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Molar Enamel Thickness and Distribution Patterns in Extant Great Apes and Humans: New Insights Based on a 3-Dimensional Whole Crown Perspective REIKO T

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Molar Enamel Thickness and Distribution Patterns in Extant Great Apes and Humans: New Insights Based on a 3-Dimensional Whole Crown Perspective REIKO T ANTHROPOLOGICAL SCIENCE Vol. 112, 121–146, 2004 Molar enamel thickness and distribution patterns in extant great apes and humans: new insights based on a 3-dimensional whole crown perspective REIKO T. KONO1* 1Department of Anthropology, National Science Museum, Hyakunincho, Shinjuku-ku, Tokyo, 169-0073 Japan Received 14 November 2003; accepted 21 December 2003 Abstract Molar enamel thickness is a key feature in the study of hominid evolution. Our understand- ing of enamel thickness and distribution patterns, however, has so far been based mostly on the limited information available from physical cross sections of the crown. In this study, the 3-dimensional (3D) whole crown enamel distribution pattern was explored in 74 extant great ape and modern human molars. Serial cross sections obtained from microfocal X-ray computed tomography were used to gen- erate digital molar reconstructions at 50 to 80 micron voxel resolution, each crown represented by two to five million voxels. Surface data of both enamel dentine junction (EDJ) and outer enamel were extracted to derive volumetric measures, surface areas, curvilinear distances, and whole crown radial thickness maps. Three-dimensional average enamel thickness (AET) was defined as enamel volume divided by EDJ surface area. In 3D AET relative to tooth size, Homo exhibited the thickest, Gorilla the thinnest, and Pan and Pongo intermediately thick enamel. This result differs from previous claims that molar enamel of Pongo is relatively thicker than that of Pan. The discrepancy between three and two-dimensional (2D) values of AET stems from a combination of local differences in within tooth enamel distribution pattern and EDJ topography between Pan and Pongo molars. It demonstrates that 2D AET is not an appropriate substitute or estimator of whole crown AET. Examination of whole crown 3D distributions of molar enamel revealed a pattern common to all four examined species, the “functional” side of the molar having thicker enamel than the opposite side. However, some unique aspects of each species were also apparent. While the Gorilla molar has relatively thin enamel through- out its crown, Pan molars are characterized by particularly thin enamel in the occlusal fovea, and Pongo molars by an accentuation of relatively thin basal and thick occlusal enamel. Human molars are characterized by relatively thick enamel throughout the crown, with relatively large contrasts between buccal and lingual, and between mesial and distal crown portions. The ancestral condition common to the four extant species can be estimated by interpreting molar enamel distribution patterns unique to each genus as likely to be derived. We hypothesize that the last common ancestor likely had interme- diately thick enamel, without particular thickening (or thinning) of enamel either occlusally or basally. Key words: enamel thickness, molar, hominoid, evolution Introduction reflects both phylogenetic heritage and the results of selec- tion for functional adaptation. Teeth are also suitable to the Dental elements in general have a greater chance to be study of morphology in relation to its formational processes, preserved and fossilized than other body parts. Therefore, since their developmental history is in part recorded as his- they often constitute a major part of fossil collections. This tological markings. For these reasons, dental morphology is true in the case of primate fossils, including fossil homi- has been intensively studied, as an important source of infor- nids. mation from both functional and phylogenetic perspectives. The dentition is functionally adapted to diet and feeding Molars show great morphological diversity among taxa. behavior. Morphogenesis of the tooth crown is controlled This is thought to be closely related to functional require- mostly by genetic factors, rather than by environmental fac- ments imposed by the physical properties of the masticated tors. While bones continue to remodel throughout an indi- food (e.g., Janis and Fortelius, 1988). For molars of extant vidual’s life, tooth enamel does not regenerate once its great apes and modern humans, morphological studies have formation is completed. Therefore tooth morphology been conducted from various perspectives. Hominoid molars share a generalized morphological pattern compared * Corresponding author. e-mail: [email protected] to those of other mammals, but also exhibit taxonomically phone: 81-3-3364-7132; fax: 81-3-3364-7104 informative differences in details (e.g., Hartman, 1988, Published online 13 April 2004 1989; Kobayashi, 2001). Molar enamel