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Effect of diet on dental development in four species of catarrhine primates.

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American Journal of Primatology 61:29–40 (2003)
RESEARCH ARTICLE
Effect of Diet on Dental Development in Four Species of
Catarrhine Primates
WENDY DIRKSn
Department of Anthropology, Division of History and Social Science,
Oxford College of Emory University, Oxford, Georgia
In this study, dental development is described in two pairs of closely
related catarrhine primate species that differ in their degree of folivory:
1) Hylobates lar and Symphalangus syndactylus, and 2) Papio hamadryas
hamadryas and Semnopithecus entellus. Growth increments in histological thin sections are used to reconstruct the chronology of dental
development to determine how dental development is accelerated in the
more folivorous species of each pair. Although anterior tooth formation
appears to be unrelated to diet, both S. syndactylus and S. entellus
initiate the slowest-forming molar earlier than the related less-folivorous
species, which supports the hypothesis that dental acceleration is related
to food processing. S. syndactylus initiates M2 crown formation at an
earlier age than H. lar, and S. entellus initiates and completes M3 at an
earlier age than P. h. hamadryas. Similar stages of M3 eruption occur
earlier in the more folivorous species; however, the sex of the individual
may also play a role in creating such differences. Although the age at M3
emergence is close to that reported for the end of body mass growth in lar
gibbons, hamadryas baboons, and Hanuman langurs, M3 emergence
may not be coupled to body mass growth in siamangs. Am. J. Primatol.
61:29–40, 2003.
r 2003 Wiley-Liss, Inc.
Key words: dental development; folivory; Hylobates; Symphalangus;
Papio; Semnopithecus
Contract grant sponsor: NSF; Contract grant number: SBR-9700822; Contract grant sponsors:
James Arthur Dissertation Fellowship; New York University Graduate School of Arts and Science;
Elizabeth S. Watts Fellowship in Nonhuman Primate Growth and Development, American Society
of Primatologists.
n
Correspondence to: Wendy Dirks, Oxford College of Emory University, 100 Hamill St., Oxford,
GA 30054. E-mail: wdirks@emory.edu
Received 10 January 2003; revision accepted 11 July 2003
DOI 10.1002/ajp.10106
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2003 Wiley-Liss, Inc.
30 / Dirks
INTRODUCTION
Several studies of primate ontogeny and life history have discussed the
relationship between diet and growth [Altmann, 1998; Janson & van Schaik,
1993; Leigh, 1994]. Janson and van Schaik [1993] suggested that the slow growth
of primates during the long juvenile period from weaning to first reproduction is a
result of increased ecological risks during that stage. Leigh [1994] found that
folivores grow more rapidly than frugivores, and suggested that this is due to
decreased ecological risk in folivores. He proposed that juvenile folivores require
acceleration of dental development to process leaves in seasonal environments,
and that their rapid growth in body mass allows for this through the correlation of
skeletal growth, size increase, and dental maturation.
Studies of dental emergence have demonstrated this acceleration of dental
development in folivores relative to that of nonfolivores [Eaglen, 1985; Godfrey
et al., 2001; Harvati, 2000; Taylor, 1997]. Histological methods can demonstrate a
more precise chronology of acceleration during the developmental period, as well
as highlight aspects of variation; however, they generally are not applied to large
sample sizes and thus preclude broad generalizations. In this study, histological
methods were used to reconstruct dental development in four species of
catarrhines to examine the effect of diet on dental development. The ages at
initiation and completion of the crowns, and the rate of root growth are compared
in a small sample comprised of two closely related hominoids: the highly
frugivorous Hylobates lar and the more folivorous Symphalangus syndactylus
[Chivers, 1972; Curtin & Chivers, 1978; Palombit, 1997]. Dental development is
also compared in two cercopithecoids with fairly eclectic diets, which differ in
their degrees of folivory: Papio hamadryas hamadryas and Semnopithecus
entellus [Bauchop, 1978; Bennett & Davies, 1994; Hladik, 1977; Kar-Gupta &
Kumar, 1994; Koenig et al., 1997; Nagel, 1973; Nystrom, 1992; Ripley, 1965,
1970].
METHODS
Study Sample
The specimens used to reconstruct dental development are listed in Table I.
