incremental dental development: methods and applications in

Incremental dental development: Methods and applications inhominoid evolutionary studies

Tanya M. Smith*

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany

Received 9 November 2006; accepted 30 September 2007

Abstract

This survey of dental microstructure studies reviews recent methods used to quantify developmental variables (daily secretion rate, period-icity of long-period lines, extension rate, formation time) and applications to the study of hominoid evolution. While requisite preparative andanalytical methods are time consuming, benefits include more precise identification of tooth crown initiation and completion than conventionalradiographic approaches. Furthermore, incremental features facilitate highly accurate estimates of the speed and duration of crown and root for-mation, stress experienced during development (including birth), and age at death. These approaches have provided insight into fossil homininand Miocene hominoid life histories, and have also been applied to ontogenetic and taxonomic studies of fossil apes and humans. It is shownhere that, due to the rapidly evolving nature of dental microstructure studies, numerous methods have been applied over the past few decades tocharacterize the rate and duration of dental development. Yet, it is often unclear whether data derived from different methods are comparable orwhich methods are the most accurate. Areas for future research are identified, including the need for validation and standardization of certainmethods, and new methods for integrating nondestructive structural and developmental studies are highlighted.! 2007 Elsevier Ltd. All rights reserved.

Keywords: Age at death; Dentine formation; Enamel formation; Incremental features; Life history

Introduction

Dental remains represent a well-established means of re-constructing the evolution of humans and their Miocene hom-inoid predecessors. Commonly noted reasons for this includetheir relative abundance in the fossil record, lack of remodel-ing (other than attrition), relatively strong genetic component,evidence for dietary preferences, and taxonomic utility. Lesscommonly noted is the temporal record of development pre-served in teeth. In a process similar to the production ofmany biological hard tissues, dental tissues are formed in anaccretional manner that permanently captures the rate andduration of their formation. Incremental manifestations of bi-ological rhythms in teeth range from a subdaily to an annualperiodicity, and have been documented by microscopists and

oral biologists for several centuries (reviewed in Boyde,1964, 1990; Dean, 1987a,b, 1995a; Smith, 2006). Anthropolo-gists have only recently turned their attention to incrementaldental development after early reports of incremental features(perikymata) on the surface of fossil hominin teeth (e.g.,Robinson, 1956) and studies of internal enamel and dentinemicrostructure in living primates (e.g., Fukuhara, 1959;Boyde, 1963; Shellis and Poole, 1977; Dean and Wood,1981). Subsequent research by Beynon, Boyde, Bromage,Dean, Martin, Reid, and Shellis ushered in a new field of den-tal microstructure studies in living and fossil apes and humans(Table 1). Research on incremental development during thepast few decades has grown quite rapidly (Smith and Hublin,2008); active areas of inquiry span the primate order andextend back to the fossil record of the earliest primates (e.g.,Schwartz et al., 2002, 2005).

Following Dean and Wood’s (1981) landmark radiographicstudy of hominoid dentitions, histological studies during the1980s and 1990s began to provide a new understanding of

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Journal of Human Evolution 54 (2008) 205e224

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Table 1Studies of incremental development in hominoid primates (1983e2007)*

Taxon E/D References

ExtantHomo (incl. archaeological) E,D Martin, 1983; Shellis, 1984a,b; Bromage and Dean, 1985; Dean, 1985; Beynon and Wood, 1987; Bullion, 1987;

Dean, 1987b; Bacon, 1989; Mann et al., 1990; Skinner and Anderson, 1991; Stringer et al., 1990; Beynon and Dean,1991; Beynon et al., 1991b; Dean and Beynon, 1991; Mann et al., 1991; Beynon, 1992; Dean et al., 1992;Hillson, 1992; Dean et al., 1993b; Beynon and Reid, 1995; Dean, 1995a,b; Dean and Scandrett, 1995;FitzGerald, 1995; Huda and Bowman, 1995; Dean and Scandrett, 1996; Berkovitz et al., 1998; Beynon et al., 1998a,b;Dean, 1998a; Reid et al., 1998b; Antoine et al., 1999; FitzGerald et al., 1999; Antoine, 2000; Reid and Dean, 2000;Dean et al., 2001; Lampl et al., 2000; Schwartz and Dean, 2001; Schwartz et al., 2001; Thomas, 2003;Guatelli-Steinberg et al., 2005; Dean, 2006; Macchiarelli et al., 2006; Reid and Ferrell, 2006; Reid and Dean, 2006;Smith et al., 2007a,c; Dean, 2007b; Guatelli-Steinberg and Reid, 2008; Reid et al., 2008; Smith et al., in press-a

Pan troglodytes E,D Martin, 1983; Beynon et al., 1991b; Beynon and Reid, 1995; Beynon et al., 1998b; Dean, 1998a; Reid et al., 1998a;Shellis, 1998; Dean and Reid, 2001; Dean et al., 2001; Schwartz and Dean, 2001; Schwartz et al., 2001; Smith, 2004;Dean, 2006; Smith et al., 2007b

Pan paniscus E Smith et al., 2003a; Ramirez Rozzi and Lacruz, 2007Gorilla gorilla E,D Martin, 1983; Shellis, 1984a; Beynon et al., 1991a,b; Beynon and Reid, 1995; Beynon et al., 1998b; Dean, 1995b;

Dean and Reid, 2001; Dean et al., 2001; Schwartz and Dean, 2001; Schwartz et al., 2001; Dean, 2006;Schwartz et al., 2006

Pongo pygmaeus E,D Martin, 1983; Beynon et al., 1991a,b; Beynon and Reid, 1995; Dean, 1995a,b; Beynon et al., 1998b; Dean, 1998a,b;Dean and Shellis, 1998; Dean, 2000; Schwartz and Dean, 2001; Schwartz et al., 2001; Dean, 2006

Hylobates lar E,D Martin, 1983; Dean, 1998b; Dirks, 1998, 2001, 2003; Dirks and Bowman, 2007Hylobates moloch E Beynon et al., 1998bSymphalangus syndactylus E,D Dean, 1998b; Dean and Shellis, 1998; Dirks, 2001, 2003; Dirks and Bowman, 2007

FossilProconsul heseloni E,D Beynon et al., 1998b; Dean and Shellis, 1998; Dean, 2006Proconsul nyanzae E,D Beynon et al., 1998b; Dean et al., 2001; Dean, 2006Afropithecus turkanensis E Kelley and Smith, 2003; Smith et al., 2003aGriphopithecus sp. E Martin, 1983; this study: Table 2Sivapithecus indicus E Martin, 1983; Mahoney et al., 2007Sivapithecus parvada E Kelley, 1997; Mahoney et al., 2007Lufengpithecus sp. E,D Zhao et al., 1999, 2000; Schwartz et al., 2003; Zhao et al., 2003; Zhao, 2004; Zhao and He, 2005; Zhao et al., 2008Dryopithecus laietanus E,D Kelley et al., 2001Graecopithecus freybergi E,D Smith et al., 2004Gigantopithecus blacki E Dean and Schrenk, 2003Australopithecus anamensis E Dean et al., 2001; Ward et al., 2001Australopithecus africanus E Bromage and Dean, 1985; Grine and Martin, 1988; Beynon, 1992; Moggi-Cecchi et al., 1998; Dean and Reid, 2001;

Dean et al., 2001; Lacruz et al., 2005; Lacruz and Bromage, 2006; Lacruz et al., 2006; Bromage et al., 2007Paranthropus robustus E,D Bromage and Dean, 1985; Beynon and Dean, 1987; Dean, 1987b; Grine and Martin, 1988; Beynon, 1992;

Dean et al., 1993a; Dean, 1995b, 1999; Dean and Reid, 2001; Dean et al., 2001; Lacruz and Bromage, 2006;Lacruz et al., 2006; Lacruz, 2007; Tafforeau and Smith, 2008

Paranthropus boisei E,D Beynon and Wood, 1986; Beynon and Dean, 1987; Beynon and Wood, 1987; Dean, 1987a,b; Grine and Martin, 1988;Beynon, 1992; Ramirez-Rozzi, 1993a,c; Ramirez Rozzi, 1993d, 1994, 1995, 1997; Ramirez Rozzi, 1998;Dean and Reid, 2001; Dean et al., 2001; Dean, in press

Paranthropus aethiopicus E Ramirez-Rozzi, 1993a; Ramirez Rozzi, 1993d, 1994; Dean et al., 2001Omo hominins E Ramirez Rozzi, 1992; Ramirez-Rozzi, 1993a,c; Ramirez Rozzi, 1994, 1995, 1997; Ramirez Rozzi, 1998;

Ramirez Rozzi, 2002Australopithecus afarensis E Bromage and Dean, 1985; Ramirez Rozzi, 1993d; Dean and Reid, 2001; Dean et al., 2001East African early Homo E,D Bromage and Dean, 1985; Dean, 1985; Beynon and Wood, 1986, 1987; Ramirez Rozzi, 1993d, 1995, 1997;

Ramirez-Rozzi, 1998; Dean et al., 2001South African early Homo E Bromage and Dean, 1985; Beynon, 1992; Dean et al., 2001Homo erectus E,D Dean et al., 2001Homo ergaster E Dean et al., 2001Homo habilis E,D Dean, 1995a, 2000; Dean et al., 2001Homo rudolfensis E Ramirez Rozzi et al., 1997; Dean et al., 2001Homo antecessor E Ramirez Rozzi and Bermudez de Castro, 2004Homo heidelbergensis E Bermudez de Castro et al., 2003; Ramirez Rozzi and Bermudez de Castro, 2004Homo neanderthalensis E,D Dean, 1985; Dean et al., 1986; Stringer et al., 1990; Mann et al., 1991; Ramirez-Rozzi, 1993b; Mann and

Vandermeersch, 1997; Stringer and Dean, 1997; Dean et al., 2001; Sasaki et al., 2002; Ramirez Rozzi andBermudez de Castro, 2004; Guatelli-Steinberg et al., 2005; Ramirez Rozzi, 2005; Macchiarelli et al., 2006;Guatelli-Steinberg et al., 2007a,b; Guatelli-Steinberg and Reid, 2008; Reid et al., 2008; Smith et al., in press-a,b

Early Homo sapiens E,D Smith et al., 2007cMSA Homo sapiens E Smith et al., 2006bUP Homo sapiens E,D Dean, 1985; Ramirez Rozzi and Bermudez de Castro, 2004* Includes reports of novel data in full-length papers/dissertations only; E¼ data on enamel formation; D¼ data on dentine formation.

