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Keywords:

  • Chad;
  • early hominins;
  • dental roots;
  • root morphology;
  • teeth evolution

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED

The evolution of the teeth in hominins is characterized by, among other characters, major changes in root morphology. However, little is known of the evolution from a plesiomorphic, ape-like root morphology to the crown hominin morphology. Here we present a study of the root morphology of the Miocene Chadian hominin Sahelanthropus tchadensis and its comparison to other hominins. The morphology of the whole lower dentition (I1–M3) was investigated and described. The comparison with the species Ardipithecus kaddaba and Ardipithecus ramidus indicates a global homogeneity of root morphology in early hominins. This morphology, characterized notably by a reduction of the size and number of the roots of premolars, is a composite between an ape-like morphology and the later hominin morphology. Trends for root evolution in hominins are proposed, including the transition from a basal hominoid to extant Homo sapiens. This study also illustrates the low association between the evolution of tooth root morphology and the evolution of crowns in hominins. Am J Phys Anthropol 153:116–123, 2014. © 2013 Wiley Periodicals, Inc.

The discoveries of Miocene and early Pliocene hominoids in Ethiopia (White et al., 1995; Haile-Selassie et al., 2004), Kenya (Senut et al., 2001) and Chad (Brunet et al., 2002, 2005) substantially changed our vision of human evolution and unveiled an unexpectedly complex part of hominoid history. The new genera, namely Orrorin, Ardipithecus and Sahelanthropus, share some plesiomorphic characters with apes and derived characters with hominins; they could be morphologically closer to the common ancestor of humans and chimpanzees than the geologically younger genera Australopithecus, Paranthropus and Homo (e.g., White et al., 1995; Senut et al., 2001; Brunet et al., 2002; Cela-Conde et al., 2003; Haile-Selassie et al., 2004; Guy et al., 2005; Zollikofer et al., 2005). On the basis of their peculiar morphology, they offer an unparalleled opportunity to explore the morphological transition from stem hominoids to hominins.

The morphological evolution of the teeth in hominins has been characterized by, among other features, the reduction of the anterior teeth, the molarization of the premolars, and the diminution of the occurrence of M3. For the subocclusal anatomy, trends in morphological evolution have been observed in Australopithecus, Paranthropus and Homo genera (e.g., Wood et al., 1988); they involve reduction of the root number and volume, changes in the curvature of the roots of the molars in Homo, and molarization of the roots of premolars in robust australopithecins (e.g., Wood et al., 1988). The number of roots and pulp canals is variable among hominoids, even among a single species (as observed in Homo erectus: Wood et al., 1988; in Homo sapiens: Lipski et al., 2005; Shields, 2005; in Pongo pygmaeus, Gorilla gorilla and Pan troglodytes: Emonet et al., 2012; Moore et al., 2013); however, links between the number and morphology of roots and the phylogeny have been successfully proposed in hominins (Wood et al., 1988).

Among modern hominoids, the genera Pan and Gorilla display very similar dental root morphologies (Emonet et al., 2012), despite their size differences. Specimens of both genera commonly exhibit two-rooted P3 with three pulp canals and three-rooted P4, M1, and M2 with four pulp canals (see Table 1 and Emonet et al., 2012). The roots of their premolars are bucco-lingually wide and diverge toward the apex; the roots of their molars are straight (Emonet et al., 2012). This “African apes” morphology is clearly distinct from the morphology of modern and fossil hominins (these species exhibit one-rooted premolars, two-rooted molars, bucco-lingually narrow roots of premolars and curved roots of molars: see Table 2, Wood et al., 1988; Shields, 2005), but shares more characters with other hominoids such as Hylobates, Pongo (Emonet et al., 2012), Khoratpithecus (Chaimanee et al., 2006) and the primitive hominoid Proconsul (MacLatchy et al., 2005). These observations are summarized in Table 2.

Table 1. Incidence of mandibular root and canal number by taxonomic categories in African apes and hominins
Number of roots1234Source
Number of pulp canals123434545
  1. a

    Australopithecus and Paranthropus (16), with the exclusion of A. bahrelghazali.

