Life-History Inference in the Early Hominins Australopithecus and Paranthropus

The life histories of early hominins are commonly characterized as being like those of great apes. However, the life histories of the extant great apes differ considerably from one another. Moreover, the extent to which their life histories correlate with the two aspects of morphology used to infer the life histories of fossil species, brain size and dental development, has remained subject to debate. Increased knowledge of great ape life histories and, more recently, dental development —in particular ages at first molar emergence— now make it clearer that the latter is strongly associated with important life-history attributes, whereas brain size, as reflected by cranial capacity, is less informative. Here we estimate ages at M1 emergence in several infant/juvenile individuals of Australopithecus and Paranthropus based on previous estimates of ages at death, determined through dental histology. These are uniformly earlier than would be predicted either by adult cranial capacity or by comparison to ages at M1 emergence in free-living extant great apes. This suggests that either, 1) the life histories of the early hominins were faster than those of all extant great apes; 2) there was selection for rapid initial dental development and presumably early weaning, but that early hominin life histories were otherwise more prolonged and consistent with adult cranial capacities; or 3) the ages at death have been systematically underestimated, resulting in underestimates of the ages at M1 emergence. We investigate the implications of each of these alternatives and, where possible, explore evidence that might support one over the others.     

Dental development and life history in Anapithecus hernyaki

The sample of Anapithecus from Rudabánya, Hungary, is remarkable in preserving a large number of immature individuals. We used perikymata counts, measurements of root length and cuspal enamel thickness, and observations of the sequence of tooth germs that cross match specific developmental stages in Anapithecus to construct the first composite picture and time scale for dental development in a pliopithecoid (Catarrhini, Primates). We conclude that the age of eruption of M1 in Anapithecus was similar to various macaque species (approximately 1.45 months), but that M2 and M3 emergence were close to 2.2 and 3.2 years, respectively (both earlier than expected for similarly sized cercopithecoids). There may have been little difference in individual tooth formation times between cercopithecoids and Anapithecus, but the degree of molar overlap during M1, M2, and M3 crown development, which is extreme in Anapithecus, is fundamentally different. Overall dental development in Anapithecus was very rapid. Old World monkeys appear derived in lacking significant molar overlap, and hominoids may be derived in having longer tooth formation times, both resulting in longer overall dental development times. This is consistent with the general conclusion that the Pliopithecoidea is an outgroup to the Cercopithecoidea and the Hominoidea. On the other hand, rapid dental formation in Anapithecus may be an apomorphy indicative of an unusually rapid life history or unique pressures related to diet and maturation. Folivory and/or predation pressure may be responsible for generating selection to more rapidly erupt permanent teeth and possibly attain adult body masses in Anapithecus. Whatever the case, Anapithecus, with an M3 emergence of approximately 3.2 years, is dramatically faster than any extant catarrhine of similar body mass. This represents yet another unusual attribute of this poorly known fossil catarrhine.     

Effect of diet on dental development in four species of catarrhine primates

In this study, dental development is described in two pairs of closely related catarrhine primate species that differ in their degree of folivory: 1) Hylobates lar and Symphalangus syndactylus, and 2) Papio hamadryas hamadryas and Semnopithecus entellus. Growth increments in histological thin sections are used to reconstruct the chronology of dental development to determine how dental development is accelerated in the more folivorous species of each pair. Although anterior tooth formation appears to be unrelated to diet, both S. syndactylus and S. entellus initiate the slowest-forming molar earlier than the related less-folivorous species, which supports the hypothesis that dental acceleration is related to food processing. S. syndactylus initiates M2 crown formation at an earlier age than H. lar, and S. entellus initiates and completes M3 at an earlier age than P. h. hamadryas. Similar stages of M3 eruption occur earlier in the more folivorous species; however, the sex of the individual may also play a role in creating such differences. Although the age at M3 emergence is close to that reported for the end of body mass growth in lar gibbons, hamadryas baboons, and Hanuman langurs, M3 emergence may not be coupled to body mass growth in siamangs.     