The generic distinction between the hylobatids follows Schultz [1933] and Roos
and Geissmann [2001]. Additional details of dental development in H. lar
NYU008 and P. h. hamadryas 73261 and 73436 that were not considered in this
study can be found in Dirks [1998] and Dirks et al. [2002]. Only permanent
mandibular teeth were used in the analysis.
Reconstruction of Dental Development
Dental development was reconstructed using the incremental growth
markers that are visible in polarized light in the enamel and dentine. These
increments include daily cross striations and longer period striae of Retzius in
enamel, as well as the corresponding daily von Ebner and longer period Andresen
lines in dentine [Dean, 1995, 2000]. The method used for reconstruction of dental
development in H. lar NYU008 is given in Dirks [1998] and Dirks et al. [2002] for
P.h. hamadryas 73436 and 73261. Dental development in S. syndactylus 1993 was
reconstructed using the method described by Reid and coworkers [1998]. Dental
development in all of the other specimens except H. lar AS1627 was reconstructed
in a similar manner using digital images generated with a Leitz Laborluxs 12 Pol
S microscope. All measurements and counts of growth increments were made
NYU008
NYU011
NYU029
AS1627
1993
1728
73436
73261
845/70
H. lar
H. lar
H. lar
H. larc
S. s. syndactylusd
S. syndactyluse
P. h. hamadryasf
P. h. hamadryasg
S. e. priam
c
b
Developing mandibular teeth only.
Not available.
C1, M33 erupting.
d
rdi2 in occlusion, LI2 erupting.
e
I1 missing, M3 erupting.
f
M2 erupting.
g
M3 erupting.
a
Specimen
Species
Unknown
Unknown
Unknown
Male
Unknown
Female
Female
Female
Female
Sex
Unknown
Unknown
Unknown
Thailand
Sumatra
Unknown
Ethiopia
Ethiopia
India
Origin
Lower
dentition
I1–2dc1–dp4M1
I1-M3
I1–2dc1-dp4M1
I1-M3
I1–2dc1-dp4M1
I2-M3
I1-M1
I1-M3
I1-M3
Upper
dentition
I1di2-dp4M1
I1-M3
N/Ab
I1–2dc1P3–4M1–3
I1i2dc1-dp4M1
N/Ab
I1-M1
I1-M3
I1-M2
C1P3–4
None
C1M2–3
None
C1-P4M2–3
None
M3
None
None
Tooth
germsa
I1–2P4M1–2
C1
I1-M3
P4-M3
I1-M3
I2-M3
I1-M3
I1-M3
I1-M3
Teeth
used
TABLE I. Description of Specimens Used in Reconstructing Dental Development in Hylobates lar, Symphalangus syndactylus, Papio hamadryas
hamadryas, and Semnopithcus entellus priam
Diet and Dental Development / 31
32 / Dirks
using the public domain NIH Image Version 1.61 (developed at the U.S. National
Institutes of Health and available on the Internet at http://rsb.info.nih.gov/nihimage). Details are given in Dirks [2001]. Dental development in H. lar AS1627
was reconstructed in the same manner using Improvision Openlab 2.0.7 image
analysis software with a Zeiss Universal photomicroscope.
Four of the specimens (H. lar AS1627, S. syndactylus 1728, P. hamadryas
73261, and S. entellus 845/70) were in the process of M3 eruption at the time of
their death. Both hylobatids were at similar stages, with cusp tips just beginning
to emerge above alveolus, and both cercopithecids were also at comparable stages,
with mesial cusps below the level of the occlusal plane, and the distal cusps just
emerging. The male lar gibbon differed from the other three specimens (all
female) in that their mandibular canines had fully erupted, while his canine cusp
tips were just beginning to emerge. The age at death in these specimens was
determined by using the growth increments visible in the roots, and adding the
root formation time to the age at which crown formation was complete. To
determine the extension rate (the rate at which the root elongated), the length of
the root was divided by the total number of days of root formation. This provides a
crude estimate of extension rate for comparative purposes only, because root
extension does not proceed at a steady pace as the root forms [Beynon et al., 1998;
Dean, 1995, 2000; Dean & Scandrett, 1995].
