Continuous dental eruption identifies Sts 5 as developmentally oldest fossil hominin and informs the...

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Journal of Human Evolution xxx (2013) 1e8

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Journal of Human Evolution

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Continuous dental eruption identifies Sts 5 as the developmentallyoldest fossil hominin and informs the taxonomy of Australopithecusafricanus

B. Villmoare a,b,*, K. Kuykendall c, T.C. Rae d, C.S. Brimacombe c

aCenter for the Advanced Study of Hominid Paleobiology, The George Washington University, USAbDepartment of Anthropology, University College London, United KingdomcDepartment of Archaeology, University of Sheffield, United KingdomdDepartment of Life Sciences, University of Roehampton, United Kingdom

a r t i c l e i n f o

Article history:Received 1 July 2013Accepted 30 September 2013Available online xxx

Keywords:AustralopithecusHomininDental developmentDental wearTooth rootSexual dimorphismFacial morphology

* Corresponding author.E-mail address: [email protected] (B. Villmoare).

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Please cite this article in press as: Villmoareand informs the taxonomy of Australopithec

a b s t r a c t

The relatively small Australopithecus africanus specimen Sts 5 has figured prominently in taxonomicdebates, and the determination of this specimen as a young male or an elderly female has the potential tooffer a great deal of resolution on this question. Sts 5 has been argued to be either a small, immature maleor a mature female based on a variety of characters.

A proposed model of continuous root remodeling and angular change for heavily worn dentition mayaccount for the extremely short tooth roots, particularly for the anterior dentition, that Sts 5 demon-strates. The anterior tooth roots of Sts 5 are oriented vertically (relative to the alveolar plane), unlikethose found in most other apes, humans, and fossil specimens, in which the tooth roots are roughlyparallel with the plane of the nasoalveolar clivus.

Computed tomography (CT) data of adult apes were examined and a relationship between the angle ofthe anterior tooth roots and their length was discovered, caused by heavily worn anterior dentitioncontinuing to erupt to maintain occlusion. The extremely short and vertically oriented anterior rootsobserved in Sts 5 thus suggest that the specimen represents an aged female specimen with extremelyworn dentition. Interestingly, this reorientation of anterior tooth roots helps account for the unusualnasoalveolar contour of Sts 5. The remodeling associated with the heavily worn teeth and reorientedroots thus resolves the taxonomic question raised by analyses identifying unusual prognathism of thissmall specimen.

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Introduction

As the most complete and undistorted cranium of Austral-opithecus africanus yet discovered, Sts 5 (also known as ‘Mrs. Ples’)has served an important role in the popular press and has also beenfrequently used as a reference point for discussion of the cranialanatomy of A. africanus (e.g., Tobias, 1967; Rak, 1983, 1985;Lockwood and Tobias, 2002; Kimbel et al., 2004). This specimenhas received special attention in the last ten years as a focus ofcontroversy over its sex and ontogenetic age at death (Grine et al.,2012). There is considerable debate over the attribution of age andgender for this specimen, and resolving these issues will play animportant role in taxonomic debates over the A. africanus holotype

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(Grine et al., 2012). Sts 5 was initially identified as female (Broom,1947; Broom and Robinson, 1950), primarily due to the size of thecanine root socket (the specimen is edentulous). The overall patternof sutural fusion is consistent with an adult, and the small size ofthe individual, along with the size of the canine root, is mostconsistent with an adult female (Broom and Robinson, 1950;Lockwood, 1997). This assignment has received broad support,largely on the basis of size (Lockwood, 1997, 1999).

It has also been argued, however, that some elements of thecraniofacial anatomy in Sts 5, such as the anterior pillars andglabella, are most consistent with a male (Rak, 1983, 1985). Morerecently it has been proposed, on the basis of craniofacial measures,that Sts 5 has the overall shape of a male (Thackeray, 1997, 2000),that the lack of sutural closure suggests sub-adult status, and eventhat it may have been in the process of forming a sagittal crest(Potze and Thackeray, 2010). Computed tomography (CT) scans ofSts 5 indicated to some researchers (Thackeray et al., 2002) that the

ruption identifies Sts 5 as the developmentally oldest fossil homininn Evolution (2013), http://dx.doi.org/10.1016/j.jhevol.2013.09.007

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Figure 1. CT scans of anterior dentition of specimens of Australopithecus in sagittal (top row) and coronal (bottom row) section. The tooth roots of Sts 5 are notably shorter thanthose of other fossil specimens, in which the roots approach the floor of the nasal aperture. This is also the condition typically found in great apes and modern humans.