206 T.M. Smith / Journal of Human Evolution 54 (2008) 205e224

hominoid dental development, driven, in part, by the goal ofcharacterizing fossil hominin development. Beynon andDean (1987) noted that, prior to the 1980s, fossil hominin den-tal development had been assessed by comparing human andape eruption sequences, which yielded only relative ages. Itwas not until studies by Bromage and Dean (1985), Deanet al. (1986), Beynon and Wood (1987), and Beynon andDean (1987) that hominin crown formation times were directlyestimated from incremental features. Subsequent studies in the1990s began to establish a framework for nonhuman primatedental development, although both sample sizes and the num-ber of reports were smaller than those for hominins. Researchconducted in the past decade has reported on aspects of incre-mental development in larger samples, as well as in a greaterdiversity of fossil hominoid taxa. This expanding databaseprovides critical insight into developmental variation withinand among hominoids, leading to more refined comparisonsof dental development and better assessment of the evolution-ary utility of these approaches.

Paleoanthropological studies of incremental developmentgenerally aim to increase knowledge of hominoid ontogeny,life history, and/or taxonomy. During the past few decadesnumerous methods have been developed to quantify toothgrowth, especially the daily secretion rate, extension rate,and/or formation time. These variables are critical to assess-ments of crown formation time, root formation time, andage at death. Studies of incremental dental development arealso used for a broader spectrum of anthropological applica-tions (reviewed in Smith, 2004), including forensic science,paleodemography, paleoepidemiology, and reconstruction ofpast diets (via isotopic studies; e.g., Humphrey et al., 2007;Tafforeau et al., 2007). Furthermore, due to the well-estab-lished relationship between dental development and life his-tory, studies of tooth growth (especially molar eruption) inimmature individuals provide important evidence of the evolu-tion of hominin and hominoid developmental biology (e.g.,Smith and Tompkins, 1995; Kelley, 1997, 2002; Dean, 2000,2006; Kelley and Smith, 2003; Skinner and Wood, 2006).

While many studies have focused on establishing theconsistent temporal nature of incremental features (reviewedin FitzGerald, 1998; Smith, 2006), less attention has beenpaid to establishing the precision or accuracy of methodsthat quantify developmental rate or time (but see exceptionsin Beynon et al., 1991a, 1998a,b; Dean et al., 1993a; RamirezRozzi, 1997; Reid et al., 1998a; Dean, 1998a; Antoine et al.,1999; Kelley et al., 2001; Smith et al., 2004; FitzGerald andSaunders, 2005; Smith et al., 2006a). As a result, little meth-odological standardization exists, and the comparability ofsome data is unclear. This issue has been compounded byrecent information on variation within and among teeth. Forexample, histological studies have demonstrated that all cuspswithin a molar and all molars within a row do not developidentically (e.g., Reid et al., 1998a,b; Reid and Dean, 2006;Smith et al., 2007a,b), implying that interspecific comparisonsof formation time should be limited to equivalent cusp andmolar types (Smith et al., 2007a). In the following sections,recent methods for quantifying incremental features are

reviewed, and evolutionary applications to hominin and hom-inoid cases are examined. Avenues for future study are sug-gested, including the need for standardization and validationof particular methods. Finally, a new approach to the integra-tion of structural and histological data using high-resolutionmicro-computed tomography (mCT) is outlined.

Background

Incremental enamel and dentine microstructure features aredefined in this review as structural phenomena that are formedwith a consistent periodic repeat interval (in contrast to aperi-odic structural features such as enamel prisms, dentine tubules,and Hunter-Schreger bands). Traditionally, this includes thefollowing enamel features: (1) cross-striations and (2) Retziuslines and their surface manifestation, known as perikymata(Fig. 1). (See Smith [2006] and Tafforeau et al. [2007] forinvestigations of intradian lines and laminations, enamel incre-mental features that are not typically used for the quantifica-tion of hominoid enamel development.) Cross-striations andRetzius lines are also frequently referred to as short-and long-period structures due to their respective 24-hourand >24-hour rhythms. They are also distinguished fromgrowth disturbances that may manifest as marked accentua-tions or disruptions of the developing enamel front, featuresreferred to as accentuated lines (also sometimes termed path-ological lines or Wilson bands) and enamel hypoplasias, whichhave an irregular periodicity that is thought to conform to anextrinsic form of stress (reviewed in Hillson and Bond,1997; Skinner and Hopwood, 2004; Schwartz et al., 2006).

Short- and long-period features of dentine microstructureare known as (1) von Ebner’s lines and (2) Andresen lines,which have been shown to correspond to cross-striations andRetzius lines in enamel, respectively (Bromage, 1991; Deanet al., 1993b; Dean, 1995a; Dean and Scandrett, 1996). Thereis evidence to suggest that Andresen lines may manifest on theroot surface of juvenile individuals as periradicular bands(Fig. 1) (Dean, 1995a; Smith et al., in press-a), which maybe equivalent to perikymata on the enamel surface. Finally,tooth cementum is believed to show an annual rhythm mani-fest as cementum annulations in tooth roots (e.g., Kay et al.,1984; Wittwer-Backofen et al., 2004), but due to the difficultyof accurately identifying these lines sequentially (Renz andRadlanski, 2006), they have not been used in hominoid evolu-tionary studies, and will not be discussed further. Given thatthe great majority of studies of incremental development focuson permanent teeth, as enamel microstructure is more difficultto image in deciduous teeth, the following review will be lim-ited to studies of permanent teeth. (See FitzGerald et al. [1999]and Macchiarelli et al. [2006] for recent data on incrementaldevelopment in deciduous teeth.)

Recent analyses of enamel and dentine microstructure havesought to characterize several developmental variables usingshort- and long-period incremental features: (1) daily secretionrate; (2) periodicity of long-period lines (number of short-period increments between successive long-period lines); (3)number and distribution of long-period lines (or their external

207T.M. Smith / Journal of Human Evolution 54 (2008) 205e224

manifestation as perikymata/periradicular bands); and (4) ex-tension rate of crown and/or root growth. The quantificationof these variables may be used to determine rate and durationof crown and/or root formation, as well as the age at death (indeveloping dentitions) and stress experienced during develop-ment. Several researchers have noted that histological methodsprovide more accurate estimates of crown formation time thanradiographic methods (Beynon et al., 1991a; Winkler, 1995;Beynon et al., 1998a; Reid et al., 1998a,b). Due to the natureof crown formation, radiographs tend to overestimate the ageat crown initiation, underestimate the age at crown comple-tion, and therefore underestimate the duration of crown forma-tion. Due to the time-consuming and partially destructivenature of traditional histological studies, studies of internaldevelopment have been limited to a small number of fossils,and only slightly greater numbers of nonhuman primates. Al-though nondestructive studies of external development (e.g.,Bromage and Dean, 1985; Ramirez-Rozzi, 1998; Lacruzet al., 2005) may be the most practical when considering valu-able fossil material, data obtained by direct sectioningmethods (e.g., Dean et al., 1993a; Reid et al., 1998a; Smithet al., 2004; Schwartz et al., 2006) or virtual sectioning (Smithet al., 2006b, 2007c; Tafforeau and Smith, 2008) are poten-tially more accurate due to the smaller number of necessaryassumptions (discussed below).

Methods and applications

Quantification of daily secretion rate

Assessment of daily secretion rate (DSR) is based on thetheory that cross-striations in enamel and von Ebner’s linesin dentine are formed every 24 hours (Schour and Poncher,1937; Mimura, 1939; Schour and Hoffman, 1939; Okada,1943; Bromage, 1991; Antoine, 2000; Smith, 2006). Determi-nation of rate is generally accomplished by dividing an empir-ical quantity, such as distance, by a known time; in enamel,the distance between two cross-striations is divided by oneday (for greater accuracy, a series of cross-striations is typi-cally measured and divided by the same number of days).Enamel DSR has been conventionally quantified and reportedin four primary ways: (1) measurements of cross-striationspacing derived from a single area or a number of unspecifiedareas within the crown (e.g., Shellis and Poole, 1977; Martin,1983); (2) measurements averaged in specific regions of thecrown (Beynon et al., 1991b); (3) the quotient of prism lengthdivided by (experimentally) known time between intervals(e.g., Dean et al., 1993b); and (4) direct counts of cross-striations between fixed-distance points (e.g., Beynon et al.,1998b; Dean, 1998a; Dean et al., 2001). In dentine, becausesuccessive daily lines are difficult to image without

demineralization (Dean, 1998b), DSR is often quantified bydividing the spacing of long-period Andresen lines by theirperiodicity, which is determined from enamel cross-striationsand Retzius lines (e.g., Dirks, 1998; Smith et al., 2004,2007b). A number of experimental studies have also usedfluorescent-labeled material to calculate rates of dentineDSR (e.g., Dean, 1993; Dean and Scandrett, 1995), and in ma-terial of exceptional quality, DSR has been calculated directlyfrom the spacing of daily lines in dentine (Dean, 1998b, 1999,2007b).