RESULTS
The estimated ages at initiation and completion of tooth crowns are given in
Table II. The age at initiation for I1 in S. entellus 845/70 is a minimum, based on
the assumption that M1 initiates at around birth, as the cusp was too worn to
indicate a more exact age. In all the other specimens, I1 precedes initiation of I2,
and this is likely to be the case in S. entellus 845/70 as well. The estimated age at
initiation of P4 in S. syndactylus 1728 is also a minimum, as cuspal enamel was
lost during preparation. The age at initiation and completion of crown formation
was similar among individuals of the same species. The greatest disparity for
crown initiation within a species was in the age at initiation of M3 in Hylobates lar
NYU029 and AS1627. However, H. lar NYU029 is a captive individual of
unknown sex, while AS1627 is a wild-caught male. This difference may be related
to earlier initiation due to captivity, or H. lar NYU029 may be a female.
The sequence of initiation and completion of incisors, canines, and premolars
differed among all four species; however, incisor initiation always preceded
premolar initiation. The chronology of development of these teeth appears to be
unrelated to diet, since there are no obvious similarities between siamangs/
langurs and baboons/lar gibbons in terms of such development.
The molar sequence was the same in all four species. Relative to the baboon,
however, the langur exhibited accelerated initiation and completion of M3.
Relative to the gibbon, the siamang had accelerated initiation, but not completion,
of M2. This acceleration of M2 initiation was apparent even when the variation
between individuals was considered. Figure 1 illustrates the chronology of molar
development in each individual in the study in which the third molar had initiated.
Table III summarizes formation times for each completed tooth crown in all
of the specimens used in the study. For all teeth, crown formation times were
shorter in langurs than in baboons. However, there was no consistent pattern of
differences in crown formation times between the two hylobatid species. In S.
syndactylus 1728, M2 took longer to form than either M1 or M3, while in H. lar
AS1627, M3 took longer to form than either of the other molars. In both folivores,
0.60–3.29
0.62–3.00
0.23–1.50
P. h. hamadryas
73436f
73261f
S. e. priam
845/70g
0.17–1.65
0.69–3.33
0.65–3.19
0.36–2.04
0.38–2.08
0.30–2.08
0.38–1.89
–
I2
0.42–2.20
0.73–3.90
0.71–3.98
0.19–incg
0.25–3.65
–
0.34–incg
–
C1
0.35–2.21
1.10–3.21
1.10–3.10
0.56–3.08
0.56–3.29
–
1.35–2.58
–
P3
0.68–1.80
1.48–3.29
1.54–3.17
0.99–2.69
1.08–2.46
1.27–2.54
1.30–2.65
1.48–3.05
P4
0.00–0.89
(–0.10)–1.38
(–0.10)–1.35
(–0.13)–1.36
(–0.18)–0.92
(–0.04)–1.12
(–0.10)–1.02
0.00–1.10
M1
1.13–2.45
1.38–3.12
1.35–2.88
0.66–2.49
0.51–2.32
1.01–2.17
0.98–2.57
1.28–2.42
M2
2.21–3.73
3.65–inch
3.75–5.71
2.61–inch
2.36–3.50
–
2.24–inch
2.94–5.00
M3
c
b
M1 based on hypoconid; M2 based on entoconid [see Dirks, 1998].
M1 based on unidentified mesial cusp (initiation) and entoconid (completion); M2 and M3 based on protoconid.
M1 and M2 based on hypoconid, M3 based on entoconid.
d
M1 based on protoconid (initiation) and hypoconid (completion); M2 and M3 based on protoconid.
e
M1 based on entoconid (initiation) and metaconid (completion); M2 based on protoconid (initiation) and hypoconid (completion); M3 based on metaconid (initiation) and hypoconid
(completion).
f
All molars based on protoconid [see Dirks et al., 2002].
g
M1 based on entoconid; M2 based on protoconid; M3 based on protoconid (initiation) and hypoconid (completion).
h
Incomplete at death.
a
0.32–2.25
–
(–0.01)–1.42
0.02–1.54
–
H. lar
NYU008a
NYU029b
AS1627c
S. syndactylus
1993d
1728e
I1
Specimen
TABLE II. Estimated Ages at Initiation and Completion of Crowns in Hylobates lar, S. syndactylus, Papio h. hamadryas, and Semnopithecus entellus
priam in years
Diet and Dental Development / 33
34 / Dirks
M1
P. hamadryas 73436
M2
+
M3
M1
P. hamadryas 73261
M2
M3
M1
S. entellus 845/70
M2
Tooth Type
M3
M1
H. lar NYU029
M2
+
M3
M1
H. lar AS1627
M2
M3
M1
M2
S. syndactylus 1993
+
M3
M1
S. syndactylus 1728
M2
M3
-1.00
0.00
1.00
2.00
3.00
4.00
5.00
6.00
7.00
Age (Years)
Fig. 1. Bar charts illustrating age at initiation and completion of molar crown formation in Papio
hamadryas hamadryas, Semnopithecus entellus, Hylobates lar, and Symphalangus syndactylus
individuals in which third molar formation had initiated. Bars represent M1–M3 in each individual.