B. Villmoare et al. / Journal of Human Evolution xxx (2013) 1e82

C and M3 root apices are open and, thus, the morphological patterncould indicate an interpretation of the specimen as a young sub-adult male.

This explanation, however, has been challenged by those whointerpret the right M3 roots as showing closed apices (Grine et al.,2012), which would only be present in a fully adult specimen.The valence of the pattern of sutural closure is also disputed.Several other clearly adult specimens possess open cranial suturesand the spheno-occipital synchondrosis is not sufficiently well-preserved to offer a clear determination (Grine et al., 2012). Simi-larly, the proposal that this specimenwas likely to develop a sagittalcrest is speculative, and this trait has been found only in particu-larly large specimens of A. africanus (Lockwood and Tobias, 1999;Grine et al., 2012).

One particularly noteworthy characteristic of Sts 5 is the rela-tively small size of the canine root. Pre-depositional erosion hasbeen proposed (Potze and Thackeray, 2010), and an abraded alve-olus would result in the appearance of a short canine root in whatwould be an artificially shallow palate. This argument has beensubsequently refuted, as the palate of this specimen is relativelydeep for this species (Grine et al., 2012), and early arguments(Broom and Robinson, 1950) for sexual dimorphism as the cause ofthe small canine root were supported (Grine et al., 2012).

Phylogenetic implications

The taxonomic status of A. africanus has been the subject ofconsiderable debate (Kimbel and White, 1988; Clarke, 1988, 1994,2008; Lockwood, 1999; Lockwood and Tobias, 1999). Variation inthe sample has led some to suggest that there may be two speciesrepresented by the Member 4 specimens found at Sterkfontein(Clarke, 1988, 1994, 2008), largely on the basis of tooth and skullsize. Sts 5 particularly presents an unusual pattern, as it metricallyfalls into a smaller morph, yet possesses qualitative traits that aresuggestive of a male (Lockwood, 1999). Kimbel and White(1988:185) highlighted the importance of the sex of Sts 5 in thisdebate, drawing attention to the high degree of prognathism in thissmaller specimen (both in tooth root size and overall size):

Please cite this article in press as: Villmoare, B., et al., Continuous dental eand informs the taxonomy of Australopithecus africanus, Journal of Huma

“Following the great ape model, under the hypothesis that thedifferences in facial prognathism are attributable to sexual dimor-phism, we should expect females to be less prognathic than males.(W)e view Sts 71 as a male. But if Sts 5 is a female, as is commonlythought, then the difference between these specimens is oppositethat which characterizes the sexes in great apes.” Therefore, theresolution of Sts 5 as either a young male or an old female haspotentially significant taxonomic implications.

Anterior dentition

Sts 5 is notable for its short tooth roots, especially in the anteriordentition (Fig. 1). Typically, the roots of the central incisors extendsuperiorly to just below the nasal margin, and this pattern ischaracteristic of great apes and early hominins alike, for both sexes.On Sts 5, however, the roots barely extend above the alveolus.While a reduced canine root might be attributable to sexualdimorphism, there is no evidence that there is a pattern of sexualdimorphism expressed in the incisor roots.

What remains unclear at present is whether there is a hominidpattern of age-related change in incisor root length and/or orien-tation. The presence of such a pattern could go someway towards amore secure age and sex determination of Sts 5 and possibly otherfossil hominins. It is proposed here that the condition seen in Mrs.Ples is consistent with that seen in senescent extant hominids withheavy tooth wear, making it more likely to be a female, due to size.The mechanism responsible for such a pattern of incisor root size/orientation is discussed below. This interpretation may also explainother seemingly unique morphological attributes of this importantearly hominin specimen and clarify the taxonomy of A. africanus.

Alveolar remodeling

The tooth roots are set in alveolar bone, a highly reactive sub-strate. Due to dental development and replacement, a continuousprocess of bone deposition and resorption occurs to maintaindental function throughout the life cycle (Kraw and Enlow, 1967;Wise and King, 2008). To maintain occlusion, teeth move by


Table 2Fossil sample.

Specimen Species Museum

Sts 5 A. africanus University of the WitwatersrandSts 71 A. africanus University of the WitwatersrandSts 17 A. africanus University of the WitwatersrandA.L. 444-2 A. afarensis Ethiopian National MuseumSK 12 P. robustus Ditsong National Museum of

Natural HistorySK 46 P. robustus Ditsong National Museum of

Natural HistorySK 79 P. robustus Ditsong National Museum of

Natural HistoryKNM-WT 17000 P. aethiopicus National Museums of KenyaOH 5 P. boisei National Museums of KenyaKNM-ER 1813 H. habilis National Museums of KenyaKNM-ER 1805 H. habilis National Museums of Kenya

Figure 2. Angles and lengths (here in specimen USNM 174706 of P. troglodytes). Thelength of the incisor root (in yellow) was measured from the interior edge (wheredamage was less likely) of the root cavity to the apex of the cavity (whether or not atooth was present). The root incisor inclination angle (in red) is determined by takingthe axis of the tooth (measured from the apex to the center of the cavity at thealveolus) against the plane of the palate. (For interpretation of the references to colourin this figure legend, the reader is referred to the web version of this article.)