Initial reports of hominoid enamel DSR were made withoutreference to the location of measurements (e.g., Shellis andPoole, 1977; Martin, 1983). As subsequent work began todemonstrate that secretion rate was not constant throughoutthe crown, Beynon et al. (1991b) proposed a method of datacollection that divided the enamel crown into eight areas:cuspal inner, middle, and outer; lateral inner, middle, andouter; and cervical inner and outer (see Fig. 2 in Beynonet al., 1991b). This model was an attempt to organize thecrown into zones that represented successive stages of devel-opment. However, Dean (1998a) noted that defining rates asinner, middle, and outer averages may mask variation, leadingto a simplified categorization of this complex developmentalprocess. Furthermore, because secretion and extension rateschange throughout development, the equally spaced divisionsproposed by Beynon et al. (1991b) are not likely to correspondto equivalent temporal divisions.

Dean et al. (1993b) presented a method for quantifyingDSR by measuring the increase in crown height over a knownperiod of time and then plotting this length against time toyield DSR (as the slope) (e.g., see Fig. 5 in Dean et al.,1993b). These types of graphs have included data on bothenamel and dentine DSR (Dean, 1993, 1995a,b; Dean et al.,1993b; Dean and Scandrett, 1995) and may include informa-tion from a series of successive teeth, provided that they areregistered with one another (Dean and Scandrett, 1996). Theadvantages of this approach are that it may provide insightinto changes in rate throughout the continuous developmentof the enamel (and/or dentine), and extreme rates at the begin-ning and end of crown formation may be apparent. However,for accurate and continuous assessment of local DSR, manysuccessive intervals must be utilized. Additionally, this methodrequires either teeth that have been experimentally labeled oridentification of a series of accentuations that can be registeredwith one another in different tissues, cusps, and/or teeth (dis-cussed further below).

Beynon et al. (1998b) and Dean (1998a, 2000) presentedDSR data as monthly box-and-whisker plots of cuspal enamelformation based on counts of cross-striations from the begin-ning to the end of cuspal formation. Dean et al. (2001) illus-trated a similar application of this method, where growth

Fig. 1. Enamel/dentine microstructure used to quantify rate and duration of development: (a) long-period perikymata, running horizontally around the crown(scale¼ 1 mm); (b) long-period periradicular bands, horizontally encircling the root (scale¼ 0.5 mm); (c) long-period Retzius lines, running diagonally to the toothsurface on the left (scale¼ 0.2 mm); (d) long-period Andresen lines, curving horizontal light and dark bands (scale¼ 0.2 mm); (e) short-period cross-striations, lightand dark bands crossing vertically oriented enamel prisms (scale¼ 0.1 mm); (f) short-period von Ebner’s lines, fine horizontal light and dark bands (scale¼ 0.05 mm).


trajectories of cuspal enamel were determined from counts ofcuspal cross-striations in 100-mm intervals from the dentinehorn to the tooth surface, and the number of days was plottedagainst increasing enamel thickness (see also Dean, 2006). Anoteworthy limitation of this method is that it requires excep-tionally high-quality sections, and sections of such quality arerare (e.g., Schwartz and Dean [2001] reported being able to dothis in only 12 of 115 sectioned canines). Furthermore, Smithet al. (2003a, 2004) noted that, even in excellent-quality mate-rial, enamel DSR may be difficult to assess along entire prismpaths due to high proportions of subdaily features (intradianlines).

Given that these different methods illuminate crown growthin different regions and over different periods of development,it is likely that certain results are not directly comparable. Ad-ditionally, Smith et al. (2003a) noted that different researchersdo not agree on the implementation of these methods. Beynonet al. (1991b), Dirks (1998), and Reid et al. (1998a,b) sug-gested that measurements of cross-striations should not bemade in the first 100 mm of enamel at the enamel-dentine junc-tion (EDJ) or in the last 100 mm at the surface because apris-matic enamel in these regions and the convergence ofRetzius lines at the tooth surface may obscure or complicatemeasurements of daily lines. When comparing chimpanzeecuspal DSR data from Reid et al. (1998a) and Dean (1998a),reported values in the former do not show the relatively widerange of values reported by the latter (summarized in Table5.15 of Smith, 2004). Dean’s (1998a) inclusion of the firstand last month of cuspal enamel formation (corresponding ap-proximately to the first and last 100 mm) often increases therange of reported DSR values (Dean, 1998a; Beynon et al.,1998b). A similar problem exists between studies that quantifycuspal secretion rates lateral to the cusp tip (e.g., see Fig. 4 inDean, 1998a) rather than directly over the dentine horn (e.g.,Smith et al., 2007b); DSR is often higher on the side of thecusp where the same cohort of cells produces a greater thick-ness of enamel (relative to the cusp tip, which often showsa slightly ‘‘compressed and gnarled’’ pattern) (e.g., seeFig. 5.5ced in Smith, 2004). In summary, a consistent andaccurate methodology is needed for determining DSR thatreflects the underlying process of accretion, that does not sub-stantially mask variation, and that may be applied to a maximalnumber of sectioned teeth.

Hominoid daily secretion rates

Two general trends have emerged from recent studies: (1)DSR increases from the EDJ to the tooth surface and (2) DSRdecreases (at equivalent depths) from the cusp to the cervix.The most commonly studied region of the crown is the cuspalenamel (see reviews in Schwartz et al., 2003; Mahoney et al.,2007), as cuspal secretion rates are important for estimates ofcrown formation time. Although Smith et al. (2007b) recentlyconcluded that DSR is consistent among cusps within Panmolars, and may be consistent among molar types, additionaldata are needed to assess trends in DSR through the dentition.

Recent work on daily secretion rates in hominoid enamelsuggests a lower limit of 2e3 mm/day and an upper limit of6e7 mm/day (reviewed in Smith, 2004). Beynon et al. (1991b)found that average molar DSR values were fairly similaramong hominoids, with Homo and Pan showing the lowestaverage values, and Gorilla showing higher averages (alsosee tables in Dirks, 1998; Reid et al., 1998a; Smith et al.,2003a, 2004; Lacruz and Bromage, 2006). Mean cuspalDSR values among Miocene and living apes appear to befairly similar, although the inner cuspal rates show somevariation, particularly when compared to living humans (seeTable 2 and Fig. 6 in Mahoney et al., 2007). When fossilhominins are considered, australopiths appear to show thehighest cuspal secretion rates, followed by early Homo, whichshows similarities with African apes (Dean et al., 2001; Lacruzand Bromage, 2006). Modern humans and Neandertals showlower cuspal rates than other hominins (Dean et al., 2001;Macchiarelli et al., 2006).

Dentine DSR in hominoid permanent teeth is similar toenamel DSR values, with mean values of axial (coronal) den-tine ranging from 2 to 4 mm/day in hominoid molars (reviewedin Table 6 of Smith et al., 2004), close to 5 mm/day in the I1 ofProconsul (Beynon et al., 1998b), and between 5 and 6 mm/day in the axial dentine of human anterior teeth (Dean andScandrett, 1995). Dentine DSR near the enamel cervix andnear the root surface (zone 1 in Dean, 1998b) has been re-ported to range from approximately 1 to 2 mm/day (Deanand Scandrett, 1995; Beynon et al., 1998b; Dean, 1998b;Smith et al., 2004, 2007b), and from 2 to 3 mm/day in slightlydeeper dentine (Dean, 2007b). Unlike the situation for enamel,few studies have systematically assessed variation in dentineDSR within a tooth, within a dentition, or among nonhumanhominoids (but see Dean, 1998b, and references therein).

Periodicity of long-period lines

The determination of the periodicity of long-period Retziuslines and Andresen lines is based on the theory that a consistentnumber of daily increments (cross-striations or von Ebner’slines) is expressed between successive long-period lines inall teeth of an individual’s dentition. This has been reviewedand tested by FitzGerald (1995, 1998) and Smith (2004,2006). Periodicity has been determined traditionally by count-ing a series of cross-striations between Retzius lines in areasthat preserve them clearly, which is often difficult to do withcertainty (Fig. 2). Two main complications are the ability tounambiguously identify long-period lines (discussed in thefollowing section) and the precise identification of a completeseries of daily lines between successive long-period lines. Theperiodicity of long-period lines is very rarely assessed in den-tine due to the difficulty of imaging successive daily incre-ments (e.g., see Fig. 7 in Dean, 1998b).

In addition to direct counts of cross-striations betweensuccessive Retzius lines, Dean et al. (1993b) and Swindlerand Beynon (1993) suggested that this variable could also bedetermined by dividing the spacing between Retzius lines bythe average (local) DSR. However, Smith et al. (2003a) noted


that this method does not necessarily produce periodicityvalues that are equivalent to direct counts of cross-striations,as DSR is not always constant between pairs of Retzius lines.Local variation, most commonly resulting from the conver-gence of Retzius lines at the tooth surface (e.g., see Fig. 2.3bin Smith, 2004), may influence DSR when cross-striationsfrom only a portion of the interval are measured. It is suggestedthat this method for periodicity determination should be ap-plied only in areas that show no evidence of changes in secre-tion rate (spacing of Retzius lines), and should ideally be usedonly to verify direct counts. Although it is rare to find areaswith clear cross-striations across multiple Retzius line intervals(e.g., see Fig. 7 in Dean, 2000), averaging counts across two ormore such intervals may be the most reliable method for accu-rately determining the periodicity of long-period lines (Fig. 2c)(see Smith [2004, 2006] for additional discussion of confound-ing factors in periodicity determination).

