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

Journal of Human Evolution 44 (2003) 307–329

Age at first molar emergence in early Miocene Afropithecus turkanensis and life-history evolution in the Hominoidea Jay Kelley 1*, Tanya M. Smith 2 1

Department of Oral Biology (m/c 690), College of Dentistry, University of Illinois at Chicago, 801 S. Paulina, Chicago, IL 60612, USA 2 Interdepartmental 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 molar emergence can therefore be used to broadly infer the life histories of fossil primate species. One method of determining age at first molar emergence is to determine the age at death of fossil individuals that were in the process of erupting their first molars. This was done for an infant partial mandible of Afropithecus turkanensis (KNM-MO 26) from the w17.5 Ma site of Moruorot in Kenya. A range of estimates of age at death was calculated for this individual using the permanent lateral incisor germ preserved in its crypt, by combining the number and periodicity of lateral enamel perikymata with estimates of the duration of cuspal enamel formation and the duration of the postnatal delay in the inception of crown mineralization. Perikymata periodicity was determined using daily cross striations between adjacent Retzius lines in thin sections of two A. turkanensis molars from the nearby site of Kalodirr. Based on the position of the KNM-MO 26 M1 in relation to the mandibular alveolar margin, it had not yet undergone gingival emergence. The projected time to gingival emergence 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 average values from extant great apes and humans for the estimated growth parameters. Even the absolute minimum value is well outside the ranges of extant large Old World monkeys for which there are data (12.5 to <25 months), but is within the range of chimpanzees (25.7 to 48.0 months). It is inferred, therefore, that A. turkanensis had a life history profile broadly like that of Pan. This is additional evidence to that provided by Sivapithecus parvada (Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations, 1997, 173) that the prolonged life histories characteristic of extant apes were achieved early in the evolutionary history of the group. However, it is unclear at present whether life-history prolongation in apes represents the primitive catarrhine pace of life history extended through phyletic increase in body mass, or whether it is derived with respect to a primitive, size-adjusted life history that was broadly intermediate between those of extant hominoids and cercopithecoids. Life history evolution in primates as a whole may have occurred largely through a series of grade-shifts, with the establishment of fundamental life-history profiles early in the histories of major higher taxa. These may have included shifts that were largely body mass dependent, as well as those 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: +1-312-996-6044 E-mail addresses: [email protected] (J. Kelley), [email protected] (T.M. Smith). 0047-2484/03/$ - see front matter  2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0047-2484(03)00005-8

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Introduction Life history is one of the most fundamental attributes of a species’ biology. The term ‘life history’ encompasses a host of specific traits, but is most commonly conceptualized in terms of a series of growth and maturational phases ultimately related to the scheduling of reproduction and lifetime reproductive output. These include gestation period, age at weaning, age at sexual maturity and first breeding, interbirth interval, and longevity. Given the importance of life history, it is not surprising that it has become an important issue in primate paleobiology. To date, most of the effort to reconstruct the life histories of extinct species has been focused on the human lineage. However, attempts to reconstruct aspects of the life histories of extinct non-human primates are becoming increasingly common (Lee and Foley, 1993; Kelley, 1997, 2002; Kelley et al., 2001; Godfrey et al., 2002; Schwartz et al., 2002). The evolution of primate life histories, and the role of life history in the adaptive radiations of major primate groups, are also beginning to receive increasing attention (Charnov and Berrigan, 1993; Kelley, 1997, 2002; Ross, 1998; Godfrey et al., 2001; Macho, 2001). Among catarrhines, extant apes and Old World monkeys can be characterized as having undergone life-history divergence; apes have relatively slow life histories for their body mass whereas monkeys appear to have relatively fast life histories for their mass (Fig. 1; see also Harvey and Clutton-Brock, 1985; Watts, 1990; Kelley, 1997). This difference is most evident in a comparison of gibbons and monkeys, as the body mass range of gibbons (approximately 5–10 kg) falls entirely within that of Old World monkeys, and average mass in the two groups is similar. For the timing of any given life-history trait in relation to body mass, gibbons lie above the primate regression line while Old World monkeys lie below (Fig. 1). It has been hypothesized that the life-history divergence between apes and Old World monkeys had its genesis soon after the cladogenesis of the two groups (Kelley, 1997), which probably took place in the late Oligocene to earliest Miocene (Kumar and Hedges, 1998). This could plausibly be

Fig. 1. Least squares regression of age at first breeding (months) against average body mass (kg), both log-transformed, in the following extant primate higher taxa (numbers of included species 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 breeding from Godfrey et al. (2001) and from K. Strier, personal communication, for Brachyteles arachnoides (Atelini); body mass data from Smith and Jungers (1997). Body masses are averages of male and female means for the included species. Results are unchanged using female mass rather than average mass.

inferred from the slowed life histories of gibbons, which probably diverged from the great apes in the early Miocene or early middle Miocene (Caccone and Powell, 1989), but ultimately this hypothesis can only be tested in the fossil record. Importantly, the above hypothesis presumes that life histories have changed in both the hominoid and cercopithecoid lineages from a primitive catarrhine condition that was broadly intermediate, with life-history prolongation in hominoids and acceleration in cercopithecoids. However, it is presently unclear that this presumption is warranted, an issue that will be further explored below. The principal means for inferring the life histories of fossil species has been through the chronology of dental development. The timing of dental development in all mammals is highly correlated with ontogeny as a whole; a functioning dentition must be in place when an animal is weaned and must develop in a way that will last for the

