How Neanderthal molar teeth grew
Roberto Macchiarelli1, Luca Bondioli2, Andre ´ Debe ´nath3, Arnaud Mazurier1,4, Jean-Franc ¸ois Tournepiche5,6,
Wendy Birch7& Christopher Dean7
Growth and development are both fundamental components of
demographic structure and life history strategy. Together with
information about developmental timing they ultimately contrib-
ute to a better understanding of Neanderthal extinction. Primate
molar tooth development tracks the pace of life history evolution
as the timing of crown and root growth. High-resolution micro-
and uncover subtle differences inadult tooth morphology that are
determined early in embryonic development3. Here we show that
the timing of molar crown and root completion in Neanderthals
matches those known for modern humans but that a more com-
plex enamel–dentine junction morphology and a late peak in root
extension rate sets them apart. Previous predictions about Nean-
derthal growth, based only on anterior tooth surfaces4,5, were
necessarily speculative. These data are the first on internal molar
ables within those known for modern humans.
enamel–dentine junction (EDJ) and about the timing of crown and
second molar (S14-5) from the Riss III level (OIS 6) of Abri Suard,
and a lower left permanent first molar (BD-J4-C9) from the Riss-
Wu ¨rm level (OIS 5e) of Abri Bourgeois-Delaunay (Supplementary
A record of growth exists in the enamel and dentine that allows us
to reconstruct their developmental history and the timing of crown
and rootformation7,8.Some morphological features ofthe crown are
theresultofsuperficialovergrowths attheenamelsurfacetoward the
end of formation as a result of a longer secretory lifespan of amelo-
blasts. Others have an earlier developmental history and are map-
ped out at the EDJ in the embryonic tooth germ3. These are formed
under the control of a signalling centre, the enamel knot, which
directs differential proliferation and folding along the inner enamel
We first used high-resolution synchrotron radiation micro-com-
puted tomography (SR-mCT) images to reveal the EDJ within both
Neanderthal molars (Fig. 1). The Neanderthal metaconid or mid-
trigonid crest, a typically diagnostic feature of Neanderthal molars11,
emerges as a distinct structure that is initially defined during early
1Laboratoire de Ge ´obiologie, Biochronologie et Pale ´ontologie Humaine, UMR 6046 CNRS, Universite ´ de Poitiers, 86022 Poitiers, France.2Sezione di Antropologia, Museo Nazionale
Preistorico Etnografico ‘L. Pigorini’, 00144 Rome, Italy.3Universite ´ de Perpignan, 66000 Perpignan, France.4Etudes Recherches Mate ´riaux, 86022 Poitiers, France.5Muse ´e
d’Angoule ˆme,16000Angoule ˆme,France.6UMR5199CNRS,Universite ´Bordeaux1,33405Bordeaux,France.7DepartmentofAnatomyandDevelopmentalBiology,UniversityCollege
London, London WC1E 6BT, UK.
Figure 1 | SR-mCT-based three-dimensional virtual reconstruction of
deciduous and permanent Neanderthal molars from La Chaise. The
transparent enamel caps are compared with a modern human permanent
molar (slightly oblique mesiobuccal views). a, Neanderthal lower right
deciduous second molar (LRm2). b, Neanderthal lower left permanent first
molar (LLM1). c, Modern human lower M1. In each of the molars from La
Chaise, the metaconid, or mid-trigonid, crest (arrow), typical of
Neanderthals but rare in modern humans, runs in both dentine and enamel
between the two anterior cusps (metaconid and protoconid); in the
human specimen. Scale bar, 2mm.
Vol 444|7 December 2006|doi:10.1038/nature05314
more complex EDJ topography relative to the enamel surface area in
both deciduous and permanent Neanderthal teeth (Supplementary
Table 1). The percentage ratio between EDJ area and enamel surface
area suggests that both modern human and Neanderthal deciduous
molars have proportionately greater EDJ surface areas than perman-
ent molars. However, both deciduous and permanent Neanderthal
molars show a more complex EDJ than is typical of modern
humans12, with about 10% greater surface area. Larger sample sizes
will be required to confirm this and focus further on how this might
relate to function13,14.We then used thin ground sections ofthe same
molar teeth and polarized light microscopy to compare the sub-
sequent timing of enamel formation, crown completion and root
formation with times known for modern humans of diverse geo-
There has been speculation, but no data, for the timing of molar
tooth formation and gingival emergence in Neanderthals17–20. We
to retrieve information about the timing and rate of enamel forma-
tion. Birth is marked in deciduous teeth and first permanent molars
by an accentuated neonatal line. The position of this line depends
upon the time of initial mineralization in utero as well as on the time
of birth. Enamel secretion rates through the first-formed molar cus-
palenamelofthe Neanderthaldeciduousmolar (Fig.2)show aslight
gradient from the EDJ to the enamel surface (increasing as modern
humans do from between 2 or 3mm per day to about 4mm per day)
formation during the immediate period after birth. The position of
the neonatal line anddurationof this reaction to the changing physi-
ology at birth is similar to that in modern humans21.
