Brief communication High-resolution assessment of the dental developmental pattern and characterization of tooth tissue proportions in the late Upper Paleolithic child from La Madeleine France.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 138:493–498 (2009) Brief Communication: High-Resolution Assessment of the Dental Developmental Pattern and Characterization of Tooth Tissue Proportions in the Late Upper Paleolithic Child From La Madeleine, France Priscilla Bayle,1,2* José Braga,1 Arnaud Mazurier,3 and Roberto Macchiarelli2,4 1 Centre d’Anthropobiologie et Imagerie Anatomique, FRE 2960 CNRS, Université Paul Sabatier, Toulouse, France Département de Préhistoire, UMR 5198-USM 204, MNHN Paris, France 3 Etudes Recherches Matériaux, Poitiers, France 4 Département Géosciences, Université de Poitiers, Poitiers, France 2 KEY WORDS dental mineralization; tissue proportions; lower deciduous dentition; late Upper Paleolithic; microtomography ABSTRACT Afﬁnities and differences in dental maturational patterns between modern humans and Neanderthals remain a matter of discussion. In particular, deciduous teeth are rare for Late Pleistocene humans, and few entire sequences have been detailed for their developmental status. Here, we report the results from the 3D virtual reconstruction and structural analysis of the deciduous lower dentition (nine teeth in situ) of the child from La Madeleine (LM4), France, the ﬁrst Upper Paleolithic specimen detailed so far by means of high-resolution microtomography (lCT). With respect to the modern dental developmental standards, age at death of this individual is now more likely estimated within the interval 3–4 years. LM4 lacks the slight discrepancy between a proportionally advanced stage of mineralization of the deciduous ﬁrst molar and a relatively delayed maturational level of the incisors, which is found in Neanderthals (Bayle et al.: J Hum Evol 56  66–75). By using a Bayesian approach, we calculated the probability that its maturational sequence is found within the extant human variation as represented by a tomographic (CT) reference sample of 45 children scored according to the same protocol (Liversidge and Molleson: Am J Phys Anthropol 123  172–180). Results show that the speciﬁc sequence of this Magdalenian individual is found three times in the comparative sample included in this study. LM4 absolute tooth size and relative dental tissue proportions are close to the modern human ﬁgures (characterized by proportionally reduced dentine volumes) and lie systematically below the values shown by the Neanderthal child from Roc de Marsal, France (OIS 5a). Am J Phys Anthropol 138:493–498, 2009. V2009 Wiley-Liss, Inc. In his extensive radiographic study of dental developmental patterns in Upper Pleistocene and Holocene populations, Tompkins (1996a) recorded a high level of similarity in relative maturation of the permanent teeth between Neanderthals (OIS 5e-3) and Upper Paleolithic humans (34-11 kya BP) from Europe and Middle East. The author (Tompkins, 1996a,b) also noted that only some minor differences characterize both fossil groups with respect to the extant human condition. Notably, Neanderthals and anatomically modern fossil humans share a relative delay in mineralization of the incisors and the third premolar associated with a general advancement of the molars, particularly of the M3. Recent high-resolution analysis of the immature specimen from Roc de Marsal, France (OIS 5a; Bayle et al., 2009) shows that a relative developmental delay of the incisors and a relative advancement of the ﬁrst molars also characterize the deciduous lower Neanderthal dentition. Deciduous teeth are rare for late Pleistocene humans (Hillson and Trinkaus, 2002: 356) and few entire sequences of the primary dentition have been qualitatively and quantitatively assessed so far for their developmental status (Legoux, 1966; Tompkins, 1991; Henry-Gambier, 2001; Hillson, 2002; Hillson and Santos Coelho, 2002). By means of high-resolution microtomography (lCT), here, we detail the maturational