does space in the jaw inﬂuence the timing of molar crown...

Does space in the jaw influence the timing of molar crowninitiation? A model using baboons (Papio anubis) and great

apes (Pan troglodytes, Pan paniscus)

Julia C. Boughnera*, M. Christopher Deanb

aDepartment of Oral Health Sciences, Faculty of Dentistry, University of British Columbia, 2199 Wesbrook Mall, Vancouver,British Columbia, V6T 1Z3, Canada

bEvolutionary Anatomy Unit, Department of Anatomy and Developmental Biology, University College London, Rockefeller Building,London WC1E 6JJ, UK

Received 5 August 2003; accepted 26 November 2003

Abstract

Radiographic and histological studies of baboon (Papio hamadryas, P. anubis) and chimpanzee (Pan troglodytes)permanent tooth development have found that periods of molar crown mineralization overlap markedly in chimpanzeesbut are staggered in baboons. Here we test the hypothesis that these intertaxon differences in molar initiation areprimarily due to the space available in the mandibles of each species for these teeth. This study includes radiographic,linear measurement, and three-dimensional (3D) coordinate landmark data taken from baboon (Papio anubis n=51)and great ape (Pan paniscus n=43, P. troglodytes n=60) mandibles and permanent molars across a broad developmentalrange for each taxon. Unexpectedly, 3D multivariate statistical shape analysis of the molar crypt, crown, and root datashows that all three species trajectories of molar row shape change are indistinguishable from each other. Qualitativeanalysis of these 3D data reveals subtle and inconclusive intergeneric differences in the space maintained betweenadjacent molars during growth. The space distal to each newly initiated molar is slightly greater in the baboon.Bivariate analyses comparing molar row and mandibular corpus proportions in Papio and Pan fail to show clear orconsistent taxonomic differences in the ratio of space afforded developing molars in the alveolar bone. Thus, there is apoor correlation between mandibular proportion and both intermolar spacing and 3D molar development pattern.Contrary to earlier studies, these results suggest that pattern of molar crown initiation and temporal overlap of adjacentmineralizing crowns is not significantly different between Papio and Pan. This may be due in part to the inclusion hereof not only 3D molar crown data but also 3D molar crypt data. This study strongly refutes the hypothesis that spaceavailable in the mandible directly underlies different times of permanent molar crown initiation between Papio and Pan.� 2004 Elsevier Ltd. All rights reserved.

Keywords: Radiography; Geometric morphometric shape analysis; Developing dentition; Molar crown mineralization; Tooth cryptdevelopment; Baboons; Chimpanzees; Bonobos; Mandible shape

* Corresponding author. Tel.: +1-604-822-7800; fax: +1-604-822-3562E-mail addresses: [email protected] (J.C. Boughner), [email protected] (M.C. Dean).

Journal of Human Evolution 46 (2004) 255–277

0047-2484/04/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.doi:10.1016/j.jhevol.2003.11.007

Introduction

Very little is understood about what determinesor regulates the timing of tooth initiation. Inprimates, a large proportion of taxonomic vari-ation in the absolute timing of odontogenesiscan be attributed to differences in sex, physio-logical development, and life history (Smith andTompkins, 1995). In contrast, it is much harder toaccount for taxonomic differences in relative timesof initial and terminal tooth mineralization. Com-pared to the development of other physiologicalsystems, such as the skeleton, odontogenesis isrelatively impervious to both intrinsic and externaldisruption and to deviation from its normal sched-ule (Olson and Hughes, 1943; Garn et al., 1965;Bailit and Sung, 1968; Demirjian, 1978; Smith,1989). This high degree of ontogenetic indepen-dence may be due to the tight genetic control underwhich postnatal tooth development appears to besubject (Garn et al., 1960; Blankenstein et al.,1990; Jernvall et al., 1994; Thesleff and Sharpe,1997; Jernvall and Thesleff, 2000; Thesleffet al., 2001; Sharpe, 2001). At the same time,normal variation in dental developmental timingwithin a single species can be marked (Garnet al., 1959; Nolla, 1960; Fanning, 1961; Fanningand Moorrees, 1969; Thompson et al., 1975;Tompkins, 1996). While genes may underpin nor-mal timing of odontogenesis, variation in, and thecombined effects of, different genes may underlieparticularly advanced or delayed schedules of den-tal ontogeny (Garn et al., 1963; Garn and Lewis,1970). Alternatively, factors such as the spaceavailable in the alveolar bone for initiating teethmay play a principal role in the timing of toothformation. It is this possibility that we investigatein this paper.

The importance of studying the tooth germ and itscrypt

A brief overview of tooth formation

Each tooth derives from interactions betweenneural crest-derived ectomesenchyme and oralepithelium (Kollar and Lumsden, 1979), which

establish the presumptive dental tissues in thedental lamina. Along the lamina, localized cellproliferation forms a series of epithelial swellings.These develop into tooth germs via continued celldivision and the invagination of the ectomesen-chyme below (Kollar and Lumsden, 1979). Afterthe cytodifferentiation of tooth cells into amelo-blasts and odontoblasts, crown morphology iscast in enamel and dentine, respectively, duringmineralization. For tooth morphology to developnormally, the tooth crypt in the alveolar boneimmediately around the follicle and the tooth germmust expand to accommodate the enlarging germ(Gruneberg, 1937; Diamond, 1944; Butler, 1956;Manson, 1967). Crypt positions also shift withinthe jaw to maintain stable relationships betweenthe developing teeth and the growing jaw at alltimes (Manson, 1967).

Spatial requirements for normal tooth germdevelopment

Butler (1956) iterated that the follicle (Fig. 1)enclosing each developing molar was essential tothe proper development and retention of toothshape, and for the proper positioning of theembryonic tooth. When Lefkowitz et al. (1953;cited in Butler, 1956) removed the follicle experi-mentally, the tooth germ flattened and the distinc-tion of cuspal outlines dissolved. Legros andMagitot (1879) found that severe crowding of thefollicles prior to initial molar mineralization dis-torted the germ. Clearly, the space around eachdeveloping tooth germ has immediate and strikingconsequences for its later crown formation. Agrowing body of evidence suggests that spatialrelationships between developing tooth germs andalveolar bone cells are under molecular regulation(Philbrick et al., 1996, 1998; Liu et al., 1998, 2000;Natchbandi et al., 2000; Wysolmerski et al., 2001;Kitahara et al., 2002). Gene misexpression ordeletion upsets normal bone deposition and/orresorption around the developing tooth germ. Thiscan affect the follicle and developing tooth, subse-quently distorting tooth morphology (Kitaharaet al., 2002). What establishes and maintains mini-mum intergerm distances is not known. However,tooth position seems to be regulated at some level

J.C. Boughner, M. Christopher Dean / Journal of Human Evolution 46 (2004) 255–277256

by molecular interactions (Thesleff and Sharpe,1997; Sarkar et al., 2000; Sharpe, 2001).

Using evidence of the tooth crypt as a useful proxyfor the appearance and growth of thecorresponding germ

The first appearance of the tooth bud histologi-cally, or of its crypt on radiographs, is arguablythe earliest time at which the presence and devel-opment of the tooth are recognizable. Yet very fewpublished radiographic or histological studies ofpermanent tooth mineralization in primates haveincluded this critical phase of early tooth forma-tion. The reasons for this are understandable. Theearly stages of tooth development are compara-tively brief and can easily be missed if data arecollected at long time intervals. Effectively visual-izing tooth mineralization in situ, particularly inlive animals, is challenging. Conventional methodssuch as radiography and computed tomographymay over-expose (Beynon et al., 1991, 1998) or failto detect the very low-density and translucent(Fanning, 1961) soft tissues of the tiny germs inwet specimens. Soft dental tissues contract afterdeath and shrink to one aspect of the crypt or even

fall out. Even if they remain in the crypt, these aredifficult if not impossible to see in radiographs ofdry specimens. Lastly, as radiographic studies oftooth mineralization have only been in a singleplane, tooth appearance, position, and orientationmay be obscured due to the overlap of developingcrowns, which often tilt and rotate during miner-alization. It is for this reason that at least twoplanes of view are required to properly view toothformation.

Dissection of the jaws allows very clear in situstudy of developing teeth (Winkler, 1995), but isinherently destructive of precious primate material.Histological analysis of dissected or emerged toothcrown tissues enables the calculation of the timeelapsed since a given tooth began to mineralize(Bromage and Dean, 1985; Dean, 1986). Thismethod can accurately document otherwiseunknown times of tooth initiation and othergrowth stages, and the minimum age of an individ-ual at death. Because both dissection and histologi-cal study are very time intensive, neither facilitatesthe study of large samples within a practical periodof time.

One way of studying the first appearance of thedeveloping tooth in the jaws is to study the

Fig. 1. Diagrammatic vertical section through a tooth germ showing the follicle surrounding the permanent molar tooth germ (fromButler, 1956).

