aspects for which fos.sil evidence has been presented.
Helplessness of Human Newborns
If a single aspect of human life history can be said to be central to reconstruc-
tions of early hominid life, it is the helplessness of our infants. Protecting our
infants from insult and death requires vigilance and limits mobility, circum-
scribing the lives of parents. It has been estimated that it takes the human
270 HOMINID LIFE HISTORY
newborn a year to reach the stage of motor development equivalent to that of a
newborn great ape (106).
As Alexander (1) points out in broad perspective, "juvenile life has two
main functions: to get to the adult stage without dying and to become the best
possible adult" (p. 22). Mammals, like birds, have evolved two major pattems
for young. Altricial young are born into a litter after a relatively short gestation
and in a less-developed state. Young are typically naked, with eyes and ears
sealed, incompletely homeothermic, and are often kept in a nest for some time.
Precocial young are usually bom as singletons or twins after a relatively long
gestation and are well developed: They have some hair, their eyes and ears are
open, they are able to regulate their own temperature, and they may locomote
within a day. Primates clearly are a precocial order, but one with delayed
motor development (35, 49, 106, 107). Motor delay is so extreme in human
infants that Portmann (106) designated human infants as "secondarily altri-
cial."
Human brains are about one fourth of adult size at birth, a small value
compared to other primates (one half in Pan and two thirds in Macaca) (35). In
most mammals, the brain grows at its fastest in utero, with rates falling off
precipitously after birth. Thus, altricial mammals like humans must complete a
large portion of their brain growth at the slower postnatal rate. Human infants,
however, manage to sustain high fetal growth rates for a full year after birth;
chimpanzees and macaques may do so only for a month or two (35). Years
ago, Washbum & Montagu suggested that the helplessness of the first year of
newborn life resulted from the channeling of most energy resources to brain
growth and maturation (96,155).
As primates, our newborns are also unusual in being heavy for maternal
weight, and data show that birth is indeed more difficult in humans than other
primates (75, 111). In humans, adult female pelvic diameter is nearly equal to
offspring head size, whereas apes have comparatively spacious pelvic outlets
(121). Washburn (155) suggested that bipedal adaptations combined with large
infant brains meant that an "obstetrical dilemma" constrained infants to be
bom at a more altricial state after a shorter gestation. There are at least two
problems with bipedalism-short gestation as a cause of human secondary
altriciality. First, human gestation is hardly short: It is both absolutely long and
relatively long for maternal body weight, and energetic investment is about
average for a precocial mammal of our size (91).2 Second, the explanation is
not general: It fails to explain why infants are more helpless in apes than
monkeys, and in monkeys than most prosimians.
Human gestation is short for adult brain weight, but only by 13 days when compared to other
primates (46). It is remarkable that mammals as small as primates can sustain gestation lengths as
long as they do—most precocial mammals are far larger than primates (123).
SMITH & TOMPKINS 271
Gestation might be better understood as a trade-off: for a given caloric
investment over a given time period, energy diverted to producing a mature
offspring that can flee or protect itself at birth means less energy is available
for brain growth (1). For example, great apes are roughly comparable to
humans in body weight and gestation length (228 days in chimpanzees and
267 in humans), but their newboms are much smaller, with more mature body
proportions and motor coordination than humans (107). The best explanation
for why we are retarded in motor development at birth—and why we remain
so for the first year—is that brain growth and development is enhanced,
ultimately producing a better adult (1, 35). Of course, such a strategy can only
evolve as parental care increases. The general explanation better accounts for
the grade shift we see across primates than does a special argument about
bipedalism. It is less clear why human infants are so large (1, 35), which is
more relevant to obstetrical difficulties than is maturational delay.
But when did human infants evolve to be so helpless? As with any other
aspect of human development, we can find a full spectmm of answers: that
australopithecines had secondarily altricial infants (61) or, not even Neander-
thals did (152). Trinkaus (152), using relationships described by Sacher &
Staffeldt (115) for all mammals, suggested that Neanderthal adult brain weight
corresponded to a gestation length of 12 months. Although the hypothesis
eventually was rejected, it stimulated much research (111). Martin (90) made a
different prediction, one that assumed that gestation length changed little in
hominid evolution. He surmised hominids might have sustained initial in-
creases in brain size through increasing maternal energy input, but after adult
cranial capacity reached 850 ml (a value typical of H. erectus), fetal rates of
brain growth would have to be extended into the postnatal period. Such an
extension would likely be accompanied by secondary altriciality.
We would expect that adult brain size and secondary altriciality probably
kept pace during hominid evolution, but this is still a prediction rather than a
fact. To date, evidence on what actually happened in the past is confined to
studies of adult pelvic diameter and cranial capacity. The adult/newborn ratio
of brain weight is an excellent measure of altriciality (107), but in the fossil
record, newborn cranial size must be estimated from adult pelvic diameters
(76). Rosenberg (111) reviews the extensive literature on fossil hominids, and
only a few remarks are made here. Although hampered by the necessity for
extrapolation, we have a rough outline of altriciality at three points in human
evolution. For A. afarensis, Tague & Lovejoy (147) estimated that Lucy's
pelvis was spacious enough to allow birth of an infant with a fan-sized
cranium without any need for secondary altriciality. Although the mechanism
of birth (orientation of fetus during birth) must have changed with bipedalism,
secondary altriciality was not a necessary accompaniment. At the other ex-
treme of the time range, the recent find of the Kebara 2 Neanderthal shows a
272 HOMINID LIFE HISTORY
pelvic inlet diameter much the same as in modern humans (109), suggesdng
(in combination with adult brain size) that secondary altriciality was well
established ( H I ) . The most intriguing case belongs to the midpoint, H. erec-
tus. Walker & Ruff (154) suggested that even allowing for a generous portion
of remaining growth, the pelvis of the Nariokotome H. erectus was so narrow
that secondary altriciality would be necessary for a newborn to develop to the
cranial size of a typical adult. Conclusions must remain tentative, however:
both Kebara 2 and Nariokotome are likely male and Nariokotome is a juvenile
male. Presently, few doubt that Neanderthals gave birth to secondarily altricial
infants, but the continuum between human and ape infants is long, and it
remains a puzzle when fully human patterns appeared.
