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 Kelley1*, Tanya M. Smith2 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)00005-8 308 J. Kelley, T.M. Smith / Journal of Human Evolution 44 (2003) 307–329 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 gesta- tion period, age at weaning, age at sexual maturity and first breeding, interbirth interval, and lon- gevity. 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. Fig. 1. Least squares regression of age at first breeding (months) However, attempts to reconstruct aspects of the against average body mass (kg), both log-transformed, in the life histories of extinct non-human primates are following extant primate higher taxa (numbers of included species in parentheses): Al, Alouattini (2); At, Atelini (2); Ca, becoming increasingly common (Lee and Foley, Callitrichinae (3); Cb, Cebinae (3); Ce, Cercopithecinae (6); Co, 1993; Kelley, 1997, 2002; Kelley et al., 2001; Colobinae (8); Ho, Hominidae (3); Hy, Hylobatidae (2); In, Godfrey et al., 2002; Schwartz et al., 2002). The Indriidae (3); Le, Lemuridae (7). Data on age at first breeding from Godfrey et al. (2001) and from K. Strier, personal evolution of primate life histories, and the role of communication, for Brachyteles arachnoides (Atelini); body life history in the adaptive radiations of major mass data from Smith and Jungers (1997). Body masses are primate groups, are also beginning to receive averages of male and female means for the included species. Results are unchanged using female mass rather than average increasing attention (Charnov and Berrigan, 1993; mass. Kelley, 1997, 2002; Ross, 1998; Godfrey et al., 2001; Macho, 2001). Among catarrhines, extant apes and Old World inferred from the slowed life histories of gibbons, monkeys can be characterized as having under- which probably diverged from the great apes in the gone life-history divergence; apes have relatively early Miocene or early middle Miocene (Caccone slow life histories for their body mass whereas and Powell, 1989), but ultimately this hypothesis monkeys appear to have relatively fast life histories can only be tested in the fossil record. for their mass (Fig. 1; see also Harvey and Importantly, the above hypothesis presumes Clutton-Brock, 1985; Watts, 1990; Kelley, 1997). that life histories have changed in both the This difference is most evident in a comparison of hominoid and cercopithecoid lineages from a gibbons and monkeys, as the body mass range of primitive catarrhine condition that was broadly gibbons (approximately 5–10 kg) falls entirely intermediate, with life-history prolongation in within that of Old World monkeys, and average hominoids and acceleration in cercopithecoids. mass in the two groups is similar. For the timing of However, it is presently unclear that this presump- any given life-history trait in relation to body tion is warranted, an issue that will be further mass, gibbons lie above the primate regression line explored below. while Old World monkeys lie below (Fig. 1). It has The principal means for inferring the life histo- been hypothesized that the life-history divergence ries of fossil species has been through the chronol- between apes and Old World monkeys had its ogy of dental development. The timing of dental genesis soon after the cladogenesis of the two development in all mammals is highly correlated groups (Kelley, 1997), which probably took place with ontogeny as a whole; a functioning dentition in the late Oligocene to earliest Miocene (Kumar must be in place when an animal is weaned and and Hedges, 1998). This could plausibly be must develop in a way that will last for the J. Kelley, T.M. Smith / Journal of Human Evolution 44 (2003) 307–329 309 projected lifetime of the individual. The link 2002). However, the relatively late date for S. between dental development and ontogeny is evi- parvada limits its usefulness as a meaningful test denced by the correlations between aspects of of the hypothesis of an early life-history diver- dental development and individual life-history gence between apes and monkeys in the latest variables (Smith, 1989, 1991, 1992). Dental devel- Oligocene. opment is, in a sense, just another life-history trait The second fossil ape was an individual of (Smith and Tompkins, 1995), but one that is Afropithecus turkanensis from the early Miocene of preserved in the fossil record. While there is Kenya (Kelley, 1999, 2002). In the following analy- systematic variation in the relationship between sis we revise the earlier estimate of age at first dental development and various life-history molar emergence for this individual, which was attributes, primarily associated with variation in preliminary and lacked a full description of the diet (Godfrey et al., 2001), as well as occasional methods of analysis. The revised estimates re- idiosyncratic variation associated with specific ported here incorporate new data on molar crown ecological demands (Godfrey et al., 2002; formation in Afropithecus (see also Smith et al., Schwartz et al., 2002), within a broad framework 2003) and a more thorough and rigorous analysis the pace of dental development serves as a reliable of relevant comparative data. Knowing the age at proxy for the pace of life history as a whole. first molar emergence in Afropithecus is important Among living primates, it has been demonstrated because it nearly doubles the antiquity of such that age at first molar emergence is a particularly estimates for fossil apes, approaching the esti- good correlate of various life-history traits (Smith, mated date of divergence of apes and Old World 1989, 1991), emergence being defined as the initial monkeys. In addition, this analysis provides penetration of the oral gingiva by the molar cusps. further data for the documentation of dental Thus, if the average age at first molar emergence development in fossil apes, which complements can be established for a fossil species, then its information on developmental chronology and general life-history profile can be characterized as crown formation times derived from histological well.