  2. b

    Number unknown, but all specimens display two roots and four canals (Shields, 2005).

P3          
 Gorilla 212 5    This study
 Pan6611 4    This study
Australopithecinsa  75     (Wood et al., 1988)
 Homo erectus2        (Wood et al., 1988)
 Homo habilis/ergaster441      (Wood et al., 1988)
 Homo sapiens4897321 1    (Shields, 2005)
 TM266-02-154-1  1      This study
 TM292-02-01  1      This study
P4          
 Gorilla  110 422 This study
 Pan  519 3   This study
Australopithecinsa   15     (Wood et al., 1988)
 Homo erectus2        (Wood et al., 1988)
 Homo habilis/ergaster7  2     (Wood et al., 1988)
 Homo sapiens53614 103    (Shields, 2005)
 TM266-02-154-1   1     This study
 TM292-02-01   1     This study
M1          
 Gorilla     17  2This study
 Pan     27   This study
 Homo sapiens   nb     (Shields, 2005)
 TM266-02-154-1     1   This study
 TM292-02-01     1   This study
M2          
 Gorilla   4213   This study
 Pan   7 19 1 This study
 Homo sapiens112  1299     (Shields, 2005)
 TM266-02-154-1     1   This study
 TM292-02-01     1   This study
Table 2. Morphology of dental roots of Proconsul and extant hominoid genera, after MacLatchy et al. (2005); Shields (2005); Emonet et al. (2012); and data from this study
 Proconsul, PongoHylobatesGorilla, PanModern HomoSahelanthropus
Roots of incisorsThin and shallow, elongated sectionBroad and deep, elongated sectionBroad and deep, elongated sectionBroad and deep, rounder sectionBroad and deep, rounder section
Root of canineRobust, strongly curvedRobust, strongly curvedRobust, strongly curvedGracile, slightly curvedRobust, slightly curved
Most common P3 number of roots/pulp canals2/31/12/31/12/3
Most common P4 number of roots/pulp canals2/42/42/41/12/4
Most common M1–2 number of roots/pulp canals3/42/43/42/43/4
Roots of premolarsBucco-lingually wideBucco-lingually wideBucco-lingually wide,Bucco-lingually narrow, only one rootBucco-lingually narrow, several roots
Separation of roots of premolarsStrong separation, divergence towards the apexStrong separation, divergence towards the apexStrong separation, divergence towards the apexOften one single root, when two roots they keep in contact and do not diverge towards the apex.Roots keep in contact and do not diverge towards the apex
Roots of molarCurvedCurvedStraightCurvedCurved

However, the transition from a stem hominoid morphology to a hominin morphology is as yet unknown. The association or the absence of association between the morphological evolution of roots and that of crowns in hominins is also unknown. These issues are important to understand the global factors, whether genetic or epigenetic, that induced the emergence of the hominin dental and cranial morphology.

Here we report a study of the dental root morphology of Sahelanthropus tchadensis. Using previously published data (Suwa et al., 2009), we compared this morphology with that of the species Ardipithecus ramidus and Ardipithecus kaddaba. This comparison was extended to modern African apes and other fossil and modern hominins, leading to a global morphological study of the evolution of the roots in hominins. The results allow conclusions on the possible association of the evolution of roots and that of crowns.

MATERIAL AND METHODS

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED

TM266-02-154-1 is a right mandible preserving P4-M3. It was discovered at Toros-Menalla site TM266 in northern Chad (Brunet et al., 2002). TM292-02-01 is a partial mandible discovered in Toros-Menalla site TM292, in northern Chad (Brunet et al., 2005). In TM292-02-01 the roots of the whole dental row are preserved. The two specimens were found in the same geological unit, and their age was estimated between 6.8 and 7.2 Ma (Lebatard et al., 2008).