condition of the mandibular deciduous dentition of the late Upper Paleolithic child from La Madeleine, France, and calculate the Bayesian probabilities that its dental mineralization sequence is found within extant human variation represented by the comparative deciduous sample included in this study. Based on recent evidence about the inﬂuence of variations in tooth tissue proportions on dental developmental patterning (Smith et al., 2007a; Bayle et al., C 2009 V WILEY-LISS, INC. C Grant sponsor: EU FP6 Marie Curie Actions (EVAN); Grant number: MRTN-CT-2005-019564; Grant sponsor: GDR (CNRS Projects); Grant number: 2152; Grant sponsor: TNT. *Correspondence to: Priscilla Bayle, Centre d’Anthropobiologie et Imagerie Anatomique, Université Paul Sabatier, 37 allées Jules Guesde, F-31000 Toulouse, France. E-mail: email@example.com Received 3 September 2008; accepted 21 November 2008 DOI 10.1002/ajpa.21000 Published online 23 January 2009 in Wiley InterScience (www.interscience.wiley.com). 494 P. BAYLE ET AL. 2009; Olejniczak et al., 2008), we also quantiﬁed and compared enamel, dentine, and pulp proportions of each tooth. MATERIALS AND METHODS The skeleton of the La Madeleine child (LM4) was discovered in 1926 in Tursac, Dordogne, in a ﬁnal Magdalenian ochred burial rich of goods and personal ornaments (Capitan and Peyrony, 1928; VanHaeren and d’Errico, 2001). A recent radiocarbon analysis (14C AMS) of the burial provided an age of 10,190 6 100 years BP (Gambier et al., 2000). Skeletal and dental age at death estimates suggest the interval of 2–4 years for this late Upper Paleolithic child (Heim, 1991; Gambier et al., 2000). Although the LM4 mixed lower dentition also consists of eight isolated permanent elements, its restored mandible currently bears in situ only nine deciduous teeth, the right canine being the only missing tooth (Heim, 1991). In 2007, the LM4 mandible has been detailed by means of high-resolution lCT at the Centre de Microtomographie of the University of Poitiers (equipment X8050-16 Viscom AG; camera 1004 3 1004). Scans were made according to the following parameters: 95 kV, 395 lA current, 32 integrations/projection, and 1,800 projections (each 0.28). The ﬁnal volume was reconstructed in 984 3 984 format with an isotropic voxel size of 50.9 lm3 using the software DigiCT v.1.15 (DIGISENS). A semiautomatic segmentation with manual corrections was carried out by means of AMIRA v.4.1.2 (Mercury Computer Systems) and Artecore v.1.0 (NESPOS Society). Threshold values between segmented components have been found according to the methodology developed by Spoor et al. (1993). For individual measurements, crowns were digitally isolated from roots following Olejniczak et al. (2008), and surface rendering was performed using triangulation and constrained smoothing from the volumetric data (marching cube algorithm; Lorensen and Cline, 1987). Assessment of the deciduous developmental pattern, which is based on the 3D independent evaluation of each virtually extracted element, follows a scoring system adapted from Liversidge and Molleson (2004; for details, see Bayle et al., 2009). The sequence of this Magdalenian individual (ﬁrst scored by P.B. and A.M. and thus independently validated by J.B. and R.M.) has been compared to those assessed (by P.B. and one independent observer) following the same scoring method on a computed tomographic (CT) reference sample of 45 living individuals (29 males and 16 females), mainly of West European origins, aged 2–5 years and distributed as follows: 2–3 years 5 14 individuals; 3–4 5 19; 4–5 5 12 (record from Braga and Treil, 2007; Bayle et al., 2009; and original unpublished data). The statistical analysis of the dental mineralization sequence was realized by using the Bayesian approach developed by Braga and Heuzé (2007), already adopted to characterize the developmental status of the Roc de Marsal Neanderthal dentition (Bayle et al., 2009). Accordingly, the LM4 sequence can be represented by a rearrangement of its ﬁve elements (di1-dm2) into a ﬁnite number