Age at First Molar Emergence in Lufengpithecus Lufengensis and Its

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Journal of Human Evolution 54 (2008) 251e257

Age at ﬁrst molar emergence in Lufengpithecus lufengensis and its implications for life-history evolution

Lingxia Zhao*, Qingwu Lu, Wending Zhang

Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China Received 9 November 2006; accepted 30 September 2007

Abstract

The late Miocene hominoid Lufengpithecus from Yunnan Province, China, is crucial for understanding hominoid evolution in Asia. Given that age at first permanent molar emergence is a key life-history trait in primates, the present study determined the age at death of the Lufeng- pithecus lufengensis juvenile PA868, which was in the process of erupting its first molar. Using a perikymata periodicity of 7e11 days, along with estimation of cusp formation time and the postnatal delay of crown mineralization, perikymata counts obtained from the permanent central incisor and canine germs indicate that the age at death of PA868 was 2.4e4.5 years based on the central incisor germ, and 2.5e4.7 years based on the canine germ. The age at the first molar emergence was actually slightly younger (by about 0.3 years), as demonstrated by tiny wear facets on this tooth, which indicate that gingival emergence had occurred sometime before death. The average age at first molar emergence of Lufeng- pithecus lufengensis PA868 is estimated to be 3.2e3.3 years, with a range of 2.1e4.4 years. In comparison to extant primates and other fossil hominoids, the life history of Lufengpithecus lufengensis is similar to that of extant great apes and the Miocene hominoids Afropithecus turkanensis and Sivapithecus parvada, as well as Plio-Pleistocene Australopithecus, and different from monkeys, gibbons, and modern humans. Ó 2007 Elsevier Ltd. All rights reserved.

Keywords: Age at ﬁrst molar emergence; Dental development; Life history; Lufengpithecus lufengensis

Introduction likely belongs to an ape, and its closest afﬁnities are to Lufeng- pithecus (Wu, 2000). However, archaeological evidence Large-bodied hominoid fossils (Woo, 1957, 1958; Xu and (Huang et al., 1995; Hou et al., 1999, 2002, 2006) from Long- Lu, 1979; Wu et al., 1986; Zheng and Zhang, 1997; Qi and gupo makes this issue complex. More comprehensive research Dong, 2006), all attributable to the genus Lufengpithecus on Lufengpithecus is necessary to discern its appropriate phy- (Wu, 1987; Gao, 1998; Qi et al., 2006) from the late Miocene logenetic placement. The present study aims to assess in of Yunnan Province, China, are critical for understanding greater detail the dental development and life history of Lu- hominoid evolution in Asia. Lufengpithecus has been generally fengpithecus lufengensis. grouped with the Sivapithecus-Pongo lineage, but further One of the profound changes in the evolution of the human study and new discoveries of Lufengpithecus suggest that lineage has been prolongation of the maturational, or life- this genus may not a member of the Ponginae, but may in history, proﬁle. Extensive debate has centered on the questions fact be a member of the Homininae (Gao, 1998; Kelley, of when in the course of human evolution and in which species 2003; Chaimanee et al., 2003, 2004; Gao et al., 2004, 2006). the major part of this change took place (Kelley, 2002; Anem- The early Pleistocene ‘‘Homo’’ mandible found at the Long- one, 2002). Therefore, more data on life history of fossil hom- gupo site of Wushan County, China (Huang et al., 1995), inoids are essential for resolving this issue. ‘‘Life history’’ refers to the timing or scheduling of events from conception to death. An animal’s life history can be sum- * Corresponding author. marized by key variables such as gestation length, neonatal E-mail address: [email protected] (L. Zhao). weight, prenatal and postnatal growth rates, weaning age,