J.C. Boughner, M. Christopher Dean / Journal of Human Evolution 46 (2004) 255–277 257

initiation and enlargement of the crypt. The con-trast between the crypt and its dense alveolar bonewall is sharp on radiographs. Times of crypt andtooth germ initiation coincide. Thus, germ initi-ation times, rates of expansion, and periods ofgerm development can be inferred from the time ofinitial crypt appearance and increase in crypt size.For a considerable time after crown initiation, thecrypt occupies a greater volume of the jaw than dothe early stages of tooth mineralization. Banks(1934) reported that the third molar crypt wascompletely formed about one year prior to full M3cusp mineralization in humans. Fanning (1961)noted that the human permanent first molar crownattained the maximum mesiodistal diameter of itscrypt when half-mineralized. Thus, comprehensivestudies of orodental space and position benefitfrom including data on crypt size and its expansionthrough time.

Earlier studies of permanent tooth formationschedules in primatesContrasting patterns of permanent molar crowninitiation times and mineralization periods inbaboons and chimpanzees

The first permanent molar begins to mineralizeat birth or earlier in higher primates (Gleiser and

Hunt, 1955; Swindler, 1961; Kraus and Jordan,1965; Swindler and Gavan, 1966; Bowen andKoch, 1970; Tarrant and Swindler, 1972; Swindleret al., 1982; Swindler and Emel, 1990; Swindlerand Meekins, 1991; Swindler and Beynon, 1993;Hillson, 1996; Dirks, 1998). At birth, M1 minerali-zation is consistently advanced in monkeys (Papio,Theropithecus, Alouatta, Macaca) compared toapes (Pan troglodytes) and modern humans(Swindler and Beynon, 1993): M1 developmentbegins weeks earlier in prenatal monkeys than inprenatal apes (Swindler and Beynon, 1993). Mon-keys, such as Macaca and Papio, share with greatapes and humans a general order of permanenttooth mineralization: M1 I1 I2 C P3 P4 M2 andM3 (Swindler and Meekins, 1991).

Radiographic and histological studies ofbaboon tooth development have identified markedtime intervals between M2 crown completion andM3 crown initiation, and little or no temporaloverlap between periods of M1 and M2 crownmineralization (Swindler and Meekins, 1991; Dirkset al., 2002) (Table 1). Conversely, using thesemethods to study permanent tooth mineralizationin the chimpanzee (P. troglodytes), Anemoneet al. (1991) and Reid et al. (1998) documented atemporal overlap of successive mineralizing molarcrowns (Table 2).

Table 1Ages at permanent molar crown initiation and completion for baboons as measured using radiographic (Swindler and Meekins,1991) and histological (Dirks et al., 2002) data

Researchers

Swindler and Meekins (1991) Dirks et al. (2002)

Method Radiography Histology

Age (years) at:M1 crown initiation Around birth Around birthM1 crown completion Less than 1.13 1.41 (mean period of crown formation)

M2 crown initiation Older than 0.9, younger than 1.9 1.35 (female 73261); 1.38 (female 73436)M2 crown completion Around 2.64 Around 3.24

M1–M2 temporal overlap?a Possibly: maximum of 0.23 years Possibly: maximum of 0.06 years

M3 crown initiation Older than 2.2, younger than 3.2 3.75 (73261); 3.64 (73436)M3 crown completion Before 4.71 Around 5.71

M2–M3 temporal overlap?a Possibly: maximum of 0.44 years None

aBoth studies found little (M1–M2) or no (M2–M3) temporal overlap between successive crown mineralization periods in theirsamples.


The aims of this study

The permanent molars are the only teeth forwhich no space is created or maintained in the jawby deciduous precursors. A number of studies(Bradley, 1961; Osborn, 1978; Dean and Beynon,1991; Tompkins, 1996) have suggested that spaceavailability in the jaws influences the time ofinitiation (and even the sequence) of tooth devel-opment. The aim of this study is to test thehypothesis that the space available in the posteriorbody of the mandible underlies differences inmolar initiation times and the overlap of molarcrown mineralization periods previously observedbetween Pan and Papio. Each molar begins as anepithelial downgrowth from the dental lamina.What triggers the time at which each crown beginsto mineralize is not known. Osborn (1978)suggested that a “zone of inhibition” surroundseach initiated germ. According to Osborn (1978),only when growth of the jaw posteriorly createssufficient space beyond the zone of inhibition is thenext tooth in the sequence able to initiate.

Here, we test the hypothesis that the compara-tively staggered molar initiation times of Papio aredue to a lack of space in the jaw not shared by Panat the same relative times during permanent molar

development. This study is the first to test ifdifferences in the timing of permanent molarinitiation in primates are actively governed byspatial restrictions throughout dental developmentor if the dentition is developmentally autonomousin this respect.

Materials and methods

Permanent molar crown and root mineraliz-ation was studied in 51 olive baboons (Papioanubis), 60 chimpanzees (Pan troglodytes) and 43bonobos (P. paniscus). The olive baboon skullswere housed in the collections of the NaturalHistory Museum (NHM) and the Royal College ofSurgeons (RCS), both in London, UK. The chim-panzee material was housed at the NHM and thePowell-Cotton Museum (PCM), Kent, UK. Thebonobo collection was housed in the MuseeRoyal de l’Afrique Centrale (MRAC), Tervuren,Belgium. All three taxa were sampled across abroad range of developmental ages. This formed acontinuum of dental development within eachtaxon. All damaged specimens were excludedexcept for a very few where minimal damage to themandible did not impede accurate data collection.

Table 2Ages at permanent molar crown initiation and completion for chimpanzees as measured using radiographic (Anemone et al., 1991)and histological (Reid et al., 1998) data.

Researchers

Anemone et al. (1991) Reid et al. (1998)

Method Radiography Histology

Age (years) at:M1 crown initiation Three weeks after birth �0.05 animal 43/87; �0.15 animals 88/89 and 28/90M1 crown completion 2.0 2.4; 3.05; 2.65, respectively

M2 crown initiation 1.3b 1.80; 1.67; 1.95, respectivelyM2 crown completion 4.0b 5.48; 4.52; 5.61, respectively

M1–M2 temporal overlap?a Yes: about 0.7 years Yes: 0.50 to 1.38 years

M3 crown initiation 3.5b 3.6; 3.62; no M3, respectivelyM3 crown completion 7.5b or older 7.0; 6.93; no M3, respectively

M2–M3 temporal overlap?a Yes: about 0.5 years Yes: 0.9 to 1.88 years

aBoth groups found significant temporal overlap between M1 and M2, and M2 and M3 crown mineralization periods.bMean or estimated mean age.


No specimens showed any signs of pathologies.Sex was determined from the teeth, external geni-talia, and nipples of most specimens (Napier, 1981;Jenkins, 1990). Remaining specimens were sexedfrom other external evidence (Napier, 1981;Jenkins, 1990). Numbers of males and femaleswere balanced as much as possible, but includedindividuals across the broadest range of permanentmolar crown formation possible. Table 3 lists thenumber of individuals of each sex per age groupfor each taxon. How each age group was defined isexplained directly below.

Ageing each individual

Almost all specimens were wildshot and thus ofunknown age. To overcome this, each individualwas carefully assigned an approximate relativedental age (ARDA) via the atlas method usingradiographs taken in two planes, lateral (bothbuccal and lingual views) and occlusal. First, radio-graphs were directly compared with histologicalsections of mineralizing permanent molar crowns(Fig. 2). These sections were taken from chimpan-zee and baboon specimens previously included instudies of permanent tooth development (Reidet al., 1998) and life history (Dirks et al., 2002).Outlines of the histological M1, M2, and M3crown sections of one chimpanzee (P. troglodytesspecimen 88/89, sex unknown) and two baboons(Papio hamadryas female 261 and P. anubis female436) were traced. Ages at crown initiation andcompletion as well as ages at progressive one-yearintervals of crown mineralization were drawn andlabeled on outlines drawn from the histologicalsections of the molar crowns. Second, permanent

antemolar tooth development was considered inassigning ARDA using the atlas published byDean and Wood (1981) and the data set out inDirks et al. (2002). Finally, ages of permanenttooth emergence documented by Smith et al.(1994) were used to refine the probable ages ofolder individuals with completely mineralized M2and M3 crowns against known data for dentaldevelopment.

Each author assigned ages to all the individuals,then both went through the entire data set againtogether looking at the three histological, antemo-lar, and emergence criteria until a single ARDAper individual was agreed upon. All specimenswere then assigned to one of four age groups(infants, younger and older juveniles, and adults)based on their ARDA. Juveniles were separatedinto younger and older groups to better managethe data. Table 4 defines the ranges of the agegroups for each genus. While these age ranges wereabsolutely different between Papio and Pan, theycorresponded to equivalent stages of ontogeneticgrowth and sexual maturity in both genera.

