Age at ﬁrst molar emergence in early Miocene Afropithecus ...bioanth/tanya_smith/pdf/age_at_first_molar.pdf · This is additional evidence to that provided by Sivapithecus parvada

Age at first molar emergence in early Miocene Afropithecusturkanensis and life-history evolution in the Hominoidea

Jay Kelley1*, Tanya M. Smith2

1Department of Oral Biology (m/c 690), College of Dentistry, University of Illinois at Chicago, 801 S. Paulina, Chicago, IL 60612, USA

2Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY 11794, USA

Received 12 July 2002; accepted 7 January 2003

Abstract

Among primates, age at first molar emergence is correlated with a variety of life history traits. Age at first molaremergence can therefore be used to broadly infer the life histories of fossil primate species. One method of determining ageat first molar emergence is to determine the age at death of fossil individuals that were in the process of erupting their firstmolars. This was done for an infant partial mandible of Afropithecus turkanensis (KNM-MO 26) from the w17.5 Ma siteof Moruorot in Kenya. A range of estimates of age at death was calculated for this individual using the permanent lateralincisor germ preserved in its crypt, by combining the number and periodicity of lateral enamel perikymata with estimatesof the duration of cuspal enamel formation and the duration of the postnatal delay in the inception of crownmineralization. Perikymata periodicity was determined using daily cross striations between adjacent Retzius lines in thinsections of two A. turkanensis molars from the nearby site of Kalodirr. Based on the position of the KNM-MO 26 M1 inrelation to the mandibular alveolar margin, it had not yet undergone gingival emergence. The projected time to gingivalemergence was estimated based on radiographic studies of M1 eruption in extant baboons and chimpanzees.

The estimates of age at M1 emergence in KNM-MO 26 range from 28.2 to 43.5 months, using minimum and averagevalues from extant great apes and humans for the estimated growth parameters. Even the absolute minimum value iswell outside the ranges of extant large Old World monkeys for which there are data (12.5 to <25 months), but is withinthe range of chimpanzees (25.7 to 48.0 months). It is inferred, therefore, that A. turkanensis had a life history profilebroadly like that of Pan. This is additional evidence to that provided by Sivapithecus parvada (Function, Phylogeny, andFossils: Miocene Hominoid Evolution and Adaptations, 1997, 173) that the prolonged life histories characteristic ofextant apes were achieved early in the evolutionary history of the group. However, it is unclear at present whetherlife-history prolongation in apes represents the primitive catarrhine pace of life history extended through phyleticincrease in body mass, or whether it is derived with respect to a primitive, size-adjusted life history that was broadlyintermediate between those of extant hominoids and cercopithecoids. Life history evolution in primates as a whole mayhave occurred largely through a series of grade-shifts, with the establishment of fundamental life-history profiles earlyin the histories of major higher taxa. These may have included shifts that were largely body mass dependent, as well asthose that occurred in the absence of significant changes in body mass.! 2003 Elsevier Science Ltd. All rights reserved.

Keywords: Miocene hominoid; dentition; dental eruption; enamel microstructure; primate life history; primate evolution

* Corresponding author. Tel.: +1-312-996-6054; fax: +1-312-996-6044E-mail addresses: [email protected] (J. Kelley), [email protected] (T.M. Smith).

Journal of Human Evolution 44 (2003) 307–329

0047-2484/03/$ - see front matter ! 2003 Elsevier Science Ltd. All rights reserved.doi:10.1016/S0047-2484(03)00005-8

Introduction

Life history is one of the most fundamentalattributes of a species’ biology. The term ‘lifehistory’ encompasses a host of specific traits, but ismost commonly conceptualized in terms of a seriesof growth and maturational phases ultimatelyrelated to the scheduling of reproduction andlifetime reproductive output. These include gesta-tion period, age at weaning, age at sexual maturityand first breeding, interbirth interval, and lon-gevity. Given the importance of life history, it isnot surprising that it has become an importantissue in primate paleobiology. To date, most of thee!ort to reconstruct the life histories of extinctspecies has been focused on the human lineage.However, attempts to reconstruct aspects of thelife histories of extinct non-human primates arebecoming increasingly common (Lee and Foley,1993; Kelley, 1997, 2002; Kelley et al., 2001;Godfrey et al., 2002; Schwartz et al., 2002). Theevolution of primate life histories, and the role oflife history in the adaptive radiations of majorprimate groups, are also beginning to receiveincreasing attention (Charnov and Berrigan, 1993;Kelley, 1997, 2002; Ross, 1998; Godfrey et al.,2001; Macho, 2001).

Among catarrhines, extant apes and Old Worldmonkeys can be characterized as having under-gone life-history divergence; apes have relativelyslow life histories for their body mass whereasmonkeys appear to have relatively fast life historiesfor their mass (Fig. 1; see also Harvey andClutton-Brock, 1985; Watts, 1990; Kelley, 1997).This di!erence is most evident in a comparison ofgibbons and monkeys, as the body mass range ofgibbons (approximately 5–10 kg) falls entirelywithin that of Old World monkeys, and averagemass in the two groups is similar. For the timing ofany given life-history trait in relation to bodymass, gibbons lie above the primate regression linewhile Old World monkeys lie below (Fig. 1). It hasbeen hypothesized that the life-history divergencebetween apes and Old World monkeys had itsgenesis soon after the cladogenesis of the twogroups (Kelley, 1997), which probably took placein the late Oligocene to earliest Miocene (Kumarand Hedges, 1998). This could plausibly be

inferred from the slowed life histories of gibbons,which probably diverged from the great apes in theearly Miocene or early middle Miocene (Cacconeand Powell, 1989), but ultimately this hypothesiscan only be tested in the fossil record.

Importantly, the above hypothesis presumesthat life histories have changed in both thehominoid and cercopithecoid lineages from aprimitive catarrhine condition that was broadlyintermediate, with life-history prolongation inhominoids and acceleration in cercopithecoids.However, it is presently unclear that this presump-tion is warranted, an issue that will be furtherexplored below.

The principal means for inferring the life histo-ries of fossil species has been through the chronol-ogy of dental development. The timing of dentaldevelopment in all mammals is highly correlatedwith ontogeny as a whole; a functioning dentitionmust be in place when an animal is weaned andmust develop in a way that will last for the

Fig. 1. Least squares regression of age at first breeding (months)against average body mass (kg), both log-transformed, in thefollowing extant primate higher taxa (numbers of includedspecies in parentheses): Al, Alouattini (2); At, Atelini (2); Ca,Callitrichinae (3); Cb, Cebinae (3); Ce, Cercopithecinae (6); Co,Colobinae (8); Ho, Hominidae (3); Hy, Hylobatidae (2); In,Indriidae (3); Le, Lemuridae (7). Data on age at first breedingfrom Godfrey et al. (2001) and from K. Strier, personalcommunication, for Brachyteles arachnoides (Atelini); bodymass data from Smith and Jungers (1997). Body masses areaverages of male and female means for the included species.Results are unchanged using female mass rather than averagemass.