B. Villmoare et al. / Journal of Human Evolution xxx (2013) 1e8 3

passive eruption, mesial drift, and lingual tipping (d’Incau et al.,2012). Mesial drift is linked with dental eruption and wear inmammals, including sequential, conveyor-belt eruption in ele-phants and continuous dental replacement with supernumeraryteeth in a few taxa, such as manatees, the wallaby, and the mole-rat(Rodrigues et al., 2011). It even occurs in those taxa typicallycharacterized as displaying distal drift; e.g., rats (Roux and Woda,1994). Across humans and apes, the patterns of remodelingappear to be consistent (Margvelashvili et al., 2011).

The angles of the incisors relative to the alveolar plane change inmodern human populations with extreme wear of the anteriordentition (Kaifu, 2000; Kaifu et al., 2003). This reorientation istermed ‘lingual tipping’, in which the incisors with interproximalwear become more perpendicular relative to the alveolar plane soas to maintain contact with the adjacent teeth (Kaifu, 2000). Thisallows incisors with occlusal wear to maintain contact with thelower incisors (Kaifu et al., 2003), although the underlying mech-anisms are not currently known.

Continuous eruption is the process of tooth crowns becomingelevated above the alveolar margin as they wear, and is a naturalcompensatory mechanism for the maintenance of tooth height lostby wear (Dean et al., 1992). It has been documented in multiplepreindustrial populations, particularly in postcanine teeth, andserves as a general explanatory model for the maintenance of oc-clusion (Kaifu et al., 2003). This process also has been identified inthe postcanine dentition of Pan troglodytes specimens with heavytooth wear, with the process only ending when there was insuffi-cient enamel to maintain occlusion of any kind (Dean et al., 1992).

To test whether these mechanisms of age-related changeexplain the morphological pattern seen in Sts 5, crania of extantand extinct hominids were examined using CT. If the conditionsfound in Mrs. Ples are consistent with aged individuals in extantforms, the fossil is unlikely to represent a male, given its diminutiveoverall size.

Materials and methods

Computed tomography scans of Australopithecus afarensis,A. africanus, Paranthropus robustus, Paranthropus boisei, Para-nthropus aethiopicus, Homo habilis, P. troglodytes, Gorilla gorilla, andPongo pygmaeuswere examined (see Tables 1 and 2 for samples andsizes). The CT data were collected from a variety of sources, andinclude all available scans of relevant specimens from the speciesanalyzed. For specimens SK 11, SK 12, SK 46, SK 79, SK 83, and SKW11, scans were made by Dr. Chris Williams at Moot AlgemeneHospital, Pretoria, on a Phillips Brilliance 40, 0.3300 mm slices withpixel size of 0.3222 mm. Specimens SK 13/14, SK 48, SK 52, Sts 17,and Sts 52 were scanned by Ms. Stephany Potze of the TransvaalMuseum at Little Company of Mary Hospital in Pretoria on aSiemens Sensation 16, 0.7500 mm slices, with voxel sizes rangingfrom 0.2929 mm to 0.3476 mm. Other fossil scans (Sts 5, Sts 71, OH

Table 1Extant sample.

Species Sample size Museum

Pan troglodytes troglodytes (CT data) 29 Smithsonian MuseumNatural History

P. troglodytes verus (CT data) 21 Peabody MuseumPongo pygmaeus (CT data) 59 Smithsonian Museum

Natural HistoryGorilla gorilla gorilla (CT data) 24 Smithsonian Museum

Natural HistoryG. gorilla beringei (CT data) 23 Smithsonian Museum

Natural HistoryPan troglodytes (X-rays) 53 Powell Cotton Museum


5, KNM-WT 17000, and A.L. 444-2) are from the digital archives atthe University of Vienna and the National Museums of Kenya.Smithsonian CT scans were made with a SIEMENS SomatomEmotion scanner, 1.0 mm slice, 0.5 mm reconstruction increment,and H90 moderately sharp kernel. The Peabody CT data werecollected with a Siemens scanner using 0.500 mm slices and a pixelsize of 0.488mm.We used ImageJ 1.42 (National Institute of Health,USA) and Amira 4.1.2 (Mercury Computer Systems) to examine theCT data.

