Inferring Plio-Pleistocene southern African biochronology from facial affinities in Parapapio and other fossil papionins.

Buried in the same South African cave deposits as Australopithecus, fossil papionins have been referred to Parapapio (Pp. whitei, Pp. broomi, Pp. jonesi, Pp. antiquus), Papio (P. izodi, P. angusticeps, P. h. robinsoni), Theropithecus (e.g., T. darti), Gorgopithecus, or Dinopithecus on the basis of postcanine tooth size and descriptive morphology of the muzzle. The morphological patterns of variation that these papionins demonstrate can help to place the Australopithecus fossils into a biochronological context and provide valuable information for reconstructing regional Plio-Pleistocene turnover. To document these patterns of variation across fossil-bearing sites, we explore morphometric affinities within Parapapio, and between Parapapio and other Plio-Pleistocene taxa (Dinopithecus ingens, Papio angusticeps, Papio izodi, and Theropithecus darti) by analyzing a sample of interlandmark distances derived from 3-D coordinate data of the most complete fossil papionin specimens available. Bivariate and multivariate analyses show that Pp. whitei exhibits as much variation between sites and between individuals as Pp. broomi and Pp. whitei combined. Diversity in Parapapio at Makapansgat and Sterkfontein may suggest substantial time depth to the caves. Theropithecus darti, Dinopithecus ingens, Papio angusticeps, Pp. whitei from Bolt's Farm (BF 43), and Pp. jonesi from Sterkfontein (STS 565) differ considerably from one another. Other Parapapio specimens across sites form a separate cluster with P. izodi from Taung, suggesting a Pliocene age for this site.

Brain growth, life history, and cognition in primate and human evolution.

This study investigates brain size ontogeny in a sample of seven anthropoid primate species (including humans) in order to evaluate longstanding ideas about the relations between brain size, brain ontogeny, life history, and cognition. First, this analysis tests the hypothesis that primate brain growth patterns vary across species. Second, the relations between the duration of the brain growth period and the duration of the pre-adult period are evaluated. Brain growth data, derived from a number of sources, are analyzed through parametric and nonparametric regressions. The results indicate that primates are characterized by significant variation in patterns of brain growth. In addition, the degree to which brain growth is allocated to either the pre- or the postnatal period varies substantially. Analyses of phylogenetically adjusted data show no correlation between the lengths of the brain growth period and the juvenile period, but there are correlations with other life-history variables. These results are explained in terms of maternal metabolic adaptations. Specifically, primates appear to present at least two major metabolic adaptations. In the first, brain growth occurs mainly during the prenatal period, reflecting heavy maternal investment. In the second, brain growth occupies large portions of the postnatal period. These differing patterns have important implications for maturation age, necessitating late maternal maturation in the first case and enabling relatively early maternal maturation in the second. Overall, these adaptations represent components of distinctive life-history adaptations, with potentially important implications for the evolution of primate cognition.

Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil.

We present the results of a 4-month field investigation of positional behavior, vertical ranging, and species differences in limb proportions and body mass in a mixed-species troop of Saguinus fuscicollis, Saguinus labiatus, and Callimico goeldii in northwestern Brazil. Despite certain similarities in overall positional repertoire, patterns of positional behavior varied significantly between species. Travel in Callimico occurred principally in the lowest levels of the canopy, and was characterized by an exaggerated form of hindlimb-dominated bounding (bounding-hop), and leaping to and from vertical trunks (55.1% of leaps). In contrast, saddle-back tamarins traveled in the lower and middle levels of the canopy, and engaged in a range of leaping behaviors, including stationary leaps (37.3%), acrobatic leaps (31.3%), and trunk-to-trunk leaps (20%). Red-bellied tamarins exploited the highest levels of the arboreal canopy. Travel in this species was dominated by quadrupedal bounding and acrobatic leaps (67% of leaps) that began and ended on thin, flexible supports. Species differences in positional behavior correlated with species differences in limb proportions and locomotor anatomy, and provide a framework for understanding niche partitioning in mixed-species troops of Saguinus and Callimico.

Estimating sexual dimorphism and size differences in the fossil record: a test of methods.

