Proc. R. Soc. B (2006) 273, 2799–2808
doi:10.1098/rspb.2006.3583
Published online 12 July 2006
Review
Tooth microstructure tracks the pace
of human life-history evolution
M. Christopher Dean*
Department of Anatomy and Developmental Biology, University College London, Gower Street,
London WC1E 6BT, UK
A number of fundamental milestones define the pace at which animals develop, mature, reproduce and
age. These include the length of gestation, the age at weaning and at sexual maturity, the number of
offspring produced over a lifetime and the length of life itself. Because a time-scale for dental development
can be retrieved from the internal structure of teeth and many of these life-history variables tend to be
highly correlated, we can discover more than might be imagined about fossil primates and more, in
particular, about fossil hominids and our own evolutionary history. Some insights into the evolutionary
processes underlying changes in dental development are emerging from a better understanding of the
mechanisms controlling enamel and dentine formation. Our own 18–20-year period of growth and
development probably evolved quite recently after ca 17 million years of a more ape-like life-history profile.
Keywords: life history; enamel; dentine; incremental markings; hominid; evolution
1. INTRODUCTION
Some of the most informative things about our own
evolutionary history have emerged from an understanding
of how morphological adaptations relate to the ways
hominoids lived their lives. Variation in life-history strategy
is dependent on a broad set of biological rules that govern
the balance between fertility and mortality rates. Some
apply across many organisms, others are characteristic of
particular phylogenetic lineages and some are specific to
local ecological circumstances. At one end of the spectrum,
for example among eusocial insects, there are large
differences in lifespan between the well-protected queens
that experience low mortality rates and the more exposed
and vulnerable workers (Keller & Genoud 1997).
Generally among animals when mortality rates are low,
reproductive success can be maximized by postponing age
at first reproduction for as long as possible and by spreading
reproductive output into adulthood over as long a period as
possible (Ashmole 1963; Charnov 1991, 1993; Harvey &
Nee 1991; Stearns 1992). In an environment where
adult mortality rates are high, the greater costs to the
mother of early and more frequent reproduction are
outweighed by the need for increased reproductive effort
to maximize reproductive success (Harvey & Zammuto
1985; Promislow & Harvey 1990, 1991). At the other end
of the spectrum, however, especially when studying more
closely related groups of animals such as primates, there
are additional influences on life-history variables to
consider (Harvey & Clutton-Brock 1985; Charnov &
Berrigan 1993). Life-history strategy is also about
optimizing available energy resources over a lifetime and
primates exploit diverse diets and habitats in very different
ways (Kozlowski & Weiner 1997; Gurven & Walker 2006;
*ucgacrd@ucl.ac.uk
Received 2 March 2006
Accepted 5 May 2006
Dirks & Bowman in press). Among primates, orang-utans
(Pongo pygmaeus) for example, are remarkable for their later
age at weaning, later age at first reproduction, long interbirth intervals (6–9 years) and lower mortality rates
compared with chimpanzees (Pan troglodytes) and gorillas
(Gorilla gorilla) (Hill et al. 2001; Wich et al. 2004). In the case
of the orang-utan, food availability, home range and foraging
strategy are thought to underlie these life-history traits as
well as just differences in mortality rates (Wich et al. 2004).
While on the one hand there is huge life-history
diversity among primates, one life-history trait, the period
of growth and development, appears to have undergone
just three major grade shifts (Schultz 1940, 1969).
Among lemurs, irrespective of body size (Schwartz et al.
2002), growth is fast. Both New and Old World monkeys,
despite differences among and between them, have a
much more prolonged period of growth than prosimian
primates and major differences exist in the period of
development between monkeys and apes (Harvey &
Clutton-Brock 1985; Kelley 1997, 2002). Similarly, the
modern human growth period is greatly prolonged with
respect to that of apes. Long periods of relative stasis in
the general pace of development seem, therefore, to
characterize primate evolution. This begs questions about
the evolutionary origins of the major shifts between
monkey-like, ape-like and modern human-like patterns of
development.