Individuals were examined in the sagittal plane, with the slicebisecting the root of the right central upper incisor (in fossils, thebetter preserved side was examined; in the case of Sts 5 and Sts 71,the left is better preserved). The length of the incisor root cavity(readily visible in CT section whether the tooth was present or not)and the angle of the root cavity relative to the plane of the hardpalate (here termed the ‘incisor inclination angle’, after Kaifu,2000) were measured using Amira 4.1.2 (Fig. 2). The axis of theroot cavity was simply the center line from the tip of the root cavityto the midpoint of the cavity at the aperture of the alveolus. Thelength of the root cavity was scaled against a measure of the size ofthe clivus, in this case prosthion to nasospinale length, which is


Figure 3. Data collected from the high-resolution X-ray sample. A. crown height, B.length of the exposed root, C. overall tooth length.


here termed ‘relative’ root length. Note that the use of the rootcavity allowed analysis of edentulous or otherwise dentallydamaged specimens (which were a significant proportion of thesample).

High resolution X-ray images of the anterior dentition of 53specimens of P. troglodytes were made using an Aribex Nomad Prohandheld portable dental X-ray. The detector was a Schick CDR Elite

Figure 4. Angle of incisor inclination (log-transformed) against length of incisor root. Notiresult indicates that as incisors become shorter, they reorient to maintain occlusion. Sts 5 falbased on the angle of inclination. This result may indicate erosion of the alveolus, as proposeother fossils examined.


Size 2 Sensor and the software used was CDR Dicom for Windows.Data collected on these specimens included crown height (Fig. 3A)and root exposure (Fig. 3B), both of which were scaled againstoverall tooth height (root plus crown, Fig. 3C).

Relative length of the incisor root was correlated with the angleof occlusion, with the expectation that as the roots became rela-tively shorter, they would become more perpendicular relative tothe plane of the hard palate to reflect the reorientation associatedwith lingual tipping (Kaifu et al., 2003). Extremely short roots suchas those seen in Sts 5 would be highly perpendicular. Because theraw angle data presented a negative logarithmic relationship, theangles were log-transformed so that standard covariance analysiscould be performed. For the X-ray data, the relative lengths of thecrown and exposed root were tested for covariance.

Because prognathism has been proposed as a distinguishingcharacter for Sts 5, we examined prognathism in the A. africanusspecimens using an angle of the nasospinaleeprosthion lineagainst the alveolar plane (as in Tobias’ [1967] alveolar profile).These angleswere collected using the CT data, with sagittal sectionsthrough the midline (for nasospinale and prosthion) and throughthe postcanine alveolus (to capture the alveolar plane). Note thatthere are varying degrees of damage to the anterior alveolus in all ofthe specimens of A. africanus. Estimations were therefore necessaryto some degree. Our interpretations can be assessed in SOM Fig. 1,where the actual angular measurements using the Amira 4.1.2angular measurement tool superimposed on CT surface renderingscan be seen.

Results

There was a highly significant relationship between the relativelength of the incisor root cavity and the incisor inclination angle forall modern samples examined (for the combined sample,r ¼ �0.6897, p < 0.000001, Pan r ¼ �0.685, p < 0.0001, Gorillar¼�0.6349, p< 0.0001, Pongo r¼�0.7384, p< 0.0001). Individuals

ce that juvenile specimens fall to the opposite end of the distribution from Sts 5. Thisls below the regression line, indicating that it has shorter roots than would be expected,d by Potze and Thackeray (2010), although it would fall close to a regression line of the


Figure 5. Scatterplot demonstrating age-related changes in root exposure and alveolusdepth with crown height due to occlusal wear in a sample of chimpanzee incisor teeth.Teeth demonstrating more occlusal wear (shorter crown height) have shallower rootcavities and more root exposed between the tooth crown and alveolar margin.


with short roots showed a more vertical inclination angle, whetherexamining the modern species or the fossil specimens. Sts 5 fallswithin the 95% confidence interval for the regression line, but it alsofalls close to the extreme end of the bivariate distribution. Weincluded subadult specimens with completely erupted incisors inthis analysis and these individuals fall to the opposite end of theregression from Sts 5 (Fig. 4).

In the Powell-Cotton Pan X-ray sample, there was a highly sig-nificant inverse correlation between relative crown height andrelative root exposure (I1 r ¼ �0.6174, p < 0.001; I2 r ¼ �0.6713,p < 0.001, Figs. 5 and 6). The process of continuous eruption withtooth wear during life appears to result in a condition with heavilyworn crowns (low crown height) and substantial root exposurebetween the tooth cervix and alveolar margin.