The two Sahelanthropus mandibles TM266-02-154-1 and TM292-02-01 were imaged using computerized microtomography with an industrial scanner (tube current 0.12 mA; tube voltage 130 kvp; voxel size 130 µm). Because of the lack of absorption contrast between fossilized dentine and bone, the roots were segmented manually from the mandible and visualized using VGStudioMax 1.2.1 (©Volume Graphics, Heidelberg, Germany). A comparative sample composed of 16 Gorilla gorilla skulls (5 males and 11 females) and 21 Pan troglodytes and P. paniscus skulls (6 males and 15 females) was also imaged using computerized microtomography (using a Philips Mx8000 medical scanner). The voxel size of the extant ape data ranges from 390 to 600 µm.

The visualization of the roots was performed using VGStudioMax 1.2.1, and led to description of the radicular morphology based notably on the robusticity, relative length and width, cross-section, orientation. and the number of the roots. In this study, roots were considered to be separate if both of them displayed a distinct apex and there was no dentine–dentine contact between them for more than one third of the length between the apex and the external enamel–dentine junction.

RESULTS

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED

Description of dental roots of Sahelanthropus tchadensis

The root morphology of the mandibles TM266-02-154-1 and TM292-02-01 are displayed in Figures 1 and 2, respectively. Measurements of maximal root length are presented in Table 3.

image

Figure 1. Radicular morphology of Sahelanthropus tchadensis TM266-02-154-1. (A) Lingual view, (B) buccal view, (C) Occlusal view, (D) ventral view. The arrow points to a small secondary root growth.

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image

Figure 2. Radicular morphology of Sahelanthropus tchadensis TM292-02-01. (A) Occlusal view, (B) ventral view, (C) buccal view of left side, (D) lingual view of left side, (E) lingual view of right side, (F) lingual view of right side.

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Table 3. Maximal root length of Sahelanthropus tchadensis specimens
 TM266-02-154-1TM292-02-01 leftTM292-02-01 right
I1  >11.5 mm
I2 >14.0 mm>10.5 mm
C1 27.97 mm>24.0 mm
P318.11 mm>12.5 mm16.53 mm
P416.44 mm16.13 mm>11.5 mm
M119.75 mm20.87 mm20.16 mm
M218.82 mm>12.5 mm>14.5 mm
M314.71 mm  

Roots of incisors are only partially preserved in TM292-02-01. They are ventrally as deep as the roots of premolars and molars and mesio-distally broad. Their transversal section is rounder than that of African apes. Canine root on TM292-02-01 is robust, especially when compared to the reduced crown, ventrally deep but only slightly curved. Its transversal section is bucco-lingually compressed.

In both TM266-02-154-1 and TM292-02-01, P3 displays two roots: one mesial root with a single pulp canal, and a distal root with two pulp canals. This distal root is bucco-lingually narrow in comparison to two-canal roots of other hominoids, especially African apes (Table 4). The mesial root is more buccal than the distal one; this character is clearer in TM266-02-154-1 than in TM292-02-01. Roots of P3 are subparallel, although the distal root is slightly more curved apically than the mesial one in TM266-02-154-1.

Table 4. Ratio between maximum mesio-distal breadth and maximum bucco-lingual breadth of the distal root of P3
 SampleMean valueStandard deviation
Tomes' rootsTwo modern Homo sapiens; two Pan troglodytes; Australopithecus africanus STS52b0.8930.031
Comparative sample (roots with two canals)One modern Homo sapiens; five Gorilla gorilla; six Pan sp.0.5240.065
Sahelanthropus tchadensisTM266-02-154-1, TM292-02-01TM266: 0.591, TM292: 0.687 

P4 of both specimens display two rectilinear, vertical, subparallel, and robust roots. The bifurcation (the point where horizontal diaphragmatic processes converge, as defined by Kovacs, 1971) of the roots is very apical, and even after the bifurcation the roots are in contact along the two thirds of their length.