J. Kelley, T.M. Smith / Journal of Human Evolution 44 (2003) 307–329308

projected lifetime of the individual. The linkbetween dental development and ontogeny is evi-denced by the correlations between aspects ofdental development and individual life-historyvariables (Smith, 1989, 1991, 1992). Dental devel-opment is, in a sense, just another life-history trait(Smith and Tompkins, 1995), but one that ispreserved in the fossil record. While there issystematic variation in the relationship betweendental development and various life-historyattributes, primarily associated with variation indiet (Godfrey et al., 2001), as well as occasionalidiosyncratic variation associated with specificecological demands (Godfrey et al., 2002;Schwartz et al., 2002), within a broad frameworkthe pace of dental development serves as a reliableproxy for the pace of life history as a whole.Among living primates, it has been demonstratedthat age at first molar emergence is a particularlygood correlate of various life-history traits (Smith,1989, 1991), emergence being defined as the initialpenetration of the oral gingiva by the molar cusps.Thus, if the average age at first molar emergencecan be established for a fossil species, then itsgeneral life-history profile can be characterized aswell.

The most straightforward approach to estimat-ing age at first molar emergence in fossil species isto determine the age at death for individuals thatdied while in the process of erupting their firstmolars, making necessary adjustments if thestage of eruption di!ers from that associated withgingival emergence. Ages at death can be deter-mined with a high degree of precision using therecord of incremental growth lines that are pre-served in all teeth, including fossilized teeth(Boyde, 1963; Bromage and Dean, 1985; Deanet al., 1986, 1993b; Dean, 1987a, 1989; Beynonet al., 1991; Macho and Wood, 1995; Kelley, 1997,2002; Dirks, 1998; Antoine et al. 1999).

To date, age at first molar emergence has beendirectly calculated for only two fossil apes. Thefirst was an individual of Sivapithecus parvadafrom a 10 Ma locality in the Siwaliks of Pakistan.This individual was found to have an age at firstmolar emergence that was well within the range ofextant chimpanzees, probably equal to or slightlygreater than the chimpanzee mean (Kelley, 1997,

2002). However, the relatively late date for S.parvada limits its usefulness as a meaningful testof the hypothesis of an early life-history diver-gence between apes and monkeys in the latestOligocene.

The second fossil ape was an individual ofAfropithecus turkanensis from the early Miocene ofKenya (Kelley, 1999, 2002). In the following analy-sis we revise the earlier estimate of age at firstmolar emergence for this individual, which waspreliminary and lacked a full description of themethods of analysis. The revised estimates re-ported here incorporate new data on molar crownformation in Afropithecus (see also Smith et al.,2003) and a more thorough and rigorous analysisof relevant comparative data. Knowing the age atfirst molar emergence in Afropithecus is importantbecause it nearly doubles the antiquity of suchestimates for fossil apes, approaching the esti-mated date of divergence of apes and Old Worldmonkeys. In addition, this analysis providesfurther data for the documentation of dentaldevelopment in fossil apes, which complementsinformation on developmental chronology andcrown formation times derived from histologicalstudies (Beynon et al., 1998; Zhao et al., 2000;Kelley et al., 2001; Smith et al., 2001, 2003;Schwartz et al., in press).

Materials and Methods

The Afropithecus specimen used in this analysisis KNM-MO 26, a partial right mandibular corpusof an infant from the site of Moruorot in Kenya(Fig. 2). Moruorot lies in the Lothidok Range westof Lake Turkana, approximately 10 km southeastof Kalodirr, the site from which most remains ofAfropithecus have been recovered (Leakey et al.,1988; Leakey and Walker, 1997). The Moruorotlocalities lie within the lower part of the KalodirrMember of the Lothidok Formation and thereforedate to approximately 17.5 Ma (Boschetto et al.,1992), or late early Miocene.

KNM-MO 26 preserves the deciduous fourthpremolar (dP4) and first molar (M1), as well as thepermanent lateral incisor (I2), canine (C) andpremolar (P) germs within their crypts (Figs. 2

J. Kelley, T.M. Smith / Journal of Human Evolution 44 (2003) 307–329 309

and 3). The M1 was in the process of eruptingwhen the individual died, with the cusp apiceslying just superior to the mandibular alveolarmargin. The alveolar bone mesial to the I2 germwas broken away, exposing the tooth within itscrypt surrounded by a hardened matrix. Thematrix within the crypt was carefully removed witha dental pick and needle probe, exposing much of

the labial and lingual surfaces of the tooth and themesial aspect of the crown apex.

Calculating age at death

Age at death for the individual representedby KNM-MO 26 can be determined using theI2 germ, which was still developing when the

Fig. 2. Infant mandible of Afropithecus turkanensis (KNM-MO 26) from Moruorot, Kenya, showing the erupting M1 and the I2 germwithin its crypt; (a) lingual, (b) occlusal.


individual died (the incisor crowns are still devel-oping when the first molar emerges in most higherprimates). Age at death is calculated by adding thetime that elapsed between birth and the inceptionof I2 crown mineralization (postnatal delay) to theduration of crown formation up until the time ofdeath.

Crown formation time is determined using theincremental growth lines preserved in the enamel.The use of incremental growth lines for determin-ing ages at death in infants is discussed in detail inBoyde (1963), Bromage and Dean (1985), Deanet al. (1986, 1993a,b), Dean (1987b), Beynon et al.(1991), Kelley (1997), Antoine et al. (1999), andRamirez Rozzi (2002) and will be only brieflyreviewed here. Enamel incremental lines includeboth short-period lines known as cross-striations,which record daily increments of enamel depo-sition, and long-period lines known as striae ofRetzius or Retzius lines, which record brief,periodic disruptions in ameloblast secretion acrossthe entire developing enamel front. Retzius lineperiodicity, which is the number of daily cross-striations between Retzius lines, is constant withinall teeth of an individual, but varies to some extent

among individuals within a species (Dean,1987a,b, 1989; Dean and Beynon, 1991; Beynonet al., 1991; Dean et al., 1993a; FitzGerald, 1998;Schwartz et al., 2001). The surface manifestationsof the Retzius lines are known as perikymata,which have, therefore, the same periodicity as theRetzius lines (Fig. 4).

Crown formation time in teeth that have notcompleted their development is calculated as thesum of the time required to form the cuspal enamelplus the time to form the amount of lateral enamelpresent at the time of death. Cuspal enamel is theearliest formed enamel, in which successive Retziuslines are completely buried under subsequentlyformed enamel. Lateral enamel is defined as theenamel formed subsequent to the first Retzius linethat reaches the crown surface (see illustrations inBromage and Dean, 1985; Beynon and Wood,1986; Macho and Wood, 1995; Ramirez Rozzi,2002; Smith et al., 2003).

