Rapid dental development in a Middle Paleolithic Belgian Neanderthal Tanya M. Smith*†, Michel Toussaint‡, Donald J. Reid§, Anthony J. Olejniczak*, and Jean-Jacques Hublin* *Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany; ‡Direction de l’Arche´ologie, Ministe`redelaRe´ gion Wallonne, 1 rue des Brigades d’Irlande, 5100 Namur, Belgium; and §Department of Oral Biology, School of Dental Sciences, Newcastle University, Framlington Place, Newcastle upon Tyne NE2 4BW, United Kingdom Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved November 1, 2007 (received for review July 29, 2007) The evolution of life history (pace of growth and reproduction) was although the timing of molar eruption is the best indicator to crucial to ancient hominin adaptations. The study of dental devel- predict development and life history parameters across primates opment facilitates assessment of growth and development in fossil (18–21). A recent study reported an age of Neanderthal first hominins with greater precision than other skeletal analyses. molar eruption based on an isolated tooth from La Chaise that During tooth formation, biological rhythms manifest in enamel and was similar to the modern human mean value (8). However, this dentine, creating a permanent record of growth rate and duration. age is difficult to determine from a fully formed and isolated Quantification of these internal and external incremental features tooth, particularly without knowledge of the mean root length at yields developmental benchmarks, including ages at crown com- first molar eruption in other Neanderthals. Additional informa- pletion, tooth eruption, and root completion. Molar eruption is tion regarding dental development and age at molar eruption is correlated with other aspects of life history. Recent evidence for necessary to clarify Neanderthal life history relative to modern developmental differences between modern humans and Nean- humans. derthals remains ambiguous. By measuring tooth formation in the Direct assessments of tooth growth are based on incremental entire dentition of a juvenile Neanderthal from Scladina, Belgium, features in enamel and dentine, representing consistent short- we show that most teeth formed over a shorter time than in and long-period biological rhythms that may yield accurate modern humans and that dental initiation and eruption were assessments of tooth formation time and age at death (for relatively advanced. By registering manifestations of stress across review, see refs. 12, 22, 23). Resolution of the debate regarding the dentition, we are able to present a precise chronology of whether Neanderthals and modern humans follow disparate Neanderthal dental development that differs from modern hu- ontogenetic trajectories has been slowed by a lack of data from mans. At 8 years of age at death, this juvenile displays a degree of histological sections of teeth (2). In particular, information on development comparable with modern human children who are long-period line periodicities (temporal repeat intervals) is several years older. We suggest that age at death in juvenile lacking (8). Studies of Neanderthal perikymata (the external Neanderthals should not be assessed by comparison with modern manifestations of long-period lines) (e.g., 6, 7) offer only a human standards, particularly those derived from populations of partial solution because their periodicity is typically estimated European origin. Moreover, evidence from the Scladina juvenile from mean values of other taxa and may be directly determined and other similarly aged hominins suggests that a prolonged only from an internal examination of tooth growth. Before this childhood and slow life history are unique to Homo sapiens. work, periodicity values from only two sectioned permanent molar teeth have been reported for Neanderthals (8, 10); in hominin ͉ human evolution ͉ life history ͉ ontogeny ͉ tooth growth neither case was it possible to assess directly the timing of molar eruption or the overall chronology of dental development. In this work, we report a unique assessment of the timing of ental development and life history in Neanderthals (Homo tooth formation in a juvenile Neanderthal by using both internal neanderthalensis) have been vigorously discussed over the D and external developmental features, including the long-period last 30 years (1–11). Some studies report that Neanderthal dental line periodicity and a record of developmental stress over several development is advanced relative to modern and Upper Paleo- years that facilitates cross-registry of the dentition. The Scladina lithic humans (e.g., 1, 3, 4, 6, 9), whereas others show that aspects cave (Sclayn, Belgium) was discovered in 1971, and since 1993 it of Neanderthal development are similar to modern humans (2, has yielded a nearly complete juvenile maxillary and mandibular 7, 8, 10, 11). Knowledge of the timing of fossil hominin dental dentition from a single layer dated to between 80,000 and development and tooth eruption is fundamental to assessments 127,000 years before present (ypb) (24–27). Previous assess- of growth and development (for review, see refs. 12–14); these ments using a variety of developmental standards have suggested former studies often contradict each another by emphasizing that the juvenile was between 8.5 and 12 years of age at death similarities or differences in life history among late Pleistocene (27). Here, we directly assess dental development and age at Homo and recent humans. Moreover, studies of Neanderthal death in the Scladina juvenile. Long-period incremental features cranial and postcranial ontogeny often use modern European on tooth crowns and roots were quantified, the periodicity of and North American standards of dental development to assign long-period lines was determined from an upper first molar, ages and make comparisons (e.g., 4, 15), although it is unclear whether Neanderthal and modern human children actually follow the same schedule of dental development and tooth Author contributions: T.M.S. and M.T. designed research; T.M.S., D.J.R., and A.J.O. per- eruption. formed research; T.M.S., M.T., D.J.R., and A.J.O. analyzed data; and T.M.S., M.T., A.J.O., and Although some scholars debate whether Neanderthals had J.-J.H. wrote the paper. shorter periods of anterior tooth growth than modern humans (6, The authors declare no conflict of interest. 7), it is known that anterior tooth growth requires more time in This article is a PNAS Direct Submission. great apes than in humans (16) and is variable among human Freely available online through the PNAS open access option. populations (17). This level of variation within and between †To whom correspondence should be addressed. E-mail: [email protected]. hominoid species suggests that anterior tooth formation times This article contains supporting information online at www.pnas.org/cgi/content/full/ are not a reliable predictor of life history (6). Furthermore, little 0707051104/DC1. is known about ages at tooth eruption in Neanderthals (5), © 2007 by The National Academy of Sciences of the USA 20220–20225 ͉ PNAS ͉ December 18, 2007 ͉ vol. 104 ͉ no. 51 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0707051104 Downloaded by guest on September 26, 2021 Table 1. Crown formation times in the Scladina juvenile Table 2. Crown extension rates for human, chimpanzee, compared with two modern human populations and Neanderthal first molars South Cusp* Taxon Mean N Range Tooth* Cusp† Scladina North European‡ N African§ N Ump Homo sapiens 5.82 14 5.28–6.66 UI2 — 1,206 1,095 Ϯ 49 16 984 Ϯ 36 22 Pan troglodytes 7.77 3 7.66–7.90 UC — 1,301 1,398 Ϯ 55 39 1,213 Ϯ 42 30 Homo neanderthalensis 7.60 1 — UM1 mp 872 1,208 Ϯ 78 7 1,088 Ϯ 66 6 Umb Homo sapiens 5.87 13 4.68–7.47 mb 811¶ 1,082 Ϯ 47 6 1,040 Ϯ 64 12 Pan troglodytes 6.93 3 5.81–7.61 UM2 mp 967 1,193 Ϯ 49 6 1,263 Ϯ 82 8 Homo neanderthalensis 8.47† 1— mb 949 1,087 Ϯ 59 9 1,206 Ϯ 74 9 LC — 1,326 1,866 Ϯ 73 13 1,494 Ϯ 56 25 Lmb Homo sapiens 6.61 18 5.35–7.42 LP3 Buccal 994 1,437 Ϯ 68 19 1,122 Ϯ 42 16 Pan troglodytes 7.94 5 7.07–8.88 Homo neanderthalensis 7.70‡ 1— Values are in days, followed by the standard deviation and sample size (N). Lml Homo sapiens 6.30 27 5.07–7.27 Anterior tooth data are from ref. 17, premolar data are from ref. 11, and molar data are from ref. 34. Pan troglodytes 8.82 5 8.00–9.43 ‡ *U, upper; L, lower; I2, lateral incisor; C, canine; P3, third premolar; M1, first Homo neanderthalensis 7.68 1— molar; M2, second molar. Values represent the length of the enamel–dentine junction (EDJ) divided †mp, mesiopalatal cusp (protocone); mb, mesiobuccal cusp (paracone). Dash by the cusp-specific crown formation time, followed by the sample size of each indicates single-cusped tooth. cusp (N) and the range (minimum to maximum values). ‡North European indicates modern humans of northern European origin. *U, maxillary; mp, mesiopalatal cusp (protocone); mb, mesiobuccal cusp (para- §South African indicates modern humans of southern African origin. cone); L, mandibular; mb, mesiobuccal cusp (protoconid); ml, mesiolingual ¶Assumes an equal amount of prenatal formation as the upper first molar cusp (metaconid). mesiopalatal cusp. †Estimated using minor reconstruction of dentine horn tip and prenatal enamel equal to mesiopalatal cusp. ‡Calculated using mCT data to virtually section tooth (optimizing for mesial patterns of postnatal developmental stress were calibrated across EDJ length); cusp-specific EDJ length was divided by formation times re- teeth, and the duration of crown formation and root develop- ported in ref.