Enamel secretion rates through the first-formed cuspal regions of
the Neanderthal permanent molar teeth (Fig. 3) show a steeper gra-
dient than in deciduous teeth, exactly as in modern humans22but
with slightly higher rates at the EDJ (increasing from about 3mm per
day rather than about 2.5 to about 5mm per day). The total crown
formation times in both deciduous and permanent molars were
nearly identical with those reported for large samples of modern
humans15,16. Protoconid initiation in the M1 occurred about 15 days
before birth (neonatal line) and metaconid initiation about 18 days
Distance from enamel dentine junction (µm)
La ChaiseModern ModernModern
100500100 500100 500
Enamel formation rate (µm d–1)
Figure 2 | Graphs of deciduous second molar enamel formation rates for
the Neanderthal and three typical modern human deciduous molars. Each
box plot is for a minimum of ten groups of five cross-striations averaged at
100-mm zones of enamel as measured from the EDJ (the horizontal lines in
each box show 25th, 50th and 75th centiles. The whiskers indicate 10th and
90th centiles). The vertical black line indicates the position of the neonatal
line with respect to the EDJ and the measurements of daily secretion rates
(red, prenatal; blue, postnatal). The positions of the neonatal line and the
recovery phase after birth are similar. In the Neanderthal, the neonatal line
occurred about 60 days after initiation in the metaconid and about 100 days
in the protoconid. The total crown formation time was about 315 days.
Monthly zones of occlusal enamel formation
Modern M1 Modern M1La Chaise
Enamel formation rate (µm d–1)
Figure 3 | Graphs of daily occlusal enamel formation rates in the
permanent Neanderthal M1 and in modern human molars. Daily rates are
averaged as a box plot (with elements defined as in Fig. 2) for successive
months of occlusal enamel formation in each molar and are essentially
similar. There is a steep gradient of increase in enamel formation rates in all
cases. Mean values of measurements in the first monthly zone (n557 from
four modern human molars) were 2.460.3mm per day (mean6s.d.). In
Neanderthals, rates during thefirst monthwere slightly higherand closerto
3mm per day. Measurements in the M1 from La Chaise (n513) were
2.960.4mm per day and in Tabun C1 (ref. 18) (n510) they were
3.260.4mm per day. Maximum rates at the surface enamel increase to
about 5 or 6mm per day in both Neanderthals and modern humans.
Root length (mm)
Root formation time (days)
400800 1,2001,6002,000 2,400
Figure 4 | Growth curves for roots of M1 for 20 modern humans (by sex)
slower growth curves between sexes in modern humans (open circles,
females; open squares, males). The Neanderthal root (filled circles) has a
rises quickly towards the end of root growth. The combined time of
protoconid formation in La Chaise M1 (1,041 days) and root formation
(2,119 days) totals 3,160 days or about 105 months (about 8.7 years). The
root formation stage in La Chaise M1 was just short of complete closure at
the time of death. Estimates of the mean age of attainment of M1 apex
formation in modern humans with the ‘root canal terminally divergent’
7.7 months) and 94.1 months, or 7.8 years, in girls (s.d. 8.1 months) with a
in boys and 102.5 months (8.54 years) in girls.
NATURE|Vol 444|7 December 2006
after birth. The protoconid took about 1,041 days to form to the
cervix and the metaconid about 865 days to the cervix, both only
(1,117655 and 936655 days). Protoconid lateral enamel forma-
tion took about 645 days and expressed about 90 surface perikymata
with a periodicity of 7 days.
The timing of root completion in the Neanderthal M1 from La
8.7 years of age in this Neanderthal. However, Neanderthal molars
are typically taurodont with a long root trunk and with late bi-
furcation or trifurcation of the roots. Rates of M1 root elongation
(root extension24) in modern humans and in this Neanderthal differ
(Fig. 4), with slow early root extension rates and a very late peak or
spurt shortly after root bifurcation in the Neanderthal (Fig. 5).