0047-2484/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2007.09.019 252 L. Zhao et al. / Journal of Human Evolution 54 (2008) 251e257 the age at first reproduction, and life span. Clearly, it is diffi- based on the fauna (Flynn and Qi, 1982; Qi, 1985, 1986). Re- cult to obtain such direct data from the fossil record. Dental cent faunal comparisons and paleomagnetic stratigraphic work development can serve as a reliable predictor of a series of indicate that L. lufengensis from Lufeng is somewhat younger critical life-history parameters. Among primates, age at first than L. hudiensis from Yuanmou (Qi et al., 2006; Yue and molar emergence is highly correlated with a variety of life- Zhang, 2006). history traits (Smith, 1991, 1992), and it can be used to Specimen PA868 preserves the right deciduous fourth pre- broadly infer the life histories of fossil primate species. molar and permanent first molar, as well as five right perma- Based on the dental development of the central incisor and nent tooth crown germs within the crypts of the mandible: canine germs, the present study estimates the age at death and I1,I2,C,P3, and P4 (Figs. 1 and 2). All five crown germs the age at first molar emergence of the Lufengpithecus lufengen- are incomplete and roots are not visible radiographically sis individual represented by the juvenile mandible PA868, and (Fig. 2). The M1 was in the process of erupting when the in- explores the life-history profile of this species. Because L. lufen- dividual died, with the crown already beyond the mandibular gensis is the latest Miocene large-bodied hominoid, this analy- alveolar margin and nearly up to the level of the fully func- sis provides important data for understanding the evolution of tional occlusal plane (Figs. 1 and 2). life history in Miocene and Plio-Pleistocene hominoids, as Two size clusters are evident in the L. lufengensis sample, well as in extant great apes and humans. and the size of the PA868 M1 crown (9.1 mm in length and 8.3 mm in breath) places it among the smaller specimens. Kel- Materials and methods ley and Xu (1991) suggested that the two clusters represent males and females, indicating that L. lufengensis was more Zhao and He (2005) previously gave a preliminary report sexually dimorphic in its postcanine dentition than living hom- on the estimation of the age at first molar emergence in inoids, perhaps exceeding all extant anthropoids. Thus, if we PA868 based only on an X-ray photograph as part of a review consider the whole assemblage to represent a single highly di- paper on dental development in the large-bodied Miocene morphic species, then it is likely that PA868 belongs to a fe- hominoids from Yunnan. In the present study, we have done male individual. more direct work on the specimen to determine its age at death, particularly using scanning electron microscopy to ex- Estimation of the age at death of PA868 amine two developing tooth crown germs (the right central incisor and canine) for estimating crown formation time, which The method used here to determine age at death is similar to is the key process for determining the age at death. In the fol- the one employed by Kelley (1997, 2002) and Kelley and Smith lowing analysis, we revise the earlier estimate of age at first (2003) to reconstruct age at death for Sivapithecus parvada molar emergence for the PA868 individual with a full descrip- specimen GSP 11536 and Afropithecus turkanensis specimen tion of the methods and a more thorough analysis. KNM-MO 26. The age at death for individual PA868 could be determined using crown formation times of the tooth germs, Condition of the specimen PA868 which were still developing when the individual died. In lingual view, the three anterior teethdI1,I2, and the caninedare ex- Specimen PA868 is a juvenile right mandibular corpus posed due to damage to the outer bone (Fig. 1). The I1 and ca- (Fig. 1), discovered in 1980 in stratigraphic level D-3, H nine are more suitable for estimating the age of this individual. square, of the Shihuiba site in Lufeng County of Yunnan Prov- Age at death was calculated by adding the time between 0 0 ince, China. The Shihuiba site (E104 4 , N25 1 ) is located birth and the initiation of I1 or canine crown mineralization about 9 km north of Lufeng town, 60 km northwest of Kunm- to the time of I1 or canine crown formation until the individ- ing. The age of the L. lufengensis layers is approximately 8 Ma ual’s death. Crown formation time in teeth that have not

Fig. 1. Juvenile mandible of L. lufengensis specimen PA868: (a) buccal view, (b) lingual view. L. Zhao et al. / Journal of Human Evolution 54 (2008) 251e257 253