Figure 6. X-rays of chimpanzee incisor teeth at different stages of occlusal wear: (left) youngand little root exposure at the alveolar margin; (right) aged adult chimpanzee with high demargin.


Sts 5 was not found to be more prognathic than other non-robust specimens of Australopithecus. The angle of prognathismfor Sts 5was 45.1

�, with Sts 17 at 45.3

�, Sts 71 at 44.4

�, and A.L. 444-2

at 36.2�(see SOM Fig. 1).

Discussion

The results of this analysis are consistent with those of Broom(1947), Broom and Robinson (1950) and Grine et al. (2012). Sts 5appears to have short root cavities because this specimen wouldhave had extremely heavily worn teeth at the time of death. Giventhe positions of the subadult specimens, the most plausibleinterpretation of this result is that Sts 5 represents a senescentadult. In fact, our interpretation of Fig. 4 is that Sts 5 is thedevelopmentally oldest hominin known, given its extreme posi-tion on the plot.

Dental development and wear

If Sts 5 was determined to be a subadult on the basis ofincomplete apical closure of the M3 roots (as proposed byThackeray et al., 2002), it was not likely to have been older thanabout 12 years of age at death, following a dental developmentschedule similar to living chimpanzees (Anemone et al., 1991;Smith, 1991; Kuykendall, 2003). In subadult and young adultapes, humans and early hominins, incisor tooth crowns and rootswould be expected to be fully formed at the time of M3 root apicalclosure (Fig. 6). Our understanding of dental development inchimpanzees and early hominins cannot provide a more refinedage estimate, but the morphology described for the tooth roots inSts 5 does not fit the pattern for recently complete, unworndentition (i.e., as expected for a subadult or young adult) becausejuvenile specimens never display both shallow roots and nearlyfused apices. The pattern is most consistent with a developmentallyadvanced stage; continued eruption of the teeth at older ages as thecrowns wear occlusally would have altered the metric relationshipbetween crown height and root length, and resulted in a shallowerdepth for tooth roots (Dean et al., 1992).

er adult chimpanzee with little occlusal wear, deeper and more elongated root cavities,gree of occlusal wear, shallow root alveoli, and extensive root exposure at the alveolar


Figure 7. Cementum build-up on lingual aspect of the root of a heavily worn Pancentral incisor (anterior three-quarter view and cross-section through the sagittalmidline). This build-up appears to be responsible, at least partially, for the reor-ientation of heavily worn incisors in the maxilla. Image courtesy of Christopher Dean


Mechanism

The change in the angle of the maxillary incisors appears to beassociated with the accumulation of cementum on the lingualaspect of the incisors. In section view of a heavily wornP. troglodytes central incisor, cementum build-up is clearly visibleand contributes to the reorientation of the incisors (Fig. 7).Cementum is a non-vascularized mineralized tissue that forms theinterface between the root dentin and the periodontal ligament(Pitaru et al., 1994; Diekwisch, 2001). There are several types ofcementum. In Fig. 6, the cementum development appears to beconsistent with the apical distribution of the relatively fast-developing cellular intrinsic fiber cementum. This type ofcementum is known to be adaptive in repair and maintenance oftooth position (Gonçalves, 2005). Acellular intrinsic fibercementum, however, is known to be responsible for mesial drift,and has been demonstrated to be thicker on the distal side of teeth,and greater thickness has been found in older individuals

Figure 8. Comparison of two specimens of Pan troglodytes with differing amounts of incisorthe bulge of bone on the alveolus surrounding the reoriented root.


(Dastmalchi et al., 1990). In either case, intrinsic fiber cementum isclearly plastic, and appears to reflect the changes in tooth positionto maintain occlusion in the incisors. Further research into thisphenomenon is warranted.

Sex of Sts 5

Since this result does not suggest that Sts 5 was a subadult male,other factors relevant to interpretations of sexual dimorphismbecome paramount. Lockwood (1999) did find some features of theupper face in Sts 5 to be more consistent with a male; however,there is considerable variation in expression in extant species withregard to supraorbital morphology (Lockwood, 1997; Lockwoodand Tobias, 1999). Overall cranial size does suggest that Sts 5 wasa female, but the continuous eruption of the anterior dentitionmakes interpretation of the canine root suspect, since the specimenwould have had heavily worn canines that would have also showedcontinuous eruption. In the Pan sample studied here, there was ahighly significant correlation between relative central incisor rootlength and relative canine root length (r ¼ 0.6080, p ¼ 0.0006), sothe shortened canine roots in the fossil are likely to be the result ofwear rather than sex. However, we are inclined to conclude that Sts5 was a female based on size, considering the degree of sexualdimorphism in this species (Lockwood,1999; Lockwood and Tobias,1999).