Radiography of the baboon and ape mandibles andmolar teeth

A Phillips Industrial Unit was used to radio-graph both the NHM and RCS specimens. Aportable Faxitron Radiographic System, model8040-310, manufactured by Field EmissionLimited, was used to radiograph specimens fromthe RCS and MRAC. Lateral and occlusal viewsof each mandible in its entirety were taken withKodak Industrex X-Ray film AA400-5. Smallerlingual intraoral views of the molar region of the

Table 3Age groups and sexes of the specimens belonging to the three primate taxa included in this study

Taxon Papio anubis Pan paniscus Pan troglodytes

Age group Infant Juvenile 1 Juvenile 2 Adult Infant Juvenile 1 Juvenile 2 Adult Infant Juvenile 1 Juvenile 2 Adult

SexMale 3 6 10 6 7 8 6 2 6 12 3 4Female 3 7 4 9 5 4 4 4 9 6 3 4Unknown 1 1 1 0 3 1 1 0 7 5 0 0Total 7 14 15 15 15 13 11 6 22 23 6 8


corpus only were taken with Kodak Ultra-speedDental film DF-50 Size 4. Image magnification anddistortion were minimized as much as possible(Boughner, 2002). For the purposes of co-ordinatedata collection, all radiographs were digitallyscanned into an Apple MacIntosh G3 computerusing an Agfa Arcus II scanner and FotoLooksoftware (Agfa SA version 3.03). Image contrast

and clarity were enhanced using AdobePhotoShop software version 4.0.1.

Three dimensional (3D) landmark data collectionfrom the molars

Our aim was to collect 3D data across a broaddevelopmental range from the mineralizing perma-nent molar crypts, crowns, and roots of the threeprimate taxa we studied. The general methodologywas as follows. 3D landmark data were collectedindirectly from the permanent molars and themandibular canal by radiographing each mandiblein two different 2D planes (lateral: [x, y]; andocclusal: [x, z]). Imaging software NIH Imageversion 1.62 on an Apple MacIntosh G3 computerenabled the collection of 2D coordinate data taken

Fig. 2. Tracings of permanent molar crown sections. The fine lines that intersect the crowns represent histological dental ages. Fromleft, M1, M2, and M3 crowns for: A) Pan troglodytes specimen 88/89, B) Papio anubis specimen 436, and C) Papio hamadryas specimen261. Adapted from Reid et al. (1998) and Dirks et al. (2002).

Table 4Age groups based on dental development for Papio and Pan

Age groups (in years)

Taxon Infant Juvenile 1 Juvenile 2 Adult

Papio 0–2.0 2.01–4.5 4.51–7.0 >7.0Pan 0–3.5 3.51–7.0 7.01–10.5 >10.5


from each plane of each scanned radiograph. Itwas imperative that all coordinates were collectedin the same sequence for each individual so thatthe 3D landmark data were homologous amongspecimens. Software written in-house (Evolution-ary Anatomy Unit, UCL), merged both sets of 2Dcoordinates per molar landmark for each individ-ual to create a single set of 3D molar coordinates(x, y, z) per specimen. The same software facili-tated the registration of all 3D molar and man-dibular canal data using nine consistent landmarkscommon to both data sets: three leadshot markerspositioned beneath the molar row and six leadshotmarkers positioned around the mandible (Fig. 3,Table 5). This methodology is explained in detailelsewhere (Boughner, 2002).

Differences in the proximity of the film to eachspecimen meant that the lateral intraoral imageswere magnified relative to the occlusal and lateralmandible images, which were of identical scale.Thus, the lateral mandible scale was used to regis-ter the lateral molar images down to the same scaleas the occlusal mandible images. The absolutelylarger lateral and occlusal radiographs of the entiremandible included both the three sub-molar andsix circum-mandibular leadshot markers. Theabsolutely smaller dental film used to x-ray themolars only fit the three sub-molar markers. Usingthe additional six markers positioned in differentplanes across larger distances around the entiremandible reduced the positional variance, andincreased the accuracy and precision of coordinate

Fig. 3. Radio-dense mandibular landmarks, buccal view.

Table 5Radio-dense landmarks (pinheads and leadshot pellets)

Landmark#

Landmarktypea

Landmark description

1 Type II Lingual tip of the mandibular condyle2 Type II Posterior-most point on the posterior border of the ascending ramus3 Type I Gonial tubercle4 Type III Approximately halfway along the inferior border of the mandibular corpus5 Type II Anteroinferior-most point of the mental symphysis6 Type III Anteriorly, on the alveolus below the canine, labially7–9 Type III From distal to mesial, three markers below the molar teeth or molar region on the lateral face of the

mandibular corpus10–12 Type III As above, but in the dental radiograph of the molar region

aType I landmarks define real biological features. Type II landmarks define changeable or inconsistent biological features. Type IIIlandmarks define features with no biological significance or mathematical basis, and are defined in relation to Type I and IIlandmarks (Bookstein, 1991; Dryden and Mardia, 1998).


registration. Variation in molar landmark pos-itions between the two planes for each individual,and variation in the positions of the nine registra-tion markers both within and between individuals,was minimal. As such, this variation did notsignificantly affect registration accuracy or theanalysis.

3D molar and mandibular canal landmarkswere chosen based on the strength of their homol-ogy between taxa (Bookstein, 1991; Marcus et al.,1996; Dryden and Mardia, 1998) and how appro-priately they visually represented overall molarmorphology and ontogenetic change. Landmarkhomology is largely dependent upon the biologicalreality of the defined point. Three different types oflandmarks defined by the strength of their homol-ogy are Type I, Type II and Type III landmarks(Bookstein, 1991; Marcus et al., 1996; Slice et al.,1998). Type I landmarks define real biologicalfeatures such as the coronal suture and have themost robust homology. Type II, landmarks definechangeable or inconsistent biological features,such as the superior-most point on the skull alongthe coronal suture. Their homology is arguablyless sound. Type III landmarks define features thathave no biological significance or mathematicalbasis, and are defined in relation to Type I and II

landmarks: for example, a point directly lateral tothe superior-most point along the coronal suture.The homology of Type III landmarks is very weak.The landmarks included in this study were largelyType I and II landmarks. Forty-nine landmarkswere derived from the radiographs of the threedeveloping molar crypts and/or crowns and roots(Fig. 4, Table 6). Prior to digitizing, a length ofdental wire was gently inserted through theentire mandibular canal of each specimen so thatthe wire emerged from both the mandibularand mental foramina. This radio-dense wiremade the canal plainly visible in the radiographs,facilitating the accurate landmarking of thecanal. Leadshot markers puttied at the mandibularand mental foramina demarcated the endpoints,and hence, the total length of the canal. Impor-tantly, the mandibular canal was a constant,relatively static biological feature against whichthe variable positions of the developing molarscould be reliably referenced. Six landmarksdescribing this canal were derived from theradiographs and taken at each foramen andat four equidistant intervals between the twoforamina (Fig. 3, Table 6). Actual digitizedlandmarks were taken at the center of eachleadshot ball. Tests of intra- and interobserver

Fig. 4. 3D landmarks defining the permanent molar crypt, crown and roots. A) 3D landmarks defining the permanent third molarcrypt. Permanent first and second molar crypts were defined by landmarks 1–16 only. B) 3D landmarks defining each mineralizingpermanent molar crown and its roots. Landmark 17 is included for the permanent third molar. This landmark described thehypoconulid on this tooth. C) 3D landmarks defining the molar crown and roots of each permanent molar tooth. The hypoconulidof the permanent third molar is defined by landmark 17 in all taxa.


error in landmark data collection found both ofthese to be negligible.

3D multivariate statistical shape analyses ofbaboon, chimpanzee, and bonobo molars

This analysis of molar row shape included land-marks representing M1, M2, and M3 crypts/crownsand roots, and the mandibular canal. All nineregistration landmarks were excluded from theanalysis. The complete 3D landmark data for alltaxa were analyzed using shape analysis softwareMorphologika (University College London). Thissoftware first eliminated differences of size, trans-lation, and rotation via the common registration ofall individual shapes sampled using GeneralisedProcrustes Analysis (GPA) (Goodall, 1991). Prin-cipal Components Analysis (PCA) then found theprincipal vectors of shape variation, which can berendered visually in 3D (O’Higgins and Jones,1998). These vectors, or principal components(PCs), can be used to explore the relationshipbetween shape and some other factor such as size,thus allowing the study of allometry. Importantly,Morphologika permits the direct visual study ofshape change using only the landmarks themselvesor a constructed “wireframe” that links adjacentlandmarks according to user specifications.

PCAs were run on a data set of combinedgenera (Papio and Pan) and on individual data setsfor each species. The nature of major shape vari-

ation was largely consistent among all data sets.Preliminary analyses that included or excludedpermutations of molar crypt/crown, root and man-dibular canal landmark data showed no significantdifferences in trajectories of molar row shapechange between taxa. The mandibular canal was astatic reference against which horizontal, vertical,and lateral molar tooth movement could be re-lated, and correlated closely with mandibulargrowth. As such, the canal was a sound proxy forthe mandible itself. Critically, the presence of themandibular canal data highlighted developmentalchanges of the molar row. This was particularlyimportant to the identification and explorationof molar shape change related to ontogeneticgrowth. Molar morphology was sufficiently similarbetween species that it did not eclipse real andsignificant taxonomic differences in the relativetiming of molar crypt and tooth development. Anysignificant taxonomic differences in the relativetiming of molar crypt and crown initiation wereexpected to be manifested as statistically differenttrajectories across major principal componentsafter a PCA (Fig. 5).

The measurement of the mandibular corpus andthe permanent molar crowns

Supplementary to the 3D shape data, 2D linearmandibular corpus and molar crown dimensionswere measured on all specimens of all three taxa.