with a dental pick and needle probe, exposing much of the surfaces of the tooth crowns (Fig. 1). The perikymata on the exposed surfaces were clear under a microscope. The exposed I1 and canine were molded using silica, and a replica was made using epoxy resin, coated with a thin layer of gold-palladium, and examined with a JEOL1600 scanning electron microscope. Montage photos were taken of the tooth surfaces from the developing cervical region to cusp edge (Fig. 3). From the montage, we obtained the perikymata number on the surface from the cusp to the developing cervix. The periodicity of perikymata, or Retzius lines, was determined from sections made using other L. lufengensis teeth (Zhao et al., 2000; Schwartz et al., 2003). Ages at initiation of I1 and canine mineralization in PA868 were estimated according to compar- Fig. 2. Radiograph of specimen PA868. ative data from all extant apes and humans for which histological data are available (Beynon et al., 1998; Reid et al., completed their development was calculated as the sum of the 1998a,b; Reid and Dean, 2006). time required to form the cuspal enamel plus the time to form the amount of lateral enamel present at the time of death. Estimating age at gingival emergence ‘‘Cuspal enamel’’ refers to appositional enamel, the earliest of M1 based on age at death formed enamel in which successive Retzius lines are com- pletely buried under subsequently formed enamel. ‘‘Lateral Because M1 had emerged and was almost in full occlusion enamel’’ refers to the imbricational enamel defined as the at the time of the PA868 individual’s death, the age of M1 enamel formed subsequent to the first Retzius line that reached emergence must be somewhat younger than the age of death. the crown surface as a perikyma. Using the process and timing of M1 eruption for modern great Cuspal formation time must be estimated nondestructively. apes, baboons, and humans as references, the time from M1 However, for the incisor and canine, the cuspal enamel forma- emergence to the death of the PA868 individual is discussed tion represents only a small percentage of the entire crown for- and estimated below. For each of the growth parameters, there mation time, and it is not as variable as in the postcanine teeth is both intra- and interspecific variation. Referring to compar- of extant great apes and humans. Referring to the values for ative data, we chose species means for calculating the age at extant great apes and humans, the estimation likely contains death and the age at M1 emergence for PA868, but we also dis- some degree of error. On the other hand, the lateral enamel cuss potential ranges of variation. formation time can be estimated more precisely by counting the perikymata. This value is calculated by multiplying the Results number of perikymata by the periodicity. To obtain the total number of the perikymata on I1 and the Initiation age of I1 crown formation canine of PA868, the following procedure was used. Given that the alveolar bone surrounding the I1 and canine germs was Crown initiation ages of permanent anterior teeth and first partially broken away, the matrix was carefully removed molars appear to conform to a common developmental

Fig. 3. SEM montage photo of the central incisor germ of specimen PA868. 254 L. Zhao et al. / Journal of Human Evolution 54 (2008) 251e257 chronology and sequence in modern humans and living great enamel in PA868. Similarly, we counted 98 perikymata for the apes (Macho and Wood, 1995). First permanent molars in imbricational enamel of the canine (Fig. 4). hominoids start calcifying shortly before or around birth, fol- Without sectioning, the perikymata (or Retzius line) period- lowed by the incisors and canines in swift succession from an- icity of PA868 must be estimated. However, several tooth sec- terior to posterior. Referring to data collected from extant tions from other L. lufengensis teeth (Zhao et al., 2000; great apes and humans (Bromage and Dean, 1985; Beynon Schwartz et al., 2003) suggest that Retzius-line periodicity et al., 1991; Reid et al., 1998a,b; Reid and Dean, 2006), we for L. lufengensis varies from 7 to 9 days. Based on the range use a mean of 0.3 years with a range 0e0.5 years for I1 crown of variation in periodicity in modern humans and great apes, initiation, and a mean of 0.5 years with a range of 0.25e0.75 we use a larger periodicity range of 7e11 days for L. lufengen- years for canine crown initiation for PA868. sis. Multiplying 7, 9, and 11 days, respectively, by the perikymata number, the lateral enamel formation time is estimated at 770, 990, and 1210 days for I1, and 686, 882, and 1078 days Cuspal enamel formation time for the canine.

Without sectioning, the cuspal enamel formation times Age at death of PA868 must be estimated based on the enamel thickness and known times for extant great apes and humans (Bromage and Dean, By summing the postnatal delay time for I initiation, cus- 1985; Beynon et al., 1991; Reid et al., 1998a,b; Reid and 1 pal enamel formation time, and lateral enamel formation time, Dean, 2006). Here, we use a mean of 0.5 years with a range the average age at death for the PA868 individual can be esti- 0.33e0.67 years for I cuspal enamel formation time, and 1 mated from I at 2.91, 3.51, and 4.11 years using periodicities a mean of 0.7 years with a range of 0.4e1.0 years for canine 1 of 7, 9, and 11 days, respectively, with a range of 2.44e4.49 cuspal enamel formation time for PA868. years. Similarly, the average age at death based on the canine can be estimated at 3.08, 3.62, and 4.18 years, with a range of e Lateral enamel formation time 2.53 4.73 years. The age-at-death results from the I1 and canine are thus very similar (Table 1).