Investigations of size variation in fossil and archaeological skeletal assemblages may be complicated by incomplete skeletons, biased representation of sexes, and the lack of morphological features that identify sex. In order to refine our ability to evaluate size variation, we test the accuracy of three methods that are currently used to estimate size differences in unsexed (pooled) samples: the means method, the median method, and a newly applied technique, the method of moments. Using body mass data from 42 primate species, we calculated actual levels of sexual dimorphism for each species and compared these values to estimates produced by each method. Multivariate regression was used to examine the effects of sample distribution characteristics, including sample size, kurtosis, skewness, sample variance, sex ratio, and intrasexual variance on the performance of the methods. None of the methods appears to be especially accurate. However, one of the simplest methods, the means method, performs relatively well. Factors that lead to inaccuracies in estimation are not readily evident based on multiple regression analysis. We urge caution in the utilization of these techniques, and advocate further analysis of simulated data. Am J Phys Anthropol 110: 95-104, 1999.

Evolution of human growth prolongation.

This investigation evaluates hypotheses that seek to explain temporal retardation or prolongation of human ontogeny. Current hypotheses that address this issue are poorly defined and conflate several distinct theoretical positions. A model that predicts homogeneity in the extension of human growth periods is evaluated. This model is contrasted with two alternatives. The first alternative predicts heterogeneity in the extension of human growth periods. The second anticipates that human growth prolongation is the result of the uniquely derived "insertion" of a human childhood period into an ancestral ontogenetic trajectory. Allometric analyses of body mass growth data from 21 species of anthropoid primates suggest that human female and male ontogenies often depart from patterns established by other primates, but these departures are not uniformly exceptional. Comparisons imply that derived changes in human growth are heterogeneous. Relative to interspecific expectations, early growth periods are much prolonged, but later growth periods are actually reduced. Moreover, the attributes of early growth periods, including growth rates, timing of growth events, and size-for-age, are highly variable across primates. Low correlations among growth periods suggest independence among growth phases. These analyses highlight minimal distinctions between competing models (heterogeneous extension and insertion hypotheses) that attempt to explain human growth prolongation. More important, the present study facilitates refinements of causal models that have been proposed to explain human growth prolongation. Specifically, human growth prolongation may be related to derived changes in patterns of brain development. Alternatively, metabolic factors may have exerted influences on human ontogeny. However, models that predict long growth periods as a byproduct of metabolic factors do not adequately explain temporal retardation of human ontogeny.

Sexual dimorphism in primate neonatal body mass.

Data were collected on neonatal body mass for 109 primate species. For 23 species with sample sizes of nine or more for each sex, dimorphism (male/female ratio) in neonatal body mass ranged from 0.94 in Galago senegalensis and Aotus trivirgatus to 1.19 in Pongo pygmaeus. Dimorphism in neonatal body mass was positively correlated both with adult body mass and with dimorphism in adult body mass, but the apparent relationship with adult mass was eliminated after controlling for the relationship with adult dimorphism. Comparative studies concerned with neonatal body mass in primates have almost always ignored sexual dimorphism. However, neonatal sexual dimorphism in primates does exist and appears to be of sufficient magnitude to be biologically significant in some species. It may be important to consider the consequences of neonatal dimorphism for a variety of research questions related to maternal investment, life history, postnatal growth, and the relationship between neonatal size and adult female pelvic dimensions, both in extant and in extinct primates.

Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care.

This paper explores relations of ontogeny, life history strategies and patterns of infant care in 11 species of small-bodied New World monkeys. Analysis of these data suggests that differences in the social systems of Aotus, Callicebus, Saimiri, Callimico, Saguinus, Leontopithecus, Cebuella and Callithrix are closely tied to both the costs of reproduction and to the ontogenetic requirements of maturing young. In Saimiri, both rapid prenatal body weight and perinatal brain growth result in relatively high metabolic costs to breeding females. These costs, coupled with minimal nonmaternal assistance in caregiving, appear to favor a reproductive strategy that limits offspring production to a single birth at 2-year intervals. In contrast, tamarins and marmosets are capable of producing twins twice in the same year. Prenatal investment in each offspring is relatively low, and the potentially high postnatal costs of nursing 2 infants are minimized by the evolution of a social system involving extensive extramaternal care-giving. Cooperative infant care in callitrichins (tamarins and marmosets) serves to distribute the metabolic costs of infant ontogeny among several group members. Callimico is also characterized by a high reproductive output, with females capable of producing a single infant twice during the year. Infants continue to grow rapidly after weaning. Patterns of infant development in Callimico are similar to those found in tamarins and marmosets and support a close phylogenetic relationship among these taxa. Aotus and Callicebus are characterized by an alternative strategy. In these taxa, a monogamous mating system is associated with paternal certainty, male parental care, and provisioning of the young. The transfer of male energetic resources to a single offspring allows night and titi monkeys to maintain a comparatively short interbirth interval (1 year). Ecological and social factors, such as predation and feeding competition, do not appear to adequately explain much of the observed variation in infant development and preadult growth rates in these platyrrhines. Instead, reproductive strategies are strongly linked to ontogenetic patterns and life histories.