Table 6Molar tooth and mandibular canal radiographic landmark

Landmark number Landmark type Landmark description

13 Type I Mandibular foramen14–17 Type III Mandibular canal, four landmarks evenly spaced disto-mesially

between the mandibular and mental foramina18 Type I Mental foramen19–35 Type II M3 crypt19–26, 35 Type II M3 crown27–34 Type II M3 roots113–128 Type II M2 crypt113–120 Type II M2 crown121–128 Type II M2 roots129–144 Type II M1 crypt129–136 Type II M1 crown137–144 Type II M1 roots


Importantly, these linear measurements enabled anindependent study of changes in corpus and molarrow proportions over time. These were also usedto test some of the conclusions drawn from thestatistical shape analysis. Measurements weretaken with manual calipers. The posterior lengthof the mandibular corpus was measured from theantero-inferior margin of the mandibular foramen

to the distal face of dm2 (infant or juvenile) orfrom the same margin to the anterior face of M1

(once dm2 is shed), measured on the lingual aspectof the corpus (Fig. 6). This is a measurement(POSTL) of the region of the corpus within whichthe permanent molars form and into which theseteeth emerge. Additionally, the maximum mesio-distal length of each emerged permanent molarcrown (MDM) was measured across its occlusalsurface between mesial and distal contact pointsfor each specimen (Fig. 6). The sum of all emergedmolar crown lengths in a single specimen equaledthe total length of the molar row for that individ-ual. All specimens were divided into three groupsbased upon the number of permanent molarcrowns emerged. The first and youngest group hadonly M1 emerged. The second group had M1 andM2 emerged. The third and oldest group had allthree molars emerged. By the time M1 has emergedinto the mouths of Papio and Pan, M2 has begunto form. The same holds for the relative timing ofM2 emergence and M3 initiation in these genera.Thus, growth in POSTL after M1 and M2 emer-gence directly reflects a creation of space in thecorpus for M2 and M3, respectively.

Microsoft Excel 97 was used to calculate meansfor posterior corpus length (xPOSTL) and mesio-distal length of the emerged molar row (xMDM)for all specimens within each of the three groups.Mean ratios of molar row length to posteriorcorpus length were calculated at stages of “M1 inocclusion,” “M2 in occlusion,” and “M3 in occlu-sion.” Each of these stages corresponded directlyto the mesiodistal length of any and all of theemerged permanent molar teeth. A notably smallerratio of molar row length to posterior corpuslength in Papio compared to Pan would suggestthat the baboon had less space in the back of itsmandible for its permanent molars than did eitherthe bonobo or the chimpanzee. This result wouldsupport the hypothesis that a deficit of space in themandibles of Papio underlies the comparativelystaggered times of molar initiation observed in thistaxon, but not in Pan.

Measurement error in a test group of eightPapio anubis where POSTL was measured threetimes on different days, in different orders, wasminimal, and varied around 0.04 cm or less. The

Fig. 5. 2D illustration of two different hypothetical schedules ofpermanent molar initiation and mineralization, A and B, todemonstrate the different changes in shapes of each molar rowacross development. Schedules A and B would be expected tomanifest as growth trajectories that are distinct relative to eachother.


mean standard deviation (SD) for all remeasure-ments of POSTL was 0.03 cm. The mean SD forraw POSTL data for all three molar emergencegroups for all three taxa was 0.09 cm. SDs forMDM raw data for all three emergence groups inall taxa ranged between 0.05 cm (MDM3, Panpaniscus) and 0.16 cm (MDM3, Papio).

Results

Statistical analysis of shape variation of thepermanent molar crypts, crowns and roots, andmandibular canal between Papio and Pan

Shape analysis of all three developing molarsand the mandibular canal showed that ontogenetictrajectories of molar row shape change are notonly curvilinear but are also indistinguishablebetween taxa on the first two PCs (Fig. 7). Shapechange on PC1 was allometric in nature. This isevident from the strong correlation (r=0.77) be-tween centroid size, a standard size measurementcalculated for each specimen during GPA, andPC1 scores, the location of each specimen relativeto PC1. However, it is clear that there is a non-linear relationship between molar row shape andsize (Fig. 7). Differences in molar shape are notsignificant between genera on higher PCs. Thissuggests that little or no significant differences inrelative times of initial molar germ and crownformation exist between Papio and Pan.

The ontogenetic shape change in the molar rowdescribed on PC1 (Fig. 8) is specifically associatedwith:

1. successive molar crypt and crown initiationand expansion, and progressive molar crownand root mineralization;

2. the horizontal position of the molars relative tothe mandibular canal;

3. the vertical position of the molars relative tothe same canal; and

4. change in molar crown orientation around thex-axis (i.e., rotation of the crowns around thelong axis of the mandibular corpus).

The non-linearity of the species scatters on PCs1 and 2 suggests that on PC2, infants and adults(at parallel ends of the scatter) share a pattern ofmolar row shape variation to the exclusion ofjuveniles (located along the curve of the scatter)(Fig. 7). Unrelated to growth, PC2 describeschanges in the symmetry, or asymmetry, of toothmorphology within the molar row and in molartooth positions relative to each other and to themandibular canal. For example, in infants andadults, the permanent molars were in very earlyand (almost) complete phases of development,respectively. Thus, the molar crowns and roots ofeach age group were similarly sized and shapedrelative to each other. Additionally, either molareruption had not begun (infants) or emergence wascomplete (adults). So in each age group, all three

Fig. 6. Lingual view of the mandible showing the linear measurements posterior corpus length (POSTL) and mesiodistal permanentfirst molar crown length (MDM1).


molars were positioned in a single common verticalplane. Conversely, in juveniles, each of the threemolars was in a different phase of mineralization(is a different shape and relative size) and eruption(is in a different vertical plane) relative to eachother and the mandibular canal.

PC1 described the greatest proportion (53.2%)of the total variance in molar row shape acrosstaxa (Table 7). Thus, over half the total shapevariance was related exclusively to ontogeneticgrowth. PC2 described a further 12.4% of the totalshape variance. PC3 described almost half as much(6.85%) of this variance in molar row shape.Subsequent PCs explained substantially less vari-ance (PCs 4–10 less than 5% each, PCs 11–25 lessthan 1% each; see Table 7). Because of errorpossibly associated with the manual collection of2D landmark data from individual scanned radio-

graphs, only major shape variance described by thefirst three PCs was trusted to have a sound biologi-cal basis independent of non-biological noise.However, comprehensive tests of intra- and inter-observer error in 3D landmark digitization clearlydemonstrated that these errors were negligiblewithin each data set for each specimen. Furthertests showed that shape variance due to digitizingerror was negligible compared to biological shapevariance in the sample.

The qualitative study of space between and distalto adjacent molar teeth

After a PCA, visual studies of the 3D molardata showed that at no time was the space betweenadjacent molars (homologous molars betweentaxa, and successive molars within one species)

Fig. 7. PCA of all developing molar crowns, roots, and mandibular canal for Papio and Pan, where PC1 is plotted against PC2. Each“wireframe” of the molar row represents molar shape at each end of PCs 1 and 2. M3 is at the left, M1 at the right of each molar row.


markedly different among the three taxa. As suc-cessive molar crypts and crowns initiated andgrew, relative distances between adjacent molarcrypts and crowns varied only subtly over time ineach species. This variation was not consistent,and did not reflect species-specific patterns ofmolar spatial arrangement.

Throughout periods of molar crown mineraliz-ation, “excess” space measured from the distalaspect of the developing M3 crypt or crown to themandibular foramen was observed in all threespecies (Fig. 9). This space lengthened as M3 cryptdevelopment advanced, but grew most duringearly and middle M3 crown mineralization. Little ifany difference in this space was observed betweenbonobos and chimpanzees. This space was margin-ally longer in baboons compared to either greatape.

In summary, no significant statistical differencesin molar row shape change that occurred through-out periods of permanent molar crypt, crown, orroot development were observed among the threespecies studied here. Additionally, there were nomarked taxonomic differences in the space avail-able for and surrounding each molar crypt andcrown at the times of its initial appearance andduring its subsequent growth. Shape change onPC1 clearly reflected the normal and sharedontogenetic processes undergone by baboon,chimpanzee, and bonobo permanent molars.

Comparing the proportion of the mandibularcorpus occupied by the molar row

In Papio and Pan, mean posterior corpus length(xPOSTL) increased most dramatically in the

Fig. 8. Chimpanzee, bonobo, and baboon molar rows from one infant, one juvenile (from the older of the two groups), and one youngadult. Each individual is represented by each wireframe, generated after a PCA of the molar row and mandibular canal landmark data.Each illustrates ontogenetic shape change across PC1. The permanent molars run from third to first, left to right, for A) Pantroglodytes, B) Pan paniscus, and C) Papio anubis.


period after M1 was in occlusion to the time M2

was in occlusion (i.e., near the time of M3 crowninitiation) (Table 8). This marked increase inxPOSTL was about 20% greater in Papio. By thetime M3 was in full occlusion, xPOSTL hadincreased again in both genera, but less dramati-cally. This increase was about one third greater inthe baboon compared to both apes, and was about20% greater in the chimpanzee compared to thebonobo. Thus, xPOSTL in both Papio and Panmandibles grew most in the period during whichM3 crown development began.