Smith et al. (2003a) reviewed periodicity values of homi-noid long-period lines, which are known to range from 4 to12 days (see Table 3 in Smith et al., 2003a). Studies of largenumbers of modern humans have demonstrated a wide rangeof Retzius line periodicities (e.g., Beynon, 1992; FitzGerald,1995, 1998); Smith et al. (2007a) recently reported periodicityin 365 modern humans, which ranged from 6 to 12 days witha mean and mode of 8 days. Few studies of fossil homininshave directly established the periodicity of the material understudy (but see Dean, 1987a; Dean et al., 1993a; Ward et al.,2001; Lacruz et al., 2006; Macchiarelli et al., 2006; Smithet al., 2007c; Smith et al., in press-a). Studies of fossil homi-nins by Bromage and Dean (1985), Dean et al. (1986), Beynonand Dean (1987), and Dean (1987b) used periodicity estimatesof 7e9 days, which are the most common values for modernhuman teeth. Others have used an estimate of 9 days to calcu-late formation time (e.g., Dean and Reid, 2001; Dean et al.,2001; Cunha et al., 2004; Ramirez Rozzi and Bermudez deCastro, 2004; Ramirez Rozzi, 2005), as a periodicity of 9days was reported as the mean and modal value of a largestudy of great apes and humans (reviewed in Dean and Reid,2001). However, when single-integer estimates are used in-stead of range data, the accuracy of these nondestructivemethods may be in question. It is clear that nondestructivetechniques are needed to determine ranges, means, and modesof long-period line periodicities in additional fossil hominins(e.g., Lacruz et al., 2006; Smith et al., 2007c; Tafforeau andSmith, 2008), which may clarify debates over differences inperikymata numbers and formation times between taxa.

Long-period line number and distribution

Long-period line number is typically determined from ei-ther histological sections or crown/root surfaces (Fig. 1aed);given their relatively distinct appearance, this often provesto be the most straightforward aspect of incremental-featurequantification. However, other features such as accentuatedlines or enamel laminations found within intervals or coinci-dent with long-period lines may make identification moredifficult (FitzGerald, 1995; see Figs. 2.5b and 3.16 in Smith,

Fig. 2. Variation in the clarity of enamel long-period line periodicity within anindividual tooth: (a) ambiguous pattern of diagonal Retzius lines, (b) areaswhere either 7 or 8 cross-striations may be seen between Retzius lines (whitebrackets), and (c) area with 16 cross-striations across two Retzius line intervals(white bracket). The periodicity in this individual is determined to be 8 days.Scale bars¼ 0.1 mm.


2004). Dean (1987a) proposed what has become a paradigmfor many histological studies of enamel long-period lines;he suggested that Retzius lines should be identified as thoselines that reach the surface as perikymata (see Fig. 4 in Kelleyand Smith, 2003; see Fig. 3 in Tafforeau and Smith, 2008) incontrast to other lines that may be superimposed on this pat-tern. Although identification of corresponding perikymata mayoften represent a reliable means of discriminating Retziuslines, convergence of these lines may sometimes result ina smooth enamel surface without obvious terminal points(Beynon and Dean, 1991; see Fig. 2.5b in Smith, 2004). Thisis partially due to the production of aprismatic subsurfaceenamel, which varies within a tooth crown (Whittaker,1982). The most reliable method of defining and counting Re-tzius lines may involve the assessment of several characteris-tics together, including their consistent appearance from theEDJ to the enamel surface, the regular spacing of successivelines, and their terminal manifestation as perikymata on thetooth surface.

Perikymata (Fig. 1a) are often visualized on high-resolutionimpressions of tooth crowns, and counts are typically madefrom the cervix to the cusp tip (or vice versa). Studies mappingthe distribution of long-period lines have typically used one oftwo approaches: (1) counts of long-period lines in each milli-meter of crown height (e.g., Dean, 1987b; Beynon et al.,1998b; Moggi-Cecchi et al., 1998; Reid et al., 1998a,b), or(2) counts of long-period lines in each decile of crown height(e.g., Reid and Dean, 2000; Dean and Reid, 2001). The lattermethod has been more commonly applied in the past fewyears, as it allows for comparisons of the distribution oflong-period lines across teeth of differing sizes.

The distribution of perikymata has often been noted as oneof the more taxonomically diagnostic features of homininenamel microstructure. Robinson’s (1956) comparison of peri-kymata patterns in fossil hominins and modern humans re-vealed that fossil hominins showed more ‘‘regular’’ spacingof cervical perikymata when compared to a modern sampleof postcanine teeth, but that Paranthropus and Australopithe-cus did not differ. However, Bromage and Dean (1985) sug-gested that perikymata spacing on incisors does distinguishParanthropus from Australopithecus, early Homo, and modernhumans. They noted that Paranthropus does not showa marked trend of perikymata ‘‘narrowing and condensation’’cervically as shown in these other taxa, implying a more uni-form pattern of cervical enamel formation and possibly a morerapid period of completion (see Fig. 5 in Beynon and Dean,1988; also see Dean, 1987b; Beynon, 1992; Dean and Reid,2001; Dean et al., 2001; Lacruz et al., 2006). A few studieshave reported developmental differences among Paranthropusspecies (Dean, 1987b; Ramirez-Rozzi, 1993a, 1998; Dean andReid, 2001; but see Lacruz et al., 2006). Dean (1987b) andDean and Reid (2001) reported that Paranthropus boiseishows a different pattern of perikymata distribution thanP. robustus; this extremely uniform cervical perikymata distri-bution in P. robustus may represent a derived condition rela-tive to other hominins. However, Ramirez-Rozzi (1998)questioned the use of perikymata spacing or counts for

taxonomic distinction, as he found that patterns of perikymataspacing did not group the Omo hominin teeth in any fashionthat agreed with the taxonomic attribution based on macro-structure. More recently, Ramirez Rozzi and Bermudez deCastro (2004) and Guatelli-Steinberg et al. (2007a) reportedthat perikymata distribution in the cervical aspect of anteriorteeth differs between Neandertals and modern humans, withNeandertals showing a more uniform pattern from the cuspto the cervix (somewhat similar to reported differences be-tween Paranthropus and Australopithecus). Guatelli-Steinberget al. (2007a) found that the degree of surface curvature inmodern humans and Neanderthals did not explain the apparenttaxonomic differences.

Considerably less attention has been paid to the number anddistribution of long-period lines in dentine (Dean et al., 1993b;Dean, 1995a; Dean and Scandrett, 1996; Smith et al., 2004)relative to the many studies of long-period lines in enamel.This is partially due to the difficulty of imaging Andresen linesfrom the beginning to the end of crown/root formation, as wellas the historically ambiguous nature of periradicular bands(Fig. 1b), which may represent external circumferential mani-festations of long-period lines on the surface of tooth roots(Newman and Poole, 1974; Dean, 1995a, 1999; 2000; Berko-vitz et al., 1998; Smith et al., in press-a). In a comprehensivereview of dentine incremental features, Dean (1995a) inferredthe periodicity of periradicular bands in the roots of OH 16based on their distribution and the expected rates of root exten-sion, and he suggested that periradicular bands were equivalentto other long-period lines (however, Dean [2007a] recentlysuggested that these features should be regarded with caution).Smith et al. (in press-a) provided both indirect and direct evi-dence for the incremental nature of periradicular bands. Thiswas done by identifying similar numbers of long-period linesbetween stress events across crowns and roots of the anteriorteeth of a single individual, and by demonstrating equal num-bers of internal and external features between accentuated linesin a single tooth root.

Correlations between periodicity and number oflong-period lines and body mass

In a large sample of human canines, Reid and Ferrell(2006) demonstrated that there is a significant negative corre-lation between long-period line periodicity and Retzius linenumber (for similar results for all human tooth types, seeGuatelli-Steinberg et al., 2005; Smith et al., 2007a; Reidet al., 2008). Apparently, in populations of living Homo, wherethere is substantial variation in periodicity, the growth periodof imbricational enamel may be constrained to produce teethwithin a certain period of time, although it remains to beseen if the relationship exists in other hominoids.

Dean (1995a) and Dean and Scandrett (1996) suggested thatthere may be a link between long-period line periodicity andbody size based on evidence from monkeys, apes, humans,and elephants. Smith et al. (2003b) examined this in 18 livingand fossil apes and found a significant positive relationship be-tween average periodicity and body mass (tested with separate


dental and skeletal body-mass estimates), and between firstmolar crown formation time and body mass. The former anal-ysis is expanded here to include hominin taxa (for a total ofn¼ 26 species; see Table 2). A highly significant correlationwas found between mean periodicity and body mass amonghominoids (Spearman’s rho¼ 0.794, p< 0.001) (Fig. 3). Thisremains highly significant when hominins are excluded (Spear-man’s rho¼ 0.830, p< 0.001), but is not significant when onlyhominins are considered (Spearman’s rho¼ 0.778, p¼ 0.069).However, when considering primates as a whole, this trendmay not hold, as large-bodied lemurs show very low values(Schwartz et al., 2002). Furthermore, it is difficult to explainthe range of variation in long-period lines within humans andother well-documented hominoids. Additional work is neces-sary to assess relationships among dental development vari-ables and biological variation (i.e., body mass, brain size, life

span), particularly among known-mass individuals and ina broader taxonomic sample of primates.

Extension rate measurement

Quantification of dental microstructure depends on the factthat growth in tissue thickness and height occurs in two ways:in an appositional manner as ameloblasts/odontoblasts moveaway from the EDJ (represented by the number and spacingof short-period lines), and by extension of newly differentiatedameloblasts/odontoblasts along the EDJ from the dentine hornto the future cervix (coronal extension) or from the cervix toroot apex (root extension) (Fig. 4). Extension rate has beenquantified using several indirect and direct methods: (1) mea-surement of the angle of intersection between the developingfront and the EDJ (e.g., Fukuhara, 1959; Boyde, 1964; Beynonand Wood, 1986; Ramirez Rozzi, 1997) or the developingfront and root surface (Dean, 1985); (2) calculation based ontrigonometric developmental models (Gohdo, 1982; Shellis,1984a,b); (3) calculation based on a geometric relationshipof secretion and extension rates (Dean, 2006, 2007b, in press;Macchiarelli et al., 2006; Dean and Vesey, 2008); (4) directmeasurements based on fluorescent labels or long-period linesalong the EDJ or root surface (e.g., Schwartz and Dean, 2001;Smith, 2004; Smith et al., 2004, 2007b); and (5) measurementof the overall rate of crown/root extension based on the heightof the crown, length of the EDJ, or length of the root dividedby the time of formation (e.g., Beynon et al., 1991a; Deanet al., 1993b; Dean, 1995b; Dirks, 1998; Smith et al., 2004,2006a, 2007c).