A complex hierarchy of interrelated factors has
contributed to the evolution of primate development,
growth and lifespan. While much of this evolutionary
history is unknowable, given only the fossil record of bones
and teeth, teeth have to grow within whatever period of
development is available. As such their growth is a
reflection of the time determined by natural selection
acting on key life-history variables (Godfrey et al. 2001;
Dirks 2003).
2799
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2800 M. C. Dean
Review
Figure 1. Calcospheritic mineralization of root dentine is shown on the left with fluorescent labels seen with confocal microscopy
(fieldwidth 130 microns), in the middle with SEM of a mineralizing root dentine front (fieldwidth 70 microns) and on the right
in a ground section of a w1.6 million year old fossil hominid root (fieldwidth 125 microns).
2. ENAMEL AND DENTINE FORMATION
The developmental processes that control the rates of
enamel and dentine formation ultimately hold the key to a
better understanding of how the timing of dental
development comes to track evolutionary change in lifehistory timing. Enamel and dentine, while fundamentally
different tissues, are both extremely hard and never
remodel. Dentine is secreted by odontoblasts. These
differentiate from the mesenchymal neural crest cells of
the dental papilla or future pulp through a long process
involving reciprocal inductive signals between oral ectoderm and peripheral dental papilla cells (Lesot et al. 2001;
Thesleff et al. 2001). Odontoblasts secrete a proteoglycanrich organic matrix, part of whose function is to delay
mineralization for several days until collagen fibre growth
and orientation within the matrix is complete ( Jones &
Boyde 1984; Linde 1984, 1985; Boyde 1990), and then
to induce hydroxyapatite formation at the predentine–
dentine boundary (Irving 1963; Veis et al. 1977; Wuthier
1984). Several growth factors, including Insulin-like
Growth Factor (IGF-1, IGF 11), Fibroblast Growth Factor
(FGF-1) and members of the Transforming Growth Factor
beta family (TGF-bs and Bone Morphogenetic Protein,
BMP-2) may act synergistically to induce terminal
odontoblast differentiation and stimulate the synthesis of
dentine matrix formation. Importantly, some of these (e.g.
TGF-b1) remain sequestered and potentially active
throughout life within mineralized dentine (Tziafas et al.
2000; Sloan et al. 2000; DenBesten et al. 2001).
Enamel matrix is secreted by ameloblasts that differentiate from the inner enamel epithelium of the tooth.
Unlike dentine, enamel contains no collagen and is even
harder. IGF-1 and IGF-11 are known to increase rates of
enamel matrix secretion and are associated with increased
expression of genes for the enamel matrix proteins
involved in mineralization, such as enamelin and amelogenin (Catón et al. 2005). The onset of enamel matrix
secretion is delayed with respect to dentine matrix
Proc. R. Soc. B (2006)
secretion by at least 30 hours, as continuing inductive
epithelial–mesenchymal signalling occurs between these
tissues (Gaunt 1967), but then mineralization, unlike
dentine, begins almost immediately (Rosser et al. 1967).
3. CIRCADIAN INCREMENTAL MARKINGS IN TEETH
It is the incremental record of tooth growth that provides a
time-scale for reconstructing life history. Circadian
rhythms are almost universal among living organisms
and the mineralizing systems of teeth, shells and corals are
no exception. Fossil coral sequences preserve a record of
the slowing of the Earth’s rotation over 350 million years
(Wells 1963; Scrutton 1964) and fossil teeth contain a
record of the daily secretory rhythms of the cells that
formed them (Dean 1987).
The experimental evidence for circadian incremental
markings in enamel rests largely on a number of labelling
experiments, where either sodium fluoride or certain
fluorescent markers have been administered at known
intervals while enamel was still forming (Schour &
Poncher 1937; Okada 1943; Bromage 1991; Smith
2006). There is also evidence for both shorter- (intradian)
and longer-period increments in enamel and dentine
(Shinoda 1984; Dean 1987, 1995; Boyde 1989; Ohtsuka &
Shinoda 1995; FitzGerald 1998; Smith 2006).