We counted 86 perikymata on the surface of the I1 (Fig. 3). The apical 2 mm (i.e., the enamel at the incisal edge) and the Time from M1 emergence to death, and age at ﬁrst cervical 1 mm of enamel (i.e., the last-formed enamel near molar emergence in PA868 the cervical line) do not express perikymata clearly. Using the spacing of the adjacent perikymata, we estimated 12 perikymata The M1 of PA868 was in the process of erupting and had each for these two parts of imbricational enamel formation. emerged from the gingiva, as indicated by tiny wear facets vis- Thus, we calculated a total of 110 perikymata for the I1 lateral ible on the buccal cusp tips. Using a microscope, tiny wear

Fig. 4. SEM montage photo of the canine germ of specimen PA868. L. Zhao et al. / Journal of Human Evolution 54 (2008) 251e257 255

Table 1 Estimation of age at death and first molar emergence in L. lufengensis specimen PA868a Tooth germ Perikymata Periodicity Imbricational enamel Cusp formation Postnatal delay Age at death Age at first molar formation time (days, years) time emergence b I1 110 7 770, 2.11 0.5 (0.33e0.67) 0.3 (0e0.5) 2.91 (2.44e3.28) 2.61 (2.14e2.98) 9 990, 2.71 3.51 (3.04e3.88) 3.21 (2.74e3.58) 11 1210, 3.32 4.12 (3.65-4.49) 3.82 (3.35-4.19) C 98 7 686, 1.88 0.7 (0.4e1.0) 0.5 (0.25e0.75) 3.08 (2.53e3.63) 2.78 (2.23e3.33) 9 882, 2.42 3.62 (3.07e4.17) 3.32 (2.77e3.87) 11 1078, 2.98 4.18 (3.63e4.73) 3.88 (3.33e4.43) a Age estimates are given in years unless otherwise noted. b Ranges of variation of the estimates are given in parentheses. facets less than 1 mm2 in size can be seen on the tips of the a model, given that Lufengpithecus is more similar to great protoconid and hypoconid. However, the tooth had not erupted apes than to gibbons and monkeys in features of dental into full functional occlusion (Figs. 1 and 2). morphology and development such as tooth size, enamel Radiographic study and oral examination of infant chim- thickness, daily cross-striation and periodicity variation of panzees indicate that it takes 5e6 months for the M1 crown perikymata, and tooth-eruption sequence and patterns (Zhao to go from the level of the alveolar margin (i.e., with the et al., 2000, 2002, 2003; Schwartz et al., 2003; Zhao and cusp apices at the alveolar margin) to fully functional occlu- He, 2005). The estimation for age at death and M1 emergence sion (Zuckerman, 1928). The interval between M1 cresting presented here extend the range of the previous estimation, of the alveolar margin and gingival emergence probably takes with the minimum value being lower and the maximum value somewhere between 4 and 5 months in chimpanzees and 3 being greater, mainly because of revised crown formation months in baboons (Kelley and Smith, 2003). Based on these time. data (see also Dean et al., 1993), we estimated the time from Compared with extant primates (Smith et al., 1994), age at M1 emergence to death of PA868 to be approximately 3e4 M1 emergence in L. lufengensis, as represented by PA868, is months, or roughly 0.3 years. much later than in Prosimii (e.g., Lemur) and Platyrrhini Based on the time from M1 emergence to death, the age at (e.g., Cebus and Callithrix) and is also later than in Cercopi- M1 emergence for PA868 is estimated, using I1, to be 2.61, thecoidea (e.g., Macaca, Papio, Cercopithecus)(Table 2). 3.31, and 3.81 years using 7, 9, and 11 days of perikymata pe- Age at M1 emergence in the latter comparative taxa is less riodicity, respectively, with a range of 2.14e4.19 years. Sim- than 2 years and less than the minimum estimate for age at first ilarly, the mean age at M1 emergence can be estimated using molar emergence in PA868. It is also probable that age at M1 the canine to be 2.78, 3.32, and 3.88 years, with a range of emergence in PA868 is later than in Hylobates, although data 2.23e4.43 years. Combining the data for I1 and the canine, for gibbons are very few and the age of 1.75 years at M1 emer- the mean age at first molar emergence is 3.21e3.32 years, gence is highly questionable (Smith et al., 1994). However, the with a range of 2.14e4.43 years for PA868 (Table 1). histological reconstruction of dental development and age at To date, several histological sections of Lufengpithecus death in a juvenile gibbon (Hylobates lar) provides some in- teeth, including L. lufengensis and L. hudiensis, have been formation (Dirks, 1998). This individual is estimated to have made (Zhao et al., 2000, 2003; Zhao and He, 2005; Schwartz died at 2.88 years of age, and at this time, I1,I2, and M1 et al., 2003). These sections show that perikymata periodicity had come into occlusion, indicating that the M1 had emerged is within 7e9 days for Lufengpithecus. Using the latter period- prior to 2.88 years, and possibly closer to or less than the min- icities, the age at death and the age at M1 emergence are 2.44e imum age estimate for PA868. Thus, it is likely that age at M1 4.17 years and 2.14e3.87 years, respectively, for PA868 emergence in gibbons is much less than the average estimated (Table 1). age for PA868. The estimated age at M1 emergence for PA868 closely resembles that of extant great apesdPan, Gorilla, and Discussion Pongodand is less than that of modern Homo sapiens, even if only the maximum estimate is considered (Table 2). In comparison to the previous data used to generate a rough Comparative data for fossil primates are limited, but several estimation of the developmental age for L. lufengensis speci- histological studies on the age at M1 emergence have been per- men PA868 (Zhao and He, 2005), the present data are more formed on fossil hominoid material (Table 2), such as Sivapi- appropriate for directly examining central incisor and canine thecus parvada specimen GSP 11536 and Afropithecus formation time in this specimen, and for discussing in greater turkanensis specimen KNM-MO 26 (Kelley, 1997, 2002; detail variation in developmental parameters based on pub- Kelley and Smith, 2003), as well as Australopithecus speci- lished comparative data. In examining dental development in mens SK 63, STS 24, and LH 2 (Bromage and Dean, 1985; PA868, we used variation in three parametersdcuspal forma- Dean et al., 1993). The estimated age at M1 emergence for tion time, postnatal delay of tooth formation, and perikymata PA868 is similar to the latter specimens, which are comparable periodicitydin extant and extinct large-bodied hominoids as to extant great apes and different from modern humans. 256 L. Zhao et al. / Journal of Human Evolution 54 (2008) 251e257