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projected lifetime of the individual. The link between dental development and ontogeny is evidenced by the correlations between aspects of dental development and individual life-history variables (Smith, 1989, 1991, 1992). Dental development is, in a sense, just another life-history trait (Smith and Tompkins, 1995), but one that is preserved in the fossil record. While there is systematic variation in the relationship between dental development and various life-history attributes, primarily associated with variation in diet (Godfrey et al., 2001), as well as occasional idiosyncratic variation associated with specific ecological demands (Godfrey et al., 2002; Schwartz et al., 2002), within a broad framework the pace of dental development serves as a reliable proxy for the pace of life history as a whole. Among living primates, it has been demonstrated that age at first molar emergence is a particularly good correlate of various life-history traits (Smith, 1989, 1991), emergence being defined as the initial penetration of the oral gingiva by the molar cusps. Thus, if the average age at first molar emergence can be established for a fossil species, then its general life-history profile can be characterized as well. The most straightforward approach to estimating age at first molar emergence in fossil species is to determine the age at death for individuals that died while in the process of erupting their first molars, making necessary adjustments if the stage of eruption differs from that associated with gingival emergence. Ages at death can be determined with a high degree of precision using the record of incremental growth lines that are preserved in all teeth, including fossilized teeth (Boyde, 1963; Bromage and Dean, 1985; Dean et al., 1986, 1993b; Dean, 1987a, 1989; Beynon et al., 1991; Macho and Wood, 1995; Kelley, 1997, 2002; Dirks, 1998; Antoine et al. 1999). To date, age at first molar emergence has been directly calculated for only two fossil apes. The first was an individual of Sivapithecus parvada from a 10 Ma locality in the Siwaliks of Pakistan. This individual was found to have an age at first molar emergence that was well within the range of extant chimpanzees, probably equal to or slightly greater than the chimpanzee mean (Kelley, 1997,

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2002). However, the relatively late date for S. parvada limits its usefulness as a meaningful test of the hypothesis of an early life-history divergence between apes and monkeys in the latest Oligocene. The second fossil ape was an individual of Afropithecus turkanensis from the early Miocene of Kenya (Kelley, 1999, 2002). In the following analysis we revise the earlier estimate of age at first molar emergence for this individual, which was preliminary and lacked a full description of the methods of analysis. The revised estimates reported here incorporate new data on molar crown formation in Afropithecus (see also Smith et al., 2003) and a more thorough and rigorous analysis of relevant comparative data. Knowing the age at first molar emergence in Afropithecus is important because it nearly doubles the antiquity of such estimates for fossil apes, approaching the estimated date of divergence of apes and Old World monkeys. In addition, this analysis provides further data for the documentation of dental development in fossil apes, which complements information on developmental chronology and crown formation times derived from histological studies (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 analysis is KNM-MO 26, a partial right mandibular corpus of an infant from the site of Moruorot in Kenya (Fig. 2). Moruorot lies in the Lothidok Range west of Lake Turkana, approximately 10 km southeast of Kalodirr, the site from which most remains of Afropithecus have been recovered (Leakey et al., 1988; Leakey and Walker, 1997). The Moruorot localities lie within the lower part of the Kalodirr Member of the Lothidok Formation and therefore date to approximately 17.5 Ma (Boschetto et al., 1992), or late early Miocene. KNM-MO 26 preserves the deciduous fourth premolar (dP4) and first molar (M1), as well as the permanent lateral incisor (I2), canine (C) and premolar (P) germs within their crypts (Figs. 2

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

and 3). The M1 was in the process of erupting when the individual died, with the cusp apices lying just superior to the mandibular alveolar margin. The alveolar bone mesial to the I2 germ was broken away, exposing the tooth within its crypt surrounded by a hardened matrix. The matrix within the crypt was carefully removed with a dental pick and needle probe, exposing much of

the labial and lingual surfaces of the tooth and the mesial aspect of the crown apex. Calculating age at death Age at death for the individual represented by KNM-MO 26 can be determined using the I2 germ, which was still developing when the

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Fig. 3. Radiograph of KNM-MO 26.

individual died (the incisor crowns are still developing when the first molar emerges in most higher primates). Age at death is calculated by adding the time that elapsed between birth and the inception of I2 crown mineralization (postnatal delay) to the duration of crown formation up until the time of death. Crown formation time is determined using the incremental growth lines preserved in the enamel. The use of incremental growth lines for determining ages at death in infants is discussed in detail in Boyde (1963), Bromage and Dean (1985), Dean et al. (1986, 1993a,b), Dean (1987b), Beynon et al. (1991), Kelley (1997), Antoine et al. (1999), and Ramirez Rozzi (2002) and will be only briefly reviewed here. Enamel incremental lines include both short-period lines known as cross-striations, which record daily increments of enamel deposition, and long-period lines known as striae of Retzius or Retzius lines, which record brief, periodic disruptions in ameloblast secretion across the entire developing enamel front. Retzius line periodicity, which is the number of daily crossstriations between Retzius lines, is constant within all teeth of an individual, but varies to some extent

among individuals within a species (Dean, 1987a,b, 1989; Dean and Beynon, 1991; Beynon et al., 1991; Dean et al., 1993a; FitzGerald, 1998; Schwartz et al., 2001). The surface manifestations of the Retzius lines are known as perikymata, which have, therefore, the same periodicity as the Retzius lines (Fig. 4). Crown formation time in teeth that have not completed their development is calculated as the sum of the time required to form the cuspal enamel plus the time to form the amount of lateral enamel present at the time of death. Cuspal enamel is the earliest formed enamel, in which successive Retzius lines are completely buried under subsequently formed enamel. Lateral enamel is defined as the enamel formed subsequent to the first Retzius line that reaches the crown surface (see illustrations in Bromage 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 of KNM-MO 26 to directly observe histological structures. Therefore, values for certain growth parameters listed above had to be estimated from studies of dental development in extant apes

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Fig. 4. Naturally fractured surface of the lateral enamel of an Afropithecus turkanensis molar (KNM-WK 24300, RM2) showing striae of Retzius meeting the surface of the enamel and forming perikymata. Note that perikymata only form where striae of Retzius reach the tooth surface. The cervix of the tooth is below the bottom right edge of the image. The field width of the image is approximately 750 µm.