of combinations, each being composed of two subsets: the ﬁrst comprises between 1 and 4 dental elements sampled from the entire set, whereas the second comprises the remaining elements. In this case, 30 comAmerican Journal of Physical Anthropology binations are possible. The probability of observing each of the 30 combinations in the reference sample is calculated by using Bayes’s rule of conditional probability (Vieland, 1998; Aitken and Taroni, 2004), with teeth being considered as statistically dependent units and prior probabilities uniform. The following 12 linear, surface, and volumetric variables describing tooth tissue proportions were digitally measured: Vt is the total tooth volume (mm3); Ve, the volume of the enamel cap (mm3); Vd, the total volume of the dentine (mm3); Vp, the total volume of the pulp (mm3); Vcdp, the volume of the coronal dentine (including the coronal aspect of the pulp chamber) (mm3); Vcd, the volume of the coronal dentine (excluding the coronal aspect of the pulp chamber) (mm3); Vcp, the volume of the coronal pulp (mm3); Vc, the total volume of the crown (mm3); Vcdp/Vc, the percent of coronal volume that is dentine and pulp; Sedj, the surface area of the enamel-dentine junction (mm2); AET, the average enamel thickness (mm); and RET is the scale-free relative enamel thickness (for methodological details, see Kono, 2004; Macchiarelli et al., 2006; Olejniczak et al., 2008). Intra- and interobserver tests for accuracy of the measures were run by two observers (P.B and A.M.). As a whole, recorded differences are less than 5%, which is compatible with previous results on similar sets of 2–3D virtually assessed variables (e.g., Kono, 2004; Suwa and Kono, 2005; Olejniczak and Grine, 2006; Bayle et al., 2009). As the LM4s lower posterior dentition (as well as the only preserved left canine) is virtually free from wear, for the molars, the average values have been calculated for all the variables listed earlier. Conversely, because of some occlusal dentine patches appearing on the incisors, the highest value within each tooth pair has been retained in the quantitative analysis. To evaluate the inﬂuence of variation in tooth tissue proportions on maturational patterns of the primary dentition, LM4 has been compared with the Neanderthal child of Roc de Marsal (left and right average estimates; Bayle, 2008; Bayle et al., 2009) and to the average values from two modern individuals (MH) of European origin aged 2–4 years, whose unworn lower dentition has been detailed by means of the same analytical procedures (Bayle, 2008). RESULTS The virtually reconstructed deciduous lower dentition of the La Madeleine 4 (LM4) late Upper Paleolithic child is shown in Figure 1. Together with the preservation quality of the dental elements, it also reveals the interventions of restoration on the mandibular body, which has been reinforced anteriorly by means of a transversally placed metal bar (Heim, 1991). As recognized by Skinner (1996), the lower left canine presents a form of localized hypoplasia. Our virtual measurement of this spot, which is set on the midlabial aspect of the crown (see Fig. 1), ranges between 1.47 and 1.52 mm2. The individual assessment of the developmental stage of the nine deciduous teeth is shown in Table 1. Three incisors and the dm1s present a beginning of root resorption (stage r), the left di2 still displaying full apical closure (h2). Compared with the canine root (g), root length of both dm2s is complete, while apices are not closed (h1). DENTAL DEVELOPMENT IN THE LA MADELEINE CHILD TABLE 1. Individual assessment of the developmental stage of the nine deciduous teeth of the LM4 child mandible Left arcade Tooth di1 di2 dc dm1 dm2 Developmental stagea Root resorption initiated (r) Apical dentine edge is sharp and apex is only just visible (h2) Root length is almost complete, but apical edges are slightly converging (g) Root resorption initiated (r) Root length complete, with apical walls converging, but apex is still open (h1) Right arcade Developmental stagea Root