Primate origins and evolution. By R. D. Martin. Princeton,NJ: Princeton University Press. 1990. ISBN 0-691-08565-X. xiv + 840 pp. $125 (cloth)

Dental emergence ages are examined for a mixed longitudinal sample of 58 chimpanzees of known age and sex (22 males, 36 females) followed over the past 10 years. This study provides the most complete data set currently available on dental emergence in chimpanzees of known age and sex. Summary statistics and cumulative frequency percentiles of emergence ages are presented for both the permanent and the primary teeth. Male and female percentiles are also compared and reveal a number of cases of sexual dimorphism in emergence ages. Comparisons of emergence means reveal some statistically significant differences between upper and lower teeth but not between antimeres in the upper or lower dentition. Kendall's rank correlation coefficient (tau) suggests a correlation in timing between first molar and incisor emergence within individuals. In addition, a significant time lag was observed between first molar and central incisor emergence. A number of emergence sequence polymorphisms are presented as well. These findings provide important baseline information for future studies of chimpanzee growth, development, and demography and also contribute to several current issues in paleoanthropology relating to dental maturation patterns in early hominids.     

Out of the mouths of baboons: stress,life history,and dental development in the Awash National Park hybrid zone,Ethiopia

The techniques of dental histology provide a method for reconstructing much of the life history of an individual, as accentuated increments visible in polarized light microscopy record incidents of physiological stress during the formation of dental tissues. Combined with counts of the normal periodic growth increments, they provide a means of reconstructing the chronology of dental development, age at death, and the ages at which stress occurs. In this study, we determine age at death and reconstruct the chronology of dental development in two male anubis baboons from Uganda and two female baboons from the Awash National Park hybrid zone. For the female baboons, we used the dates of death and rainfall records for the region to determine date of birth, ages at periods of physiological stress, dates at which these stresses occurred, and rainfall amounts for those months.Ages determined histologically for each specimen are comparable to ages estimated from dental emergence schedules and dental scores for wild baboons. Crown formation times are longer than those reported in radiographic studies of captive yellow baboons. Age at initiation of crown formation is similar to that reported for radiographic studies, but ages at completion of crown formation are consistently later. The pattern of stresses is similar in the two female baboons, suggesting that individual life history intersects with local ecology to produce a pattern of accentuated increments occurring during the weaning process and at the onset of menarche, as well as during the first postweaning dry and rainy periods.     

Dental Ontogeny in Pliocene and Early Pleistocene Hominins

Until recently, our understanding of the evolution of human growth and development derived from studies of fossil juveniles that employed extant populations for both age determination and comparison. This circular approach has led to considerable debate about the human-like and ape-like affinities of fossil hominins. Teeth are invaluable for understanding maturation as age at death can be directly assessed from dental microstructure, and dental development has been shown to correlate with life history across primates broadly. We employ non-destructive synchrotron imaging to characterize incremental development, molar emergence, and age at death in more than 20 Australopithecus anamensis, Australopithecus africanus, Paranthropus robustus and South African early Homo juveniles. Long-period line periodicities range from at least 6–12 days (possibly 5–13 days), and do not support the hypothesis that australopiths have lower mean values than extant or fossil Homo. Crown formation times of australopith and early Homo postcanine teeth fall below or at the low end of extant human values; Paranthropus robustus dentitions have the shortest formation times. Pliocene and early Pleistocene hominins show remarkable variation, and previous reports of age at death that employ a narrow range of estimated long-period line periodicities, cuspal enamel thicknesses, or initiation ages are likely to be in error. New chronological ages for SK 62 and StW 151 are several months younger than previous histological estimates, while Sts 24 is more than one year older. Extant human standards overestimate age at death in hominins predating Homo sapiens, and should not be applied to other fossil taxa. We urge caution when inferring life history as aspects of dental development in Pliocene and early Pleistocene fossils are distinct from modern humans and African apes, and recent work has challenged the predictive power of primate-wide associations between hominoid first molar emergence and certain life history variables.     

Dental development in Megaladapis edwardsi (Primates, Lemuriformes): implications for understanding life history variation in subfossil lemurs

Teeth grow incrementally and preserve within them a record of that incremental growth in the form of microscopic growth lines. Studying dental development in extinct and extant primates, and its relationship to adult brain and body size as well as other life history and ecological parameters (e.g., diet, somatic growth rates, gestation length, age at weaning), holds the potential to yield unparalleled insights into the life history profiles of fossil primates. Here, we address the absolute pace of dental development in Megaladapis edwardsi, a giant extinct lemur of Madagascar. By examining the microstructure of the first and developing second molars in a juvenile individual, we establish a chronology of molar crown development for this specimen (M1 CFT = 1.04 years; M2 CFT = 1.42 years) and determine its age at death (1.39 years). Microstructural data on prenatal M1 crown formation time allow us to calculate a minimum gestation length of 0.54 years for this species. Postnatal crown and root formation data allow us to estimate its age at M1 emergence (approximately 0.9 years) and to establish a minimum age for M2 emergence (>1.39 years). Finally, using reconstructions or estimates (drawn elsewhere) of adult body mass, brain size, and diet in Megaladapis, as well as the eruption sequence of its permanent teeth, we explore the efficacy of these variables in predicting the absolute pace of dental development in this fossil species. We test competing explanations of variation in crown formation timing across the order Primates. Brain size is the best single predictor of crown formation time in primates, but other variables help to explain the variation.     

Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past

A chronology of dental development in Pan troglodytes is arguably the best available model with which to compare and contrast reconstructed dental chronologies of the earliest fossil hominins. Establishing a time scale for growth is a requirement for being able to make further comparative observations about timing and rate during both dento-skeletal growth and brain growth. The absolute timing of anterior tooth crown and root formation appears not to reflect the period of somatic growth. In contrast, the molar dentition best reflects changes to the total growth period. Earlier initiation of molar mineralization, shorter crown formation times, less root length formed at gingival emergence into functional occlusion are cumulatively expressed as earlier ages at molar eruption. Things that are similar in modern humans and Pan, such as the total length of time taken to form individual teeth, raise expectations that these would also have been the same in fossil hominins. The best evidence there is from the youngest fossil hominin specimens suggests a close resemblance to the model for Pan but also hints that Gorilla may be a better developmental model for some. A mosaic of great ape-like features currently best describes the timing of early hominin dental development.     

Natural selection on molar size in a wild population of howler monkeys (Alouatta palliata)

Dental traits have long been assumed to be under selection in mammals, based on the macroevolutionary correlation between dental morphology and feeding behaviour. However, natural selection acting on dental morphology has rarely, if ever, been documented in wild populations. We investigated the possibility of microevolutionary selection on dental traits by measuring molar breadth in a sample of Alouatta palliata (mantled howler monkey) crania from Barro Colorado Island (BCI), Panama. The age at death of the monkeys is an indicator of their fitness, since they were all found dead of natural causes. Howlers with small molars have significantly decreased fitness as they die, on average, at an earlier age (well before sexual maturity) than those with larger molars. This documents the existence of phenotypic viability selection on molar tooth size in the BCI howlers, regardless of causality or heritability. The selection is further shown to occur during the weaning phase of A. palliata life history, establishing a link between this period of increased mortality and selection on a specific morphological feature. These results provide initial empirical support for the long-held assumption that primate molar size is under natural selection.     

Frequency and chronological distribution of dental enamel hypoplasia in enslaved African Americans: A test of the weaning hypothesis

The dentition of 27 enslaved African Americans from archaeological sites in Maryland and Virginia were examined. All 17 males and 7 of the 10 females in this study exhibited enamel hypoplastic defects indicative of systemic nutritional and disease stresses interfering with amelogenesis. Estimates of the ages of occurrence of these defects show that most occur between 1.5 and 4.5 years of age, 0.5–3.75 years later than historically documented weaning age (9–12 months of age) in similar plantation populations. Comparisons are made with studies of dental enamel hypoplasia in contemporaneous enslaved and free African American populations, including our data on 75 individuals from the First African Baptist Church cemetery in Philadelphia. These populations were highly stressed. While there appears to be a modest effect of early weaning stress, no direct relationship of peak frequencies to weaning age can be shown. These data raise questions about the attribution of peak hypoplasia frequencies to age at weaning or “post-weaning” stresses in previous paleopathological studies. High hypoplasia frequencies during the middle years of enamel development are more likely the result of a combination of 1) multiple environmental stresses, 2) differences in hypoplastic susceptibility in enamel, and 3) random factors. © 1994 Wiley-Liss, Inc.     

Teeth, brains, and primate life histories

This paper explores the correlates of variation in dental development across the order Primates. We are particularly interested in how 1) dental precocity (percentage of total postcanine primary and secondary teeth that have erupted at selected absolute ages and life cycle stages) and 2) dental endowment at weaning (percentage of adult postcanine occlusal area that is present at weaning) are related to variation in body or brain size and diet in primates. We ask whether folivores have more accelerated dental schedules than do like-sized frugivores, and if so, to what extent this is part and parcel of a general pattern of acceleration of life histories in more folivorous taxa. What is the adaptive significance of variation in dental eruption schedules across the order Primates? We show that folivorous primate species tend to exhibit more rapid dental development (on an absolute scale) than comparably sized frugivores, and their dental development tends to be more advanced at weaning. Our data affirm an important role for brain (rather than body) size as a predictor of both absolute and relative dental development. Tests of alternative dietary hypotheses offer the strongest support for the foraging independence and food processing hypotheses.     