Counts and packing patterns of perikymata on anterior tooth
surfaces show that the large incisors and canines of Neanderthals
formed more quickly than in some modern humans4,5. Period-
icities of perikymata determined in this study and from Tabun C1
(ref. 18) (7 and 8 days, respectively) bolster these conclusions.
However, gingival emergence of the first permanent molar is a more
reliable measure of relative dental development than are anterior
tooth crownformation times andis also tightly correlated with brain
size in anthropoid primates1,2. Our data now allow us to predict M1
emergence time in Neanderthals with more certainty. If about 8mm
of root were formed at an average ofabout 5.7mmper day at gingival
emergence, then this would have occurred at about 6.7 years of age,
well within the human range (6.260.8 years (mean 6 s.d.))23. This,
together with the modern human-like position of the neonatal line,
suggests both similar timing of tooth initiation relative to birth in
Neanderthals and modern humans, and a predictable extended per-
iod between birth and M1 emergence, by which time about 90% of
brain volume would have been attained1,25.
Onehundredand fifty yearsafterthe discovery oftheNeanderthal
type specimen, the prospects for further work on the complex rela-
tionships between jaw size and jaw growth26, early permanent molar
initiation27,28and those factors that underlie rates of tooth eruption
that are faster than usual29are good. Moreover, improved imaging
techniques30combined with further histological analyses of decidu-
ous and permanent tooth enamel are likely to reveal evidence for any
changing patterns of perinatal stress as Neanderthals approached
extinction and so provide critical evidence about the shift in balance
between adult mortality rates, fertility rates and infant survival
among more recent Neanderthals than those at La Chaise.
Micro-computed tomography analysis. Virtual three-dimensional reconstruc-
tions and measurements (Supplementary Information) are based on a high-
resolution SR-mCT record performed at the beamline ID17 set at the
European Synchrotron Radiation Facility, Grenoble (http://www.esrf.fr/
UsersAndScience/Experiments/Imaging/ID17/; experiments SC-1587 and SC-
1749). The system is characterized by a continuous energy spectrum, a high
photon flux, an intense monochromatic X-ray beam, nearly parallel projections
point. Monoenergetic X-ray beams enable absolute linear attenuation co-
efficients to be measured and avoid the risk of beam-hardening artefacts in the
reconstruction of images from dense specimens such as highly mineralized fos-
sils30. Scans of the two Neanderthal teeth from La Chaise were performed at
energies of 51keV (deciduous) and 70keV (permanent). Projections (of 22.6
taken every 0.12u and were collected by a 2,04832,048 fibre-optical taper
charge-coupled device Frelon camera. Final sections were reconstructed from
sinograms and saved in a 32-bit floating-point raw format at a resolution (voxel
size) of 45.5345.5345.7mm3. The final eight-bit volumes (23932623351
pixels for the deciduous molar and 49333573237 pixels for the permanent
molar) were analysed by means of AMIRA v. 4.0 (Mercury Computer Systems,
Inc.). Segmentation of the volume was done semi-automatically with manual
corrections. The original SR-mCT record is available at the NESPOS website
Histological analysis. Longitudinal ground sections of molars were prepared in
last-formed enamel at the mesiobuccal cervix and through the long axis of the
root. Often, the apical portion of the root turned distally with respect to this
plane of section andwas thereforecut obliquelythereafter. Onlysections with at
least 10mm of root true to the plane of section were included in this study. An
initial 200–300-mm slice was made with a circular diamond saw. Each slice was
for routine polarizedlight microscopy. Additional detailsabout calculatingroot
extension rates are provided in Supplementary Information.
Received 20 July; accepted 3 October 2006.
Published online 22 November 2006.
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Supplementary Information is linked to the online version of the paper at
Acknowledgements We thank A. Bravin, C. Nemoz and P. Tafforeau for
at the University of Poitiers; the Department of Physics at the University of
assistance. The research was supported by the French CNRS, the EU TNT Project
(to R.M.), the Re ´gion Poitou-Charentes (to A.M.), and The Leverhulme Trust and
The Royal Society (to C.D.).
Author Information Reprints and permissions information is available at
www.nature.com/reprints. The authors declare no competing financial interests.
Correspondence and requests for materials should be addressed to C.D.
NATURE|Vol 444|7 December 2006