resorption initiated (r) Root resorption initiated (r) Tooth di1 di2 – Root resorption initiated (r) Root length complete, with apical walls converging, but apex is still open (h1) dm1 dm2 a Adapted from Liversidge and Molleson (2004); see Bayle et al. (2009). With respect to the modern standards of age-related dental development published by Moorrees et al. (1963), Ubelaker (1989), and Liversidge and Molleson (2004), as well as to the reference sample of immature dentitions available in our ﬁles (see earlier), the most likely age at death interval estimated for this child is between 3 and 4 years. Within the modern comparative sample of 45 cases considered in this study, the maturational sequence displayed by LM4 (r-r-g-r-h1) is found three times, in two male and one female individuals, all aged 3.5 years. In the reference series, this pattern is the fourth more common among the 25 sequences represented. For the Bayesian analysis of the LM4 sequence (see Fig. 2), all theoretically possible probabilities associated to the formed combinations (n 5 30) have been calculated, the results being distributed as follows: 30% of probabilities are superior to 0.75 and 70% comprised between 0.25 and 0.75. Although the value of 0.75 does not represent an absolute cutoff in a continuous probability distribution ranging from 0 to 1, in such kind of analyses, probabilities greater than this formal threshold indicate very likely events, whereas lower values are more likely associated to random events (Braga and Heuzé, 2007). Comparative dental tissue proportions in LM4, Roc de Marsal (RdM; Bayle, 2008; Bayle et al., 2009), and modern humans (MH; Bayle, 2008) are shown in Table 2. Although in both fossil specimens the canines and the molars are virtually free from occlusal dental wear, on the Magdalenian child, and to a minor extent on Roc de Marsal, the central incisors show from minimal to extensive dentine patches (stage from 3 to 4 of the scoring diagram elaborated by Smith, 1984), and some minimal dentine patches also emerge on the lateral incisors (stage 2/3; Smith, 1984). For the total tooth volume (Vt), all values displayed by LM4 are close to the modern ﬁgures and lie below the Neanderthal condition as represented by Roc de Marsal, which systematically shows larger teeth, especially the 495 incisors. Even in terms of tooth position within the dental arcade, a similar pattern is shown also by the surface area of the enamel-dentine junction (Sedj). However, these differences are not homogeneously distributed among enamel, dentine, and pulp in terms of relative volumes. In facts, although the Neanderthal deciduous enamel is absolutely (AET) and relatively (RET) thinner than Magdalenian and modern enamel, the absolute volumes (Ve) are similar. Conversely, dentine and pulp volumes are signiﬁcantly larger in Roc de Marsal (for estimates on permanent Neanderthal molars, see Macchiarelli et al., 2008; Olejniczak et al., 2008). This clearly results from the percent of coronal volume that is dentine and pulp (Vcdp/Vc), the values ranging from 56 to 65% in the Moderns (LM4 and MH) and from 67 to 76% in the Neanderthal child. DISCUSSION AND CONCLUSIONS According to Tompkins (1996a), although dental developmental patterns have continued to slightly evolve through the Late Pleistocene to the present, both Neanderthals and fossil modern humans are hardly distinguishable from post-Pleistocene populations because of signiﬁcant variation in mineralization. Nonetheless, the high-resolution analysis of the mixed dentition of the Neanderthal child from Roc de Marsal (Bayle et al., 2009) showed that neither its deciduous nor its permanent mandibular sequences were precisely found within a modern reference sample made of 32 and 343 living children, respectively. In both cases, the most inﬂuential factor affecting the probabilistic analysis is represented by a slight discrepancy in Roc de Marsal between the stage of mineralization of the ﬁrst molar, which is proportionally advanced, and the maturational level reached by its