Prognathism in Sts 5 and taxonomic implications

Despite the obvious importance of cementum build-up, it isclear that the bony alveolus remodels as well to accommodate thechanges to the angle of the anterior dentition. This pattern can beseen in CT images of P. troglodytes (Fig. 8), where the anteriordentition shows heavy occlusal wear, a shorter root cavity resultsfrom continuous eruption of the incisor, and the angle of the rootcavity displays a more vertical incisor inclination angle (Fig. 7) (alsovisible in profiles of the Pan specimens: see Figs. 8 and 9). The re-sults here highlight this element of anatomy on the alveolus of Sts 5(Fig. 1). Viewed in profile (the nasoalveolar contour of Kimbel et al.,1984), Sts 5 can be seen to have a protruding alveolus. Otherspecimens of A. africanus typically display a more direct line,slightly convex, between the nasal aperture and the dental arcade.This is also the condition normally seen in the great apes. However,when the roots of the anterior dentition reorient vertically, thealveolar bone must remodel to maintain occlusion of the teeth.

This phenomenon can be seen in a transparent overlay of Sts 5over Sts 71 (Fig.10), where the faces are scaled and rotated tomatchthe supraorbital morphology, inferior nasal aperture, cranial base,and alveolar planes. On Sts 71, the nasoalveolar contour is slightly

wear. Note on the right specimen the heavily worn incisor, the short, vertical root, and


Figure 9. Specimens used to generate the X-rays in Fig. 4 (PCM ZIV 51 and PCM M234). Note the difference in the bulge at the alveolus (right), as a part of reorientation of theanterior dental roots.


convex, but roughly in a direct line from the inferior nasal apertureto prosthion. On Sts 5 the main profile is shared, but the lowercontour bulges to accommodate the incisor roots.

Sts 5 has been identified as having an unusual degree ofprognathism (Robinson, 1956; Tobias, 1967; Kimbel et al., 2004).In our study, however, Sts 5 falls among the other non-robustspecimens of Australopithecus. Our explanation is that the pres-ence of the bulge resulting from reoriented dental roots has led tointerpretations of significant prognathism for this specimen,whereas the actual measure of prognathism and the angle of thesubnasal facial profile of Sts 5 is actually very similar to that seenin other specimens of A. africanus (as in Fig. 10). Tobias (1967)proposed that Sts 5 was more prognathic than other specimens

Figure 10. Transparent overlay of Sts 71 over Sts 5, adjusted to scale. Notice theprotruding bulge of Sts 5 due to the remodeled bone surrounding the roots of theanterior dentition (point A and red arrow). The red line indicates the maxilla of Sts 71and, as there is considerable damage to that specimen in the anterior alveolus, theyellow dotted line continues that line to the plane of the anterior alveolus in Sts 5(point B and yellow arrow), which is where we expect that prosthion for Sts 71 wouldhave fallen. The extreme wear of Sts 5 may therefore account, in part, for the unusuallyalveolar bulge seen in this individual, and the profile of Sts 71 likely represents thecondition that would have been seen in Sts 5 prior to reorientation of the anteriordentition. (For interpretation of the references to colour in this figure legend, thereader is referred to the web version of this article.)


of A. africanus, but did not attempt to quantify this impression.Kimbel and White (1988) used the sellioneprosthion line asmeasured from photographic profiles, where the protrusion atthe alveolus strongly influences the calculation of prognathismand all protrusion below sellion is aggregated. When calculatedat the midline using CT data, the angle of subnasal prognathismfor Sts 5 is not unusual for A. africanus (note that in Fig. 10 thealveolar planes of the two specimens are aligned). Sts 71 hasdamage to the anterior alveolus, but in Fig. 10 we extended theline along the clivus to the plane of the anterior alveolus in Sts 5.If this location (Fig. 10B) represents the likely location of pros-thion in Sts 71, then we predict that the profile of Sts 5 prior toreorientation of the anterior dentition would have been strikinglysimilar to Sts 71.

The resolution of the apparent prognathism of Sts 5 mitigatesmuch of the conflict over the taxonomy of A. africanus. If Sts 5 is afemale with highly worn teeth, then the alveolar bulge can bediscounted and the variation in the sample can be attributed tosexual dimorphism or normal population variation. As noted byLockwood (1999) and Lockwood and Tobias (1999, 2002), whenmetric variation is used as the standard, sexual dimorphism in thisspecies is less than that found in gorillas, and not unexpected giveninterpretations of early hominin sexual dimorphism.