It was not possible to section the teeth ofKNM-MO 26 to directly observe histologicalstructures. Therefore, values for certain growthparameters listed above had to be estimated fromstudies of dental development in extant apes

Fig. 3. Radiograph of KNM-MO 26.


and other fossil primates, and from informationderived from a histological study of two Afro-pithecus molars (see Smith et al., 2003). For eachof the growth parameters there is both intra andinterspecific variation. Thus, several estimates ofage at death and age at M1 emergence werecalculated for KNM-MO 26, using combinationsthat incorporated conservative minimum values, aswell as average values. The estimates of age at M1emergence reported here therefore include a mini-mum estimate, as well as a range of more probableestimates, since it is improbable that any oneindividual will express the minimum known valuesfor all growth parameters. We also calculated asingle maximum estimate for age at M1 emergenceusing the maximum known values for each esti-mated growth parameter. Specific issues pertainingto the estimates or calculations of each of thegrowth parameters are discussed below.

Postnatal delay in the inception of I2mineralization

To estimate the postnatal delay in theKNM-MO 26 I2, we compiled comparative data

on I2 postnatal delay from all extant apes andhumans for which histological data were available[histological and radiological determinations of theinception of mineralization can di!er substan-tially, with histological determination being moreaccurate (Beynon et al., 1998; Reid et al.,1998a,b)]. Comparable data were also available forthe I2 of Proconsul heseloni (Beynon et al., 1998), apossibly closely related contemporary of Afro-pithecus (Begun et al., 1997; Leakey and Walker,1997; Harrison, 2002).

Duration of cuspal enamel formationThis growth parameter also had to be estimated

from published values for extant apes and humans,and for P. heseloni, since the I2 of KNM-MO 26could not be sectioned for direct observation.Cuspal enamel formation time is related to enamelthickness, although the relationship between thetwo will vary among species depending uponameloblast secretion rates and the degree ofsinuosity of the enamel prisms as they course fromthe enamel-dentine junction (EDJ) to the toothsurface (Dean, 1998). As stated above, the cuspal

Fig. 4. Naturally fractured surface of the lateral enamel of an Afropithecus turkanensis molar (KNM-WK 24300, RM2) showing striaeof Retzius meeting the surface of the enamel and forming perikymata. Note that perikymata only form where striae of Retzius reachthe tooth surface. The cervix of the tooth is below the bottom right edge of the image. The field width of the image is approximately750 µm.


enamel thickness of the KNM-MO 26 I2 isunknown. While cuspal enamel thickness and theduration of cuspal enamel formation have beencalculated for two A. turkanensis molars (Smithet al., 2003), it cannot be assumed that incisorcuspal enamel will have the same values (Dean andReid, 2001).

Duration of lateral enamel formationThis value is calculated by multiplying the

number of perikymata times the periodicity(number of cross-striations between Retzius lines).To obtain a count of the perikymata on theKNM-MO 26 I2, the tooth was molded within itscrypt using Coltene" President Plus RegularBody, and a replica made using Ciba-GeigyAraldite" GY 506 epoxy resin cured withhardener HY 956. The replica was then sputter-coated with a thin layer of gold-palladium andexamined with a JEOL scanning electron micro-scope. A photo montage was constructed of themesio-labial tooth surface from the developingcervical region to a point near the crown incisaledge.

Perikymata were not expressed over the apical2.5 mm of the I2 crown, due to a combination ofpost-depositional chemical weathering or abrasionand a true fading out of perikymata expressionover the apical-most portion of this interval. Thelatter is most likely due to the acute angle ofincidence of the Retzius lines to the tooth surfaceapically, which sometimes results in the non-expression of perikymata for the apical-mostRetzius lines of lateral enamel. A similar trend inperikymata expression was seen in the two Afro-pithecus molars reported on by Smith et al. (2003).Even when there are no apical perikymataexpressed, histological sections of hominoidpermanent anterior teeth demonstrate that thefirst Retzius line reaching the tooth surface(delineating cuspal from lateral enamel) is invari-ably near the incisal edge (C. Dean, personalcommunication). Thus, the number of Retziusintervals in the apical-most 2.5 mm of theKNM-MO 26 I2 crown had to be estimated. Thiswas done using perikymata counts over the sameinterval in two lower lateral incisor crowns of P.heseloni and P. nyanzae (Beynon et al., 1998,

Appendix 1), combined with the spacing ofperikymata adjacent to the non-expressed regionon the KNM-MO 26 I2.

The periodicity of Retzius lines was determinedin two Afropithecus molars that were sectioned aspart of a separate study on enamel thickness andmicrostructure (Smith et al., 2003), using twomethods described by Dean et al. (1993a,b) andSwindler and Beynon (1993). Where possible,direct counts of the number of cross-striationsbetween adjacent Retzius lines were made by usingboth scanning electron and polarized light micro-scopic images. Additionally, the average spacingbetween Retzius lines was divided by the averagespacing of cross-striations measured from prismsin the same area, and the number rounded to thenearest whole integer (see Smith et al., 2003 fordetails of specimen preparation and methodology).

Estimating age at gingival ermergence of M1based on age at death

As previously noted, the individual representedby KNM-MO 26 died before the erupting M1would have emerged from the gingiva. Sincegingival emergence is the standard for comparisonof age at M1 eruption among extant species, theage at which this would have occurred inKNM-MO 26 must be estimated. This was doneusing comparative data on M1 emergence in extantbaboons, and compared to results from a previousstudy on chimpanzees (Zuckerman, 1928).

From June, 1995 through June, 1999 the seniorauthor carried out a longitudinal radiographicstudy of M1 emergence and root formation on acaptive breeding colony of Papio anubis housedat the Biological Research Laboratories at theUniversity of Illinois at Chicago. Approximatelyevery three months, all of the baboons in thecolony were sedated for TB testing. While undersedation, all infant individuals between approxi-mately one and three years of age were given oralexaminations, and periapical x-rays were taken ofthe M1 and lower deciduous premolars.

On several occasions, examination coinci-dentally occurred either just as the M1 mesial cusps(the first to present) were emerging from thegingiva, with emergence clearly having taken place


within the preceding few days, or when the M1mesial cusps were visible beneath a thin layer ofgingival tissue, from which it was determined thatgingival emergence was imminent. For four ofthese individuals, there was a radiographic recordof previous examinations that could be used toestimate the time interval between gingival emer-gence and the developmental stage equivalent tothat of the KNM-MO 26 individual when it died;that is, with the M1 cusp apices just above themandibular alveolar margin.

Similar, although less precise, data on M1eruption and gingival emergence were reported fortwo infant chimpanzees by Zuckerman (1928).