and other fossil primates, and from information derived from a histological study of two Afropithecus molars (see Smith et al., 2003). For each of the growth parameters there is both intra and interspecific variation. Thus, several estimates of age at death and age at M1 emergence were calculated for KNM-MO 26, using combinations that incorporated conservative minimum values, as well as average values. The estimates of age at M1 emergence reported here therefore include a minimum estimate, as well as a range of more probable estimates, since it is improbable that any one individual will express the minimum known values for all growth parameters. We also calculated a single maximum estimate for age at M1 emergence using the maximum known values for each estimated growth parameter. Specific issues pertaining to the estimates or calculations of each of the growth parameters are discussed below. Postnatal delay in the inception of I2 mineralization To estimate the postnatal delay in the KNM-MO 26 I2, we compiled comparative data

on I2 postnatal delay from all extant apes and humans for which histological data were available [histological and radiological determinations of the inception of mineralization can differ substantially, with histological determination being more accurate (Beynon et al., 1998; Reid et al., 1998a,b)]. Comparable data were also available for the I2 of Proconsul heseloni (Beynon et al., 1998), a possibly closely related contemporary of Afropithecus (Begun et al., 1997; Leakey and Walker, 1997; Harrison, 2002). Duration of cuspal enamel formation This 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 26 could not be sectioned for direct observation. Cuspal enamel formation time is related to enamel thickness, although the relationship between the two will vary among species depending upon ameloblast secretion rates and the degree of sinuosity of the enamel prisms as they course from the enamel-dentine junction (EDJ) to the tooth surface (Dean, 1998). As stated above, the cuspal

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enamel thickness of the KNM-MO 26 I2 is unknown. While cuspal enamel thickness and the duration of cuspal enamel formation have been calculated for two A. turkanensis molars (Smith et al., 2003), it cannot be assumed that incisor cuspal enamel will have the same values (Dean and Reid, 2001). Duration of lateral enamel formation This 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 the KNM-MO 26 I2, the tooth was molded within its crypt using Colte`ne President Plus Regular Body, and a replica made using Ciba-Geigy Araldite GY 506 epoxy resin cured with hardener HY 956. The replica was then sputtercoated with a thin layer of gold-palladium and examined with a JEOL scanning electron microscope. A photo montage was constructed of the mesio-labial tooth surface from the developing cervical region to a point near the crown incisal edge. Perikymata were not expressed over the apical 2.5 mm of the I2 crown, due to a combination of post-depositional chemical weathering or abrasion and a true fading out of perikymata expression over the apical-most portion of this interval. The latter is most likely due to the acute angle of incidence of the Retzius lines to the tooth surface apically, which sometimes results in the nonexpression of perikymata for the apical-most Retzius lines of lateral enamel. A similar trend in perikymata expression was seen in the two Afropithecus molars reported on by Smith et al. (2003). Even when there are no apical perikymata expressed, histological sections of hominoid permanent anterior teeth demonstrate that the first Retzius line reaching the tooth surface (delineating cuspal from lateral enamel) is invariably near the incisal edge (C. Dean, personal communication). Thus, the number of Retzius intervals in the apical-most 2.5 mm of the KNM-MO 26 I2 crown had to be estimated. This was done using perikymata counts over the same interval in two lower lateral incisor crowns of P. heseloni and P. nyanzae (Beynon et al., 1998,

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Appendix 1), combined with the spacing of perikymata adjacent to the non-expressed region on the KNM-MO 26 I2. The periodicity of Retzius lines was determined in two Afropithecus molars that were sectioned as part of a separate study on enamel thickness and microstructure (Smith et al., 2003), using two methods described by Dean et al. (1993a,b) and Swindler and Beynon (1993). Where possible, direct counts of the number of cross-striations between adjacent Retzius lines were made by using both scanning electron and polarized light microscopic images. Additionally, the average spacing between Retzius lines was divided by the average spacing of cross-striations measured from prisms in the same area, and the number rounded to the nearest whole integer (see Smith et al., 2003 for details of specimen preparation and methodology). Estimating age at gingival ermergence of M1 based on age at death As previously noted, the individual represented by KNM-MO 26 died before the erupting M1 would have emerged from the gingiva. Since gingival emergence is the standard for comparison of age at M1 eruption among extant species, the age at which this would have occurred in KNM-MO 26 must be estimated. This was done using comparative data on M1 emergence in extant baboons, and compared to results from a previous study on chimpanzees (Zuckerman, 1928). From June, 1995 through June, 1999 the senior author carried out a longitudinal radiographic study of M1 emergence and root formation on a captive breeding colony of Papio anubis housed at the Biological Research Laboratories at the University of Illinois at Chicago. Approximately every three months, all of the baboons in the colony were sedated for TB testing. While under sedation, all infant individuals between approximately one and three years of age were given oral examinations, and periapical x-rays were taken of the M1 and lower deciduous premolars. On several occasions, examination coincidentally occurred either just as the M1 mesial cusps (the first to present) were emerging from the gingiva, with emergence clearly having taken place

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

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

Species

Months

Source

Species

Months

Source

Proconsul heseloni Hylobates lar Gorilla gorilla Pan troglodytes

1.5 3.7 11.0 2.5 7.9 8.4 13.0 0 4.8 8.3

Beynon et al., 1998 Dirks, 1998 Beynon et al., 1991 Reid et al., 1998a Reid et al., 1998a Reid et al., 1998a Beynon et al., 1991 Dean and Beynon, 1991 Reid et al., 1998b Dean et al., 1993a

Proconsul heseloni Hylobates lar Gorilla gorilla Pan troglodytes

4.0 4.5 4.0 5.3,6.4† 5.8 6.0,6.8† 6.4 5.5 5.8 7.0,7.7† 8.0

Beynon et al., 1998 Dirks, 1998 Beynon et al., 1991 Reid et al., 1998a Reid et al., 1998a Reid et al., 1998a Reid et al., 1998a Reid et al., 1998b Reid et al., 1998b Reid et al., 1998b Reid et al., 1998b

Pongo pygmaeus Homo sapiens

Homo sapiens

†

within the preceding few days, or when the M1 mesial cusps were visible beneath a thin layer of gingival tissue, from which it was determined that gingival emergence was imminent. For four of these individuals, there was a radiographic record of previous examinations that could be used to estimate the time interval between gingival emergence and the developmental stage equivalent to that of the KNM-MO 26 individual when it died; that is, with the M1 cusp apices just above the mandibular alveolar margin. Similar, although less precise, data on M1 eruption and gingival emergence were reported for two infant chimpanzees by Zuckerman (1928).