A tradeoff between reproduction and growth in contemporary Finnish women

Women have been suggested to trade growth in height for reproduction, as an earlier age at menarche and first birth seem to be related to shorter adult stature. Although women likely accrue fitness benefits by maturing and starting reproduction at young age, short adult stature may be selected against by natural and sexual selection later in their life. We studied how age at menarche and first reproduction affected adult height and whether adult height in turn was related to lifetime reproductive success in Finnish women born 1946–1958. Our results show that a delay of 1 year in age at menarche and first reproduction was related to a 0.43- and 0.20-cm increase in adult height, respectively. The sex of the first-born offspring was not related to adult height. Moreover, women gained fitness benefits by starting reproduction early but not by growing tall. These findings among Finnish women are thus compatible with tradeoffs between reproduction and growth, by showing a compromised adult height at the cost of early age at menarche and first birth. However, in these women, natural selection favored those women who traded their stature for young motherhood.     

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

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 approximately 17.5 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 M(1)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 M(1)eruption in extant baboons and chimpanzees.The estimates of age at M(1)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.     

Interspecific allometry of the mandible,dental arch,and molar area in anthropoid primates: Functional morphology of masticatory components

Allometric equations relating the lengths and widths of the mandible and dental arch, and of molar area, were obtained in a wide range of anthropoid primates grouped into four subsets, pongids, cercopithecids, nonmarmoset platyrrhines, and marmosets. Mandibular width is negatively allometric against length across anthropoids but cercopithecids had relatively wider mandibles than nonmarmosets of the same size class. Mandibular length relative to dental arch length was isometric within and between the four groups but dental arch width scaled negatively against all the other dimensions examined in this study, indicating a functional dissociation between the dental arcade and the bony mandible. Molar area showed various scaling patterns relative to mandibular length (isometry) and width (positive). There were no parameters that scaled positively against body weight across groups, except for molar area in cercopithecids (strongly) and nonmarmoset (moderately). Notable functional specializations include relatively long dental arches in cercopithecoids, related to large, elongate bilophodont molars, and the tendency to increase relative jaw length across the range of anthropoid sizes, reflecting negative allometry of the brain (cranial bicondylar width). We caution that various allometry and functional patterns may be masked by generalizing from broad taxonomic comparison involving a large sweep of adaptative patterns.     

Brief communication: on the optimum number of metacarpals for roentgenogrammetric measurement

Interpretation of dental development of fossil hominids requires understanding of and comparison with the pattern and timing of dental development among living humans and pongids. We report the first study of crown and root calcification in the lower permanent molar teeth among chimpanzees (Pan troglodytes) of known chronological age. A series of 99 lateral head radiographs of 16 captive-born chimpanzees were analyzed. Radiographs were taken at irregular intervals throughout the entire postnatal period of dental development from birth to 13 years of age. Permanent mandibular molars were rated on an eight-point maturation scale from initial radiographic appearance through crown and root calcification and apical closure of the root canals. In addition, we were able to document initial crown calcification and completion, as well as root completion and apical closure in incisors, canines, and premolars. Our results show several differences from the widely cited developmental schedule for pongid dentitions of Dean and Wood (Folia Primatol. 36:111–127, 1981). We found a much greater degree of temporal overlap in calcification of the crowns of adjacent molars, a pattern very unlike that usually seen in human dental development, which is characterized by delays between the onset of crown calcification in the molar series. Also, the ages and durations of crown and root formation in our chimp sample differ from the estimates proposed by Dean and Wood. By more clearly establishing the nature of developmental schedules and the timing of major events in the pongid dentition, these results should aid in the ongoing controversies concerning the human or pongid nature of dental development among Plio-Pleistocene hominids.     

Mixing at young ages reduces fighting in unacquainted domestic pigs

Under normal farming practices, piglets from different litters are often mixed around the time of weaning, and a high incidence of fighting and minor injuries often occur. The aim of this experiment was to determine the effect of age on the incidence of fighting in piglets mixed before weaning, at different ages between 5 and 26 days. We found no significant relationship between age and the likelihood that a pair of piglets would fight during the first 75 min after mixing. However, the duration of the first fight observed increased from 101+/-38 s at 5 days to 621+/-278 s at 26 days, mainly because of higher levels of unretaliated harassment and resting during the bouts. Younger pigs also showed 80% fewer injuries from the fighting. The results suggest some potential welfare advantage to allowing litters to mix at younger ages.     

Detecting menarcheal status through dental mineralization stages?