Black is cusp formation, light gray is imbricational (lateral and cervical) enamel formation, and
dark gray is total crown formation. Plus signs indicate incomplete crown at death.
the formation of the slowest-forming molar appeared to be accelerated relative to
that in the less folivorous species.
For one specimen of each species, Table IV lists the age at which M3 was
erupting at the time of death. Table IV also includes the length of the erupting M3
roots as a proportion of the total length of the complete M2 roots, as well as the
average daily extension rate of the distal M3 root. The larger, more folivorous
female siamang was a year younger than the male lar gibbon at a comparable
stage of M3 eruption. The more folivorous female Hanuman langur was 2 yr
younger than the female hamadryas baboon at comparable stages of M3 eruption.
However, in both pairs the folivore had a slower average root extension rate,
which suggests that it is the difference in the chronology of crown formation,
rather than root extension, that creates accelerated molar development in
folivores. Although the average extension rate in the mesial M3 roots could not be
determined in all of the specimens due to the plane of section, an average
extension rate of 17.6 mm per day was determined in the mesial M3 root of S.
entellus 845/70. Root extension was faster in both cercopithecids than in the
hylobatids, which points to phylogenetic effects on root growth rather than
dietary effects. Cercopithecids may simply have faster rates of root growth than
hominoids, regardless of diet.
DISCUSSION
Dietary studies indicate that although gibbons can spend 22–25% of their
feeding time consuming young leaves, their diets are largely based on ripe fruit,
Diet and Dental Development / 35
TABLE III. Estimated Crown Formation Times in Hylobates lar, S. syndactylus, Papio
hamadryas hamadryas, and Semnopithecus entellus priam in years
Specimen
I1
I2
C1
P3
P4
M1
M2
M3
H. lar
NYU008a
NYU011b
NYU029c
AS1627d
1.43
–
1.52
–
1.78
–
1.51
–
–
3.08
–
–
–
–
1.23
–
1.27
–
1.35
1.57
1.16
–
1.12
1.10
1.16
–
1.59
1.14
–
–
–
2.06
S. syndactylus
1993e
1728f
1.93
–
1.68
1.70
–
3.40
2.52
2.73
1.70
1.38
1.49
1.10
1.83
1.81
–
1.14
P. h. hamadryas
73436g
73261g
2.69
2.38
2.64
2.54
3.17
3.27
2.11
2.00
1.81
1.63
1.48
1.45
1.74
1.53
–
1.96
S. e. priam
845/70h
1.27
1.48
1.78
1.86
1.12
0.89
1.32
1.52
a
M1 based on hypoconid; M2 based on entoconid [see Dirks, 1998].
C1 based on worn specimen; minimum estimate.
M1 based on unidentified mesial cusp (initiation) and entoconid (completion); M2 and M3 based on protoconid.
d
M1 and M2 based on hypoconid, M3 based on entoconid.
e
M1 based on protoconid (initiation) and hypoconid (completion); M2 and M3 based on protoconid.
f
M1 based on entoconid (initiation) and metaconid (completion); M2 based on protoconid (initiation) and
hypoconid (completion); M3 based on metaconid (initiation) and hypoconid (completion).
g
all molars based on protoconid [see Dirks et al., 2002].
h
M1 based on entoconid; M2 based on protoconid; M3 based on protoconid (initiation) and hypoconid (completion).
b
c
TABLE IV. Root Development and Age at M3 Emergence Based on Age at Death in Specimens
of Hylobates lar, S. syndactylus, Papio hamadryas hamadryas, and Semnopithecus entellus
priam
Specimen
H. lar AS1627
S. syndactylus 1728
P. h. hamadryas 73261
S. e. priam 845/70
Mesial
root
length
(mm)
Proportion
formed
Distal
root
length
(mm)
Proportion
formeda
Average
extension
rate
(mm/day)b, c
Age
at death
(yrs)
2.80
5.29
–
6.16
0.45
0.55
–
0.71
2.78
2.57
7.55
3.88
0.44
0.27
0.73d
0.48
6.8
4.3
19.9
11.4
6.1
5.2
6.8
4.7
a
Based on total length of M2 root; length M3/length M2.