incisors, which are proportionally delayed. Although such discrepancies between the Neanderthal child and a comparative sample of limited size and narrow geographic origin should not be interpreted as necessarily reﬂecting deep biological differences, it is noteworthy that the deciduous mineralization sequence displayed by the late Upper Paleolithic immature from La Madeleine (LM4) is found three times in a similar sample of 45 extant individuals, with a rank and a probability distribution suggesting that this pattern is relatively common, at least in Holocene Western European populations. Also, on radiographic ground, the probabilistic analysis of the deciduous mineralization sequence displayed by the penecontemporary immature specimen GE2 from Grimaldi, Italy (Henry-Gambier, 2001) ﬁts that of LM4 and, again, differs from the Neanderthal condition. The same is true also for the deciduous mineralization sequence displayed by the Middle Paleolithic anatomically modern child Qafzeh 13, Israël (Tillier, 1999), which ﬁts the extant human standards. Even if the canine of the Magdalenian specimen is affected by localized enamel hypoplasia and some occlusal wear is found on the incisors of both fossil children, present comparative estimates of relative tooth size, inner morphology, and volumetric dental tissue proportions point to a closer structural resemblance between LM4 and the modern human condition, which differs from the Neanderthal one (Mazurier and Macchiarelli, 2005; Macchiarelli et al., 2006, 2007, 2008; Smith et al., 2007a; Bayle, 2008; Bayle et al., 2009; Olejniczak et al., 2008). Accordingly, we suggest that some maturational characteristics of the deciduous and permanent NeanderAmerican Journal of Physical Anthropology Fig. 1. Microtomographic-based 3D virtual reconstruction (volume rendered in transparency) of the LM4 child mandible (in lateral oblique view) from the late Upper Paleolithic site of La Madeleine, France, bearing 10 deciduous teeth. Traces of restoration of the specimen are evident. Scale bar is 1 cm. Fig. 2. The maturational sequence of the LM4 deciduous lower dentition (ﬁve elements shown in the top row). Developmental stages (r-r-g-r-h1) adapted from Liversidge and Molleson (2004; details in Bayle et al., 2009). Distinctly for any of the 30 calculated combinations (i.e., 100% of theoretically possible), each cell shows the probability (p) that, given the maturational combination (or unit) below the line, the speciﬁc LM4 developmental subset shown above the line is found within a comparative reference sample of 45 modern humans (see Materials and Methods). The LM4 sequence is found three times within the comparative sample. 497 DENTAL DEVELOPMENT IN THE LA MADELEINE CHILD TABLE 2. Linear, surface, volumetric estimates and dental tissue proportions of the La Madeleine (LM4) lower deciduous teeth compared with those of the Neanderthal child of Roc de Marsal (Bayle, 2008; Bayle et al., 2009) and to the average values from two modern individuals (MH) showing a similar dental developmental stage (Bayle, 2008) di1 LM4 MH LM4/MH RdM LM4/RdM di2 LM4 MH LM4/MH RdM LM4/RdM dc LM4 MH LM4/MH RdM LM4/RdM dm1 LM4 MH LM4/MH RdM LM4/RdM dm2 LM4 MH LM4/MH RdM LM4/RdM Vt (mm3) Ve (mm3) Vd (mm3) Vp (mm3) Vcdp (mm3) Vcd (mm3) Vcp (mm3) Vc (mm3) Vcdp/ Vc (%) Sedj (mm2) AET (mm) RET 71.20a 62.43 1.14 125.35a 0.57 10.16a 10.37 0.98 12.72a 0.80 55.03 45.50 1.21 100.63 0.55 6.01 6.56 0.92 12.00 0.50 18.94 16.76 1.13 40.53 0.47 17.50 14.72 1.19 37.42 0.47 1.44 2.03 0.71 3.11 0.46 29.10a 27.13 1.07 53.25a 0.55 65a 62 1.05 76a 0.86 31.66 34.07 0.93 60.48 0.52 0.32a 0.30 1.05 0.21a 1.53 12.04a 11.90 1.01 6.12a 1.97 100.75a 95.84 1.05 159.01a 0.63 16.96a 15.87 1.07 18.49a 0.92 75.67 68.98 1.10 123.04 0.62 8.12 10.99 0.74 17.48 0.46 25.86 20.54 1.26 44.47 0.58 24.12 18.26 1.32 40.55 0.59 1.74 2.28 0.76 3.92 0.44 42.82a 36.41 1.18 62.96a 0.68 60a 56 1.07 71a 0.86 47.11 44.87 1.05 67.61 0.70 0.36a 0.35 1.02 0.27a 1.32 12.17a 12.92 0.94 7.72a 1.58 210.01 183.25 1.15 281.37 0.75 32.87 32.38 1.02 33.16 0.99 