No rhythms are known for growth factor synthesis in
tooth germs, but circadian rhythms clearly exist in
predentine matrix synthesis, dentine mineralization, odontoblast cell process morphology (Boyde 1990) and during
tooth eruption (Risinger & Proffitt 1996). Both mineralization and eruption rhythms have been shown to be
maximal at the end of the light (or active) period and to be
linked, respectively, with peak adrenal cortex activity and the
late evening secretion of growth hormone and thyroid
hormone (Miani & Miani 1971; Risinger & Proffitt 1996;
Craddock & Youngson 2004). All of this is likely to be
controlled by the suprachiasmatic nucleus, and temporary
Review
M. C. Dean 2801
cementum
cementoblasts
dentine
fully differentiated
odontoblasts
cells of surrounding
dental follicle
developing pulp
epithelial
root sheath
developing alveolar
bone
Figure 2. The rate at which odontoblasts differentiate determines the rate of root extension. The original angle of alignment of
the fully differentiated odontoblasts to the root surface (the cementum) can be reconstructed (black arrows) from the orientation
of the incremental markings in roots to the root surface. In ground sections of Proconsul heseloni tooth roots, the incremental lines
in a deciduous second molar root (the middle image) are near parallel in their orientation to the root surface (extension rate ca
18 mmK1), while in a permanent premolar root (image on far right) they form a greater angle to the root surface (extension rate
ca 8 mmK1). In both cases, the origin of the arrow begins 200 mm (ca 80 days) deep to the root surface.
or permanent obliteration of this nucleus results in the loss of
a circadian rhythm during dentine formation (Ohtuka-Isoya
et al. 2001). However, it is highly likely that there are one or
more as yet unidentified intracellular clocks operating
during enamel and dentine formation of the kind that
regulate intradian, circadian and developmental timing (e.g.
Smith et al. 1987; Moore 1999; Adoutte 2000).
The circadian mineralizing lines in dentine are
distinguished by their characteristic appearance that is
described as calcospheritic (see figure 1). Small spheres of
mineralizing dentine increase in size until they eventually
coalesce with each other. It is the mineralizing increments
in dentine that are especially well preserved in fossils
(Boyde 1990; Furseth-Klinge et al. 2005). Okada (1943)
summarized a series of elegant experiments that together
suggest that the mechanism underlying the appearance of
mineralizing lines in dentine is the daily change in
acid–base balance that accompanies alternating periods
of activity and rest (see also Lutz & Rhoads 1977; Boyde
1979). Ultimately, this is manifest as regions of differing
refractive index that appear lighter or darker in transmitted light microscopy, and as light or dark bands under
back-scattered scanning electron microscopy that reflect
regular shifts density of mineral laid down (Boyde 1979,
1989).
4. LIFE-HISTORY VARIABLES AND THE ERUPTION
OF MOLAR TEETH
Permanent molar teeth develop in sequence between birth
and adulthood. In particular, their emergence into the
mouth is in each case a developmental milestone that can
be used as a proxy to determine the pace of life history in
fossil primates. Modern human permanent molars (M1,
M2, M3) emerge roughly 6 years apart at ages 6, 12 and
18 years. Modern chimpanzee permanent molars emerge
roughly at 3.5, 6.5 and 10.5 years and those of macaque
monkeys at roughly 1.3, 3.5 and 5.5 years of age (Smith
et al. 1994). Gingival emergence of M1 correlates best
with several life-history traits (Smith 1989, 1991, 1992;
Kelley 2002, 2004). For example, completion of 90% of
brain growth occurs at M1 emergence in all primates
Proc. R. Soc. B (2006)
(Ashton & Spence 1958; Smith 1989; Allman &
Hasenstaub 1999) and skeletal maturity correlates broadly
with M3 emergence (Demisch & Wartmann 1956; Watts
1990; Trinkaus & Tompkins 1990). Thus, many of the
crucial questions about the pace of life history in fossil
hominoids depend on being able to reconstruct the timing
of gingival emergence in molar teeth.