Microns per day, averaged over total period of root formation (see text for details).
Based on distal root.
d
Based on M2 mesial root.
b
c
especially figs [Bartlett, 1999; Ellefson, 1974; Palombit, 1997; Raemakers, 1984;
Ungar, 1993]. Siamangs are more folivorous, but their diet also includes a high
proportion of figs and other fruits [Chivers, 1972, 1974; Gittins & Raemaekers,
1980; MacKinnon & MacKinnon, 1980; Palombit, 1997]. The amount of fruit in
the diet of both lar gibbons and siamangs varies according to its abundance;
however, where they are sympatric, the siamang always includes more leaves in
36 / Dirks
its diet–ranging from 16% of feeding time in some studies to 44% of the yearly diet
in others [MacKinnon & MacKinnon, 1980; Palombit, 1997; Raemakers, 1984].
Even though lar gibbons (mean female body mass=5.34 kg) are approximately half the size of siamangs (mean female body mass=10.7 kg) in the
Sumatran subspecies [Smith & Jungers, 1997], it may take as long (or longer) for
a crown to form in gibbons than it does in siamangs. In addition, molar emergence
appears to be completed a year earlier in female siamangs than in male lar
gibbons. The sample in this study was too small to allow the effect of sex on
differences in molar emergence to be taken into account. Nevertheless, the results
support the hypothesis that dental development is accelerated in the more
folivorous siamang.
Figure 1 shows intraspecific variation in ages at onset and completion of
crown formation. The greatest variation is in the degree of overlap between the
end of M2 crown formation and the onset of M3 crown formation. H. lar NYU029
and S. syndactylus 1728 show overlap, while H. lar AS1627 and S. syndactylus
1993 do not. A previous study found no evidence of overlap in H. lar NYU008
[Dirks, 1998]. Some of this variation may reflect the fact that not all cusps were
used in determining crown formation (Table II). If all cusps for each tooth were
used, there would be less time between the completion of M2 and the initiation of
M3, as cusp formation is not simultaneous [Dirks, 2001]. Another possible reason
for the observed variation may be differences between the sexes. If this is the case,
it is possible that both H. lar NYU029 and S. syndactylus 1728 are female, and
H. lar NYU008, H. lar AS1627, and S. syndactylus 1993 are male. The only two
specimens of known sex were S. syndactylus 1728 (a female with overlap in M2
and M3 development) and H. lar AS1627 (a male without overlap). It seems less
likely that these differences are due to more rapid dental development in captive
animals compared to wild animals [Phillips-Conroy & Jolly, 1988], because both
NYU029 (with overlap in M2 and M3 development) and NYU008 (without overlap)
[Dirks, 1998] were captive individuals. Both S. syndactylus 1728 and H. lar
AS1627 were wild-caught individuals.
Although both hamadryas baboons and Hanuman langurs have highly
eclectic diets, langurs consume a higher proportion of mature leaves. The baboons
in this study were from the Awash National Park hybrid zone, an area of contact
and gene flow between populations of hamadryas and anubis baboons [Dirks et al.,
2002]. Baboon diets in the hybrid zone are heavily based on flowers and beans of
the Acacia species, but also include grass shoots, sedge roots, fruits, and some
leaves [Nagel, 1973]. These diets are similar to hamadryas diets elsewhere in
Ethiopia, where beans and dry leaves of acacia account for 84% of the diet during
the dry season, with a shift to acacia flowers and grass seeds during the long rains
[Kummer, 1968]. The diet of Semnopithecus entellus priam has not yet been
studied; however, the yearly diet of the closely related subspecies S.e. thersites
consists of 21% mature leaves, 27% new leaves, 7% flowers, and 45% fleshy fruits
(especially figs) [Hladik, 1977].
Hanuman langurs and baboons are similar in body mass, although both
species vary considerably in terms of geographic range. The mean female body
mass of S.e. priam is 9.9 kg [Napier, 1985; Roonwal, 1981]. The mean female
body mass of baboons from the Awash hybrid zone has also been reported to be
9.9 kg [Phillips-Conroy & Jolly, 1981]; however, this was determined during a
drought, and it is believed that the mean female body mass is actually slightly
heavier (C.J. Jolly, personal communication). Nevertheless, the total period of
crown formation, as well as crown formation time for individual teeth, is much
shorter in the langur than in the baboon.