Results Postnatal delay in the inception of I2 mineralization Data on the postnatal delay in I2 mineralization in extant apes and humans, and in P. heseloni, are shown in Table 1. Values among extant apes and humans range from 0 to 13.0 months, with a mean of 6.6 months. Based on these limited data, there are no obvious associations between the duration of the postnatal delay in mineralization and either body size or phylogeny, although the two highest values are most likely the males of the two largest extant apes. Where there are data on intraspecific variation it appears to be substantial; for example, there is more than an eight month difference

Antimeres from the same individuals.

between the earliest and latest onsets among three human I2s. These data make it difficult to establish any criteria by which to choose the most appropriate estimate for the postnatal delay in the KNM-MO 26 I2. Therefore, in keeping with our methodological protocol, we selected the minimum and average values of 0 and 6.6 months, respectively, as estimates for the Afropithecus infant. Duration of cuspal enamel formation Data on the duration of I2 cuspal enamel formation in extant apes and humans, and in P. heseloni, are shown in Table 2. Values for extant apes and humans range between 4.0 and 8.0 months, with a mean of 6.0 months. Both intraspecific and interspecific variation for the duration of cuspal enamel formation are substantially less than for the postnatal delay in I2 mineralization. Duration of lateral enamel formation The labial face of the KNM-MO 26 I2 preserves 82 perikymata (Fig. 5). Perikymata are expressed from within about 2.5 mm of the crown apex down to the last formed immature enamel close to the advancing cervical line. Our estimate of the number of Retzius lines unexpressed as surface perikymata over the apicalmost 2.5 mm of lateral enamel is based in part on the number of perikymata over the same part of

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the crown in P. nyanzae and P. heseloni. Starting from the incisal edge, perikymata counts in 1 mm increments over the apical 3.0 mm of the crown of a P. nyanzae I2 (KNM-RU 1716) are 2, 8 and 8; the same values in an I2 of P. heseloni (KNM-RU 7290) are 8, 11 and 13 (Beynon et al., 1998). Eliminating half of the perikymata over the cervical-most 1 mm increment (to equal 2.5 mm) results in totals of 14 and 26 perikymata over this interval, with a mean of 20. We thus used 14 as our conservative estimate and 20 as an average estimate of the number of unexpressed perikymata in the apical 2.5 mm of lateral enamel in the Afropithecus I2. The total number of perikymata plus lateral enamel Retzius lines not expressed as perikymata in the KNM-MO 26 I2 was therefore estimated to be 96 or 102 (82 plus either 14 or 20). Perikymata on the Afropithecus I2 itself suggest that the higher estimate is likely to be closer to the actual value. The apical-most 1 mm of the KNM-MO 26 I2 crown over which perikymata are expressed (adjacent to the non-expressed region) contains 12 or 13 perikymata. Since perikymata spacing over the entire labial crown surface is highly uniform (see Fig. 5), it seems likely that perikymata numbers closer to those of the P. heseloni incisor would have been present in the Afropithecus I2 as well. The Retzius line periodicities in the two sectioned Afropithecus molars were determined to be 7 and 8 days, respectively (Fig. 6; see also Smith et al., 2003). Multiplying these values by the lateral enamel perikymata estimates of 96 and 102 gives an estimated range for the duration of lateral enamel formation in the KNM-MO 26 I2 of between 672 days (22.2 months) and 816 days (26.9 months) (Table 3). Age at death of KNM-MO 26

Fig. 5. SEM montage of the mesio-labial face of the KNM-MO 26 Afropithecus I2 showing the development of perikymata. The interval over which perikymata are expressed equals 5.8 mm. Cervical is toward the bottom.

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

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Fig. 6. Polarized light micrograph of the outer lateral enamel of Afropithecus turkanensis (KNM-WK 24300, RM2). The surface of the tooth 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 eight cross-striations, each representing one daily increment of enamel deposition. Note that there are seven cross-striations between Retzius lines, the eighth being on the Retzius line. The field of width of the image is approximately 155 µm.

line periodicities, are 26.2 and 29.4 months. Using the average values for the estimated growth parameters results in estimated ages at death of 34.8 to 39.5 months, also based on 7 and 8 day Retzius line periodicities. Time from death to M1 emergence in KNM-MO 26 Our estimate of the time interval between the developmental stage of KNM-MO 26 at the time

of death and the eventual time of M1 emergence is based on the progression and timing of first molar eruption in extant baboons and chimpanzees. In all four of the baboons for which M1 gingival emergence was observed, the radiograph taken three months prior reveals the M1 mesial cusps to be at or just below the level of the alveolar margin (Figures 7 and 8). This is a slightly earlier eruption stage than had been reached by the KNM-MO 26 individual when it died, in which the M1 cusp apices are just above the alveolar margin (Figs. 2

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

Minimum Average

Retzius periodicity

I2 postnatal delay

I2 cuspal enamel

I2 lateral enamel

Age at death

7 8 7 8

0.0 0.0 6.6 6.6

4.0 4.0 6.0 6.0

22.2–23.6 25.4–26.9 22.2–23.6 25.4–26.9

26.2–27.6 29.4–30.9 34.8–36.2 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, the cuspal enamel formation time and the lateral enamel formation time. The ranges for the duration of I2 lateral enamel formation reflect the use of either 96 or 102 lateral enamel perikymata (see text). Minimum and average estimates explained in text.