5. HOW TOOTH ROOTS GROW IN LENGTH
A clearer understanding of the comparative processes
involved in root growth is allowing us to recover more
information about the timing of dental development in
living and fossil hominoids. It is the cells of the internal
layer of the epithelial root sheath that induce the
peripheral cells of the dental papilla to differentiate into
odontoblasts and go on to form tooth roots (figure 2).
Initially, preodontoblast cells of the dental papilla align
themselves along the basal lamina that separates them
from the epithelial root sheath. A gradient of differentiation then begins that may initially be regulated by
signals from the epithelium and subsequently by a lateral
relay mechanism between odontoblasts (Lesot et al. 2001;
Thesleff et al. 2001). This process ends with final
polarization of the root odontoblasts, predentine secretion
and mineralization (Thomas 1995).
The rates of odontoblast differentiation and rates of
dentine formation can still be determined from longitudinal ground sections of tooth roots (figure 2). Daily
incremental markings in the root indicate that mineralization rates begin slowly close to the root surface and that
for at least the first 200 mm of dentine formation, the
gradient of increasing rate is comparable in both living and
fossil hominoids (Dean 1993, 1998). Based on the average
spacing of daily mineralizing lines, the first 200 mm of root
dentine takes ca 80 days to form. Longer-period
accentuated incremental markings in the root reflect the
former position and orientation of the odontoblast cell
sheet at any one time during root formation. The angle
these longer-period lines make to the root surface reflects
the rate of differentiation of new odontoblasts during root
development (Dean & Wood 1981). For example, in
2802 M. C. Dean
Review
16
root extension rate (microns/day)
14
12
10
8
6
4
Gorilla/Pongo
Homo
2
Pan
0
200
500 1000 2000 3000 4000 5000 6000 7000 8000 9000 10 000
mesiobuccal root length (microns)
Figure 3. Root extension rates for the first 10 mm of mesiobuccal root length in hominoid M1s show the gradual rise and fall
typical of permanent molar teeth. The different extension rates in each taxon reflect both overall tooth height and the amount of
time available to grow the root.
80 days, a wave of differentiation proceeding at 10 mmK1
will extend 800 mm down the root, whereas a differentiation rate of just 4 mmK1 will extend only 320 mm. The
rate of odontoblast differentiation determines the rate of
root elongation, and this relationship has been formally
described and referred to as the root extension rate (Shellis
1984). Calculating the changing root extension rates from
ground sections of fossil primate tooth roots allows us to
compare their growth with living primates.
A number of studies present data for rates of root
extension in humans. Stack (1967) measured the increase
in length of deciduous incisor tooth roots, which appear to
grow linearly at ca 19 mmK1. This is likely to be as fast as
human tooth roots ever grow. Root growth in permanent
teeth is, however, characteristically nonlinear and more
complex. Human permanent tooth roots can take up to 7
years to complete, and all the evidence suggest that rates of
molar root extension begin slowly, reach a peak and then
reduce in rate again as the apex of the root closes (figure 3).
Gleiser & Hunt (1955) estimated initial rates of root
extension to be ca 4 mmK1 for first permanent molars.
Feasby (1981) and Inoue & Suzuki (1992) all present data
for other permanent tooth roots that initiate with
comparably slow rates, but then rise to maximal rates of
between ca 8 and 18 mmK1 (Gleiser & Hunt 1955;
Takeshima et al. 2004).
There is a consensus that eruption rates come to exceed
rates of root growth as a tooth approaches occlusion
(Gleiser & Hunt 1955; Schumaker & El Hadary 1960;
Ando et al. 1965; Darling & Levers 1976; Feasby 1981;
Inoue & Suzuki 1992; Takeshima et al. 2004). The spurt in
root growth and the eruption surge are far from equal in
magnitude, and eruption rates can exceed root growth by
as much as 4.6 mm yrK1 in humans (Feasby 1981), and
can to some extent be predicted from the height of the jaws
(Takeshima et al. 2004).