The interval between M1 and M2 emergence isthe most critical to this study as it is during periodsof advanced M2 crown mineralization or earlyeruption that M3 crypt/crown formation begins(Table 8). Note that mean posterior corpus lengthis consistently greater in Papio compared to Pan,but that this difference is only prominent afterM1 emergence and greatest after M2 emergence(Table 8). It is interesting that near the time of M1

emergence, xPOSTL is equivalently greater in thebaboon and the chimpanzee compared to thebonobo. The greatest increase in xPOSTL occursduring the interval between M1 and M2 emergencein all three taxa. In no taxon does the permanentmolar row occupy the entire length of the posteriorcorpus at any time.

Studied at intervals of successive completedmolar emergence, permanent molar row length

occupied a slightly greater proportion of POSTLin Pan compared to Papio (Table 9). These relativedifferences were greatest at and after M2emergence. Thus, space in the mandible for thedeveloping permanent molars appears to be ata marginally greater premium in both apescompared to the baboon, and was highest inthe bonobo. Note (Table 9) that M1 occupies thesmallest proportion (33%) of POSTL in thebaboon and the greatest (42%) in the bonobo. Thispattern remains consistent as M2 and M3 emergeinto occlusion. The implication is that there is moreroom for the developing permanent molars in theposterior corpus of the baboon than there is in thebonobo, and perhaps in the chimpanzee, despitethe baboon having the longest molar crowns.

Spatial relationships between molar row lengthsand posterior corpus lengths as expressed in Table9 were not conclusively different between Panpaniscus and P. troglodytes either within or be-tween emergence ages. These data fail to accountfor any differences that may be observed betweenpatterns of molar development in these sister taxa.However, P. paniscus molars occupy a greaterproportion of the posterior corpus than do thoseof P. troglodytes or, particularly, Papio anubis.This evidence weakens, if not nullifies, the argu-ment that spatial relationship between permanentmolars and the posterior corpus have any bearingupon times of molar crown initiation in theseprimates.

If anything, there appears to be more room inthe growing mandible of the baboon for successivemolar crypt and crown initiation. This is strongevidence against the hypothesis that a lack of spacein the mandible of Papio yields more staggeredtimes of permanent molar initiation in this primatecompared to either species of Pan.

Discussion

Variation in the positions, proportions andorientations of the developing molars

Several growth-related changes occur in molartooth positions relative to each other and to themandibular canal. Many of these changes are in

Table 7PCA output for molar crypts, crowns, roots, and mandibularcanal for Papio and Pan

PC Eigenvalue Proportion oftotal variance

Cumulativeproportion

1 0.469 53.2a 53.22 0.110 12.4 65.73 0.0604 6.85 72.54 0.0424 4.81 77.45 0.0275 3.12 80.56 0.0220 2.50 83.07 0.0196 2.23 85.28 0.0144 1.63 86.89 0.0127 1.44 88.310 0.00961 1.09 89.4

aThe largest proportion of total shape variance is describedacross PC1.


vertical and horizontal molar positions. Some ofthese are associated with root growth, and withmolar eruption and emergence. Others are relatedto the lengthening of the mandibular corpus andthe widening of the ascending ramus duringgrowth. In part, this mandibular growth may carrythe molars through the jaw and facilitate theanterior migration of the molar row. In additionto, or instead of, this mechanism, the molars maymigrate forward through the jaw on their own at arate faster than that at which the mandible length-ens. Either way, this migration helps create space

at the back of the corpus for M2 and M3. Changesin the horizontal position of the molars relative tothe mandibular canal also reflect the elongation ofthe canal itself as mandible length increases withgrowth.

Variation in molar crown and root proportionsfrom infancy to adulthood mirrors the normaldevelopment of all three permanent molars as theygrow from small germs into larger, completelymineralized teeth in Papio and Pan. Taxonomicvariation in mesiodistal permanent molar crownlength is also reflected in this analysis, where

Fig. 9. Wireframes of M1 and M2 complete crown, M3 crypt and mandibular canal data for A) Pan troglodytes, B) Pan paniscus, andC) Papio anubis, generated after a PCA by the shape analysis software. Note the space distal from M2 to the mandibular foramen isvery similar between the apes and even greater in the baboon. The space distal from M3 to the mandibular foramen is almost identicalin all three taxa, and perhaps greatest in the baboon.


M2<M1<M3 in Papio, and M3<M2<M1 in Pan.The permanent third molars are particularlyelongated in the baboon compared to those ofchimpanzees and bonobos.

On PC1, the occlusal-ward rotation of thelingually tilted permanent molar crowns is verynoticeable in Pan. The development of youngmineralizing molars on their sides and the subse-quent turning of each crown as it mineralizes areshared by other great apes (Dean and Beynon,1991). This may be an effective strategy to fit apermanent molar into the jaw as early as possible,even before the corpus is wide enough to house thebuccolingual breadth of the crown (Dean andBeynon, 1991). By comparison, very little tilting orchange in molar orientation was seen in Papio. Inthis primate, only the occlusal-ward rotation of theM3 crown was notable. If this rotation is indeed aneffective method of creating space for permanentmolar initiation where there might otherwise benone, it is perhaps strange that other primates suchas the baboon, which may be under greater press-ure to make room for its longer molars, do notshare it more.

Timing and pattern of ontogenetic shape variationin the molar row

Trajectories of ontogenetic molar row shapechange were indistinguishable among baboons,chimpanzees, and bonobos. This result stronglysuggests that relative times and rates of molarcrown initiation are not markedly differentbetween these genera (Papio and Pan) or sisterspecies (Pan troglodytes and P. paniscus). Thisoutcome contradicts published studies of perma-nent molar crown mineralization in baboons andchimpanzees that identified significantly differentpatterns of temporal overlap in the molars of eachof these primates (Anemone et al., 1991; Reidet al., 1998). The marked similarity in timingobserved here could reflect a wider range of nor-mal molar initiation ages. Conversely, it mightindicate a broader range of normal molar crowncompletion times. Either of these scenarios couldtemper the apparently dramatic and contrastingtemporal overlap (Pan) or temporal gaps (Papio)in permanent molar crown mineralization reportedearlier by other workers (Anemone et al., 1991;Reid et al., 1998).

The inclusion here of the additional crypt initi-ation data may be principally responsible forthis difference between our results and others’(Anemone et al., 1991; Reid et al., 1998). Perma-nent molar germ development has previously beenstudied in apes and baboons (Oka and Kraus,1969; Siebert and Swindler, 1991; Swindler andMeekins, 1991; Winkler, 1995). However, theemphasis has overwhelmingly been on document-ing initial cusp mineralization rather than on thedevelopment of the germ and crypt. These datahave not been included in this context in

Table 8Mean posterior corpus length (xPOSTL) after M1, M2, and M3 emergence, and ratios of xPOSTL after the emergence ofsuccessive molars for Papio anubis, Pan troglodytes, and Pan paniscus

xPOSTL (cm) after M1, M2 and M3 emergence Ratios of xPOSTL values

Taxon M1 M2 M3 M1/M1M2 M1M2/M1M2M3

Papio anubis 3.4 5.0 6.2 0.68 0.81Pan troglodytes 3.3 4.1 4.9 0.80 0.84Pan paniscus 2.4 3.4 4.1 0.71 0.83

Table 9Ratios of mean molar row length (xMDM) to mean posteriorcorpus length (xPOSTL) after times of M1, M2, and M3

emergence

xMDMy/xPOSTL after M1,M2 and M3 emergence

Taxon M1 M2 M3

Papio anubis 0.33 0.47 0.59Pan troglodytes 0.34 0.58 0.66Pan paniscus 0.42 0.60 0.69


previously published studies of ape and baboontooth mineralization. Initiation times have conven-tionally been derived from first observations ofalready mineralizing crowns, which may overesti-mate initiation ages. Our crypt data has extendedthe earliest period of molar tooth development inPapio and Pan by pushing back documented molarinitiation ages.

It is possible, however, that our results areartifacts of sample size or of the new methodolo-gies we used. But this is unlikely consideringthe comparatively large number of individualsincluded in our sample. While our application ofthis shape analysis technique is new, its robusticityand reliability have been proven repeatedly whenused appropriately by other workers. Thus, themost probable and principal source of the differ-ence between our results and those of others(Anemone et al., 1991; Reid et al., 1998) is ourincorporation of the molar crypt landmark data.Further studies of crypt/germ initiation times andtheir ranges of variation are clearly needed to fullyexplain these different results and to resolve thisimportant issue properly.

Establishing and maintaining distances betweenand distal to developing permanent molar toothgerms and crowns

Relative spatial relationships between the lengthof the molar row and the posterior corpus (Table9) were not conclusively different between Panpaniscus, P. troglodytes, and Papio anubis eitherbefore or after the emergence of successive perma-nent molars. These data fail to account for anyobserved differences in patterns of molar initiationbetween Papio and Pan. Additionally, faster ratesof corpus elongation in Papio compared with Pan,particularly P. paniscus (Table 8), fail to supportthe idea that adequate space was not made by thegrowing mandible in time for the developing per-manent molars. If anything, more space was avail-able in the baboon mandible for the developingpermanent molars at any given time during growthcompared to either ape.