Results

Postnatal delay in the inception of I2mineralization

Data on the postnatal delay in I2 mineralizationin extant apes and humans, and in P. heseloni, areshown in Table 1. Values among extant apes andhumans range from 0 to 13.0 months, with a meanof 6.6 months. Based on these limited data, thereare no obvious associations between the durationof the postnatal delay in mineralization and eitherbody size or phylogeny, although the two highestvalues are most likely the males of the two largestextant apes. Where there are data on intraspecificvariation it appears to be substantial; for example,there is more than an eight month di!erence

between the earliest and latest onsets among threehuman I2s. These data make it di"cult to establishany criteria by which to choose the most appropri-ate estimate for the postnatal delay in theKNM-MO 26 I2. Therefore, in keeping with ourmethodological protocol, we selected the minimumand average values of 0 and 6.6 months, respec-tively, as estimates for the Afropithecus infant.

Duration of cuspal enamel formation

Data on the duration of I2 cuspal enamelformation in extant apes and humans, and in P.heseloni, are shown in Table 2. Values for extantapes and humans range between 4.0 and 8.0months, with a mean of 6.0 months. Both intra-specific and interspecific variation for the durationof cuspal enamel formation are substantially lessthan for the postnatal delay in I2 mineralization.

Duration of lateral enamel formation

The labial face of the KNM-MO 26 I2 preserves82 perikymata (Fig. 5). Perikymata are expressedfrom within about 2.5 mm of the crown apex downto the last formed immature enamel close to theadvancing cervical line.

Our estimate of the number of Retzius linesunexpressed as surface perikymata over the apical-most 2.5 mm of lateral enamel is based in part onthe number of perikymata over the same part of

Table 1Postnatal delay in the inception of I2 mineralization inProconsul heseloni and extant hominoids

Species Months Source

Proconsul heseloni 1.5 Beynon et al., 1998Hylobates lar 3.7 Dirks, 1998Gorilla gorilla 11.0 Beynon et al., 1991Pan troglodytes 2.5 Reid et al., 1998a

7.9 Reid et al., 1998a8.4 Reid et al., 1998a

Pongo pygmaeus 13.0 Beynon et al., 1991Homo sapiens 0 Dean and Beynon, 1991

4.8 Reid et al., 1998b8.3 Dean et al., 1993a

Table 2Duration of I2 cuspal enamel formation in Proconsul heseloniand extant hominoids

Species Months Source

Proconsul heseloni 4.0 Beynon et al., 1998Hylobates lar 4.5 Dirks, 1998Gorilla gorilla 4.0 Beynon et al., 1991Pan troglodytes 5.3,6.4† Reid et al., 1998a

5.8 Reid et al., 1998a6.0,6.8† Reid et al., 1998a6.4 Reid et al., 1998a

Homo sapiens 5.5 Reid et al., 1998b5.8 Reid et al., 1998b

7.0,7.7† Reid et al., 1998b8.0 Reid et al., 1998b

†Antimeres from the same individuals.


the crown in P. nyanzae and P. heseloni. Startingfrom the incisal edge, perikymata counts in 1 mmincrements over the apical 3.0 mm of the crown ofa P. nyanzae I2 (KNM-RU 1716) are 2, 8 and 8;the same values in an I2 of P. heseloni (KNM-RU7290) are 8, 11 and 13 (Beynon et al., 1998).Eliminating half of the perikymata over thecervical-most 1 mm increment (to equal 2.5 mm)results in totals of 14 and 26 perikymata over thisinterval, with a mean of 20. We thus used 14 as ourconservative estimate and 20 as an average esti-mate of the number of unexpressed perikymata inthe apical 2.5 mm of lateral enamel in the Afro-pithecus I2. The total number of perikymata pluslateral enamel Retzius lines not expressed asperikymata in the KNM-MO 26 I2 was thereforeestimated to be 96 or 102 (82 plus either 14 or 20).

Perikymata on the Afropithecus I2 itself suggestthat the higher estimate is likely to be closer to theactual value. The apical-most 1 mm of theKNM-MO 26 I2 crown over which perikymata areexpressed (adjacent to the non-expressed region)contains 12 or 13 perikymata. Since perikymataspacing over the entire labial crown surface ishighly uniform (see Fig. 5), it seems likely thatperikymata numbers closer to those of the P.heseloni incisor would have been present in theAfropithecus I2 as well.

The Retzius line periodicities in the two sec-tioned Afropithecus molars were determined to be7 and 8 days, respectively (Fig. 6; see also Smith etal., 2003). Multiplying these values by the lateralenamel perikymata estimates of 96 and 102 givesan estimated range for the duration of lateralenamel formation in the KNM-MO 26 I2 ofbetween 672 days (22.2 months) and 816 days(26.9 months) (Table 3).

Age at death of KNM-MO 26

A range of estimates of the age at death for theKNM-MO 26 individual using the calculated andestimated growth parameters detailed above isshown in Table 3. Two sets of estimates are given,one using the minimum values for the growthparameters estimated from extant apes and Pro-consul species, and the other using average values.The minimum estimates, using 7 and 8 day Retzius

Fig. 5. SEM montage of the mesio-labial face of the KNM-MO26 Afropithecus I2 showing the development of perikymata. Theinterval over which perikymata are expressed equals 5.8 mm.Cervical is toward the bottom.


line periodicities, are 26.2 and 29.4 months. Usingthe average values for the estimated growthparameters results in estimated ages at death of34.8 to 39.5 months, also based on 7 and 8 dayRetzius line periodicities.

Time from death to M1 emergence inKNM-MO 26

Our estimate of the time interval between thedevelopmental stage of KNM-MO 26 at the time

of death and the eventual time of M1 emergence isbased on the progression and timing of first molareruption in extant baboons and chimpanzees.

In all four of the baboons for which M1 gingivalemergence was observed, the radiograph takenthree months prior reveals the M1 mesial cusps tobe at or just below the level of the alveolar margin(Figures 7 and 8). This is a slightly earlier eruptionstage than had been reached by the KNM-MO 26individual when it died, in which the M1 cuspapices are just above the alveolar margin (Figs. 2

Fig. 6. Polarized light micrograph of the outer lateral enamel of Afropithecus turkanensis (KNM-WK 24300, RM2). The surface of thetooth is at the right and the cervix is toward the bottom. Enamel prisms are shown running from left to right, with striae of Retzius(large white arrows) and cross-striations (small white arrows) crossing the prisms. The periodicity of adjacent Retzius lines is eightcross-striations, each representing one daily increment of enamel deposition. Note that there are seven cross-striations between Retziuslines, the eighth being on the Retzius line. The field of width of the image is approximately 155 µm.


and 3). Judging by the amount of tooth movementthat took place in the four baboons during thethree month interval between the first x-ray andgingival emergence (Figures 7 and 8), we estimatethat the small di!erence in the M1 eruption stagebetween KNM-MO 26 and the four baboons atthe time of the first x-ray corresponds to at mostone month. According to the baboon eruptionschedule, therefore, KNM-MO 26 would havedied approximately two months prior to gingivalemergence. While the eruption schedules in thesecaptive baboons may be somewhat acceleratedcompared to those of wild baboons (see data inTable 5; also Phillips-Conroy and Jolly, 1988), thepercentage di!erence is not likely to be significantfor the time interval being discussed here of only afew months (see further below).