It is clear that root extension and tooth eruption are
independent processes and that only root length at the
time of gingival emergence is a useful comparator for
Proc. R. Soc. B (2006)
mm
25
20
15
10
5
0
mesiobuccal root length
Pan
Gorilla / Pongo
Homo sapiens
crown height
total tooth height
Figure 4. Measurements from radiographs (Dean & Wood
1981, 2003) and directly from some museum specimens
indicate that total M1 mesial tooth height, from the cusps tips
to the root apex, is made up of predictable proportions of
mesial crown height and of mesiobuccal root length. Among
fossil primates, knowledge of crown height alone can be used
to predict how much root would have been formed at gingival
emergence.
gauging differences in developmental timing. Total tooth
height at gingival emergence is made up of similar
proportions of root and crown height in great apes and
modern humans (figure 4). Hence, the proportions in
living taxa allow us to calculate the likely amount of root
formed at gingival emergence in fossil primates on the
basis of measurements of crown height.
6. LIFE HISTORY AND THE EARLIEST APES
Many Miocene apes were a morphological mosaic of
characters that we recognize today as specific to either
modern apes or monkeys. Great apes have a prolonged
life-history profile compared with Old World monkeys.
They have reduced rates of mortality, longer gestation
Review
periods, mature more slowly and have and much later ages
at first reproduction (Harvey & Clutton-Brock 1985;
Kelley 1997, 2002). Kelley (1997) suggested that besides
studying their morphological attributes, M1 emergence
times in Miocene fossil apes might, in addition, identify
the first evidence of a shift to a modern ape-like life-history
profile.
Age at first permanent molar emergence has been
calculated for several fossil apes now, using the various
daily and longer-period increments preserved in fossil
enamel. These include Sivapithecus parvada (Kelley 1997,
2002), a 10 million year old ape from the Siwaliks of
Pakistan, Afropithecus turkanensis (Kelley 2002; Kelley &
Smith 2003), a 17 million year old ape from Moruorot in
northern Kenya, Dryopithecus laietanus from Can Llobateres, a 9.5 million year old site in Spain (Kelley et al.
2001) and two species of Proconsul, dated to 17.5–17.9
million years ago, Proconsul heseloni and Proconsul nyanzae
from Rusinga Island, Kenya. The consensus is that
Sivapthecus, Afropithecus and Dryopithecus had mean age
of M1 emergence times that place them firmly within the
known range for modern chimpanzees (Kelley 2004).
Harrison (1987) has argued that the various species of
Proconsul were stem catarrhines. Owing to the potential
phylogenetic implications that a modern Old World
monkey-like or modern great ape-like life-history profile
might therefore have, an age for M1 emergence in Proconsul
has been viewed as more controversial that in other Early
Miocene apes. Proconsul heseloni and P. nyanzae were both
arboreal quadrupeds, with long narrow trunks that showed
few signs of any forelimb suspensory behaviour, but
possessed frontal sinuses and a larger than expected cranial
capacity for their body size (Walker 1997). Kelley (1997),
on the basis of cranial capacity estimates, cautiously
proposed that M1 emergence in the smaller siamangsized 9–12 kg P. heseloni may have been close to 20.6
months and interpreted this as being later into development than might be expected in an Early Miocene
catarrhine. This age for M1 emergence can now be
matched using data for enamel and dentine growth
combined with data for M1 crown height in P. heseloni.
Histological data for M1 crown formation times
suggest that this took between 1 and 1.2 years (Beynon
et al. 1998), but estimates for M1 root extension rates and
of how much root might have been formed at gingival
emergence have been harder to make (Walker & Shipman
2005). Smith et al. (2006) concluded that the method
described by Shellis (1984) for calculating extension rates
and used by Beynon et al. (1998) is prone to error when
used on teeth with short, rapid periods of development.