M1 and M2 in both specimens display three robust roots, two mesial ones and a distal root. The mesial roots are connected through a very thin blade (as defined by Kupczik, 2003) for half of their length. In TM266-02-154-1, the mesio-buccal root of M2 divides itself at half of its length, leading to the formation of a small secondary root in central position (Fig. 1). This rare configuration is observed in extant specimens [in our comparative sample, in a M1 of Pan troglodytes and a M2 of Gorilla gorilla; Kovacs (1971), also reports its appearance in modern Homo sapiens, Gorilla gorilla, and several Carnivora] and linked to the folding of the epithelial diaphragm during the penetrative phase of root development (Kovacs, 1971). Its single occurrence is likely to have an epigenetic origin (Kovacs, 1971; Kupczik, 2003). Mesial roots of M1 and M2 are slightly curved, mesio-distally thin and bucco-lingually narrow. Distal roots of M1 and M2 are very deep, rectilinear and bucco-lingually narrow. They display two pulp canals, which converge toward the apex. In TM266-02-154-1, the separation between the penetrative and eruptive phase (Kovacs, 1971) of the distal root of M1 is marked by a deep groove.

In TM266-02-154-1, the mesial roots of M3 are similar to those of M1. The distal root is a short, rectilinear, robust root with a triangular section. This morphology of the distal root of M3 is observed in all extant and fossil hominoid species (Emonet et al., 2012).

Comparison with other hominoids

A count of roots and pulp canals, collected from previous studies (Wood et al., 1988; Shields, 2005) and new data, is proposed in Table 1. TM266-02-154-1 and TM292-02-01 display the same number of roots and pulp canals for each tooth, which suggests that this morphology was at least not uncommon in Sahelanthropus tchadensis. The morphology of roots of premolars (two roots and three canals for P3, two roots and four canals for P4) corresponds to the most common morphology in Gorilla, Pan and Australopithecus (Wood et al., 1988; Table 1), which is also found, though uncommonly, in fossil and extant Homo species (Wood et al., 1988; Shields, 2005; Table 1). Ardipithecus ramidus and A. kaddaba display a slightly different morphology, with only one root in P4 (Suwa et al., 2009). In Sahelanthropus specimens, the morphology of roots of M1 and M2 (three roots and four canals) is also the most common morphology in African apes (Table 1) but not in modern Homo sapiens. In the latter species, the large majority of specimens display two roots and three or four canals (Shields, 2005).

The reduction of the size of the crown of C1 in Sahelanthropus tchadensis and Ardipithecus ramidus when compared to extant and fossil apes (Brunet et al., 2002, 2005; Suwa et al., 2009) is not reflected in the root morphology. The length of root of TM292-02-01 (Table 3) is comparable to that of Pan troglodytes (26.8–30.7 mm, Kupczik, 2008), much larger than the length of modern Homo sapiens (13.2–19.2 mm, Kupczik et al., 2008; Le Cabec et al., 2012) or Homo neanderthalensis (17.2–25.6 mm, Le Cabec et al., 2012). The roots of C1 are robust and ventrally deep in Sahelanthropus tchadensis and Ardipithecus ramidus, even more so in S. tchadensis than in A. ramidus (Suwa et al., 2009). This morphology for early hominins is much like that of Pan or Gorilla, while the roots of C1 are thinner and ventrally shallower in australopithecins and Homo (Wood et al., 1988; Kupczik, 2003; Shields, 2005).

The morphology of P3 roots in Sahelanthropus, including the buccal position of the mesial root and the bucco-lingual compression of the distal root, differs from the morphologies observed in African apes. This peculiar morphology is also commonly reported in australopithecins (Wood et al., 1988). The distal root has two pulp canals, but its bucco-lingual breadth is low for a two-canals root (especially in TM292-02-01, Table 4), closer to the values observed in Tomes' roots than other distal roots with two canals (Table 4). Tomes' roots are frequent in early Homo (Wood et al., 1988) and observed also in extant humans (Shields, 2005). The morphology observed in Sahelanthropus could thus represent in a morphological series an intermediary state between African ape morphology and the hominin morphology.