The results of the shape analysis of the spacesurrounding the developing permanent molarssupport this outcome. Differences in intermolar

crown distances and changes in these distancesover time were very subtle among the three taxa.Later in molar crown mineralization, the distancebetween M2 and M3 in the baboon exceeded thatfound in either ape at a comparative age. Allintermolar distances were equivalent in Pan trog-lodytes in later periods of crown mineralization. Incontrast, M2–M3 distance was smaller thanM2–M1 distance in older P. paniscus. This is thespecies with the absolutely smallest molars, albeitin the most diminutive jaw. Unexpectedly, thisimplies that the bonobo rather than the baboonhad the least space for the developing M2 and M3.

The space distal to each subsequent mineraliz-ing molar crown was, if anything, greater in thebaboon than in either ape, particularly during thesecond half of the molar crown mineralizationperiod. This in itself is very strong evidence thatthere was no “pressure” on space in the mandibleof the baboon and no “extra” space in the mandi-bles of either ape. However, it should be remem-bered that, at this position, not only corpus lengthbut also corpus width contributes to the volume ofspace available for the teeth.

The space between adjacent developing molarsmirrors relative size differences between earlier andlater initiated teeth. In other words, two neigh-boring molars that are further developed arelarger, and hence, have closed more of the distancebetween themselves via their growth. Conversely,if one of these molars is newly initiated, and hence,relatively small, the distance between it and itsmore developed neighbour is greater. Variation inintermolar spacing over time may also reflect sub-tle differences in timing and/or rate of the mesialmigration of the molars within a group. Weemphasize that differences in adjacent intermolardistances were small. Furthermore, should spacedecrease between, for example, M2 and M3, thisdistance would not necessarily be smaller than thatbetween M1 and M2. In this study, variation in thespace maintained around adjacent developingmolars throughout mineralization was deemed toosubtle to have any significant bearing upon differ-ent times of molar crown initiation between taxa.This result and the lack of significant differences inmolar row growth trajectories between speciesstrongly support the idea that space does not affect


the timing of molar tooth initiation in these taxa.We think that this finding is likely to be extensibleto permanent molar development in at least someother primate species. However, further testing isnecessary to confirm this hypothesis.

How might space between developing molarprimordia be regulated?

Understanding the development of otherectodermally-derived organs such as feathers maybe a good model with which to rethink this prob-lem in teeth. As with teeth, feathers form from aswath of embryonic epithelium, fated here tohouse feather primordia. This swath is subdividedinto discrete primordia by the interchanging ex-pression of genes that induce feather formationand others that inhibit it at specific sites (Junget al., 1998). Patel et al. (1999) identified theexpression of the gene Follistatin lateral to andaround the base of each feather bud. This gene isan antagonist to the bone morphogenetic proteins(BMPs) expressed across the feather formationfield: BMPs inhibit the growth of feather primor-dia (Patel et al., 1999). Follistatin cancels theinhibitory influence of BMPs, allowing feather budformation in given locations (Patel et al., 1999).This is the opposite of Osborn’s zone of inhibitionin that the zone that surrounds (or emits from) theprimordium is active rather than inhibitory. Inother words, the default state along the field is oneof inhibition, punctuated by zones of “activation.”The competence to positively respond to genesignaling and thus to form feathers is positiondependent, as is the time of initiation and thedirection of primordial response (Jung et al.,1998). Applying this model to murine toothembryogenesis, Peterkova et al. (2000) proposedthat incomplete delimitation of inhibitory zonesbetween tooth placodes, for example, due to insuf-ficient cell death, can result in the incorporationof otherwise segregated tooth primordia, subse-quently generating novel cusp patterns and crownmorphologies.

The distances between tooth primordia andthose maintained between mineralizing toothcrowns might be determined by a similar system of

gene suppression by antagonists and subsequenttissue competence. Yet this fails to resolve whatestablishes the size of these intervals of tissueincompetence. It is possible that this might behighly conserved not only among teeth but alsoectodermally-derived materials such as feathers orhair. It would be interesting to compare thesedistances among several different taxa. It is alsopossible that spatial arrangements between pri-mordia are established by physical principles thatprohibit the successful development of the cellsand structures within a given distance of eachother. Thus, physiological or physicochemical fac-tors as much as genetics may establish the baselineminimum distance maintained between teethfrom their inception. An example of this kind offundamental spatial organization is the width ofthe periodontal ligament, which seems to averagebetween 1

3 to 14 mm (i.e., 330 microns or 250

microns) in most animal taxa in which it has beenmeasured (Klein, 1928; Louridis et al., 1974;Schroeder, 1986).

Unresolved questions of timing

More progress appears to have been made inunderstanding positional and morphological deter-minants of dental development than in under-standing what controls times and rates of toothgerm initiation and tooth formation. In their re-view of morphogen gradients and cell receptivity,Gurdon and Bourillot (2001) favoured a scenarioin which cells alter their gene response accordingto changes in ambient gradient concentrationsacross time. Future research on genes and signal-ling cascades should focus on cell receptivity tothese signals and thus on what triggers or controlstimes and rates of activity and growth and how.

Conclusions

No significant differences in the space surround-ing and distal to the molar crypts and crowns wereobserved in Papio anubis compared with Pan trog-lodytes or P. paniscus. Thus, any relative delay in


molar crown initiation observed in the babooncannot be attributed to a lack of space in themandible. Whether and to what degree real differ-ences in the relative timing of molar crowninitiation exist between Papio and Pan needsfurther study. However, it seems clear that spacedoes not directly affect crown initiation times inthese taxa.

The study of permanent molar germ initiationand growth is integral to future studies of primatedental development. This is because the timing ofthese earliest events rather than any extrinsic fac-tor appears to have the greatest influence on thetiming of molar crown morphogenesis and initialmineralization. Times of tooth initiation andperiods of crown mineralization have importantimplications for studies of primate life history andhave been interpreted as evidence with which todraw phylogenetic conclusions about living andextinct primate groups (e.g., Smith, 1986, 1989;Bromage, 1987; Beynon and Dean, 1988; Conroyand Vannier, 1991a,b; Dean et al., 1993; Ramirez-Rozzi, 1995; Anemone et al., 1996; Moggi-Cecchi,1998, 2000; Dean and Reid, 2001; Dean et al.,2001). For these reasons among others, ourknowledge of tooth development times, rates, andperiods and what regulates them must be as clearand as comprehensive as possible.

In summary, this comparative study of thetiming and spacing of permanent molar toothdevelopment in Papio anubis, Pan troglodytes, andP. paniscus found that:

1. Ontogenetic changes in the shape and timing ofthe permanent molar row were not statisticallydifferent between Papio and Pan.

2. Distances between adjacent molars were notsignificantly or consistently different betweenthe two genera or between sister species Panpaniscus and P. troglodytes.

3. At any comparative age, space distal todeveloping permanent molars was, if anything,greater in Papio compared to either Panpaniscus or P. troglodytes.

4. The proportion of the posterior corpus occu-pied by the permanent molar row was notablysmaller in Papio compared with Pan at times of

M2 and M3 initiation. This indicates thatPapio has more space in this key regionof its mandible at equivalent stages of molardevelopment than does Pan paniscus or P.troglodytes.

5. These results strongly refute the idea that a“lack” of space in Papio mandibles for thepermanent molar teeth underlies a more stag-gered schedule of molar crown initiation whencompared to Pan troglodytes or P. paniscus.

6. Future studies of primate tooth developmentshould include data on times of crypt initiationand rates of crypt enlargement, without whichanalyses of dental development are incomplete.

Acknowledgements

We would like to thank Sam Cobb, NathanJeffery, Nick Jones, Kornelius Kupczik, DavidPolly, Fernando Ramirez-Rozzi, and GarySchwartz for helpful discussions, sound advice,and ready support in collecting and analyzing ourdata. We thank Don Reid for his histologicaltracings of chimpanzee and baboon molarchronologies. We are also especially grateful toLouise Humphrey, Paul O’Higgins, and Jim Rohlffor their invaluable comments on the design of thestudy and the statistical methods used here. We areindebted to the curators at the Natural HistoryMuseum, London, the Musee Royal de l’AfriqueCentrale, Tervuren, the Powell-Cotton Museum,Kent, and the Royal College of Surgeons ofEngland. In particular, Paula Jenkins (NHM),Wim Wendelen (MRAC), John Harrison andMalcolm Harman (PCM), and Barry Davis (RCS)who accommodated our unusual data collectionprocedures. We thank Jane Pendjiki and ChrisSym of the Photographic Unit of the AnatomyDepartment at UCL, who generously providedequipment and advice. We would like to thank twoanonymous reviewers for helpful comments andsuggestions. This research was funded in part byThe Overseas Research Students Awards Schemeand The Graduate School, UCL and by grants toMCD from The Leverhulme Trust and The RoyalSociety.