If complete adult female pelvises are so rare in the fossil record, we might
hope for another line of evidence on altriciality. Teeth might be useful here
because they, like any other organ, may or may not be mature at birth (140,
146). Neonatal lines preserved in fossil teeth should track the skeletal advance-
ment of infants at birth. An evolutionary series of pelvic diameters, brain sizes,
and dental status at birth might improve our chance of unraveling the evolu-
tionary history of altriciality, obstetrics, and parental behavior.
The Adolescent Growth Spurt
Humans, especially males, show a spurt in growth at adolescence affecting all
body segments and facial dimensions (reviewed in 137). Although many other
mammals add weight at adolescence, a spurt in linear dimensions is not usual.
Centered at about 14 years of age in males and 12 in females in the West, the
growth spurt is characteristic of all human populations, although poor nutrition
can delay it or lower its amplitude. We have no theory to predict precisely
when humans evolved the adolescent growth spurt, but we can suggest some-
thing of its function and test for its presence in the fossil record.
One might think that a growth spurt is a mechanism for becoming a taller
adult, but merely continuing ordinary growth could achieve size alone; the
importance of the growth spurt is more likely as a distinct pattern of achieving
adult size. Gavan (45) first compared relative growth curves in chimpanzees
and humans: In childhood, humans fell below the chimpanzee curve, then rose
above it at adolescence, finally to rejoin it. Gavan's work suggested that
human children might be regarded as growth suppressed, with the spurt repre-
senting catch-up growth. For example, the preadolescent chimpanzee (7 years
of age) has attained 88% of his adult body size, whereas the comparable
human boy (11 years) has attained only 81%, a difference that will disappear
only after the boy completes his adolescent growth spurt. One might say that
an 11-year-old human male well under 5-feet-tall "pretends" to be more child-
like than he really is. Why would such a pattern evolve? A marked spurt in
stature must influence entry into the adult social hierarchy, but the real advan-
SMITH & TOMPKINS 273
tage in resembling a younger form is thought to be that it elicits parental
behavior—care rather than competition—from adults (10). The human pattern
of growth suppression-growth spurt should function to prolong human child-
hood—a period of intense learning and parental care (10, 11). It is also an
evolutionary novelty that prolongs childhood without altering timing of sub-
sequent life stages.
At first glance, the adolescent growth spurt seems a poor candidate for
study in the fossil record, but recovery of an adolescent male early H. erectus
from Nariokotome (KNM-WT 15000) suggests how this analysis might be
done (137). The youth's deciduous upper canines were in place, and he died
not long after erupting second permanent molars, events placing him firmly in
early adolescence by comparison with any hominoid. Judged according to
human standards, his dental age (11 years) is in some conflict with bone age
(13 years) and his stature age (15 years). By chimpanzee standards, however,
dental and bone ages are in near perfect agreement (both 7 years of age), and
his large size is more explicable. What is interesting is less his chronological
age than the pattern of age discordance (indeed, his true age was probably
neither 7 nor 11, but something in between). Smith (137) suggested that the
reason for the large stature of the Nariokotome youth is that the distinct human
pattern of growth suppression-growth spurt had not yet evolved in early H.
erectus. Because of this, any early H. erectus youth would seem to us to be too
large.
Although the Nariokotome youth is but a single specimen, his study can
generate a method and predictions, some of which could be tested on material
already available. If the growth spurt was present in Neanderthals, juveniles of
any age will show concordance or random discordance between dental devel-
opment and stature. If not, discordance will be patterned: preadolescents will
seem tall for dental age (and tall relative to known adult heights), whereas
older adolescents will seem to be of more ordinary size. One day we will know
when—and in what hominid species—the adolescent growth spurt evolved.
For the present, we suggest that it functions to increase the length of the period
of intense parental investment and that it had not evolved in early H. erectus.
CONCLUSION
Why do humans live so long? Why do we take so long to grow up? Why are
our babies so helpless? When did we evolve our life cycle? These questions
are inherently interesting to us, but in addition, the evolutionary record of
human life cycles can be used to test general theories about growth and aging.
The benefits of adopting method and theory of life-history studies into anthro-
pology, however, go both ways: as Cartmill (18) points out, a science of
paleoanthropology that is interesting and persuasive must explore to what
274 HOMINID LIFE HISTORY
degree human characteristics follow general rules that apply to other organ- the Taungs child, or how old is "Australopi-
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Supported by grants SBR-9408408 (to BHS) and BNS-8918011 (to RLT) hundred years of paleoanthropology. Am.
Sci. 74:410-20
from the National Science Foundation.
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may be purchased from the Annual Reviews Preprints and Reprints service. female primates have such long lifespans
1-800-347-8007; 415-259-5017; email: arpr@class.org and so few babies? Or life in the slow lane.
Evol. Anthropol 1:191-94
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