Boyde (1964) suggested that the angle of intersection be-tween the developing enamel front and the EDJ providesevidence of the differentiation rate of new enamel-formingcells, with smaller angles indicating faster rates (see Fig. 6.3in Boyde, 1964). Ramirez Rozzi (1997) attempted to validatethis approach by comparing angle of intersection in cuspal, lat-eral, and cervical regions with the average spacing between

Fig. 3. Relationship between mean long-period line periodicity and body massamong living and fossil hominoids (excluding the outlier Gigantopithecus).Hominins are represented by open triangles, and living and fossils apes arerepresented by closed circles.

Table 2Body mass and periodicity in living and fossil hominoids

Taxon Age (Ma)1 Mass (kg)2 Periodicity3

n Range Mean

Proconsul major 19e20 63.5 1 w8e9 8.5Proconsul africanus 19e20 27.0 1 w5e6 5.5Proconsul heseloni 17e18.5 10.0 2 5 5Proconsul nyanzae 17e18.5 31.9 2 6 6Afropithecus turkanensis 17e17.5 34.5 2 7e8 7.5Griphopithecus sp. 15.5e16 48 1 8 8Equatorius africanus 15e15.5 28.5 1 9 9Sivapithecus indicus 8.5e12.5 41 1 8 8Sivapithecus parvada 10 83.2 1 9 9Dryopithecus laietanus 9.5e10 26.8 3 6e7 6.3Graecopithecus freybergi 9e9.5 76.8 1 8 8Lufengpithecus hudienensis 7e9 40.0 2 7 7Lufengpithecus lufengensis 7e9 55.0 1 8 8Gigantopithecus blacki 1e0.5 300 1 11 11Pan troglodytes Extant 45.0 61 6e7 6.4Pan paniscus Extant 39.4 2 6e7 6.5Pongo pygmaeus Extant 57.0 24 8e11 9.5Gorilla gorilla Extant 124.5 36 7e10 8.7Hylobates lar Extant 5.6 3 4 4Symphalangus syndactylus Extant 11.3 3 4e5 4.7

Australopithecus anamensis 4.2e3.9 42 2 7 7Australopithecus africanus 3.0e2.4 35.5 6 6e8 7Paranthropus boisei 2.3e1.4 41.5 1 7 7Paranthropus robustus 1.9e1.4 36 8 6e9 7Homo neanderthalensis 0.3e0.03 71 2 7e8 7.5Homo sapiens Extant 62 365 6e12 8.3

1 Age¼ ranges in millions of years (Ma) from Klein (1999) and Hartwig(2002).2 Mass¼ average body mass estimates from dental and postcranial estimates

(for fossils) when possible in kilograms (kg). Dental estimates were calculatedfrom Conroy’s (1987) dental regressions rounded to nearest 0.5 kg (tooth-sizedata from Pilbeam, 1969; Swindler, 1976; Koufos, 1993; Kelley and Plavcan,1998; Kelley et al., 2002), or are from Leakey and Walker (1997). Values de-rived from cranial and postcranial regressions were taken from Rafferty et al.(1995), Moya-Sola and Kohler (1996), Leakey and Walker (1997), McHenryand Coffing (2000), and Kelley (2001). Extant ape body masses were takenfrom Smith and Jungers (1997), as an average of both sexes for all subspeciesof each species.3 For periodicity, number of individuals (n), range of long-period line values

taken from sources in Table 1, and mean of individual long-period line valuesare given (‘‘w’’ represents uncertainty).


Retzius lines at the EDJ (although the periodicity of Retziuslines was unknown in this material). His results showed a gen-eral agreement between the pattern of increasing angles anddecreasing spacing of Retzius lines from the cuspal to cervicalregions, suggesting that trends in the angles of intersectionrepresent trends in the extension rate. Smith et al. (2004)also found that low angles between the developing enamelfront and the EDJ represent rapid extension, provided thatDSR remains constant along the EDJ. However, becauseenamel secretion rates have been shown to decrease fromthe inner cuspal to the inner cervical enamel (near the EDJ),angular values may not be directly comparable among regions.Smith et al. (2004) illustrated this in a fossil hominoid molarby showing an area of enamel (underlying the cingulum)with high angles of intersection formed via rapid extensionand secretion. In this instance, Boyde’s (1964) model wouldhave predicted a low extension rate from the high angles inthis area. This possibility should be considered when makingcomparisons among primates that have different rates of

enamel secretion (also see Smith [2004] for a review of addi-tional factors that influence assessment of extension rate fromangles of intersection).

On the basis of Boyde’s (1964) model of extension, Shellis(1984a,b) proposed a formula to quantify coronal extensionrate using cross-striation repeat interval (DSR), the angle be-tween prisms and the EDJ, and the angle between the develop-ing enamel front and the EDJ. Shellis (1984a,b) applied thisformula to determine crown formation time by summing thetime of extension along the EDJ (discussed below). Smithet al. (2006a) tested the accuracy of Shellis’s formula in exper-imentally labeled macaque teeth and found that this formulatypically overestimated extension rate (and therefore underes-timated crown formation time) in fast-forming teeth. Theyconcluded that additional research should be conducted priorto the continued use of this formula for either extension rateor formation time estimation.

Dean (2006, 2007b) described a novel method for calculat-ing root extension rates based on identification of accentuatedlines in dentine (Owen’s lines) and estimation of the meanDSR (typically assumed to be 2.5 mm/day) in the root dentinebelow the granular layer of Tomes (see Fig. 1 in Dean, 2007b).The advantages of this approach are that it does not rely on in-formation from crown growth (e.g., long-period line periodic-ity), and that it may be applied in areas where incrementalfeatures are indistinct (Dean, 2007b). Successive applicationsalong the root surface of modern human first molars yieldlongitudinal records of root extension rates that are similarto those calculated by other methods (Dean, 2007b). However,this method requires knowledge of the mean dentine DSR, andmakes the assumption that this rate is constant from the ce-mento-enamel junction to the root apex. Dentine DSRs ofless than 2.0 mm/day have been recorded in hominoid enamelnear the cemento-enamel junction/root surface (Dean, 1995a;Dean and Scandrett, 1995; Dean, 1998b; Smith et al., 2004,2007b), and it was found that chimpanzee root extension ratesfor the first 1e2 mm were overestimated by this method whencompared to rates calculated directly from the number andspacing of Andresen lines (Smith et al., 2007b). Additionalsystematic data on dentine DSR within and among hominoidroots would help to establish the accuracy of this approachfor additional taxa.

Another approach to assess extension rates involves tracingeither experimentally introduced labels or long-period incre-ments to the EDJ or root surface, and measuring the distancebetween labels or long-period lines (Schwartz and Dean, 2001;Smith et al., 2004, 2006a, 2007b). Schwartz and Dean (2001)measured the length of EDJ formed for every 20 Retzius lines,and plotted cumulative crown height against formation time,yielding extension rates as the slope of these graphs (seeFig. 4 in Schwartz and Dean, 2001). They also noted that, incontrast to Retzius lines at the EDJ, measurements of corre-sponding perikymata (at the tooth surface) do not yield directinformation on extension rates. Perikymata spacing is influ-enced by both local appositional growth and by the extensionof the advancing enamel-forming front. While these methodsusing known intervals of time may be the most accurate,

Fig. 4. Schematic of a cusp/tooth section illustrating common conventionsused to quantify crown and root formation. Enamel is typically divided intocuspal and imbricational enamel components, separated by the first Retziusline to reach the tooth surface (dashed line). Dentine is divided into coronaland root dentine, separated by the final Andresen line to meet the cervix (dot-ted line). Directions of enamel and dentine formation are indicated by arrows,illustrating the processes of apposition (vertical arrows moving away from thedentine horn) and extension (arrows paralleling the enamel-dentine junctionand root surface).


measurements are limited to labeled samples or sections withclear expression of long-period lines, which are quite rare forthe later stages of root formation.

Finally, several studies have quantified overall extensionrates from the length of the EDJ or root surface divided bythe respective crown or root formation time (determinedindependently). Smith et al. (2004) used data on cusp-specificcrown-formation time to empirically derive an overall coronalextension rate for the Miocene hominoid Graecopithecusfreybergi and subsequently applied this approach to other pri-mates (Smith et al., 2006a, 2007b, in press-a). Beynon et al.(1991a) worked iteratively from the age at death to determineroot extension rates for several developing Gorilla teeth (alsosee Dean and Beynon, 1991; Dirks, 1998). A disadvantage ofquantifying overall extension rates in this manner is the lack ofinformation on rate variation; molar coronal extension beginsrapidly and slows down (Dean, 1998a; Smith et al., 2004),while molar root extension begins slowly, speeds up, andmay fluctuate before apical closure (Dean, 1985, 2000,2006, 2007b; Macchiarelli et al., 2006; Smith et al., 2007b).Therefore, overall extension rates derived from developingEDJs or roots of different lengths (or developmental stages)may not be comparable. As is the case for secretion rate, nu-merous methods have been developed to quantify extensionrate; a number of these approaches would benefit from valida-tion, particularly to assess if data derived from differentmethods are comparable.