References

Anemone, R.L., Mooney, M.P., Siegel, M.I., 1996. Longitudi-nal study of dental development in chimpanzees of knownchronological age: implications for understanding the age atdeath of Plio-Pleistocene hominids. Am. J. phys. Anthrop.99, 119–133.

Anemone, R.L., Watts, E.S., Swindler, D.R., 1991. Dentaldevelopment of known-age chimpanzees, Pan troglodytes(Primates, Pongidae). Am. J. phys. Anthrop. 86, 229–241.

Bailit, H.L., Sung, B., 1968. Maternal effects on the developingdentition. Arch. Oral Biol. 13, 155–161.

Banks, H.V., 1934. Incidence of third molar development. TheAngle Orthodontist 4, 223–233.

Beynon, A.D., Clayton, C.B., Ramirez-Rozzi, F.V., Reid, D.J.,1998. Radiographic and histological methodologies in esti-mating the chronology of crown development in modernhumans and great apes: a review, with some applications forstudies on juvenile hominids. J. hum. Evol. 35, 351–370.

Beynon, A.D., Dean, M.C., 1988. Distinct dental developmentpatterns in early fossil hominids. Nature 335, 509–514.

Beynon, A.D., Dean, M.C., Reid, D.J., 1991. Histologicalstudy on the chronology of the developing dentition ingorilla and orangutan. Am. J. phys. Anthrop. 86, 189–203.

Blankenstein, R., Cleaton-Jones, P.E., Luk, K.M., Fatti, L.P.,1990. The onset of eruption of the permanent dentitionamong South African black children. Arch. Oral Biol. 35,225–228.

Bookstein, F.L., 1991. Morphometric Tools for LandmarkData: Geometry and Biology. Cambridge University Press,Cambridge.

Boughner, J.C., 2002. Dental and mandibular growth in Papioand Pan. Ph.D. Dissertation, University of London.

Bowen, W.H., Koch, G., 1970. Determination of age in mon-keys (Macaca irus) on the basis of dental development.Laboratory Animals 4, 113–123.

Bradley, R.E., 1961. The relationship between eruption, calci-fication, and crowding of certain mandibular teeth. TheAngle Orthodontist 41, 230–236.

Bromage, T.G., 1987. The biological and chronologicalmaturation of early hominids. J. hum. Evol. 16, 257–272.

Bromage, T.G., Dean, M.C., 1985. Re-evaluation of the age atdeath of immature fossil hominids. Nature 317, 525–527.

Butler, P.M., 1956. The ontogeny of molar pattern. BiologicalReview 31, 30–70.

Conroy, G.C., Vannier, M.W., 1991a. Dental development inSouth African australopithecines. Part I: Problems of pat-tern and chronology. Am. J. phys. Anthrop. 86, 121–136.

Conroy, G.C., Vannier, M.W., 1991b. Dental development inSouth African australopithecines. Part II: Dental stageassessment. Am. J. phys. Anthrop. 86, 137–156.

Dean, C., Leakey, M.G., Reid, D., Schrenk, F., Schwartz, G.,Stringer, C., Walker, A., 2001. Growth processes in teethdistinguish modern humans from Homo erectus and earlierhominins. Nature 414, 628–631.

Dean, M.C., 1986. Homo and Paranthropus: similarities in thecranial base and developing dentition. In: Wood, B.A.,

Martin, L., Andrews, P. (Eds.), Major Topics in Primateand Human Evolution. Cambridge University Press,Cambridge, pp. 249–265.

Dean, M.C., Beynon, A.D., 1991. Tooth crown heights, toothwear, sexual dimorphism and jaw growth in hominoids.Z. Morph. Anthrop. 78, 425–440.

Dean, M.C., Reid, D.J., 2001. Perikymata spacing and distri-bution on hominid anterior teeth. Am. J. phys. Anthrop.116, 209–215.

Dean, M.C., Thackaray, J.F., Macho, G., 1993. Histologicalreconstruction of dental development and age at death ofa juvenile Paranthropus robustus specimen, SK 63, fromSwartkrans, South Africa. Am. J. phys. Anthrop. 91,401–419.

Dean, M.C., Wood, B.A., 1981. Developing pongid dentitionand its use for ageing individual crania in comparativecross-sectional growth studies. Folia primatol. 36, 111–127.

Demirjian, A., 1978. Dentition. In: Falkner, F., Tanner, J.M.(Eds.), Human Growth: A Comprehensive Treatise: Post-natal Growth; Neurobiology. Plenum, New York, pp.413–444.

Diamond, M., 1944. The patterns of growth and developmentof the human teeth and jaws. J. Dent. Res. 23, 273–303.

Dirks, W., 1998. Histological reconstruction of dental develop-ment and age at death in a juvenile gibbon (Hylobates lar).J. hum. Evol. 35, 411–425.

Dirks, W., Reid, D.J., Jolly, C.J., Phillips-Conroy, J.E., Brett,F.L., 2002. Out of the mouths of baboons: stress, lifehistory, and dental development in the Awash NationalPark hybrid zone, Ethiopia. Am. J. phys. Anthrop. 118,239–252.

Dryden, I.L., Mardia, K.V., 1998. Statistical Shape Analysis.John Wiley, London.

Fanning, E.A., 1961. A longitudinal study of tooth formationand root resorption. New Zealand Dental Journal 57,202–217.

Fanning, E.A., Moorrees, C.F.A., 1969. A comparison ofpermanent mandibular molar formation in Australian Abo-rigines and Caucasoids. Arch. Oral Biol. 14, 999–1006.

Garn, S.M., Lewis, A.B., 1970. The gradient and the pattern ofcrown-size reduction in simple hypodontia. The AngleOrthodontist 40, 51–58.

Garn, S.M., Lewis, A.B., Blizzard, R.M., 1965. Endocrinefactors in dental development. J. Dent. Res. 44, 243–258.

Garn, S.M., Lewis, A.B., Polachek, D.L., 1959. Variability oftooth formation. J. Dent. Res. 38, 135–148.

Garn, S.M., Lewis, A.B., Polachek, D.L., 1960. Sibling simi-larities in dental development. J. Dent. Res. 39, 170–175.

Garn, S.M., Lewis, A.B., Vicinus, J.H., 1963. Third molarpolymorphism and its significance to dental genetics.J. Dent. Res.. 42, 1344–1363.

Gleiser, I., Hunt, E.E. Jr, 1955. The permanent mandibular firstmolar: its calcification, eruption and decay. Am. J. phys.Anthrop. 13, 253–283.

Goodall, C.R., 1991. Procrustes methods in the statisticalanalysis of shape. Journal of the Royal Statistical Society ofLondon, Series B 53, 285–339.


Gruneberg, H., 1937. The relations of endogenous and exogen-ous factors in bone and tooth development, the teeth of thegrey lethal mouse. J. Anat. London 71, 236–244.

Gurdon, J.B., Bourillot, P.Y., 2001. Morphogen gradientinterpretation. Nature 413, 797–803.

Hillson, S., 1996. Dental Anthropology. Cambridge UniversityPress, Cambridge.

Jenkins, P.D., 1990. Catalogue of Primates in the BritishMuseum (Natural History) Part V: The Apes, SuperfamilyHominoidea. British Museum (Natural History), London.

Jernvall, J., Kettunen, P., Karavanova, I., Martin, L.B.,Thesleff, I., 1994. Evidence for the role of the enamel knotas a control centre in mammalian tooth cusp formation:non-dividing cells express growth stimulating Fgf-4 gene.International Journal of Developmental Biology 38,463–469.

Jernvall, J., Thesleff, I., 2000. Reiterative signaling and pattern-ing during mammalian tooth morphogenesis. Mechanismsof Development 92, 19–29.

Jung, H.S., Francis-West, P.H., Widelitz, R.B., Jiang, T.X.,Ting-Berreth, S., Tickle, C., Wolpert, L., Chuong, C.M.,1998. Local inhibitory action of BMPs and their relation-ships with activators in feather formation: implications forperiodic patterning. Dev. Biol. 196, 11–23.

Kitahara, Y., Suda, N., Kuroda, T., Beck, F., Hammond, V.E.,Takano, Y., 2002. Disturbed tooth development in para-thyroid hormone-related protein (PTHrP)-gene knockoutmice. Bone 30, 48–56.

Klein, A., 1928. Systematische Untersuchungen uber diePeriodontalbreite. Zeitschrift fur Stomatologie 26, 417–439.

Kollar, E.G., Lumsden, A.G.S., 1979. Innervation and toothinitiation in the mouse embryo. Journal de Biologie Buccale7, 49–60.

Kraus, B.S., Jordan, R.E., 1965. The Human Dentition BeforeBirth. Henry Kimpton, London.

Lefkowitz, W., Bodecker, C.F., Mardfin, D.F., 1953. Odon-togenesis of the rat molar: prenatal stage. J. Dent. Res. 32,749–772.

Legros, C., Magitot, E., 1879. Morphologie fu follicule dentairechez les mammiferes. J. Anat. Paris 15, 248–293.

Liu, J.G., Tabata, M.J., Yamashika, K., Matsumura, T.,Iwamoto, M., Kurisu, K., 1998. Developmental role ofPTHrP in murine molars. European Journal of Oral Science106, 143–146.