Zuckerman (1928) presented similar oralexamination and radiographic data on twoinfant chimpanzees, which, as expected, suggest asomewhat slower M1 eruption schedule than inbaboons. The data for one animal in particular,Clarence, are su"ciently precise for comparisonwith the baboon results described above. An initialradiograph revealed the M1 “crown” to be levelwith the alveolar margin, which we interpret tomean that the cusp apices were at the alveolarmargin. In a second radiograph six months laterthe M1 was described as being “fully erupted,”which presumably means that the tooth was levelwith the occlusal plane of the deciduous premo-lars. An oral examination was made sometimebetween five and six months after the first radio-graph was taken and revealed that the M1s “werecutting the gums” (Zuckerman, 1928, p. 25).Taken together, these observations suggest that the

interval between M1 cresting the alveolar marginand gingival emergence probably takes somewherebetween four and five months in chimpanzees, incontrast to the three months that it takes inbaboons.

Combining the baboon and chimpanzee data,the additional time that would have been needed toachieve M1 gingival emergence in the KNM-MO26 infant can be estimated to be between abouttwo and four months. Adding two and fourmonths to each of the estimates of the age at deathof KNM-MO 26 produces minimum estimates forthe age at M1 emergence of 28.2 and 31.4 monthsusing the baboon schedule of M1 eruption (basedon 7 and 8 day Retzius periodicity, respectively),or 30.2 and 33.4 months using a chimpanzeeschedule (Table 4). Estimates of age at M1 emer-gence using average rather than minimum valuesfor estimated I2 crown growth parameters rangebetween 36.8 and 43.5 months. Although notincluded in the various calculated estimates, themaximum estimated age at M1 emergence inKNM-MO 26 using the maximum values of allestimated growth parameters, combined withthe highest estimate of missing lateral enamelperikymata (26) and an 8 day periodicity, is 53.4months. Since the principal concern of this studywas to determine whether or not age at M1 emer-gence in the KNM-MO 26 individual was earlierthan in extant chimpanzees, the maximum esti-mate will not be discussed further. We simply notethat it is equally unlikely that one individual woulduniformly express the maximum known valuesof all the estimated growth parameters as thatit would uniformly express all the minimumvalues.

Table 3Estimated ages at death in KNM-MO 26 (months)

Retzius periodicity I2 postnatal delay I2 cuspal enamel I2 lateral enamel Age at death

Minimum 7 0.0 4.0 22.2–23.6 26.2–27.68 0.0 4.0 25.4–26.9 29.4–30.9

Average 7 6.6 6.0 22.2–23.6 34.8–36.28 6.6 6.0 25.4–26.9 38.0–39.5

Retzius periodicity in days; all other values expressed in months. Age at death equals the sum of the I2 postnatal delay, thecuspal enamel formation time and the lateral enamel formation time. The ranges for the duration of I2 lateral enamel formationreflect the use of either 96 or 102 lateral enamel perikymata (see text). Minimum and average estimates explained in text.



Figures 7 and 8. Periapical radiographs of the mandibular deciduous premolars and erupting M1 in two infant Papio anubis, Nos. 6216(Fig. 7) and 6219 (Fig. 8), housed at the Biological Research Laboratories, The University of Illinois at Chicago. For both individuals(a) was taken 6/24/96 and (b) was taken 9/25/96, the latter coincident with the initial gingival emergence of the first cusp as revealedby oral examination.


Discussion

Age at first molar emergence and life history inAfropithecus

While the minimum estimate for age at M1emergence in KNM-MO 26 presented here is onlyslightly later than previously reported for thisindividual (Kelley, 1999, 2002), the other newlycalculated estimates greatly extend the range intowhich the actual age probably falls. This extendedrange is partly due to the addition here of actualdata on Retzius line periodicity in A. turkanensis,which is greater than the estimated value used inthe earlier reports. It also reflects increases in theestimates for the duration of incisor cuspal enamelformation and the postnatal delay in incisormineralization, based on a more thorough analysisof the comparative data from extant species.

The estimates for the age at M1 emergence inKNM-MO 26 (28.2–43.5 months) fall within therange of Pan troglodytes (25.7–48.0 months), andencompass the chimpanzee mean of 38.9 months(Table 5). The means of the range of estimatesusing baboon and chimpanzee schedules of M1eruption are, respectively, 34.9 and 36.9 months.What is most important from our perspective,however, is that even the absolute minimum esti-mate of 28.2 months is well outside the ranges ofM1 emergence of even the largest extant cerco-pithecids for which there are reliable data, themaximum age being less than 25 months (Table 5).

Most of the comparative data in Table 5, how-ever, are from captive animals. As noted by Smithet al. (1994), data are equivocal regarding thedegree to which wild and captive populationsmight be expected to di!er in their dental eruption

schedules. Phillips-Conroy and Jolly (1988)reported that the eruption schedules of captivebaboons were accelerated compared to those ofwild-living animals, but neither Kahumbu andEley (1991) nor Iwamoto et al. (1987) found anysystematic di!erences between wild and captivepopulations of, respectively, baboons andmacaques. The baboon data in Table 5 tend tosupport accelerated dental development and erup-tion in captive animals. Of the two Papio anubis

Table 4Estimated ages at M1 emergence in KNM-MO 26 (months)

Retzius periodicity Age at death Age at M1 emergence (baboon model) Age at M1 emergence (chimpanzee model)

Minimum7 26.2–27.6 28.2–29.6 30.2–31.68 29.4–30.9 31.4–32.9 33.4–34.9

Average 7 34.8–36.2 36.8–38.2 38.8–40.28 38.0–39.5 40.0–41.5 42.0–43.5

Retzius periodicity in days; all other values expressed in months. Age at death estimates from Table 3. The baboon model addstwo months to the age at death while the chimpanzee model adds four months (see text for explanation). Minimum and averageestimates explained in text.