thickness is known in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.03106 to vary among the extant hominoids, apparently exhibiting © 2004 The Anthropological Society of Nippon 121 122 R.T. KONO ANTHROPOLOGICAL SCIENCE substantial functional and/or phylogenetic information (e.g., human molars based on linear measurements. They reported Martin, 1983; Shellis et al., 1998). that enamel was thicker in humans than in apes at multiple Lawrence Martin and his colleagues discussed the evolu- positions of the molar tooth crown. They proposed that the tion of hominoid enamel thickness by comparing extant thick human enamel, together with the low cusps, was great apes, modern humans, and fossil hominoids and homi- adapted to a crushing-grinding function, although no func- nids (Martin, 1983, 1985; Grine and Martin, 1988; Andrews tional rationale was presented (Molnar and Gantt, 1977). and Martin, 1991). Martin physically sectioned molars at a Kay (1981) measured enamel thickness on the worn occlusal plane that passes approximately through the tips of the two surface of molars in a wide range of primate taxa, and plot- mesial cusps (mesial cusp section, MCS), and made various ted thickness against the mesiodistal length of the tooth. He thickness measurements on those sections. He concluded noticed that enamel tends to be thicker in frugivorous spe- that the “average enamel thickness (AET)”, calculated as cies, whereas the more folivorous taxa tend to have thinner enamel area divided by length of the enamel-dentine junc- enamel (Kay, 1981). Among great apes, according to his tion (EDJ), was the most reliable measure of the amount of interpretation, Pongo has relatively thick enamel, which enamel, since it was supposedly less variable than compara- might be an adaptation to eating very hard fruits, while ble measures taken at other section positions (Martin, 1983). Gorilla has relatively thin enamel and well-developed shear- Moreover, he devised a measure called “relative enamel ing crests, which are likely to be adaptations to leaf-eating thickness” as a means to compare thicknesses between taxa (Kay, 1981). with different tooth sizes. Relative enamel thickness is cal- More recently, Macho, Schwartz and colleagues studied culated as the AET standardized by the square root of den- enamel thickness patterns within the molar crown, and dis- tine area of the crown at that section. Using this relative cussed their functional significance (Macho and Berner, thickness value, he proposed four categories of thickness, 1993, 1994; Spears and Macho, 1995, 1998; Schwartz, “thick”, “intermediate~thick”, “intermediate~thin”, and 1997, 2000a, b; Macho and Spears, 1999). Macho and “thin”. He assigned gorilla and chimpanzee molars to “thin”, Berner (1993) showed that the values of “average” and “rel- orangutan molars to “intermediate~thick”, and human ative enamel thickness” introduced by Martin (1983) dif- molars to “thick” categories (Martin, 1983, 1985). These fered between tooth types within the human molar row. They variables, average and relative enamel thicknesses, have thus proposed the necessity to investigate enamel thickness since been used frequently in species comparisons (Grine patterns seen among tooth type, or within a tooth, rather than and Martin, 1988; Andrews and Martin, 1991; Dumont, simply obtaining a representative thickness value for the 1995; Beynon et al., 1998; Shellis et al., 1998). entire tooth and/or species (Macho and Berner, 1993). They Martin furthermore related enamel thickness with prism measured enamel thickness at multiple positions on the packing patterns, and concluded that enamel was thick and MCS, and suggested that the first upper molars have a pat- formed fast in the last common ancestor of extant large-bod- tern of enamel distribution different from that of the second ied hominoids (including humans), while enamel had and third upper molars. Human upper first molars were become thin in the gorilla and chimpanzee because of a sec- found to be characterized by distinctly thicker lingual and ondary decrease in enamel formation speed (Martin, 1983, thinner buccal enamel. The posterior two molars exhibited 1985; Andrews and Martin, 1991). Later, however, Beynon overall thicker enamel than the first molar, and with less dis- et al. (1991) reexamined hominoid molar histology, and crepancy between lingual and buccal enamel thicknesses, so showed that no such decrease in enamel formation speed is that the “non-functional” buccal cusps have somewhat in fact seen in gorilla and chimpanzee molars. In all four spe- thicker enamel. This was interpreted as reflecting different cies that the latter authors examined, enamel formation functional roles of the first and posterior two molars (Macho speed was found to gradually increase from EDJ to the outer and Berner, 1993, 1994). enamel surface (OES). They therefore rejected Martin’s Using finite element analysis, they further investigated
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