Menarche is an indicator frequently used to study variation in growth, development, and related health conditions among members of living populations. As a life event, menarche is often associated with changes in an individual's social identity. The reproductive lifespan, which for females starts with menarche, is a paramount feature of palaeodemographic studies. Determination of menarche status from the skeletal remains of individuals of past populations can be obtained by assessing the developmental status of the iliac crest, as well as the hand and wrist bones, which are, unlike teeth, often poorly recovered in bioarchaeological contexts. The present study seeks to evaluate the link between dental mineralization and menarche in a population of known menarche status. The relationship between permanent teeth mineralization and menarche status was investigated by using data of developing permanent teeth (167 radiographs) rated in accordance with the well‐known standards of Demirjian et al. and Moorrees et al. collected among 73 living French females of known menarcheal status. Using correlation ratios, GLMM and CART algorithm, menarcheal status is correlated with mineralization of the premolars. Menarcheal status is predicted correctly for 92 and 77% of radiographs of the learning and validation samples, respectively. Although promising, the results require caution prior to generalization to other populations. The age of menarche in this particular sample may simply coincide with the development of the premolars in this particular sample. Therefore, further investigation applied to populations with various mean ages of menarche is required in order to provide new evidence of variation in human growth and development from the correspondence between the mineralization of the permanent teeth and menarche.     

Reproduction, development and growth of Akodon lindberghi (Hershkovitz, 1990) (Rodentia, Muridae, Sigmodontinae) raised in captivity

The reproduction, development and growth of Akodon lindberghi were studied in captivity. The colony was derived from animals captured in Sim?o Pereira, Minas Gerais state, which represents a new area of geographical distribution known for this species. Twelve males and twelve females were crossed, producing 144 young in 53 litters. Post-partum oestrus was observed and gestation length was estimated in 23 days. Litter size ranged from 1 to 4 with a mean of 2.72 (SD = 0.97, n = 53) and modal size of 3. Sexual dimorphism was neither present in body mass at birth nor at weaning. There was a significant negative correlation between litter size and mass at birth or weaning. Permanent emergence of adult external appearance occurred at 15 days. Puberty for males and females was 43 and 42 days, respectively, and the first fecundation event for two females was recorded at 47 and 54 days of age. The weight growth was described by fitting a Gompertz model. No significant difference was found in any parameter of growth curves for males and females. Measurements (head-body, tail, hind foot and internal and external ear lengths) obtained for adult individuals also did not reveal the presence of sexual dimorphism.     

Genetic determinants and dynamics of permanent teeth emergence in Northwest Indian twins: A chronogenetic study

The understanding of the role of genetic factors in phenotypic variation in the emergence of secondary teeth in humans remains is incomplete. Dental emergence data based on a mixed longitudinal study were collected on 111 twin pairs from an urban population of Chandigarh. The observations over time on a single individual varied from one to nine, thus giving a total of 595 entities. Female twins manifested emergence priority over males. The differences between zygosities in mean emergence ages were significant for only 6 of 16 (37%) instances. Magnitude of variations seen between twins and singletons in their mean emergence timings and duration of the hiatus between two dental phases of emergence were of the order observed among different samples from the same population/ethnic group. Heritability estimates for the specified number of the teeth emerged showed age variations. These estimates were highest in the first two age groups (from 5 to 7 years), when the first molars and incisors emerged. Maxilla-mandible differences were seen for tooth emergence timings and sequence patterns. Heritability for tooth emergence timings was higher in maxilla than in mandible. Multifactorial model of inheritance was the best fit model to explain variations observed in dental emergence timings and dental sequence pattern polymorphisms and there were significant genetic components of variation for both of these. There were sex differences in heritability; females had higher estimates than males. Genetic factors accounted for about 60% of the total phenotypic variation in the length of hiatus interval between two active stages of permanent teeth emergence.     

Growth curves,dental emergence norms,and supplementary morphological observations in known-age captive orangutans

Postnatal development in known-age captive orangutans was studied by collating new data from seven orangutans at Chicago Zoological Park, Brookfield, Illinois, with published and unpublished data from 76 additional captive orangutans. Norms were tabulated for deciduous and permanent dental emergence. Growth curves for weight and linear dimensions in females and males were compared in captive-reared and wild-reared subjects. Hand-reared and mother-nursed captives were compared with respect to dental emergence and weight increase. Differential relative growth of extremity segments was investigated. Pedigree data are presented relative to genetics of hallucal nail absence. Males of various ages were compared with respect to testis size and location and cheek-pad development.