Hominoid crown and root extension rates

Fukuhara (1959) presented some of the earliest data on theangle of intersection between the developing enamel front andthe EDJ, which was greatest in anthropoids and hominoidsrelative to other primates. A number of subsequent studieshave presented similar data for living and fossil apes and hu-mans (e.g., Beynon and Wood, 1986; Beynon and Reid, 1995;Beynon et al., 1998b; Ramirez Rozzi, 1997; Ramirez-Rozzi,1998; Ramirez Rozzi, 2002; Smith et al., 2003a, 2004; Lacruzet al., 2006). Beynon and Reid (1995) reported similar patternsamong extant hominoids; angles show an increase from thecuspal enamel to the cervical enamel. This may imply a de-crease in extension rate (but not necessarily), which also cor-responds to the pattern of decreasing DSR towards the cervix.Among fossil hominins and hominoids, variation in angulartrends has been seen from the cuspal to cervical enamel(e.g., Ramirez-Rozzi, 1998; Smith et al., 2003a; Lacruzet al., 2006). A comparison of average angles in two Miocenehominoids suggested that differences exist between buccal andlingual cusps within regions (cuspal, lateral, and cervicalthirds of the crown) (Smith et al., 2003a, 2004). Additional in-formation is necessary on extension-rate variation among cuspand molar types before differences in these angles may befully understood among hominoid taxa.

Empirically derived rates of crown and root extension areknown for few hominoids. Crown extension in the M3 proto-conid of G. freybergi ranged from 14 mm/day to less than3 mm/day, with an overall value of 6 mm/day (Smith et al.,

2004). Smith et al. (2007b) presented overall values for chim-panzee molars in their Table 7, which ranged from 4 to 9 mm/day and were higher in lower molars than in respective uppermolars. Smith et al. (in press-a) presented similar data for twoNeandertal molars, which showed values more similar tochimpanzees than to humans. More data are available on hom-inoid root extension rates (e.g., Beynon et al., 1991a; Dean andBeynon, 1991; Dean, 1995a, 2006; Liversidge, 1995; Dirks,1998, 2003; Moggi-Cecchi et al., 1998; Dean et al., 2001; Kel-ley et al., 2001; Macchiarelli et al., 2006; Smith et al., 2007b;Dean and Vesey, 2008). It appears that anterior teeth typicallyshow higher rates than posterior teeth (Beynon et al., 1991a;Liversidge, 1995; Dirks, 1998; Simpson and Kunos, 1998),and that great apes and most fossil hominins show highervalues than living humans (e.g., Beynon et al., 1991a; Deanet al., 2001; Dean, 2006; Smith et al., 2007c, in press-a,b). Ad-ditional data on crown and root extension rates are neededfrom the beginning to the end of formation, particularly asthis may facilitate nondestructive estimates of crown and/orroot formation time from high-resolution mCT scans of devel-oping material, or possibly from knowledge of tooth crownheight (Dean, 2006, 2007b).

Estimation of crown formation time

Analyses of incremental features may permit accurate esti-mation of crown and/or root formation time, as well as age atdeath in developing material (Antoine et al., 1999; Antoine,2000; Smith, 2004; Smith et al., 2006a). Enamel formationis often divided into cuspal and imbricational components ofthe crown, while dentine may be quantified in the coronal re-gion and/or root (Fig. 4). Several primary methods have beenemployed to estimate crown formation: (1) counts of succes-sive cross-striations (cuspal and/or total crown formationtime); (2) application of extension rate along the EDJ (cuspaland/or total time); (3) division of the prism path length by theDSR (cuspal, imbricational, and/or total time); and (4) estima-tion of cuspal enamel time added to counts of long-periodlines multiplied by their periodicity (imbricational time),which is summed for total time. In the following sections,methods will be reviewed for quantification of the entirecrown, cuspal, and imbricational formation times.

‘‘Whole-crown approaches.’’ Asper (1916) suggested thatcounts of cross-striations provide an accurate determinationof the period of crown formation, which was employed firstby Gysi (1931; see also Boyde, 1963, 1990; Antoine, 2000).However, this method requires sections of exceptional quality(such as the Spitalfields archaeological material used by An-toine), as it is quite rare that successive cross-striations canbe counted from the dentine horn to the tip of the cuspal enamel(Schwartz and Dean, 2001) and along prisms throughout theentire crown. A second ‘‘whole-crown approach’’ was pro-posed by Shellis (1984a,b, 1998), who applied his extension-rate formula to determine the duration of enamel formation,where crown formation time is equal to the sum of times de-rived from segments of the EDJ divided by corresponding ex-tension rates (but see discussion above and Smith et al., 2006a).


Massler and Schour (1941, 1946) suggested that prismlength could be divided by the ‘‘characteristic rate of apposi-tion,’’ or DSR, to determine the time of formation. Beynonet al. (1991a) and Reid et al. (1998a) applied this approachto calculate crown formation times of extant ape teeth (seeFig. 1 in Reid et al., 1998a) and compared these results tothose derived from the more common ‘‘cuspal plus imbrica-tional approach.’’ Reid et al. (1998a) found differences rang-ing from an 8.6% underestimate to a 20.9% overestimate forthe ‘‘rate of apposition approach’’ relative to the alternativemethod. A related method used in recent studies of fossilapes involved division of axial dentine thickness (coronal den-tine directly beneath the dentine horn) by the mean axial den-tine DSR (e.g., Beynon et al., 1998b; Kelley et al., 2001). Themain advantage of this latter method is that it may be appliedto slightly worn teeth, and it is based on dentine tubule paths,which are straighter than cuspal enamel prisms. When com-pared to estimates derived from enamel, this method may yieldsimilar or slightly lower values (Kelley et al., 2001; Smithet al., 2004). Smith et al. (2004) noted that, although thismethod is promising, it is prone to error in oblique sectionsthat do not preserve the actual tip of the dentine horn. Further-more, it is difficult to calculate dentine DSR in the earliest-formed dentine due to the lack of clearly defined incrementalfeatures.

Risnes’s (1986) commonly cited research on enamel prismpath lengths suggests that, due to the three-dimensional (3D)nature of prism paths, formation-time calculation requires anadjustment of the linear enamel thickness with a correctionfactor. Although several early studies applied Risnes’s correc-tion factor to estimations of cuspal enamel formation time,several others have noted that this factor may not be appropri-ate for all hominoids (reviewed in Smith et al., 2003a; see alsoMacho et al., 2003). Hominins or hominoids with fairlystraight prisms paths, such as Paranthropus or G. freybergi,may not require a correction factor (Smith et al., 2004), whileother hominoids may show more marked prism deviation(Dean, 1998a). Additionally, little is known about the variationof prism paths in different regions of the crown, differentcusps in the same tooth, or different tooth types and positions(Shimizu et al., 2005). More work is needed to better under-stand the relationship between the 3D course of a prism andthe linear thickness of enamel (Macho et al., 2003), whichmay be possible with phase contrast X-ray synchrotron micro-tomography (Tafforeau and Smith, 2008).

Cuspal formation time. Cuspal formation time is typicallymore difficult to assess than imbricational formation time,partially due to the lack of developmental features expressedexternally. This difficulty is underscored by the number ofquantitative approaches developed in the past two decades:(1) counts of cross-striations in the cuspal enamel (e.g.,Beynon and Dean, 1987; Dean et al., 1993a; Dean, 1998a);(2) counts of Retzius lines in the cuspal enamel (e.g., Bul-lion, 1987; Dirks, 1998; Ramirez Rozzi, 1998); (3) countsof Andresen’s lines in the corresponding coronal dentine(Smith et al., 2004); (4) cuspal prism path length dividedby average cuspal DSR (e.g., Dean et al., 1993a; Dean,

1998a; FitzGerald et al., 1999); (5) cuspal enamel thicknessdivided by average cuspal DSR (e.g., Reid et al., 1998a,b);(6) axial dentine length divided by dentine DSR (e.g.,Dean, 1998a; Schwartz et al., 2003); and (7) cumulativelength of the cuspal EDJ divided by the local extensionrate (Dean, 1998a).

In addition to these methods, Schwartz and Dean (2001)and Dean et al. (2001) presented regression equations ofenamel thickness against DSR, which have been used to pre-dict cuspal enamel formation time (from cuspal enamel thick-ness). This method can be applied to sectioned teeth withpoor cross-striation visibility or to virtually sectioned materialusing high-resolution mCT (Smith et al., 2006b, 2007c, inpress-a), which may yield accurate linear measurements non-destructively (Olejniczak and Grine, 2006). Given the widerange of linear-thickness values reported for humans andchimpanzees (e.g., Suwa and Kono, 2005; Smith et al.,2007b), this approach yields more precise estimates of cuspalformation time in material that may not be physicallysectioned.

In an important test of four methods for estimating cuspalenamel formation time, Dean (1998a) compared results from(1) direct counts of cross-striations, (2) axial dentine lengthdivided by average dentine DSR, (3) prism length dividedby average enamel DSR, and (4) division of cuspal EDJ lengthby the estimated extension rate. The results of all four methodswere within 5e10% of one another; however, because actualcuspal formation times were unknown, it is not clear whichmethod is the most accurate. In a subsequent test of the accu-racy of crown formation time and age at death estimation,Smith et al. (2006a) found that section obliquity confoundedestimation of cuspal formation time due to inflated thicknessand potentially inflated secretion rates (see also Dean et al.,1993a; Smith et al., 2004). Careful section preparation is es-sential for accurate assessment of cuspal formation time usingany of the methods described above.

Imbricational enamel formation. Numerous studies of fos-sil hominins have estimated the imbricational aspect ofcrown formation time from counts of perikymata at theenamel surface or from Retzius lines in naturally fracturedteeth, as these are nondestructive analytical methods. Oneof the major limitations of this approach is that an individ-ual’s long-period line periodicity must be determined froman internal surface, or an estimated value must be used. Asmall error in the total number of long-period lines may af-fect estimates by a few weeks, but an error in the determi-nation of the periodicity by a single day (cross-striation)may result in a difference of a few months to more thanhalf a year (depending on tooth type). This difference maybe seen when comparing data on chimpanzee molar crownformation times from Reid et al. (1998a) with revised valuesfrom Smith et al. (2007b); misidentification of Retzius lineperiodicity in the former study resulted in overestimated mo-lar formation times. Due to limitations in imaging, equiva-lent long-period lines in coronal dentine are rarely countedto assess corresponding enamel formation (but see Smithet al., 2004).