Conclusion

Continuous remodeling of the roots of the anterior dentition(and likely overall, see Dean et al., 1992) appears to be the norm ingreat apes (including humans). The length of the roots of centralincisors corresponds to the incisor inclination angle, and bothchange as individuals wear down the dentition over time. Basedon these results, it appears that Sts 5 was highly unlikely to be ajuvenile specimen, which supports the assignation of this spec-imen as female, based on size. This remodeling phenomenon alsoappears to account for much of the variation in the nasoalveolarcontour, at least within species, and may partially account for theunusual alveolar bulge that has been documented in thisindividual.

Resolving the interpretations of unusual prognathism presentedby Sts 5 eliminates a significant paradox in the taxonomic debatesover A. africanus. The prognathism of this specimen stands out asthe greatest apparent source of conflict in determining whetherother specimens in the Sterkfontein Member 4 assemblage shouldbe included in A. africanus, since other anatomical features, bothmetric and non-metric, can be explained by reference to normalpatterns of variation seen in great apes. If Sts 5 is simply anextremely senescent female with an unusual pattern of alveolarmorphology resulting from heavy dental wear, then the status ofA. africanus as a single species is confirmed.



Acknowledgments

We thank Stephany Potze and the Ditsong Natural HistoryMuseum, Matt Tocheri and the Smithsonian Museum of NaturalHistory, and Dan Leiberman and the Peabody Museum for use oftheir of CT data; and Fred Spoor, Jean-Jacques Hublin, Emma Mbuaand the Department of Earth Sciences, National Museums of Kenya,for access to CT scans and facilities for analysis. Additional thanksare extended to Christopher Dean for use of images and for assis-tance and thoughtful advice during the development of this project.Funding for CT scanning of hominin fossils was provided by theUniversity of Sheffield and University of Roehampton. The authorswish to thank Sarah Elton, the Associate Editor, and two anony-mous reviewers for their prompt review and very helpful com-ments on this manuscript.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jhevol.2013.09.007.

References

Anemone, R.L., Watts, E.S., Swindler, D.R., 1991. Dental development of known-agechimpanzees, Pan troglodytes (Primates, Pongidae). Am. J. Phys. Anthropol. 86,229e241.

Broom, R., 1947. Discovery of a new skull of the South African ape-man, Plesian-thropus. Nature 159, 672.

Broom, R., Robinson, J.T., 1950. Man contemporaneous with the Swartkrans ape-man. Am. J. Phys. Anthropol. 8, 151e155.

Clarke, R.J., 1988. A new Australopithecus cranium from Sterkfontein and its bearingon the ancestry of Paranthropus. In: Grine, F.E. (Ed.), Evolutionary History of the‘Robust’ Australopithecines. Aldine de Gruyter, New York, pp. 175e192.

Clarke, R.J., 1994. Advances in understanding the craniofacial anatomy of SouthAfrican early hominids. In: Corruccini, R.S., Ciochon, R.L. (Eds.), Integrative Pathsto the Past. Paleoanthropological Advances in Honor of F. Clark Howell. PrenticeHall, Englewood Cliffs, pp. 205e222.

Clarke, R.J., 2008. Latest information on Sterkfontein’s Australopithecus skeleton anda new look at Australopithecus. S. Afr. J. Sci. 104, 443e449.

d’Incau, E., Couture, C., Maureille, B., 2012. Human tooth wear in the past and thepresent: Tribological mechanisms, scoring systems, dental and skeletal com-pensations. Arch. Oral Biol. 573, 214e229.

Dastmalchi, R., Polson, A., Bouwsma, O., Proskin, H., 1990. Cementum thickness andmesial drift. J. Clin. Periodontol. 17, 709e713.

Dean, M.C., Jones, M.E., Pilley, J.R., 1992. The natural history of tooth wear, contin-uous eruption and periodontal disease in wild shot great apes. J. Hum. Evol. 22,23e39.

Diekwisch, T., 2001. Developmental biology of cementum. Int. J. Dev. Biol. 45, 695e706.

Gonçalves, P., 2005. Dental cementum reviewed: development, structure, compo-sition, regeneration, and potential complications. Braz. J. Oral Sci. 4, 651e658.

Grine, F., Weber, G., Plavcan, J.M., Benazzi, S., 2012. Sex at Sterkfontein: ‘Mrs. Ples’ isstill an adult female. J. Hum. Evol. 62, 593e604.


Kaifu, Y., 2000. Tooth wear and compensatory modification of the anterior den-toalveolar complex in humans. Am. J. Phys. Anthropol. 111, 369e392.