The morphology of P4 of TM266-02-154-1 and TM292-02-01 also differs from that of African apes. The ventrally deep, very straight roots are in contact for at least the two thirds of their length (TM266-02-154-1) up to the three quarters (TM292-02-01); only the most apical parts of the roots are clearly separated. As a result, the transversal section of the root appears like a rounded square (Figs. 1 and 2). This rare morphology is not reported in African apes, but is sometimes observed in Australopithecus (e.g., KNM-ER 3734, 1483, 1501; OH16, 23, 37; Wood et al., 1998). Like for P3, the morphology of roots of P4 in Sahelanthropus evokes that of later hominins, notably Tomes' root (Ardipithecus kaddaba, Australopithecus) and single-rooted P4 (Ardipithecus ramidus, Australopithecus, Homo), and could be interpreted in a morphological series as an intermediary state between African apes and human morphologies.

The roots of M1 and M2 are rectilinear in African apes, while they are curved in humans, concave to the distal (respectively mesial) side for the mesial (distal) roots. The roots of molars of Sahelanthropus are curved like those of humans, even if the distal root of the first molar is only slightly curved (Figs. 1 and 2). They are also absolutely longer (Table 3) than those of Homo sapiens (14.6–15.3 mm for M1, 14.7–15.8 mm for M2, Kupczik et al., 2008, 2010) and Pan troglodytes (12.1–15.4 mm for M1, 11.1–14.3 mm for M2, Kupczik et al., 2008).

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED

Dental root morphology and phylogenetic position of Sahelanthropus tchadensis

The morphology of dental roots of Sahelanthropus is a composite of African ape-like characters, such as the robustness of root of C1 and the three-rooted P3, Australopithecus-like or Homo-like characters, like the section of roots of incisors and the curvature of roots of molars, and intermediary characters between ape-like and human-like morphologies, notably the disposition of premolar roots (Table 2). The characters shared with African apes and not Homo (the robust root of canine, premolars with two roots, molars with three roots), and some characters shared with modern Homo but not African apes (curved roots of molars), are also shared with Pongo and the primitive hominoid Proconsul (MacLatchy et al., 2005); it is therefore more parsimonious to consider them as primitive characters. On the other hand, some characters shared with Australopithecus or Homo, and characters intermediary between African apes and hominins, are not shared with Pongo and Proconsul. They should be considered as derived characters, whose primitive state is found in pongids and Proconsul. When only considering the root morphology, Sahelanthropus shares only plesiomorphies with Pan and Gorilla, while it displays some apomorphies of hominins (Table 2); it is therefore more parsimonious to consider Sahelanthropus as a basal hominin. This result is congruent with previous conclusions from other studies (Brunet et al., 2002, 2005; Guy et al., 2005; Zollikofer et al., 2005).

With the exception of the P4, the root morphology of Sahelanthropus is shared with both species of Ardipithecus, suggesting the existence of an “early hominin” morphology evolutive grade for dental roots.

Evolution of the dental root morphology in hominins

In the African apes-hominins clade, four morphologies can be distinguished for dental roots. Figure 3 illustrates general trends of these morphologies in cross-section. The “African apes” morphology is characterized by incisor roots with an elongated cross-section; a large, ventrally deep root of canine; P3 with either three roots, the distal roots being clearly separated one from another, or uncommonly one-rooted P3 in chimpanzees; two clearly separated roots in P4 with two pulp canals each and two deep and straight roots in M1 and M2. With the exception of the straight roots of molars, this morphology is shared with hominoids excluded from the African apes and Homo clade such as Pongo, Khoratpithecus (Chaimanee et al., 2006) and the primitive hominoid Proconsul (MacLatchy et al., 2005). It is therefore parsimonious to consider this morphology as primitive for hominins.

image

Figure 3. Proposed evolutionary trends in roots of I1–P4 in fossil hominoids. Outlines are cross-section of roots at midlength.

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The “early hominin” morphology is observed in Sahelanthropus and Ardipithecus but also in Australopithecus specimens from Hadar (Ward et al., 1982), Laetoli (White, 1977) and Koobi Fora (Wood et al., 1988). It differs from the “African apes” morphology by the rounder cross-section of the root of incisors; the bucco-lingual reduction and the lingual position of the distal roots of P3; the reduction of the roots of P4, which could be observed as a partial junction of the roots (S. tchadensis, A. afarensis), the Tomes' roots morphology (A. kaddaba) or even a single-rooted P4 (A. ramidus); and the curvature of the roots of molars. Among this “early hominin” morphology, at least some of the australopithecin specimens (e.g., KNM-KP29281; KT-12/H1) display a gracile, short root of C1, which distinguishes them from Miocene hominins.