and 3). Judging by the amount of tooth movement that took place in the four baboons during the three month interval between the first x-ray and gingival emergence (Figures 7 and 8), we estimate that the small difference in the M1 eruption stage between KNM-MO 26 and the four baboons at the time of the first x-ray corresponds to at most one month. According to the baboon eruption schedule, therefore, KNM-MO 26 would have died approximately two months prior to gingival emergence. While the eruption schedules in these captive baboons may be somewhat accelerated compared to those of wild baboons (see data in Table 5; also Phillips-Conroy and Jolly, 1988), the percentage difference is not likely to be significant for the time interval being discussed here of only a few months (see further below). Zuckerman (1928) presented similar oral examination and radiographic data on two infant chimpanzees, which, as expected, suggest a somewhat slower M1 eruption schedule than in baboons. The data for one animal in particular, Clarence, are sufficiently precise for comparison with the baboon results described above. An initial radiograph revealed the M1 “crown” to be level with the alveolar margin, which we interpret to mean that the cusp apices were at the alveolar margin. In a second radiograph six months later the M1 was described as being “fully erupted,” which presumably means that the tooth was level with the occlusal plane of the deciduous premolars. An oral examination was made sometime between five and six months after the first radiograph was taken and revealed that the M1s “were cutting the gums” (Zuckerman, 1928, p. 25). Taken together, these observations suggest that the

interval between M1 cresting the alveolar margin and gingival emergence probably takes somewhere between four and five months in chimpanzees, in contrast to the three months that it takes in baboons. Combining the baboon and chimpanzee data, the additional time that would have been needed to achieve M1 gingival emergence in the KNM-MO 26 infant can be estimated to be between about two and four months. Adding two and four months to each of the estimates of the age at death of KNM-MO 26 produces minimum estimates for the age at M1 emergence of 28.2 and 31.4 months using the baboon schedule of M1 eruption (based on 7 and 8 day Retzius periodicity, respectively), or 30.2 and 33.4 months using a chimpanzee schedule (Table 4). Estimates of age at M1 emergence using average rather than minimum values for estimated I2 crown growth parameters range between 36.8 and 43.5 months. Although not included in the various calculated estimates, the maximum estimated age at M1 emergence in KNM-MO 26 using the maximum values of all estimated growth parameters, combined with the highest estimate of missing lateral enamel perikymata (26) and an 8 day periodicity, is 53.4 months. Since the principal concern of this study was to determine whether or not age at M1 emergence in the KNM-MO 26 individual was earlier than in extant chimpanzees, the maximum estimate will not be discussed further. We simply note that it is equally unlikely that one individual would uniformly express the maximum known values of all the estimated growth parameters as that it would uniformly express all the minimum values.

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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 revealed by oral examination.

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Table 4 Estimated ages at M1 emergence in KNM-MO 26 (months) Retzius periodicity Minimum7 8 Average 7 8

Age at death

Age at M1 emergence (baboon model) Age at M1 emergence (chimpanzee model)

26.2–27.6 29.4–30.9 34.8–36.2 38.0–39.5

28.2–29.6 31.4–32.9 36.8–38.2 40.0–41.5

30.2–31.6 33.4–34.9 38.8–40.2 42.0–43.5

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

Discussion Age at first molar emergence and life history in Afropithecus While the minimum estimate for age at M1 emergence in KNM-MO 26 presented here is only slightly later than previously reported for this individual (Kelley, 1999, 2002), the other newly calculated estimates greatly extend the range into which the actual age probably falls. This extended range is partly due to the addition here of actual data on Retzius line periodicity in A. turkanensis, which is greater than the estimated value used in the earlier reports. It also reflects increases in the estimates for the duration of incisor cuspal enamel formation and the postnatal delay in incisor mineralization, based on a more thorough analysis of the comparative data from extant species. The estimates for the age at M1 emergence in KNM-MO 26 (28.2–43.5 months) fall within the range of Pan troglodytes (25.7–48.0 months), and encompass the chimpanzee mean of 38.9 months (Table 5). The means of the range of estimates using baboon and chimpanzee schedules of M1 eruption are, respectively, 34.9 and 36.9 months. What is most important from our perspective, however, is that even the absolute minimum estimate of 28.2 months is well outside the ranges of M1 emergence of even the largest extant cercopithecids for which there are reliable data, the maximum age being less than 25 months (Table 5). Most of the comparative data in Table 5, however, are from captive animals. As noted by Smith et al. (1994), data are equivocal regarding the degree to which wild and captive populations might be expected to differ in their dental eruption

Table 5 Age at M1 emergence (months) in Afropithecus turkanensis, Pan troglodytes and extant cercopithecids Afropithecus turkanensis† Extant species Pan troglodytes Macaca mulatta M. fascicularis M. nemestrina M. fuscata Cercopithecus aethiops Papio anubis 1 P. anubis 2

Mean 39.1 16.2 16.4 16.4 18.0 10.0 20.0 16.7

28.2–43.5 Minimum 25.7 12.5 14 – – 7.9 >16 15.7

Maximum 48.0 22.6 20 18.6+ <24 12.0 <25 <21

Sources: Pan troglodytes (Smith et al., 1994); Macaca mulatta, Cercopithecus aethiops (Hurme and van Wagenen, 1961); Macaca fascicularis (Bowen and Koch, 1970); Macaca nemestrina (Swindler, 1985; B.H. Smith, personal communication—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 (Smith et al., 1994; B.H. Smith, personal communication—based on data in Kahumbu and Eley, 1991); Papio anubis 2 (J. Kelley, unpublished data from a longitudinal study of M1 eruption in a captive colony at The University of Illinois at Chicago). Reliability of range data for extant species varies depending on methodology and sample size. † Range of estimates.