Reanalysis of the P. heseloni M1 roots reveals average
extension rates of 9–10 mmK1 over 7 mm of root
formation. Two M1 crowns are each ca 4 mm tall (Beynon
et al. 1998). Assuming crown height to be the same
proportion of total tooth height as it is in modern
chimpanzees (62–68%), then root length formed at
gingival emergence (figure 4) will be 32–38% of total
tooth height or 47–61% of crown height. It follows,
therefore, that between 1.88 and 2.45 mm of root is likely
to have been formed at M1 emergence in P. heseloni. At an
average of 9.5 mmK1, this translates as 198–258 days of
root formation in P. heseloni. Even adding the shortest
enamel formation time estimate of 1 year to this (Beynon
et al. 1998) gives a likely age at M1 emergence as
Proc. R. Soc. B (2006)
M. C. Dean 2803
18.5–20.4 months, a remarkably close match with Kelley’s
previous estimate of 20.6 months (Kelley 1997). Even
though the small body size of P. heseloni makes it awkward
to make direct comparisons with living apes (especially
with so little data for living gibbons and siamangs; Dirks
1998), this age for M1 emergence suggests a more
prolonged life history than would be expected for an
Early Miocene catarrhine of the same body mass (Kelley
1997) and certainly contrasts with the faster enamel and
dentine formation rates of the first known fossil Old World
monkey, Victoriapithecus macinnesi (Dean & Leakey 2004).
The larger small chimpanzee-sized Proconsul nyanzae
upper M1 crown analysed by Beynon et al. (1998) is
6 mm tall and took 2 years to form its enamel in the crown.
Only 540–690 microns of the root are preserved either
buccally or lingually in this M1. It now seems likely, by the
same argument, that root length at gingival emergence
would have been 47–61% of crown height and therefore,
that 2.83–3.66 mm of root would have been formed at
gingival emergence. Extension rates in this root average
6.25 microns/day, which compares well with those known
for modern chimpanzees. Similar calculations for the sum
of crown and root formation time give an age for M1
emergence at between 3.26 and 3.6 years, which is well
within the age range known for M1 gingival emergence in
modern chimpanzees.
All these data for Miocene apes suggest that ca 18
million years ago in the hominoid lineage there was a
prolonged life-history profile that broadly matched that of
living great apes. It is important to recognize, however,
that within this profile a fast–slow dental/life-history
continuum remains even today that reflects both the
apportionment of available energy resources and population mortality rates (Godfrey et al. 2001; Dirks 2003;
Kelley 2004; Nargolwalla et al. 2005; Dirks & Bowman in
press). How this might have evolved is a more complex
issue, perhaps as an adaptive prolongation of a shorter lifehistory profile in an as yet unidentified catarrhine
ancestor, or as a simple extension of a prolonged lifehistory profile in a small bodied ancestor that simply kept
pace with increasing body size (Kelley & Smith 2003).
7. WHEN AND WHY DID OUR MODERN
LIFE-HISTORY PATTERN EVOLVE?
Modern humans have big brains, walk on two feet and
have small teeth and jaws. The earliest bipedal fossil
hominids from Chad and Kenya are dated at between 6
and 7 million years ago, but for at least the first 4 million
years of hominid evolution there is little evidence for an
increase in brain size. Brain size and body proportions
seem to have changed significantly with the emergence of
the genus Homo at about 2 million years and changes in
brain size are closely linked with many life-history traits
(Smith 1989; Allman & Hasenstaub 1999). Initially, it was
thought, almost by definition, that the earliest hominids
would show evidence of a human-like life-history profile,
but it is now generally accepted this cannot be substantiated (Bromage & Dean 1985; Smith 1986). There
are several lines of evidence that allow us to track the
evolution of life-history traits among fossil hominids.
Various incremental markings in enamel have been used to
estimate an age at M1 emergence, as have their relatively
small cranial capacities, and both approaches conclude
2804 M. C. Dean
enamel thickness (microns)
(a) 2500
2250
2000
1750
1500
1250
1000
750
500
250
0
African apes
Homo sapiens
C. torquatus
enamel thickness (microns)
(b) 2500
2250
2000
1750
1500
1250
1000
750
500
250
0
Review
African apes
Homo sapiens
Early Homo
Australopiths
100
200
300
400
500 600
enamel formation time (days)
700
Figure 5. (a) Rates of occlusal enamel formation are slowest
in modern humans, intermediate in African great apes and
fastest in the sooty mangabey (Cercocebus torquatus), irrespective of how thick enamel eventually grows. These distinct
trajectories appear to reflect the general grade shifts in
maturational rate among primates. (b) None of the early
australopithecines or fossils attributed to early Homo
(H. habilis and H. erectus) have slow occlusal enamel
formation trajectories resembling those in modern humans
(Dean et al. 2001).
these ages fall within the range known for living great apes
(Bromage & Dean 1985; Smith 1986, 1989). However,
within this generally ape-like picture, we should expect as
much variation among early hominids as we see today
among living apes and there may be hints of this in the
fossil record.