Table 5Age at M1 emergence (months) in Afropithecus turkanensis,Pan troglodytes and extant cercopithecids

Afropithecus turkanensis† 28.2–43.5Extant species Mean Minimum MaximumPan troglodytes 39.1 25.7 48.0Macaca mulatta 16.2 12.5 22.6M. fascicularis 16.4 14 20M. nemestrina 16.4 – 18.6+M. fuscata 18.0 – <24Cercopithecus aethiops 10.0 7.9 12.0Papio anubis 1 20.0 >16 <25P. anubis 2 16.7 15.7 <21

Sources: Pan troglodytes (Smith et al., 1994); Macacamulatta, Cercopithecus aethiops (Hurme and van Wagenen,1961); Macaca fascicularis (Bowen and Koch, 1970); Macacanemestrina (Swindler, 1985; B.H. Smith, personalcommunication—based on Swindler data); Macaca fuscata(Smith et al., 1994; B.H. Smith, personal communication—based on data in Iwamoto et al., 1987); Papio anubis 1 (Smithet al., 1994; B.H. Smith, personal communication—based ondata in Kahumbu and Eley, 1991); Papio anubis 2 (J. Kelley,unpublished data from a longitudinal study of M1 eruptionin a captive colony at The University of Illinois at Chicago).Reliability of range data for extant species varies dependingon methodology and sample size.

†Range of estimates.


populations reported upon in Table 5, P. anubis 1was a wild population whereas P. anubis 2 is thebreeding colony at The University of Illinois atChicago. The mean percent acceleration in the ageat M1 emergence in the captive population is16.5%, but, as noted by Iwamoto et al. (1987), thismay simply reflect genetic di!erences betweenthese two particular populations, rather thana systematic e!ect to be expected from allwild-captive comparisons.

Importantly, with respect to interpretation ofKNM-MO 26, it is still the case that the upperlimit of the cercopithecid range data is for the wildP. anubis population. Given the broad relationshipwithin higher taxa between body size and life-history variables (including dental development), itis likely that the wild P. anubis maximum fromTable 5 is near the upper limit of the range of atM1 emergence ages for all cercopithecoids.

While it is possible that KNM-MO 26 repre-sents an individual that is near the maximum ofthe A. turkanensis range of M1 emergence ages, it ismore probable as a simple consequence of centraltendency that it is closer to the species mean. Toproduce a mean age of M1 emergence in A. turka-nensis that is within the cercopithecid range, andtherefore outside the chimpanzee range, wouldrequire that, (1) the minimum estimate for age atM1 emergence in KNM-MO 26 is the closest of thevarious estimates to the actual age, and (2) thateven this age is near the maximum for the speciesas a whole. This is a possible, but much lessprobable, set of circumstances, we conclude,therefore, that even though our analysis is for asingle individual, the mean age of M1 emergence inA. turkanensis was within the range of extantchimpanzees, and perhaps close to the chimpanzeemean.

As noted earlier, among primates, age at M1emergence is correlated with a variety of life-history attributes (Smith, 1989, 1991; also Fig. 9).Because these analyses encompass species repre-senting all major groups of extant primates, age atM1 emergence can be used to infer life history infossil primates that lie within the extant primateradiation. The strength of the M1 emergence-lifehistory relationships show that M1 emergence datacan legitimately be used to generally categorize the

life histories of fossil species, for example as OldWorld monkey-like, ape-like or human-like. How-ever, the correlations between life-history variablesand M1 emergence in extant primates are insu"-ciently robust, and the errors in estimates of age atM1 emergence in fossil species are too large, toreliably calculate the values of specific life-historyvariables in fossil species based solely on estimatesof age at M1 emergence (see Smith et al., 1995;Smith, 1996). The estimated age at M1 emergencein KNM-MO 26, and the implications of thisestimate for characterizing age at M1 emergence inA. turkanensis as a whole, suggest that life historyin this early hominoid can be broadly character-ized as having been like that of living great apes.

First molar emergence and life-history evolution inHominoidea and other primates

In the following discussion of life-history evolu-tion, age at M1 emergence is used as a substitute orproxy variable for the overall pace of life history.There are several reasons for doing this rather thanusing the specific life-history traits with which ageat M1 emergence is correlated, and that more

Fig. 9. Least squares regression of age at weaning against age atM1 emergence, both in months and log-transformed, for 20extant non-human primate species. Included species are thosefrom Table 6, with the following exclusions because of a lack ofweaning age data: Cheirogaleus medius, Galago senegalensis,Macaca fuscata, and Homo sapiens. Age at weaning fromGodfrey et al. (2001); age at M1 emergence from Smith et al.(1994).


directly reflect reproductive and maturationalmilestones. First, in many species, average age atM1 emergence is known more reliably than are theaverage values for many other life-history vari-ables. Second, it is likely that there is more facul-tative intraspecific variation in reproductive andmaturational traits than there is in age at M1emergence. Plasticity in life-history traits, evenover the course of individual life spans, appears tobe an important aspect of life-history adaptation.Such plasticity is not likely to be reflected in dentaldevelopment. Finally, at present, M1 emergence isone of only two or perhaps three variables (theothers being brain size and possibly molar crownformation time) by which extinct species can beincluded in discussions of life history.

Regarding molar crown formation, a recentstudy by Macho (2001) demonstrated that, withinprimates as a whole, both M1 crown formationtime and average molar crown formation time aresignificantly correlated with a number of life-history traits. However, there are a number ofreasons for withholding judgment on these results.Among these are the use of the primate life-historydata compiled by Harvey and Clutton-Brock(1985), much of which is now known to be either inerror or at least unreliable (see, for example, Smithet al., 1995 and Smith and Jungers, 1997). More-over, many of the crown formation times inMacho’s study are calculated estimates rather thandirect histological measurements (Shellis, 1998),some of which are demonstrably in error whencompared to known crown eruption ages (Smithet al., 1994). Finally, for some species (e.g.,chimpanzees and humans) molar crown formationtimes simply do not reflect known di!erences inlife-history values, di!erences that are more or lessconcordant with average ages at M1 emergence.The reason for this may have to do with variationin rates of root formation, especially initial rootformation. Disparities between crown formationtimes and inferred or calculated ages at M1 emer-gence are beginning to become apparent amongfossil apes as well, exemplified by comparisonsbetween the similarly sized Proconsul nyanzae,Dryopithecus laietanus, and Afropithecus turkanen-sis (Beynon et al., 1998; Kelley et al., 2001; Smithet al., 2003). It can be expected that further study

of additional extant and fossil species will help toelucidate the relationships between molar crownformation times, ages at molar emergence, and lifehistory attributes.

It has been hypothesized that the slowed lifehistories that characterize the extant apes, particu-larly the great apes, might have had their genesisduring the early evolutionary history of theHominoidea, and that they might in fact have beenthe fundamental adaptive shift underlying thecladogenesis of hominoids and cercopithecoids(Kelley, 1997). Prior to the analysis described here,the oldest fossil ape for which age at M1 emergencehad been determined was a 10 Ma individual ofSivapithecus parvada from the Siwaliks of Pakistan(Kelley, 1997, 2002). The estimate of age at M1emergence for the 17.5 Ma individual of A. turka-nensis nearly doubles the antiquity of such esti-mates for fossil hominoids and hominids. Thefinding of an age at M1 emergence that is essen-tially like that of extant chimpanzees, and theinference therefore of an essentially moderngreat ape life history in A. turkanensis, couldbe viewed as lending additional support to theabove hypothesis of life-history evolution in theHominoidea.