schedules. Phillips-Conroy and Jolly (1988) reported that the eruption schedules of captive baboons were accelerated compared to those of wild-living animals, but neither Kahumbu and Eley (1991) nor Iwamoto et al. (1987) found any systematic differences between wild and captive populations of, respectively, baboons and macaques. The baboon data in Table 5 tend to support accelerated dental development and eruption in captive animals. Of the two Papio anubis

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populations reported upon in Table 5, P. anubis 1 was a wild population whereas P. anubis 2 is the breeding colony at The University of Illinois at Chicago. The mean percent acceleration in the age at M1 emergence in the captive population is 16.5%, but, as noted by Iwamoto et al. (1987), this may simply reflect genetic differences between these two particular populations, rather than a systematic effect to be expected from all wild-captive comparisons. Importantly, with respect to interpretation of KNM-MO 26, it is still the case that the upper limit of the cercopithecid range data is for the wild P. anubis population. Given the broad relationship within higher taxa between body size and lifehistory variables (including dental development), it is likely that the wild P. anubis maximum from Table 5 is near the upper limit of the range of at M1 emergence ages for all cercopithecoids. While it is possible that KNM-MO 26 represents an individual that is near the maximum of the A. turkanensis range of M1 emergence ages, it is more probable as a simple consequence of central tendency that it is closer to the species mean. To produce a mean age of M1 emergence in A. turkanensis that is within the cercopithecid range, and therefore outside the chimpanzee range, would require that, (1) the minimum estimate for age at M1 emergence in KNM-MO 26 is the closest of the various estimates to the actual age, and (2) that even this age is near the maximum for the species as a whole. This is a possible, but much less probable, set of circumstances, we conclude, therefore, that even though our analysis is for a single individual, the mean age of M1 emergence in A. turkanensis was within the range of extant chimpanzees, and perhaps close to the chimpanzee mean. As noted earlier, among primates, age at M1 emergence is correlated with a variety of lifehistory attributes (Smith, 1989, 1991; also Fig. 9). Because these analyses encompass species representing all major groups of extant primates, age at M1 emergence can be used to infer life history in fossil primates that lie within the extant primate radiation. The strength of the M1 emergence-life history relationships show that M1 emergence data can legitimately be used to generally categorize the

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

life histories of fossil species, for example as Old World monkey-like, ape-like or human-like. However, the correlations between life-history variables and M1 emergence in extant primates are insufficiently robust, and the errors in estimates of age at M1 emergence in fossil species are too large, to reliably calculate the values of specific life-history variables in fossil species based solely on estimates of age at M1 emergence (see Smith et al., 1995; Smith, 1996). The estimated age at M1 emergence in KNM-MO 26, and the implications of this estimate for characterizing age at M1 emergence in A. turkanensis as a whole, suggest that life history in this early hominoid can be broadly characterized as having been like that of living great apes. First molar emergence and life-history evolution in Hominoidea and other primates In the following discussion of life-history evolution, age at M1 emergence is used as a substitute or proxy variable for the overall pace of life history. There are several reasons for doing this rather than using the specific life-history traits with which age at M1 emergence is correlated, and that more

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directly reflect reproductive and maturational milestones. First, in many species, average age at M1 emergence is known more reliably than are the average values for many other life-history variables. Second, it is likely that there is more facultative intraspecific variation in reproductive and maturational traits than there is in age at M1 emergence. Plasticity in life-history traits, even over the course of individual life spans, appears to be an important aspect of life-history adaptation. Such plasticity is not likely to be reflected in dental development. Finally, at present, M1 emergence is one of only two or perhaps three variables (the others being brain size and possibly molar crown formation time) by which extinct species can be included in discussions of life history. Regarding molar crown formation, a recent study by Macho (2001) demonstrated that, within primates as a whole, both M1 crown formation time and average molar crown formation time are significantly correlated with a number of lifehistory traits. However, there are a number of reasons for withholding judgment on these results. Among these are the use of the primate life-history data compiled by Harvey and Clutton-Brock (1985), much of which is now known to be either in error or at least unreliable (see, for example, Smith et al., 1995 and Smith and Jungers, 1997). Moreover, many of the crown formation times in Macho’s study are calculated estimates rather than direct histological measurements (Shellis, 1998), some of which are demonstrably in error when compared to known crown eruption ages (Smith et al., 1994). Finally, for some species (e.g., chimpanzees and humans) molar crown formation times simply do not reflect known differences in life-history values, differences that are more or less concordant with average ages at M1 emergence. The reason for this may have to do with variation in rates of root formation, especially initial root formation. Disparities between crown formation times and inferred or calculated ages at M1 emergence are beginning to become apparent among fossil apes as well, exemplified by comparisons between the similarly sized Proconsul nyanzae, Dryopithecus laietanus, and Afropithecus turkanensis (Beynon et al., 1998; Kelley et al., 2001; Smith et al., 2003). It can be expected that further study