Despite similar infant diets, great ape deciduous tooth
wear patterns vary with early or late first intake of
supplementary food during the weaning period and seem
also to reflect their longer or shorter inter-birth intervals
(Aiello et al. 1991). Clearly, early hominids had diverse
diets and this is reflected in the thinner or thicker enamel
(both deciduous and permanent) of some australopithecines. Australopithecines at around 3.5 million years (e.g.
LH-2, Australopithecus afarensis) show much less deciduous
tooth wear at chronological age ca 3.5 years than later ones
at ca 2 million years (e.g. Taung, Australopithecus africanus).
But some juveniles that are chronologically younger (ca 2.5
years) show even greater degrees of dentine exposure (e.g.
KNM-ER 1477, Paranthropus boisei ) despite having thicker
enamel to counter this. It is difficult to attribute all of these
differences in deciduous tooth wear to their infant diets and
equally likely there were contrasting life-history strategies
among australopithecines that mirrored both the availability
and quality of food and their evolutionary history (Aiello
et al. 1991). In some late surviving australopithecines, heavy
Proc. R. Soc. B (2006)
deciduous tooth wear early in life may have been linked to
early first intake of supplementary food, early weaning and
shorter inter-birth intervals. Significant adaptive changes in
reproductive strategy and life history may have kept up with
pressure to survive over millions of years. After 2 million
years, only the ‘robust’ australopithecines (P. boisei from
East Africa and P. robustus from South Africa) remain in the
fossil record and these were extinct by 1 million years ago.
Cumulative trajectories describing enamel growth over
time in monkeys, apes and humans (figure 5a,b) appear to
show evidence of the major grade shifts in the pace of
general somatic growth (Dean et al. 2001). All early
hominid enamel growth trajectories fall among the African
great apes and have shorter enamel crown formation times
compared with those in modern humans (Beynon & Wood
1987; Dean et al. 2001; Reid & Dean 2005; Lacruz et al. in
press). This alone suggests that dental development as a
whole took less time than in modern humans. M1
emergence times for Homo erectus have been predicted
from average cranial capacity estimates (Smith 1992;
Smith & Tompkins 1995) and are a close match for those
derived from dental histology. The combined evidence
from both the enamel and the root extension rates in a
single H. erectus specimen from Java (S7-37) indicates that
M1 emergence times were close to 4.5 years rather than 6
years in modern humans and that M2 emergence times
were nearer to 8 years than 12 years (Dean et al. 2001). On
the one hand, this is the first evidence for a significant
change from the broadly ape-like life-history profile for ca
17 million years. On the other hand, it seems that even at
this relatively late stage of human evolution there was still
on average a faster life-history profile than in modern
humans today, but one that had slowed in parallel with a
significant increase in brain size.
The link between brain size, tooth development and a
slower life-history profile is a clear one but a curious one
(Smith 1989; Allman & Hasenstaub 1999; Godfrey et al.
2001). Kelley (2004) has argued that the whole changing
life-history profile during primate evolution has influenced
brain growth and that it is this that has ultimately
facilitated cognitive evolution. Longer periods of embryonic development have extended many phases of human
brain growth, including glial cell mitosis, dendritic growth,
synapogenesis, dendritic pruning and myelination
(McKinney 2002). Just three or four extra days of
embryonic development between E40 and E43 result in
three or four more rounds of founder cell mitosis in the
brain, which is enough to account for the 10-fold larger
human cortex than of a macaque monkey (Rakic 1995;
Hill & Walsh 2005). Brain size as well as brain complexity
is, therefore, time dependent as is dental development and
simply yet another part of the life-history package (Allman &
Hasenstaub 1999). Brain size might not then have been
driven solely by selection for cognitive ability. The sequence
of events may have begun with a shift in life-history strategy
and growth of a bigger more complex brain, which then
increased the likelihood of selection for increased cognitive
ability. And in the end, increased cognitive ability is bound to
contribute towards a further reduction in adult mortality
rates (Kelley 2004).