There are, however, a number of ways to inter-pret the data on M1 emergence in primates as awhole, with di!erent implications for life-historyevolution in the Hominoidea and other higherprimate taxa. Fig. 10 shows two di!erent interpre-tations of the relationship between M1 emergenceand body mass in extant primates. Plotted in eachare the 24 extant primate species (includinghumans) for which there are reliable data on age atM1 emergence (Table 6). Fig. 10a shows a singlelinear regression for all the included extant species,purposely left unidentified. Fig. 10b shows thevarious species identified by higher taxonomicgroup, and also includes estimates of age at M1emergence and body mass for A. turkanensis andS. parvada. Statistics for the various regressionsdepicted in Fig. 10 are shown in Table 7.

Based on Fig. 10a, the late age at M1 emergencein Afropithecus could be interpreted as a simpleconsequence of large body mass (estimated aver-age mass=30 kg), without any necessary phylo-genetic implications. The correlation between age


at M1 emergence and body mass for all theincluded species is highly significant (Table 7). Bythis interpretation, any primate with the bodymass of a small chimpanzee would be expectedto have an age of M1 emergence within thechimpanzee range, and, by implication, anoverall life history that was similar to that of achimpanzee.

In Fig. 10b, there is still a significant relation-ship between age at M1 emergence and bodymass within the di!erent higher taxa (exceptinghominoids, which is a simple consequence of smallsample size). However, the four included highertaxa (plus Homo) are also characterized by a seriesof apparent grade-shifts in age at M1 emergence.The grade-shifts from lemuriforms to each ofthe anthropoid groups, from cercopithecids tohominoids, and from non-human hominoids toHomo are clear. Interpretation of the cebid regres-sion is less so, as it implies that a cebid the size ofa chimpanzee would have an age at M1 emergencethat is greater than that of modern Homo.

Understanding life-history evolution in platyr-rhines is in fact critical for interpreting the signifi-cance of M1 emergence data among fossilhominoids, and for understanding life-history evo-lution in hominoids more generally. A plausibleinterpretation of the data in Fig. 10b is that bothplatyrrhines (here represented only by cebids) andhominoids broadly represent the primitive anthro-poid condition and that cercopithecids are derivedwith respect to both, having accelerated lifehistories (see also Fig. 1). In this case, the abso-lutely more prolonged life histories of apes relativeto platyrrhines would be most reasonably inter-preted as a simple consequence of increasingbody size. However, the platyrrhine regression inFig. 10b has a very limited representation of taxa,consisting of several callitrichines and two speciesof Cebus. The slope is substantially greater than ineither of the other anthropoid groups, but could besignificantly altered with a more representativesample of taxa. If life history has slowed in Cebusrelative to some or most other platyrrhine genera,or if life history has accelerated in callitrichines,perhaps in association with dwarfing, then theslope is artificially high. If so, then the primitivecondition for platyrrhines, and for catarrhines

Fig. 10. Two possible interpretations of age at M1 emergence inrelation to body mass in primates (all regressions are leastsquares—regression statistics in Table 7); (a): Phylogeny-neutral interpretation; (b): Phylogeny-based interpretationrevealing apparent grade-shifts in age at M1 emergence.Symbols for (b): Lemuriformes (circles), Cebidae (triangles),Cercopithecoidea (squares), Afropithecus turkanensis (A),Homo sapiens (H), Pan troglodytes (P), and Sivapithecusparvada (S). For extant species, age at M1 emergence fromSmith et al. (1994) and Smith et al. (1995); body masses(average male and female mass) from Smith and Jungers (1997).For A. turkanensis, average body mass estimated at 30 kg basedon postcranial size (Leakey et al., 1988) and an estimated malemass of 35 kg (Kappelman et al., in press); age at M1 emergenceestimated at 36 months (see text). For S. parvada, average bodymass estimated at 61 kg based on postcranial size (see Kelley,1988), and age at M1 emergence estimated at 43 months(Kelley, 1997; Kelley et al., in preparation).


as well, might be intermediate between that ofhominoids and cercopithecids; note, for example,the position of the Alouattini with respect tothe other platyrrhine taxa in Fig. 1. In this

case, life-history evolution in catarrhines wouldrepresent a true divergence, with life-historyacceleration in cercopithecoids and prolongationin hominoids, and with both states being derived.

Table 6Age at M1 emergence and body mass in extant primates

Species Age at M1 emergence (months) Average body mass (kg)

Cheirogaleus medius 0.84 0.18Varecia variegata 5.76 3.58Lemur catta 4.08 2.21Eulemur fulvus 5.04 2.13E. macaco 5.16 1.82Propithecus verreauxi 2.64 3.55Galago senegalensis 1.20 0.21Callithrix jacchus 3.72 0.37Saguinus fuscicollis 4.10 0.35S. nigricollis 3.35 0.48Cebus albifrons 12.72 2.74C. apella 13.80 3.09Saimiri sciureus 4.44 0.72Aotus trivirgatus 4.32 0.78Cercopithecus aethiops 9.96 3.62Macaca fascicularis 16.44 4.48M. fuscata 18.00 9.51M. mulatta 16.20 6.54M. nemestrina 16.44 7.58Papio anubis 20.04 18.10P. cynocephalus 20.04 17.05Trachypithecus cristata1 12.00 6.44Pan troglodytes 39.12 53.00Homo sapiens2 66.03 59.00

M1 emergence data from Smith et al. (1994) and body mass data from Smith and Jungers (1997), with the followingexceptions:

1M1 emergence data from Wolf (1984).2M1 emergence data from Smith et al. (1995).

Table 7Statistics for Fig. 10 least squares regressions

Regression y-intercept Slope Correlation % Variance p

Primate (ln)1 1.142 0.595 0.911 0.831 0.000Primate (untransformed)2 5.144 0.876 0.941 0.886 0.000Lemuriformes3 0.946 0.538 0.896 0.803 0.006Cebidae3 1.833 0.636 0.960 0.922 0.001Cercopithecidae3 2.053 0.341 0.799 0.638 0.017Hominoidea (less Homo)3 2.438 0.305 0.972 0.944 0.152

1Fig. 10a.2Not figured.3Fig. 10b.


In the overall scheme of Fig. 10b, the age at M1emergence in Afropithecus may largely be a func-tion of its being a hominoid. Certainly a lemuri-form or cercopithecoid with the body mass ofAfropithecus would be expected to have an age atM1 emergence that is substantially earlier (seefurther below). It is unclear at this point if thiswould also be the case for platyrrhines, or at leastfor some platyrrhines. If platyrrhines and homi-noids together broadly represent the primitiveanthropoid condition, then the M1 emergence ageof Afropithecus would again largely be a functionof its size.