Hominoid crown formation times

Crown formation times are most commonly reported forextant hominoid canines and molars, partially due to interestin sexual dimorphism and molar enamel thickness. Asidefrom studies of great ape incisors and canines (Dean andReid, 2001; Schwartz and Dean, 2001; Schwartz et al.,2001) and chimpanzee molars (Smith et al., 2007b), histolog-ically derived crown formation times have been described fora maximum of four dentitions per ape species (Beynon et al.,1991a; Dirks, 1998, 2003; Reid et al., 1998a; Schwartz et al.,2006; Ramirez Rozzi and Lacruz, 2007). Schwartz et al.(2006) recently demonstrated a wide range of crown formationtimes in two Gorilla dentitions, and Smith et al. (2007b) foundeven greater variation among common chimpanzee molars.Crown formation times in most fossil and living ape molarsfall within chimpanzee ranges, except for Proconsul heseloniand Hylobates lar, which are at the low end, and Gigantopithe-cus blacki, which is at the high end (reviewed in Table 7 ofSmith et al., 2003a; also see Dean and Schrenk, 2003;Mahoney et al., 2007). The proportion of cuspal to imbrica-tional formation time may yield better distinction among hom-inoids than total molar formation times (Smith et al., 2003a,2004), although this would benefit from further study.

Several researchers have recently established crown forma-tion times for modern humans using histological methods, not-ing that variation exists among populations. Reid and Dean(2006) and Reid et al. (2008) reported crown formation timesin South African and northern European teeth, which showedfairly consistent population differences in anterior teeth andpremolars, but less differences among molars. Smith et al.(2007a) examined only unworn and lightly worn molar sec-tions in a more diverse sample (including that used by Reidand Dean, 2006) and found a number of differences among hu-man populations, emphasizing the need for data from addi-tional modern human populations. When human molars werecompared to equivalent chimpanzee molar and cusp types,Smith et al. (2007a) found that crown formation times weregreater in humans, although some overlap was found. Limiteddata exist for fossil hominin crown formation times; estimatesfor early hominins suggest shorter periods than respectivemodern human teeth (e.g., Bromage and Dean, 1985; Beynonand Dean, 1987; Beynon and Wood, 1987; Dean, 1987b; Deanet al., 1993a; Dean and Reid, 2001; Dean et al., 2001; Lacruz,2007). Beynon and Wood (1987) reconstructed crown forma-tion times in Paranthropus boisei and early Homo, and con-cluded that enamel development in P. boisei shows a patternsimilar to that seen in modern human deciduous teeth, whichmay imply that there was strong selective pressure to growteeth rapidly with very thick enamel (see also Beynon andDean, 1987; Grine and Martin, 1988). Dean et al. (2001) sug-gested that early fossil Homo formation times fall betweenaustralopiths and living Homo. Limited data on Neandertalsappear to indicate greater similarity with modern humancrown formation times than with earlier hominins (e.g.,Mann et al., 1991; Dean et al., 2001; Guatelli-Steinberget al., 2005; Macchiarelli et al., 2006; Guatelli-Steinberg and

Reid, 2008; but see Ramirez Rozzi and Bermudez de Castro,2004; Smith et al., in press-a). Small samples of Early andMiddle Stone Age Homo sapiens show crown formation timessimilar to modern humans (Smith et al., 2006b, 2007c). Inshort, there appears to be a trend for hominin crown formationtimes to increase over the past several million years, as is thecase for hominin brain and body size (e.g., Ruff et al., 1997;McHenry and Coffing, 2000; Skinner and Wood, 2006).

Root formation time, age at death, life history, anddevelopmental chronology

In a similar approach to the calculation of root extensionrates, root formation times have been typically quantified by(1) counts of Andresen lines (Smith et al., 2006a, 2007b);(2) application of extension rate along the root surface (e.g.,Beynon et al., 1998b; Dean, 2006; Macchiarelli et al., 2006);(3) division of tubule length by dentine DSR along successiveroot segments (Smith et al., 2007b); and (4) subtraction of theage at crown completion from the age at death (in developingroots) (e.g., Beynon et al., 1991a; Dirks, 1998; Smith et al.,2007c). Several early histological estimates of hominoid rootformation time came from studies of juvenile dentitions(e.g., Beynon et al., 1991a; Dean and Beynon, 1991; Deanet al., 1992; Dirks, 1998). When an individual dies prior toroot completion, formation is halted (and registered) acrossthe dentition, allowing rates and times to be determined itera-tively with knowledge of age at death, crown formation, andinitiation age. Other studies have used accentuated lines, hypo-plasias, or fluorescent labels to register teeth and estimate theduration of root formation between events (e.g., Dean et al.,1993b; Reid et al., 1998a). As noted above, few studies havequantified root formation time directly from incrementalgrowth due to the difficulty of imaging successive incrementalfeatures in dentine, representing one of the more challengingareas of histological research on teeth.

Boyde (1963, 1990) suggested that histological assessmentsof dental development are more reliable than assessments ofskeletal development for determining the age at death ofyoung individuals, as dental development is less variable.However, he speculated in 1963 that this time-consumingmethod was not likely to find widespread application, whichproved true until the 1980s. In order to accurately assess chro-nological age in hominoids, an accentuated line formed atbirth, known as the neonatal line (Rushton, 1933; Schour,1936), is identified in the first molar, which begins formationapproximately 15e60 days before birth (Beynon et al., 1991a;Dirks, 1998; Reid et al., 1998a,b; Schwartz et al., 2006; Smithet al., 2007b). Chronological age is calculated as the develop-mental time of enamel and root dentine formed after the neo-natal line (provided that the individual has not completed rootformation). An alternative approach to reconstruct age at deathis to estimate the amount of postnatal delay prior to initiationof a specific tooth, adding subsequent crown and root forma-tion time (e.g., Bromage and Dean, 1985; Kelley and Smith,2003; Smith et al., 2007c). Dean (1987a) noted that usingmodern human estimates for initiation ages is likely to lead


to overestimation when applied to fossil hominins that demon-strate a faster period of overall dental development. However,Smith et al. (2007c) noted that this may be less of a problemfor early-forming teeth than for later-forming teeth, as there isless variation among living great apes and humans in the for-mer case. New histological data on crown-initiation ages fromdiverse human populations would be particularly valuable, asthese data have been reported for very few individuals to date(Dean et al., 1993b; Reid et al., 1998b; Antoine, 2000), yet arecrucial to nondestructive studies of fossil hominins.

Bromage and Dean (1985) were the first to apply incremen-tal-feature quantification to assess age at death for severalfossil hominins, suggesting that juvenile Australopithecusafarensis, A. africanus, Paranthropus robustus, and earlyHomo individuals demonstrated developmental stages moresimilar to extant great apes than to modern humans. A numberof studies have subsequently estimated age at death for fossilmaterial (Table 3), as well as for recent human and ape indi-viduals (e.g., Beynon et al., 1991a; Dean and Beynon, 1991;Reid et al., 1998a; Dirks, 1998; Antoine, 2000; Schwartzet al., 2006; Smith et al., 2007b). The results of these investi-gations have led to a dramatic reinterpretation of the timing ofgrowth and development in hominin evolution (e.g., Bromageand Dean, 1985; Beynon and Dean, 1988; Dean et al., 1993a,2001; Dean, 1995a, 2000, 2006; Smith and Tompkins, 1995;Smith et al., 2007c). Dean et al. (2001) demonstrated that earlyhominins showed a more rapid developmental profile (of cus-pal enamel growth) than great apes, and early Homo showeda very similar profile to great apes, suggesting that slow,prolonged developmental processes are a relatively recent evo-lutionary development in human evolution. As noted above,studies of Neandertals are equivocal, and more data are neededto assess if there are differences in mean crown formation

times or ages at molar eruption (Kelley, 2004). Crown calcifi-cation stages and dental eruption patterns in an early Moroc-can H. sapiens juvenile from 160,000 years ago suggeststhat modern human life history may have originated with theadvent of H. sapiens (Smith et al., 2007c), although moredata are needed on incremental development in middle Pleis-tocene hominins (e.g., Bermudez de Castro et al., 2003;Ramirez Rozzi and Bermudez de Castro, 2004).

A number of studies have also used incremental features toprovide insight into life history trends among nonhuman hom-inoids (e.g., Kelley, 1997, 2002; Dirks, 2001; Kelley et al.,2001; Macho, 2001; Kelley and Smith, 2003; Schwartz et al.,2006; Zhao et al., 2008). Macho (2001) suggested that crownformation time is positively correlated with several life-historytraits across primates, although there is some uncertainty aboutthe accuracy of the crown-formation and life-history data usedin this study (Kelley and Smith, 2003). Limited data on age atM1 emergence in Proconsul nyanzae, Afropithecus turkanensis,Sivapithecus parvada, and Lufengpithecus lufengensis suggestthat hominoids with dental developmental schedules similarto those of chimpanzees may have evolved as long ago as theearly Miocene (Kelley, 1997, 2002; Kelley and Smith, 2003;Zhao and He, 2005; Dean, 2006; Zhao et al., 2008).