Table 2 Of the Miocene apes for which age at M1 emergence has Age at M1 emergence (in years) in L. lufengensis specimen PA868 and other been estimated using histological methods, L. lufengensis is fossil hominoids and extant primates the geologically youngest: Sivapithecus parvada specimen Taxon Age at M1 Source GSP 11536 derives from a 10-Myr-old locality in the Siwaliks emergence of Pakistan (Kelley, 1997), and Afropithecus turkanensis spec- (male/female) imen KNM-MO 26 derives from the site of Moruorot in e Lufengpithecus 2.1 4.4 This study Kenya, dated to approximately 17.5 Ma. All of these species lufengensis PA868 Afropithecus turkanensis 2.4e3.6 Kelley and Smith, 2003 had life histories similar to those of extant great apes. Kelley KNM-MO 26 (2003) hypothesized that the slow life history of great apes in Sivapithecus 2.2e4.5 Kelley, 1997 comparison to other primates might have been a critical com- parvada GSP 11536 ponent of the origin and early evolution the Hominoidea. More e Australopithecus 3.0 4.0 Dean et al., 1993 evidence bearing on the life histories of extinct and extant robustus SK 63 Australopithecus 3.3 Bromage and Dean, 1985 hominoids, including hylobatids, is needed for this hypothesis africanus STS 24a to be supported. Australopithecus 3.3 Bromage and Dean, 1985 The present results also imply that the latest Miocene hom- a afarensis LH 2 inoids conserved features of life history that had evolved in the Propithecus verreauxi 0.22 Smith et al., 1994 early Miocene. When and how the unique pattern of human Lemur catta 0.34 Smith et al., 1994 Callithrix jacchus 0.31 Smith et al., 1994 life history evolved has been an important topic during recent Cebus apella 1.15 Smith et al., 1994 decades. The pattern and timing of dental development of Macaca mulatta 1.35 (1.37/1.32) Smith et al., 1994 Plio-Pleistocene Australopithecus has been debated. Histolog- Papio anubis 1.67 (1.71/1.63) Smith et al., 1994 ical reconstructions have been used to estimate age at death for Papio cynocephalus 1.67 (1.58/1.75) Smith et al., 1994 three Australopithecus individuals who died at or very near to Cercopithecus aethiops 1.71 Smith et al., 1994 Hylobates sp. 1.75 Smith et al., 1994 the time of M1 emergence through the gingiva (Bromage and Pan troglodytes 3.26 (3.33/3.19) Smith et al., 1994 Dean, 1985; Dean et al., 1993). Age at ﬁrst molar emergence Gorilla gorilla 3.5 Smith et al., 1994 was estimated to be between three and four years for these Pongo pygmaeus 3.5 Smith et al., 1994 b specimens, which is within the range of great apes, and differ- Pongo pygmaeus 4.6 Kelley and Schwartz, 2005 ent from that of modern humans. All of the evidence supports Homo sapiens 6.24 (6.33/6.15) Smith et al., 1994 a the view that the unique pattern of human life history was not Age assigned to Australopithecus juveniles who died at or shortly after in place at the australopith stage of human evolution, and it is emergence of the mandibular ﬁrst molar, using a 7-day perikymata periodicity. b Maxillary M1 emergence age. likely to have evolved after the emergence of Homo.