of additional extant and fossil species will help to elucidate the relationships between molar crown formation times, ages at molar emergence, and life history attributes. It has been hypothesized that the slowed life histories that characterize the extant apes, particularly the great apes, might have had their genesis during the early evolutionary history of the Hominoidea, and that they might in fact have been the fundamental adaptive shift underlying the cladogenesis of hominoids and cercopithecoids (Kelley, 1997). Prior to the analysis described here, the oldest fossil ape for which age at M1 emergence had been determined was a 10 Ma individual of Sivapithecus parvada from the Siwaliks of Pakistan (Kelley, 1997, 2002). The estimate of age at M1 emergence for the 17.5 Ma individual of A. turkanensis nearly doubles the antiquity of such estimates for fossil hominoids and hominids. The finding of an age at M1 emergence that is essentially like that of extant chimpanzees, and the inference therefore of an essentially modern great ape life history in A. turkanensis, could be viewed as lending additional support to the above hypothesis of life-history evolution in the Hominoidea. There are, however, a number of ways to interpret the data on M1 emergence in primates as a whole, with different implications for life-history evolution in the Hominoidea and other higher primate taxa. Fig. 10 shows two different interpretations of the relationship between M1 emergence and body mass in extant primates. Plotted in each are the 24 extant primate species (including humans) for which there are reliable data on age at M1 emergence (Table 6). Fig. 10a shows a single linear regression for all the included extant species, purposely left unidentified. Fig. 10b shows the various species identified by higher taxonomic group, and also includes estimates of age at M1 emergence and body mass for A. turkanensis and S. parvada. Statistics for the various regressions depicted in Fig. 10 are shown in Table 7. Based on Fig. 10a, the late age at M1 emergence in Afropithecus could be interpreted as a simple consequence of large body mass (estimated average mass=30 kg), without any necessary phylogenetic implications. The correlation between age

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Fig. 10. Two possible interpretations of age at M1 emergence in relation to body mass in primates (all regressions are least squares—regression statistics in Table 7); (a): Phylogenyneutral interpretation; (b): Phylogeny-based interpretation revealing 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 Sivapithecus parvada (S). For extant species, age at M1 emergence from Smith 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 based on postcranial size (Leakey et al., 1988) and an estimated male mass of 35 kg (Kappelman et al., in press); age at M1 emergence estimated at 36 months (see text). For S. parvada, average body mass 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).

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at M1 emergence and body mass for all the included species is highly significant (Table 7). By this interpretation, any primate with the body mass of a small chimpanzee would be expected to have an age of M1 emergence within the chimpanzee range, and, by implication, an overall life history that was similar to that of a chimpanzee. In Fig. 10b, there is still a significant relationship between age at M1 emergence and body mass within the different higher taxa (excepting hominoids, which is a simple consequence of small sample size). However, the four included higher taxa (plus Homo) are also characterized by a series of apparent grade-shifts in age at M1 emergence. The grade-shifts from lemuriforms to each of the anthropoid groups, from cercopithecids to hominoids, and from non-human hominoids to Homo are clear. Interpretation of the cebid regression is less so, as it implies that a cebid the size of a chimpanzee would have an age at M1 emergence that is greater than that of modern Homo. Understanding life-history evolution in platyrrhines is in fact critical for interpreting the significance of M1 emergence data among fossil hominoids, and for understanding life-history evolution in hominoids more generally. A plausible interpretation of the data in Fig. 10b is that both platyrrhines (here represented only by cebids) and hominoids broadly represent the primitive anthropoid condition and that cercopithecids are derived with respect to both, having accelerated life histories (see also Fig. 1). In this case, the absolutely more prolonged life histories of apes relative to platyrrhines would be most reasonably interpreted as a simple consequence of increasing body size. However, the platyrrhine regression in Fig. 10b has a very limited representation of taxa, consisting of several callitrichines and two species of Cebus. The slope is substantially greater than in either of the other anthropoid groups, but could be significantly altered with a more representative sample of taxa. If life history has slowed in Cebus relative to some or most other platyrrhine genera, or if life history has accelerated in callitrichines, perhaps in association with dwarfing, then the slope is artificially high. If so, then the primitive condition for platyrrhines, and for catarrhines

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

Age at M1 emergence (months)

Average body mass (kg)

Cheirogaleus medius Varecia variegata Lemur catta Eulemur fulvus E. macaco Propithecus verreauxi Galago senegalensis Callithrix jacchus Saguinus fuscicollis S. nigricollis Cebus albifrons C. apella Saimiri sciureus Aotus trivirgatus Cercopithecus aethiops Macaca fascicularis M. fuscata M. mulatta M. nemestrina Papio anubis P. cynocephalus Trachypithecus cristata1 Pan troglodytes Homo sapiens2

0.84 5.76 4.08 5.04 5.16 2.64 1.20 3.72 4.10 3.35 12.72 13.80 4.44 4.32 9.96 16.44 18.00 16.20 16.44 20.04 20.04 12.00 39.12 66.03

0.18 3.58 2.21 2.13 1.82 3.55 0.21 0.37 0.35 0.48 2.74 3.09 0.72 0.78 3.62 4.48 9.51 6.54 7.58 18.10 17.05 6.44 53.00 59.00

M1 emergence data from Smith et al. (1994) and body mass data from Smith and Jungers (1997), with the following exceptions: 1 M1 emergence data from Wolf (1984). 2 M1 emergence data from Smith et al. (1995).

Table 7 Statistics for Fig. 10 least squares regressions Regression 1

Primate (ln) Primate (untransformed)2 Lemuriformes3 Cebidae3 Cercopithecidae3 Hominoidea (less Homo)3

y-intercept

Slope

Correlation

% Variance

p

1.142 5.144 0.946 1.833 2.053 2.438

0.595 0.876 0.538 0.636 0.341 0.305

0.911 0.941 0.896 0.960 0.799 0.972

0.831 0.886 0.803 0.922 0.638 0.944

0.000 0.000 0.006 0.001 0.017 0.152

1

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

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

case, life-history evolution in catarrhines would represent a true divergence, with life-history acceleration in cercopithecoids and prolongation in hominoids, and with both states being derived.