Louridis, O., Demetriou, N., Bazapoulou-Kyrkanidou, E.,1974. Periodontal ligament thickness as related to age andmesiocclusal drifting of teeth: a histometric study. J.Periodontology 45, 862–865.

Liu, J.G., Tabata, M.J., Fujii, T., Oomori, T., Abe, M., Ohsaki,Y., Kato, J., Wakisaka, S., Iwamodo, M., Kurisu, K., 2000.Parathyroid hormone-related peptide is involved in protec-tion against invasion of tooth germs by bone via promotingthe differentiation of osteocytes during tooth development.Development 95, 189–200.

Manson, J.D., 1967. The Mechanics of Tooth Support: ASymposium. Bone Changes Associated with ToothEruption. Wright, Bristol, pp. 98–101.

Marcus, L.F., Corti, M., Loy, A., Naylor, G.J.P., Slice, D.(Eds.), 1996. Advances in Morphometrics. Plenum Press,New York.

Moggi-Cecchi, J., 1998. Patterns of dental development ofAustralopithecus africanus, with some inferences on theirevolution with the origin of the genus Homo. In: Tobias,P.V., Raath, M.A., Moggi-Cecchi, J, Doyle, G.A. (Eds.),Humanity from African Naissance to Coming Millenium:Colloquia in Human Biology and Palaeoanthropology.Firenze University Press, Firenze, Italy, pp. 125–133.

Moggi-Cecchi, J., 2000. Fossil children: what can they tell usabout the origin of the genus Homo?. In: Aloisi, M.,Battaglia, B., Carafoli, E., Danieli, G.A. (Eds.), The Originof Humankind: Conference Proceedings of the Inter-national Symposium. IOS Press, Oxford, pp. 35–50.

Napier, P.H., 1981. Catalogue of Primates in the BritishMuseum (Natural History) Part II: Family Cercopithecoi-dea, Subfamily Cercopithecinae. British Museum (NaturalHistory), London.

Natchbandi, I.A., Weir, E.E., Insogna, K.L., Philbrick, W.M.,Broadus, A.E., 2000. Parathyroid hormone induces spon-taneous osteoclast formation via a paracrine cascade. Proc.natl. Acad. Sci. 97, 7296–7300.

Nolla, C.M., 1960. The development of the permanent teeth.Journal of Dentistry for Children 4, 254–266.

O’Higgins, P., Jones, N., 1998. Facial growth in Cercocebustorquatus: an application of three-dimensional geometricmorphometric techniques to the study of morphologicalvariation. J. Anat. 193, 251–272.

Oka, S.W., Kraus, B.S., 1969. The circumnatal status of molarcrown maturation among the Hominoidea. Arch. Oral Biol.14, 639–659.

Olson, W.C., Hughes, B.O., 1943. Growth of the child as awhole. In: Barker, R.G., Kounin, J.S., Wright, H.F. (Eds.),Child Behaviour and Development. McGraw-Hill BookCompany, Inc, London, pp. 199–208.

Osborn, J.W., 1978. Morphogenetic gradients: fields versusclones. In: Butler, P.M., Joysey, K.A. (Eds.), Development,Function and Evolution of Teeth. Academic Press, London,pp. 171–201.

Patel, K., Makarenkova, H., Jung, H.S., 1999. The role of longrange, local and direct signaling molecules during chickfeather bud development involving the BMPs, Follistatinand the Eph receptor kinase Eph-A4. Mechanisms ofDevelopment 86, 51–62.

Peterkova, R., Peterka, M., Viriot, L., Lesot, H., 2000. Denti-tion development and budding morphogenesis. Journal ofCraniofacial Genetics and Developmental Biology 20,158–172.

Philbrick, W.M., Dreyer, B.E., Natchbandi, I.A., Karaplis,A.C., 1998. Parathyroid hormone-related protein is re-quired for tooth eruption. Proc. natl. Acad. Sci. 95,11846–11851.

Philbrick, W.M., Wysolmerski, J.J., Galbraith, S., Holt, E.,Orloff, J.J., Yang, K.H., Vasavada, R.C., Weir, E.C.,Broadus, A.E., Stewart, A.F., 1996. Defining the roles of


parathyroid hormone-related protein in normal physiology.Physiological Reviews 76, 127–173.

Ramirez-Rozzi, F.V., 1995. Time of crown formation in Plio-Pleistocene hominid teeth. In: Moggi-Cecchi, J. (Ed.), As-pects of Dental Biology: Palaeontology, Anthropology andEvolution. International Institute for the Study of Man,Florence, pp. 217–237.

Reid, D.J., Schwartz, G.T., Dean, M.C., Chandrasekera, M.S.,1998. A histological reconstruction of dental developmentin the common chimpanzee, Pan troglodytes. J. hum. Evol.35, 427–448.

Sarkar, L., Cobourne, M., Naylor, S., Smalley, M., Dale, T.,Sharpe, P.T., 2000. Wnt/Shh interactions regulate ecto-dermal boundary formation during mammalian toothdevelopment. Proc. natl. Acad. Sci. 97, 4520–4524.

Schroeder, H.E., 1986, The Periodontium. Handbook ofMicroscopic Anatomy. V/5. Springer, Berlin.

Sharpe, P.T., 2001. Neural crest and tooth morphogenesis. In:Tziafas, D. (Ed.), Advances in Dental Research. Proceed-ings of the International Meeting on Signalling Mechanismsin Dentin Development, Regeneration, and Repair: FromBench to Clinic. International Association for DentalResearch. Alexandria, Virginia, pp. 4–7.

Siebert, J.R., Swindler, D.R., 1991. Perinatal dental develop-ment in the chimpanzee (Pan troglodytes). Am. J. phys.Anthrop. 86, 287–294.

Slice, D.E., Bookstein, F.L., Morcus, L.F., Rohlf, F.J., 1998. Aglossary for geometric morphometrics, Parts 1 and 2.World wide web, http://life.bio.sunysb.edu/morph/glossary/gloss7.html, and http://life.bio.sunysb.edu/morph/glossary/gloss2.html, respectively.

Smith, B.H., 1986. Dental development in Australopithecus andearly Homo. Nature 323, 327–330.

Smith, B.H., 1989. Dental development as a measure of lifehistory in primates. Evolution 43, 683–688.

Smith, B.H., Crummet, T.L., Brandt, K.L., 1994. Ages oferuption of primate teeth: a compendium for aging individ-uals and comparing life histories. Yearb. phys. Anthrop. 37,177–231.

Smith, B.H., Tompkins, R.L., 1995. Toward a life history of theHominidae. A. Rev. Anthrop. 24, 279.

Swindler, D.R., 1961. Calcification of the first mandibularmolar in rhesus monkeys. Science 134, 566.

Swindler, D.R., Beynon, A.D., 1993. The development andmicrostructure of the dentition of Theropithecus. In:

Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of aPrimate Genus. Cambridge University Press, Cambridge,pp. pp. pp. 351–381.

Swindler, D.R., Emel, L.M., 1990. Dental development,skeletal maturation and body weight at birth in pig-tailmacaques (Macaca nemestrina). Arch. Oral Biol. 35,289–294.

Swindler, D.R., Gavan, J.A., 1966. Variability of mandibulartooth formation in the rhesus monkey. Dental Research 45,1234.

Swindler, D.R., Meekins, D., 1991. Dental development of thepermanent mandibular teeth in the baboon, Papiocynocephalus. Am. J. hum. Biol. 3, 571–580.

Swindler, D.R., Olshan, A.F., Sirianni, J.E., 1982. Sex differ-ences in permanent mandibular tooth development inMacaca nemestrina. Hum. Biol. 54, 45–52.

Tarrant, L.H., Swindler, D.R., 1972. The state of the deciduousdentition of a chimpanzee fetus (Pan troglodytes). J. Dent.Res. 51, 677.

Thesleff, I., Keranen, S., Jernvall, J., 2001. Enamel knots assignaling centers linking tooth morphogenesis and odonto-blast differentiation. In: Tziafas, D. (Ed.), Advances inDental Research. Proceedings of the International Meetingon Signaling Mechanisms in Dentin Development, Regen-eration, and Repair: From Bench to Clinic. InternationalAssociation for Dental Research, Alexandria, Virginia, pp.14–18.

Thesleff, I., Sharpe, P.T., 1997. Signaling networks regulatingdental development. Mechanisms of Development 67,111–123.

Thompson, G.W., Anderson, D.L., Popovich, F., 1975. Sexualdimorphism in dentition mineralization. Growth 39,289–301.

Tompkins, R.L., 1996. Human population variability in rela-tive dental development. Am. J. phys. Anthrop. 99, 79–102.

Winkler, L.A., 1995. A comparison of radiographic and ana-tomical evidence of tooth development in infant apes. Foliaprimatol. 65, 1–13.

Wysolmerski, J.J., Cormier, S., Philbrick, W.M., Dann, P.,Zhang, J.P., Roume, J., Delezoid, A.L., Silve, C., 2001.Absence of functional type I parathyroid hormone (PTH)/PTH-related protein receptors in humans is associated withabnormal breast development and tooth impaction. Journalof Clinical Endocrinology and Metabolism 86, 1788–1794.


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