As important to this discussion is the homi-noid regression. Since it includes only threespecies, two of which are extinct species withestimated ages at M1 emergence based on singleindividuals, its slope must also be regarded ashighly uncertain. Moreover, the slope is largelydetermined by the body mass and age at M1emergence estimates for A. turkanensis. Anychanges in the estimates that we chose to repre-sent A. turkanensis (30 kg average mass and 36months for age at M1 emergence, the overallmean of the estimates) are likely to significantlyalter the slope. The true nature of the relation-ship between body mass and age at M1 emer-gence in hominoids will only become clear whenthere are reliable data for the other great apes,particularly Gorilla, and for gibbons.

The possibility at least of phylogeneticallyassociated grade shifts in age at M1 emergence—and, by extension, in life history more generally—that appear to have been established during theearly evolutionary history of the higher primategroups is interesting in a broader context. In aseries of empirical studies of life-history variationin mammals as a whole, Harvey and colleagues(Harvey et al., 1989a,b; Read and Harvey, 1989)found that a disproportionate amount of the vari-ation was at higher taxonomic levels, suggestingthe early establishment of fundamental life-historysuites that are subject to comparatively littlechange during the subsequent evolutionary historyof the group, sometimes even in the event ofsignificant changes in body size. Likewise, Martinand MacLarnon (1990) found evidence for con-servative life-history evolution in the fossil record

of equids, again even with substantial phyletic sizeincrease.

A similar pattern has recently been reportedin members of two lemuriform sister-taxa, oneextant (Indriidae) and one subfossil (Palaeo-propithecidae) (Schwartz et al., 2002). Includingsubfossil species, members of these two groupsspan the body mass range from average-sizedmonkeys to chimpanzees. Indriids are remarkablefor having exceptionally precocious dental devel-opment and an age at M1 emergence that isstrongly temporally dissociated from many otherlife-history parameters (Godfrey et al., 2001,2002). The recent confirmation of this phenom-enon in the chimpanzee-sized subfossil Palaeo-propithecus (Schwartz et al., 2002), is compellingadditional evidence for the importance ofphylogeny as well as body size in life-historyevolution.

However, as noted earlier in the discussion ofthe platyrrhine data, it cannot be assumed atpresent that all members of the di!erent primatehigher taxa plotted in Fig. 10b will fall within thelife-history grade characteristic of the particulartaxon. Both the cebid and the lemuriform regres-sion lines are based on two clusters of species ofsubstantially di!erent body mass. Not only are theregression lines uncertain as a consequence, butthe addition of species of intermediate or largerbody mass might reveal departures among lowertaxonomic ranks (ie., genera/tribes) from whateverdominant grade level that emerges. There might infact be a greater expectation of this in older, morebiologically diverse clades such as the platyrrhinesor lemuriforms than in more recent clades like theextant cercopithecids.

It can be anticipated that many plausible inter-pretations of life-history evolution in primates willbe eliminated as the data on age at M1 emergenceimprove for both extant and fossil primates.Extant taxa that are especially important forimproving the database include, in addition to theother great apes and gibbons noted above, atelidsand additional cebids, smaller cercopithecines,additional colobines, and additional non-lemuridstrepsirhines. Especially important fossil taxainclude primitive catarrhines and species thatextend the body mass ranges of their respective


groups, such as the fossil Theropithecus, very largesubfossil lemurs, and smaller fossil apes.

Summary

Estimates of the age at death were calculated foran infant of early Miocene A. turkanensis,KNM-MO 26, that was in the process of eruptingits first molar. The estimates were based on theperikymata preserved on the lateral incisor germ inthe mandible, combined with data on the durationof cuspal enamel formation and the length of thepostnatal delay in the inception of I2 mineraliz-ation in extant apes and humans, as well as inspecies of Proconsul. A range of estimates wascalculated to accommodate both intra and inter-specific variation in the latter growth parameters.Perikymata periodicity was determined from histo-logical sections of two A. turkanensis molars. Asthe eruption stage of the M1 in the A. turkanensisinfant reveals that it had not yet achieved gingivalemergence when the animal died, estimates of theprojected age at M1 emergence were calcu-lated from the age at death estimates combinedwith radiographic data on the progression of M1eruption in baboons and chimpanzees.

Estimates for the age at M1 emergence inKNM-MO 26 ranged from approximately 28 to43 months, well outside the ranges of largeextant cercopithecids for which there arecomparable data, but comfortably within therange of chimpanzees. It is inferred from this resultthat life history in A. turkanensis was essentiallylike that of extant chimpanzees. This inference iscompatible with the hypothesis that there was ashift to the prolonged life histories that charac-terize extant apes early in the evolution of theHominoidea. However, this presumes a primitivecondition for life history in catarrhines thatwas faster, when adjusted for body size, than inchimpanzees. Limited data from extant platyr-rhines may indicate that this is not the case. Aplausible interpretation of these data is that extantplatyrrhines and hominoids together represent theprimitive condition for life history, and that onlycercopithecoids among living anthropoids havederived life histories, being highly accelerated.

It is proposed that life-history evolution inprimates more generally occurred as a series ofgrade shifts among higher level taxa. Some or allof these shifts may largely reflect phylogeny,irrespective of body size. Others may reflectnothing more than changes in body size, stillphylogenetically based, but along a commontrajectory for the pace of life history. Regardless ofthe predominant mode of change, it is becomingincreasingly clear that phylogeny as well as bodysize must be taken into account when attemptingto reconstruct the life histories of fossil primatespecies.

Acknowledgements

We gratefully acknowledge the Governmentof Kenya and the National Museums of Kenyafor permission to study the Afropithecus fossils(Permit OP/13/001/10C 354 issued to JK). Wethank Meave Leakey and William Anyonge, pastHeads of the Palaeontology Division, and EmmaMbua, then Collections Manager of Palaeoanthro-pology, for facilitating our work at the KNM.JK expresses special gratitude to Je! Fortman,Associate Director, and Sam Rosado and theother sta! of the Biological Resources Laboratory,The University of Illinois at Chicago for theirinvaluable long-term assistance with the baboonradiographic project. We thank Chris Dean,Meave Leakey, Lawrence Martin, Don Reid, andHolly Smith for innumerable valuable discussionsrelating to the work reported here, and TerryHarrison plus three anonymous reviewers forcomments on the manuscript. This research wassupported by National Science Foundation grantSBR-9408664 to JK.

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Age at ﬁrst molar emergence in early Miocene Afropithecus ...bioanth/tanya_smith/pdf/age_at_first_molar.pdf · This is additional evidence to that provided by Sivapithecus parvada