The “robust Australopithecins” morphology is characterized by a “molarization” of roots of premolars (Wood et al., 1988), and is observed mainly in some Australopithecus and Paranthropus specimens (e.g., specimens from Koobi Fora KNM-ER 403, 404, 725, 729, and 733; specimen from Peninj; Wood et al., 1988). This “molarization” leads to premolars with two asymmetrical roots, with the mesial root larger at buccal side and distal root larger at lingual side; the bucco-lingual widening of roots, especially the mesial root of P3; and the development of large pulp canals, sometimes leading to a single canal per root.

Finally, the “human” morphology of roots, which includes the genus Homo, is characterized by a very reduced and straight root of canine, the large predominance of single-rooted premolars (Wood et al., 1988; Shields, 2005), and molars with two curved, apically converging roots.

Relationship between root and crown evolution

Roots of the C1 in early hominin genera Sahelanthropus and Ardipithecus are deep, large and robust, like that of African apes. However, the crowns of these teeth are reduced in early hominins in comparison with African apes, even in male specimens (White et al., 1995; Brunet et al., 2002, 2005; Suwa et al., 2009). This observation suggests that the reduction of the crown of C1 was anterior to that of the root and illustrates the mosaic evolution of the morphology of the C1. This unsynchronized evolution of crowns and roots in the same tooth position suggests that the morphology of the C1 crown and that of the root are not tightly associated. As proposed previously (e.g., Shimizu, 1999; Kupczik et al., 2005), the determinative factors are likely to include at least some genetic factors. The observed unsynchronized evolution therefore strongly suggests that changes in some of the genes coding for the shape of the crown did not result in change of the morphology of the roots of canine; this observation may mean that these genes do not code for the shape of the root. This hypothesis has already been proposed in other mammals (e.g., Shimizu 1995) and is supported by results on the molecular control of differentiation of odontoblasts and cementoblasts (Tummers et al., 2003; Huang et al., 2012).

CONCLUSION

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED

The root morphologies of Sahelanthropus tchadensis, Ardipithecus ramidus and Ardipithecus kaddaba are largely similar and lead to the definition of an “early hominin” root morphology. In this group, Ardipithecus species display a slightly more derived P4 than S. tchadensis. This “early hominin” morphology is a composite of primitive ape-like characters and derived Australopithecus- and/or Homo-like characters, and confirms previous observations and analyses about the general morphology of Sahelanthropus and Ardipithecus. It also unveils a new chapter of dental evolution of hominin: the transition from an ape-like root morphology to an Australopithecus- and Homo-like one. Finally, the plesiomorphic morphology of the root of C1, contrasting with the synapomorphic reduction of the tooth's crown, suggests decoupled evolution of crown and root in hominins.

These results, enlightening the composite dental morphology of Sahelanthropus, raise several questions on the evolution of hominins, the answers to which require additional data. First, the dental root morphology of other hominins, including Orrorin and early Homo, should be precisely described, quantified and compared to that of Sahelanthropus, Ardipithecus and Australopithecus. Second, additional fossil hominins from different parts of Africa, both from Late Miocene and Pliocene, are needed to allow an overview of dental root diversity in hominins. Third, the morphological association of the roots with the crown should be precisely described and quantified, in fossil and extant species. Finally, a better understanding of heritability and environmental determinism of dental root morphology is required in terms of phylogeny and evolution.

ACKNOWLEDGMENTS

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED

The authors thank all the members of the Mission Paléoanthropologique Franco-Tchadienne, including all our friends and colleagues who participated in acquisition of the field data. They also thank G. Florent and C. Noël for their administrative guidance and X. Valentin for his technical support.

LITERATURE CITED

  1. Top of page
  2. ABSTRACT
  3. MATERIAL AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSION
  7. ACKNOWLEDGMENTS
  8. LITERATURE CITED
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