Beynon et al. (1991a) presented the first use of enamel mi-crostructure for inferring the overall chronology of tooth de-velopment in individual Pongo and Gorilla specimens. Thiswas possible due to the developmental arrest at death, aswell as the presence of hypoplasias and/or tetracycline labelsin all of the teeth. Gustafson (1955) demonstrated that patternsof (nonincremental) accentuated lines in enamel are remark-ably similar in related teeth of the same type (contralateralpairs), allowing identification of an equivalent point in devel-opmental time across the dentition (see also Boyde, 1963,

Table 3Age at death for fossil hominoid specimens, as determined from incremental dental development

Taxon Specimen Age (yrs)* Sources

Afropithecus turkanensis KNMeMO 26 2.2e3.3 Kelley and Smith, 2003Sivapithecus parvada GSP 11536 2.5e4.8 Kelley, 1997Lufengpithecus lufengensis PA 868 2.4e4.7 Zhao and He, 2005; Zhao et al., 2008Australopithecus afarensis LH2 3.3e3.5 Bromage and Dean, 1985; Beynon and Dean, 1988Australopithecus africanus Taung 3.3e3.9 Bromage and Dean, 1985; Lacruz et al., 2005

Sts24a 3.3 Bromage and Dean, 1985Stw151 5.2e5.3 Moggi-Cecchi et al., 1998

Paranthropus robustus SK 62 3.3e3.5 Bromage and Dean, 1985SK 63 3.1e4.5 Bromage and Dean, 1985; Dean et al., 1993a; Dean, 1999

Paranthropus boisei KNM-ER 1477 2.5e3.0 Dean, 1987bKNM-ER 812 2.5e3.0 Dean, 1987bKNM-ER 1820 2.5e3.1 Dean, 1987bOH 30 2.7e3.2 Dean, 1987b

Early Homo KNM-ER 820 5.3 Bromage and Dean, 1985Homo erectus KNM-WT 15000 >8, <12 Dean et al., 2001Homo neanderthalensis Dederiyeh 1 1.4e1.5 Sasaki et al., 2002

Devil’s Tower 3.1e4.4 Dean et al., 1986; Stringer et al., 1990; Stringer and Dean, 1997Hortus II-III 6.5e7.9 Ramirez Rozzi, 2005Scladina 8.0 Smith et al., in press-aObi-Rakhmat 7.2e8.6 Smith et al., in press-b

Homo sapiens Irhoud 3 7.8 Smith et al., 2007c

* Estimates for all specimens, except for SK 63, Dederiyeh 1, Scladina, and Irhoud 3, are based on estimated periodicity values.


1964, 1990; FitzGerald and Saunders, 2005). Since theseinitial studies, numerous studies have used accentuated linesor hypoplasias to establish a developmental chronology amongcusps or teeth within individual dentitions (e.g., Beynon et al.,1998b; Dirks, 1998; Reid et al., 1998a,b; Antoine, 2000;Dirks, 2003; Thomas, 2003; Smith et al., 2004; Schwartzet al., 2006; Smith et al., 2007b, in press-a). This aspect ofhard tissue registry permits more precise estimates of cuspinitiation and completion than is possible using conventionaldissection or radiographic techniques.

Taxonomic applications

Early studies by Fukuhara (1959), Boyde (1963), Shellisand Poole (1977), and Martin (1983) suggested that differentcombinations of incremental and nonincremental featurescould distinguish primates from other mammals, prosimiansand platyrrhines from catarrhines, or among hominoids (butsee Beynon et al., 1991b; Risnes, 1998). As detailed in the pre-ceding sections, recent work has pointed to taxonomic differ-ences in hominoid daily secretion rates, average long-periodline periodicities, long-period line spacing, extension rates,and crown formation times, in addition to differences in prismpaths and Retzius line morphology (e.g., Bromage and Dean,1985; Beynon and Wood, 1986, 1987; Beynon and Dean,1988; Grine and Martin, 1988; Dean and Shellis, 1998; Ram-irez Rozzi, 1998; Dean et al., 2001; Macho et al., 2003; Smithet al., 2003a; Ramirez Rozzi and Bermudez de Castro, 2004;Lacruz and Bromage, 2006; Lacruz et al., 2006; Guatelli-Steinberg et al., 2007a; Mahoney et al., 2007). The studies re-viewed here generally suggest that a combination of features(e.g., secretion rate, perikymata spacing, extension rates, andenamel thickness) may provide the best discrimination be-tween closely related genera, although there are still unre-solved questions about the degree of developmental variationfound within genera and species (e.g., Ramirez Rozzi, 1998;Smith et al., 2003a; Lacruz, 2007). On going and future stud-ies of developmental variation in living apes and humans maybetter inform taxonomic studies by documenting developmen-tal variation throughout the dentition at the level of popula-tions, species, and genera.

Summary and concluding remarks

This paper presents a comprehensive review of methodologyemployed for assessment of enamel and dentine incrementaldevelopment, including daily secretion rate (DSR), long-periodline periodicity and number, extension rate, and crown and rootformation times. Evolutionary studies have benefited from tax-onomic, forensic, and ontogenetic applications of incrementaldevelopment, although data obtained from different methodsare not always comparable. Numerous approaches employedto quantify DSR are reviewed here. It is apparent that enameldaily secretion rate (DSR) differs with crown position, increas-ing from inner to outer enamel and from cervical to cuspal re-gions, and ranging from approximately 2 to 7 mm/day amonghominoids. This variable is fairly similar among hominoids of

differing tooth and/or body size, although cuspal enamel valuesmay distinguish certain hominoids. Known DSR values are alsobroadly similar between enamel and dentine, although addi-tional data are needed from hominoid roots.

Determination of long-period line periodicity is one of themost difficult aspects of quantifying incremental develop-ment, partially due to the requirement of internal featurevisualization. Nondestructive applications of confocal mi-croscopy or phase contrast X-ray synchrotron microtomogra-phy may allow for periodicity assessment in larger numbersof hominin fossils, leading to greater precision in formation-time estimation. Hominoid periodicity values are known torange from 4 to12 days, and from 6 to 12 days within hu-mans. It is demonstrated that long-period line periodicity issignificantly correlated with hominoid body mass, and in hu-mans the former variable is inversely correlated with long-period line number.

As with DSR, numerous methods of quantifying extensionrate have been developed, leading to multiple types of data thatare not necessarily comparable. Approaches involving com-parisons of angles of intersection of the developing enamelfront with the enamel-dentine junction would benefit from as-sessment of variation within and between cusps, along withconsideration of the effects of DSR variation. Both coronaland root extension appear to vary among tooth types; withinmolars, first molars may show higher rates than posterior mo-lars, and lower molars may have higher rates than respectiveupper molars. Given variation in root extension rates, it issuggested that rate comparisons should be made betweenequivalent roots at similar stages of development.

As is the case for long-period line periodicity, estimation ofcuspal enamel formation time has also proven to be relativelycomplicated, and a minimum of eight different approacheshave been developed. Although several of these methodshave been shown to give consistent results with one another,the accuracy of many of these methods has yet to be demon-strated. For imbricational enamel formation (or root formationtime) where it is not possible to assess the long-period line pe-riodicity, it is suggested here that estimates of formation timeshould be based on a range of periodicity values, rather thanupon a single integer. Reports characterizing crown and rootformation times have been limited by a paucity of comparativedata, although recent studies have provided crown formationtimes for the entire dentition of two modern human popula-tions. It appears that crown formation time has increasedthroughout the hominin lineage.

Finally, assessments of age at death, life history, and devel-opmental chronology in developing dentitions are reviewed.Based on estimates of age at death and molar eruption, evidencefrom Australopithecus, Paranthropus, and early Homo suggeststhat modern human life history appeared recently. The earliestevidence for modern human developmental patterns is froma juvenile dated to 160,000 years ago, although little is knownabout hominins from the middle Pleistocene. Additional infor-mation on crown initiation ages is needed, which wouldstrengthen estimates of age at death in hominin and hominoidfossils.


A final goal of this review was to identify ways that futurework may complement and refine our current understandingof the complex process of tooth formation. Additional researchmay include experimental studies on long-period line etiologyand defect formation, particularly as accentuated lines andenamel hypoplasias have been the subject of a number of recentstudies of living and fossil primates (e.g., Guatelli-Steinberg,2001; Thomas, 2003; Guatelli-Steinberg, 2004; Skinner andHopwood, 2004; FitzGerald and Saunders, 2005). Advancesin microscopy and tomography may represent a means to in-creased knowledge of the three-dimensional paths of amelo-blasts and their secretory products (e.g., Radlanski et al.,2001; Tafforeau and Smith, 2008). It is anticipated thathistological studies may continue to assess variation in dailyapposition (Dean, 1998b, 2004) and extension (Smith et al.,2004; Dean, 2007b), which may facilitate more precise nonde-structive studies.

Nondestructive micro-computed tomography (mCT) isproving to be an important methodological addition, yieldingcomplementary insight into tooth structure and development(e.g., Avishai et al., 2004; Skinner et al., 2008), linear enamelthickness (e.g., Suwa and Kono, 2005; Smith et al., 2006b,2007c, in press-a), and extension rates (Smith et al., inpress-a). Smith et al. (in press-a) used mCT for virtual orienta-tion of a tooth crown prior to physical sectioning, facilitatingprecise physical sectioning of rare fossil material. Moreover,advances in X-ray synchrotron microtomographic techniques,which provide a nondestructive means of exploring incremen-tal development (Tafforeau et al., 2007; Smith et al., 2007c;Tafforeau and Smith, 2008), may hold the key to producing ac-curate three-dimensional models of tooth growth, as well asgreater understanding of hominoid evolutionary developmen-tal biology.

Acknowledgements

Special thanks to Don Reid, Lawrence Martin, WilliamJungers, Fred Grine, and Jean-Jacques Hublin for adviceand support. Two anonymous reviewers, Allison Cleveland,Chris Dean, Robin Feeney, Anthony Olejniczak, Bill Kimbel,and Don Reid provided helpful comments on this manuscript.Chris Dean, Gary Schwartz, Jay Kelley, Rodrigo Lacruz, Fer-nando Ramirez Rozzi, and Wendy Dirks provided helpful dis-cussions. Financial support was obtained from the StonyBrook University IDPAS Travel and Research Awards, NSFDissertation Improvement Grant award 0213994, EVANMarie Curie Research Training Network MRTN-CT-019564,and by the Max Planck Society.

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