What then of Neanderthals whose brains were bigger
than modern humans, but whose life-history profile is
described either as at the lower limit of the modern human
range on the basis of shorter enamel formation times
Review
(Dean et al. 1986; Stringer et al. 1990; Tompkins 1996;
Guatelli-Steinberg et al. 2005) and patterns of molar tooth
wear (Wolpoff 1979; Caspari & Lee 2004) or as being
distinct and 15% shorter than modern humans (Ramirez
Rozzi & Bermudez de Castro 2004)? Clearly, the late
surviving Neanderthals were under considerable demographic pressure from both sudden colder, drier climatic
conditions and from incoming biologically and behaviourally modern human populations (Mellars 2006).
Neanderthals are likely to have experienced high levels
of infant and adult mortality. It makes no biological sense
for any primate to take 18–20 years to grow up only to die
as a young adult (Trinkaus & Tompkins 1990), but then
again the Neanderthals did not survive. Understanding
the demise of the Neanderthals may ultimately come from
a better understanding of our own survival.
At present, it is simply not clear when and where a
prolonged modern human-like growth period evolved, nor,
as with large brains, if this arose independently in
Neanderthals and modern humans (Dean 2000). The
evidence from life-history theory suggests that a reduction
in adult mortality rates is likely to have played a big role, but
providing evidence for this in the fossil record is fraught
with difficulty. Caspari & Lee (2004) calculated the ratio of
older to younger adults in successive time periods through
the hominid fossil record. They concluded that while there
was a significant and successive increase in longevity
between all the groups they examined, adult survivorship
increased most dramatically among the modern humans of
the Early Upper Palaeolithic in Europe compared with
Neanderthals (see also Trinkaus & Tompkins 1990).
A prolonged life-history profile and a long period of
dependency are costly, and it may be that modern humans
have evolved mechanisms for offsetting these costs through
increased rates of reproduction. Slow human growth
between weaning and puberty reduces the energetic
demands on parents with multiple dependents (Gurven &
Walker 2006). Delayed maturation, slower growth, shorter
inter-birth intervals, increased fertility and longevity are all
associated with early cessation of reproduction in modern
humans and the menopause (Wich et al. 2004). These
observations have implications for the importance of
investment by older generations in their children’s offspring
as a selective advantage in ensuring their survival and
thereby contributing to population increase (Hawkes et al.
1998; O’Connell et al. 1999). Effectively, we may have quite
recently, perhaps in parallel with our prolonged life-history
profile, evolved mechanisms for escaping some of
the constraints imposed by extremely slow maturation
(Allman & Hasenstaub 1999).
8. CONCLUSIONS
Primates are ecologically diverse and achieve a balance
between fertility and mortality rates by optimizing energy
resources in many different ways. Major shifts in lifehistory profile seem to have been rare during the last 20
million years of primate evolution, but even today there is
considerable variation on the broad ape-like life-history
theme as there was always likely to have been during the
early stages of human evolution. It seems our own
extended life-history profile may have evolved quite
recently and primarily in response to low adult mortality
rates. However, this may now be linked to novel ways of
Proc. R. Soc. B (2006)
M. C. Dean 2805
investing more time and energy in our young, but at the
same time increasing reproductive rates by reducing interbirth intervals. The future prospects for retrieving more
about primate life histories from fossil teeth are promising.
Moreover, the better we come to understand the processes
involved in controlling rates of enamel and dentine
formation, the closer we get to defining the mechanisms
that underlie evolutionary changes in developing primate
dentitions.
I am grateful for the helpful comments of three referees.
I thank The Leverhulme Trust and The Royal Society for
grants awarded to me for research on comparative dental
development. I am grateful to the National Museums of
Kenya for access to fossil primate material in their care.
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