150.80 120.23 1.25 187.56 0.80 26.34 30.64 0.86 60.65 0.43 59.76 52.87 1.13 79.57 0.75 56.16 47.54 1.18 70.35 0.80 3.60 5.33 0.67 9.22 0.39 92.63 85.25 1.09 112.73 0.82 65 62 1.04 71 0.91 70.76 71.70 0.99 96.05 0.74 0.46 0.45 1.03 0.35 1.35 11.88 12.03 0.99 8.03 1.48 285.34 284.39 1.00 405.38 0.70 56.82 52.97 1.07 55.11 1.03 196.14 183.47 1.07 281.80 0.70 32.38 47.95 0.68 68.47 0.47 101.26 91.01 1.11 142.22 0.71 89.99 78.78 1.14 122.18 0.74 11.27 12.23 0.92 20.05 0.56 158.08 143.98 1.10 197.33 0.80 64 63 1.01 72 0.89 99.78 103.67 0.96 135.26 0.74 0.57 0.51 1.11 0.41 1.40 12.22 11.36 1.08 7.81 1.57 517.80 446.61 1.16 563.52 0.92 129.94 101.54 1.28 102.14 1.27 327.75 251.62 1.30 359.12 0.91 60.11 93.45 0.64 102.26 0.59 178.02 164.03 1.09 204.67 0.87 163.96 150.59 1.09 177.46 0.92 14.06 13.44 1.05 27.22 0.52 307.96 265.57 1.16 306.81 1.00 58 62 0.94 67 0.87 152.85 150.17 1.02 191.07 0.80 0.85 0.68 1.26 0.53 1.59 15.11 12.35 1.22 9.07 1.67 Vt, total tooth volume (mm3); Ve, volume of the enamel cap (mm3); Vd, total volume of the dentine (mm3); Vp, total volume of the pulp (mm3); Vcdp, volume of the coronal dentine (including the coronal aspect of the pulp chamber) (mm3); Vcd, volume of the coronal dentine (excluding the coronal aspect of the pulp chamber) (mm3); Vcp, volume of the coronal pulp (mm3); Vc, total volume of the crown (mm3); Vcdp/Vc, percent of coronal volume that is dentine and pulp; Sedj, surface area of the enamel-dentine junction (mm2); AET, average enamel thickness (mm); RET, scale-free relative enamel thickness. a Estimates affected by occlusal wear. thal dentition (Legoux, 1965, 1966; Wolpoff, 1979; Tillier, 1996; Tompkins, 1996a; Granat and Heim, 2003; Smith et al., 2007a; Bayle et al., 2009; but see Guatelli-Steinberg et al., 2005 for maturational similarities to some modern human groups) may result from the inﬂuence on dental developmental patterning of absolute and relative differences with respect to the modern human condition in tissue proportions between front and cheek teeth. The high-resolution microtomographic investigation and 3D characterization of immature human fossil specimens are bringing new critical evidence to the understanding of changes in timing and patterning of dental mineralization and eruption occurred through the Pleistocene (Macchiarelli et al., 2006, 2007; Smith et al., 2007a,b, in press; Bayle et al., 2009). Nonetheless, to assess the relationships between dental developmental patterns and tooth size endostructural variation in anatomically modern fossil humans and to precise the behavioral implications of changes in dental maturational patterns through the Late Pleistocene (Tompkins, 1996a), the subtle quantitative assessment of Upper Paleolithic dental sequences deserves greater attention in the future. ACKNOWLEDGMENTS The French Musée National de Préhistoire, Les Eyzies-de-Tayac, kindly granted access to the original fossil record (courtesy of J.-J. Cleyet-Merle). The UMR CNRS 5199 PACEA-LAPP (M. Bessou, B. Maureille, and P. Murail) provided comparative materials for high-resolution analyses. We acknowledge the ESRF beamline ID17, Grenoble (A. Bravin and C. Nemoz), the Centre de Microtomographie at the Univ. of Poitiers (P. Sardini), and the NESPOS Society (www.nespos.org) for technical collaboration. Thanks to the CHU Pellegrin, Bordeaux (V. Dousset, C. Douws, and C. Thibaut), and to the Hospital Necker, Paris, for access to their CT datasets (data anonymized and numbered exclusively storing the information of age and gender). Thanks to M. Coquerelle for collaboration on the CT record and to L. Bondioli for discussion. The present version was greatly improved by comments from the editor and two anonymous reviewers. The original lCT record of the La Madeleine mandible is available at the NESPOS website https:// www.nespos.org/display/openspace/Home. LITERATURE CITED Aitken C, Taroni F. 2004. Statistics and the evaluation of evidence for forensic scientists, 2nd ed. Chichester: Wiley. Bayle P. 2008. 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