Age at M emergence can be used as a substitute, or proxy 1 Acknowledgments variable, for the overall pace of life history among extant primates because it is highly correlated with a variety of life- We thank Jean-Jacques Hublin and Tanya Smith for invit- history traits (Smith, 1989, 1991; Kelley, 1997, 2002, 2003). ing the first author to participate in the 2006 workshop in Leip- Thus, it is useful for inferring life history of fossil primate spe- zig and for providing the opportunity to contribute this paper cies. If the estimated age at M emergence in PA868 is repre- 1 to this JHE special issue. We thank Lifen Zhang for helping sentative of L. lufengensis, then the results of the present study with the techniques used for this study, Jay Kelley for valuable suggest that this late Miocene hominoid was characterized by discussions, Holly Smith for encouraging English publication, a slow life history, similar to that observed in extant great apes, and three anonymous reviewers for comments on the manu- but not as slow as the prolonged life history of modern script. This research was supported by the Major Basic Re- humans. search Projects (2006CB806400) of MST of China and Interpreting the present findings regarding L. lufengensis is National Science Foundation of China (40672011). helpful for understanding the evolution of life history in hominoids generally and the human lineage specifically. Kelley (2003) argued that phylogeny and body size must be taken References into account when attempting to reconstruct the life history of fossil primate species. In extant primates, the correlation Anemone, R.L., 2002. Dental development and life history in hominid evolution. In: Minugh-Purvis, N., McNamara, K.J. (Eds.), Human Evolution between age at M1 emergence and body mass is highly signif- through Developmental Change. The Johns Hopkins University Press, Bal- icant. At the same time, species with similar ages at M1 timore, pp. 249e280. emergence are grouped in a series of apparently phylogeny- Beynon, A.D., Dean, M.C., Leakey, M.G., Reid, D.J., Walker, A., 1998. Com- associated grade-shifts, such as Lemuriformes, Cebidae, Cerco- parative dental development and microstructure of Proconsul teeth from pithecoidea, apes, and humans. The body mass of L. lufengensis Rusinga Island, Kenya. J. Hum. Evol. 35, 163e209. is estimated to have been 20e40 kg for females and 40e60 kg Beynon, A.D., Dean, M.C., Reid, D.J., 1991. Histological study on the chronology of the developing dentition in gorilla and orangutan. Am. J. for males, within the range of extant great apes. Therefore, the Phys. Anthropol. 86, 189e203. slow life history inferred for L. lufengensis can be interpreted Bromage, T.G., Dean, M.C., 1985. Re-evaluation of the age at death of imma- as a function of both phylogeny and body mass. ture fossil hominids. Nature 317, 525e527. L. Zhao et al. / Journal of Human Evolution 54 (2008) 251e257 257

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