Diet and Dental Development / 37
Smith and coworkers established a correlation between the timing of the
emergence of the first permanent molar and weaning [Smith, 1989a, b, 1992;
Smith et al., 1994]. The emergence of the permanent molars is critical to food
processing, and the need for folivores to accelerate molar development has been
addressed in a number of previous studies. Eaglen [1985] suggested that variation
in the timing of tooth emergence in Malagasy lemurs is related to differences in
seasonal and interspecific differences in the degree of folivory during ontogeny.
Leigh [1994] found that body mass increased more rapidly in folivores during
ontogeny than in nonfolivores of similar adult body mass, and that it may be more
efficient for relatively larger subadults to obtain nutrients from leaves during
weaning and periods of seasonal dependence on foliage. He further suggested that
a genetic correlation between dental development and skeletal/body growth, and
the need to process leaves at relatively young ages leads to accelerated dental
development. He proposed that reduced ecological risk in folivores [Janson & van
Schaik, 1993] permits an acceleration in growth relative to that in nonfolivores.
The age at emergence of the third molars in the specimens in this study was
consistent with data on body mass growth in all species except the siamangs.
Captive lar gibbons reach adult size at ~6 yr of age [Kirkwood & Stathatos, 1992;
Leigh & Shea, 1995], while siamangs grow until they reach the age of B7.5 yr
[Leigh & Shea, 1995]. The earlier emergence of M3 in the siamang is consistent
with the hypothesis that folivores experience accelerated dental development, but
suggests that dental development and body mass growth are uncoupled in
siamangs. This uncoupling of dental development and body mass was recently
demonstrated in a histological study of dental development in a subfossil lemur
[Schwartz et al., 2002]. Wild hamadryas baboons do not change in appearance
after ~5.6 years of age; however, body mass may increase until B7 yr [Sigg et al.,
1982]. Female Hanuman langurs appear to reach adult body mass at about 4.5–5
yr in captivity and at Pollanaruwa [Leigh, 1994; Ripley, 1965]. M3 emergence is
close to the end of body mass growth in both cercopithecids.
The notion of accelerated dental development has also been explored in
studies of dental emergence [Godfrey et al., 2001; Harvati, 2000]. Harvati [2000]
examined dental emergence sequences in seven colobine taxa, and found that
molar emergence occurred earlier in the overall sequence in six of these taxa than
it did in macaques. However, the most folivorous taxon did not exhibit the
greatest degree of accelerated molar emergence, and it was suggested that life
history, body size, phylogeny, and facial morphology may also play a role [Harvati,
2000].
Godfrey and coworkers have conducted a number of studies on accelerated
dental development in a wide range of primate taxa, with a focus on Malagasy
lemurs [Godfrey et al., 2002; King et al., 2001; Schwartz et al., 2002]. In a
synthesis testing a number of hypotheses concerning variation in primate dental
development, Godfrey et al. [2001] found that folivores did exhibit accelerated
development by the age at weaning. They suggested that dietary hypotheses
based on foraging independence and food processing explain developmental
variation better than those that connect dental development to life history or its
correlates. While they did not examine dental development beyond the age at
weaning, the results of this study support their food-processing hypothesis, which
suggests that selection has acted on these animals’ ability to process a folivorous
diet by accelerating dental development [Godfrey et al., 2001]. Because of the
small sample size, limited comparisons, and degree of intraspecific variation in
the current study, the results must be interpreted with caution. Nevertheless, it
was found that, in comparison with less-folivorous species, the folivores initiated
38 / Dirks
crown formation of the slowest-forming molar earlier, had a shorter period of
crown formation, and experienced earlier emergence of the third molar.
ACKNOWLEDGMENTS
I gratefully acknowledge the assistance of Terry Harrison, Tim Bromage,
Todd Disotell, Cliff Jolly, and Sara Stinson (New York Consortium in
Evolutionary Primatology); Randall White (New York University); Don Reid,
Ian Bell, Pam Walton (Department of Oral Biology, Dental School, University of
Newcastle-upon-Tyne); and R.D. Martin, Nina Bahr, and Margrit Peltier
(Anthropologisches Institut of the Universität Zürich-Irchel). Gary Schwartz
and two anonymous reviewers offered helpful comments on an earlier draft of this
work.
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