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In the overall scheme of Fig. 10b, the age at M1 emergence in Afropithecus may largely be a function of its being a hominoid. Certainly a lemuriform or cercopithecoid with the body mass of Afropithecus would be expected to have an age at M1 emergence that is substantially earlier (see further below). It is unclear at this point if this would also be the case for platyrrhines, or at least for some platyrrhines. If platyrrhines and hominoids together broadly represent the primitive anthropoid condition, then the M1 emergence age of Afropithecus would again largely be a function of its size. As important to this discussion is the hominoid regression. Since it includes only three species, two of which are extinct species with estimated ages at M1 emergence based on single individuals, its slope must also be regarded as highly uncertain. Moreover, the slope is largely determined by the body mass and age at M1 emergence estimates for A. turkanensis. Any changes in the estimates that we chose to represent A. turkanensis (30 kg average mass and 36 months for age at M1 emergence, the overall mean of the estimates) are likely to significantly alter the slope. The true nature of the relationship between body mass and age at M1 emergence in hominoids will only become clear when there are reliable data for the other great apes, particularly Gorilla, and for gibbons. The possibility at least of phylogenetically associated grade shifts in age at M1 emergence— and, by extension, in life history more generally— that appear to have been established during the early evolutionary history of the higher primate groups is interesting in a broader context. In a series of empirical studies of life-history variation in mammals as a whole, Harvey and colleagues (Harvey et al., 1989a,b; Read and Harvey, 1989) found that a disproportionate amount of the variation was at higher taxonomic levels, suggesting the early establishment of fundamental life-history suites that are subject to comparatively little change during the subsequent evolutionary history of the group, sometimes even in the event of significant changes in body size. Likewise, Martin and MacLarnon (1990) found evidence for conservative life-history evolution in the fossil record

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of equids, again even with substantial phyletic size increase. A similar pattern has recently been reported in members of two lemuriform sister-taxa, one extant (Indriidae) and one subfossil (Palaeopropithecidae) (Schwartz et al., 2002). Including subfossil species, members of these two groups span the body mass range from average-sized monkeys to chimpanzees. Indriids are remarkable for having exceptionally precocious dental development and an age at M1 emergence that is strongly temporally dissociated from many other life-history parameters (Godfrey et al., 2001, 2002). The recent confirmation of this phenomenon in the chimpanzee-sized subfossil Palaeopropithecus (Schwartz et al., 2002), is compelling additional evidence for the importance of phylogeny as well as body size in life-history evolution. However, as noted earlier in the discussion of the platyrrhine data, it cannot be assumed at present that all members of the different primate higher taxa plotted in Fig. 10b will fall within the life-history grade characteristic of the particular taxon. Both the cebid and the lemuriform regression lines are based on two clusters of species of substantially different body mass. Not only are the regression lines uncertain as a consequence, but the addition of species of intermediate or larger body mass might reveal departures among lower taxonomic ranks (ie., genera/tribes) from whatever dominant grade level that emerges. There might in fact be a greater expectation of this in older, more biologically diverse clades such as the platyrrhines or lemuriforms than in more recent clades like the extant cercopithecids. It can be anticipated that many plausible interpretations of life-history evolution in primates will be eliminated as the data on age at M1 emergence improve for both extant and fossil primates. Extant taxa that are especially important for improving the database include, in addition to the other great apes and gibbons noted above, atelids and additional cebids, smaller cercopithecines, additional colobines, and additional non-lemurid strepsirhines. Especially important fossil taxa include primitive catarrhines and species that extend the body mass ranges of their respective

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

Summary Estimates of the age at death were calculated for an infant of early Miocene A. turkanensis, KNM-MO 26, that was in the process of erupting its first molar. The estimates were based on the perikymata preserved on the lateral incisor germ in the mandible, combined with data on the duration of cuspal enamel formation and the length of the postnatal delay in the inception of I2 mineralization in extant apes and humans, as well as in species of Proconsul. A range of estimates was calculated to accommodate both intra and interspecific variation in the latter growth parameters. Perikymata periodicity was determined from histological sections of two A. turkanensis molars. As the eruption stage of the M1 in the A. turkanensis infant reveals that it had not yet achieved gingival emergence when the animal died, estimates of the projected age at M1 emergence were calculated from the age at death estimates combined with radiographic data on the progression of M1 eruption in baboons and chimpanzees. Estimates for the age at M1 emergence in KNM-MO 26 ranged from approximately 28 to 43 months, well outside the ranges of large extant cercopithecids for which there are comparable data, but comfortably within the range of chimpanzees. It is inferred from this result that life history in A. turkanensis was essentially like that of extant chimpanzees. This inference is compatible with the hypothesis that there was a shift to the prolonged life histories that characterize extant apes early in the evolution of the Hominoidea. However, this presumes a primitive condition for life history in catarrhines that was faster, when adjusted for body size, than in chimpanzees. Limited data from extant platyrrhines may indicate that this is not the case. A plausible interpretation of these data is that extant platyrrhines and hominoids together represent the primitive condition for life history, and that only cercopithecoids among living anthropoids have derived life histories, being highly accelerated.

It is proposed that life-history evolution in primates more generally occurred as a series of grade shifts among higher level taxa. Some or all of these shifts may largely reflect phylogeny, irrespective of body size. Others may reflect nothing more than changes in body size, still phylogenetically based, but along a common trajectory for the pace of life history. Regardless of the predominant mode of change, it is becoming increasingly clear that phylogeny as well as body size must be taken into account when attempting to reconstruct the life histories of fossil primate species.

Acknowledgements We gratefully acknowledge the Government of Kenya and the National Museums of Kenya for permission to study the Afropithecus fossils (Permit OP/13/001/10C 354 issued to JK). We thank Meave Leakey and William Anyonge, past Heads of the Palaeontology Division, and Emma Mbua, then Collections Manager of Palaeoanthropology, for facilitating our work at the KNM. JK expresses special gratitude to Jeff Fortman, Associate Director, and Sam Rosado and the other staff of the Biological Resources Laboratory, The University of Illinois at Chicago for their invaluable long-term assistance with the baboon radiographic project. We thank Chris Dean, Meave Leakey, Lawrence Martin, Don Reid, and Holly Smith for innumerable valuable discussions relating to the work reported here, and Terry Harrison plus three anonymous reviewers for comments on the manuscript. This research was supported by National Science Foundation grant SBR-9408664 to JK.

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