Kaifu, Y., Kasai, K., Townsend, G.C., Richards, L.C., 2003. Tooth wear and the ‘design’of human dentition: a perspective from evolutionary medicine. Yrb. Phys.Anthropol. 46, 47e61.

Kimbel, W.H., White, T.D., 1988. Variation, sexual dimorphism and the taxonomy ofaustralopithecines. In: Grine, F.E. (Ed.), Evolutionary History of the ‘Robust’Australopithecines. Aldine de Gruyter, New York, pp. 175e192.

Kimbel, W.H., White, T.D., Johanson, D., 1984. Cranial morphology of Austral-opithecus afarensis: a comparative study based on a composite reconstruction ofthe adult skull. Am. J. Phys. Anthropol. 64, 337e388.

Kimbel, W.H., Rak, Y., Johanson, D., 2004. The Skull of Australopithecus afarensis.Oxford University Press, Oxford.

Kraw, A.G., Enlow, D.H., 1967. Continuous attachment of the periodontal membrane.Am. J. Anat. 120, 133e148.

Kuykendall, K.L., 2003. Reconstructing australopithecine growth and development:What do we think we know? In: Thompson, J.L., Krovitz, G.E., Nelson, A.J. (Eds.),Patterns of Growth and Development in the Genus Homo. Cambridge UniversityPress, Cambridge, pp. 191e218.

Lockwood, C., 1997. Variation in the face of Australopithecus africanus and otherAfrican hominoids. Ph.D. Dissertation, University of Witwatersrand.

Lockwood, C., 1999. Sexual dimorphism in the face of Australopithecus africanus. Am.J. Phys. Anthropol. 1081, 97e127.

Lockwood, C., Tobias, P., 1999. A large male hominin cranium from Sterkfontein,South Africa, and the status of Australopithecus africanus. J. Hum. Evol. 36, 637e685.

Lockwood, C., Tobias, P., 2002. Morphology and affinities of new hominin cranialremains from Member 4 of the Sterkfontein Formation, Gauteng Province,South Africa. J. Hum. Evol. 42, 389e450.

Margvelashvili, A., Ponce de León, M., Zollikofer, C., 2011. Dentoalveolar remodelingin hominoids. Am. J. Phys. Anthropol. S144, 206.

Pitaru, S., McCullough, C.A., Narayanan, S.A., 1994. Cellular origins and differentialcontrol mechanism during periodontal developmental and wound healing.J. Periodont. Res. 29, 81e94.

Potze, S., Thackeray, J.F., 2010. Temporal lines and open sutures revealed on cranialbone adhering to matrix associated with Sts 5 ‘Mrs Ples’, Sterkfontein, SouthAfrica. J. Hum. Evol. 58, 533e535.

Rak, Y., 1983. The Australopithecine Face. Academic Press, New York.Rak, Y., 1985. Australopithecine taxonomy and phylogeny in light of facial

morphology. Am. J. Phys. Anthropol. 66, 281e287.Robinson, J., 1956. Dentition of Australopithecinae. Transvaal Museum Memoir No.

9. Transvaal Museum, Pretoria.Rodrigues, H.G., Marangoni, P., Sumbera, R., Tafforeau, P., Wendelen, W., Viriot, L.,

2011. Continuous dental replacement in a hyper-chisel tooth digging rodent.Proc. Natl. Acad. Sci. 108, 17355e17359.

Roux, D., Woda, A., 1994. Biometric analysis of tooth migration after approximalcontact removal in the rat. Arch. Oral Biol. 3912, 1023e1027.

Smith, B.H., 1991. Dental development and the evolution of life history in Homi-nidae. Am. J. Phys. Anthropol. 862, 157e174.

Thackeray, J.F., 1997. Cranial bone of ‘Mrs Ples’ Sts 5: Fragments adhering to matrix.S. Afr. J. Sci. 93, 169e170.

Thackeray, J.F., 2000. ‘Mrs Ples’ from Sterkfontein: Small male or large female?S. Afr. Archaeol. Bull. 55, 155e158.

Thackeray, J.F., Braga, J., Treil, J., Niksch, N., Labuschagne, J.H., 2002. ‘Mrs Ples’ (Sts 5)from Sterkfontein: an adolescent male? S. Afr. J. Sci. 98, 21e22.

Tobias, P., 1967. Olduvai Gorge, vol. 2. Cambridge University Press, Cambridge.Wise, G.E., King, G.J., 2008. Mechanisms of tooth eruption and orthodontic tooth

movement. J. Dent. Res. 875, 414e434.




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