Evolution of human growth spurts.

This study investigates subadult growth spurts in a large sample of anthropoid primates, including humans. Analyses of body mass growth curves show that humans are not unique in the expression of female and male body mass growth spurts. Subadult growth spurts are observed in both New World and Old World anthropoid primates and are more common in males than in females. Allometric analyses of growth spurts indicate that many aspects of primate growth spurts are strongly correlated with species size. Small species tend not to exhibit growth spurts. Although male and female scaling patterns for velocity and size measures are comparable, scaling relations of variables that measure the timing of growth spurts differ by sex. These patterns can be related to sexual differences in life histories. Scaling analyses further show that humans do not depart substantially from patterns that describe other anthropoid primates. Thus, in relative terms, human growth spurts are not exceptional compared to this sample of primates. The long absolute delay in the initiation of the human growth spurt may be of substantial evolutionary importance and serves to distinguish humans from other primates. In essence, humans exhibit growth spurts that are comparable to other primates in many respects. However, human growth spurts are shifted to very late absolute ages.

Ontogeny of body size variation in African apes.

Size variation in African apes (Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes ["common" chimpanzee]) is substantial, both within and between species. We investigate the possible evolutionary significance of this variation through an analysis of the ontogeny of size variation in this group. In addition, we highlight possible areas of future endocrinological research, and evaluate recently proposed alternative models that attempt to account for ontogenetic variation in apes. The present study shows that intergeneric variation in size is largely a consequence of differences among species in the rate of body weight growth. Interspecific size variation in Pan is a product of both rate and duration differences in growth. The ontogenetic bases of sexual dimorphism vary in this group. Dimorphism is largely a result of sex differences in the duration of body weight growth in gorillas and pygmy chimpanzees, but results from differences in the rate of growth in common chimpanzees. Ontogenetic analyses largely confirm earlier interpretations, but with better data and methods. The great degree of ontogenetic variation within and among these species, especially in the timing and magnitude of "pubertal" growth spurts, implies that studies of endocrine growth control in African apes could be a productive line of future research. We also suggest that ontogenetic variation can be understood with respect to ecological risks. Growth rates seem to be negatively correlated with ecological risk in African apes, suggesting links between ontogenetic patterns and social and ecological variables. High growth rates in gorillas compared to Pan are most consistent with this model. Variation between chimpanzees and pygmy chimpanzees (especially females) also seem to fit predictions of this model.

Asymmetric vault modification in Hopi crania.

Cradleboarding was practiced by numerous prehistoric and historic populations, including the Hopi. In this group, one result of cradleboarding was bilateral or asymmetric flattening of the posterior occipital. We test whether cradleboarding had significant effects on the morphology of the cranial vault, cranial base, and face. Additionally, we examine associations between direction of flattening and asymmetric craniofacial growth. A skeletal sample of Hopi from the Old Walpi site includes both nonmodified (N = 43) and modified individuals (N = 39). Three-dimensional coordinates of 53 landmarks were obtained using a diagraph. Thirty-six landmarks were used to define nine finite elements in the cranial vault, cranial base, and face. Finite element scaling was used to compare average nonmodified individuals, with averages of bilaterally, right, and left modified individuals. The significance of variation among "treatment" groups was evaluated using a bootstrap test. Pearson product-moment correlations test the association of asymmetry with direction of modification. Hopi cradleboarding has a significant effect on growth of the cranial vault, but does not affect morphology of the cranial base or face. Bilateral flattening of the cranial vault leads to decreased length and increased width of the cranial vault. Flattening of the right or left cranial vault results in ipsilaterally decreased length and width coupled with a corresponding increased length and width on the contralateral side of the cranial vault. There is a significant correlation of size asymmetry with direction of modification in the cranial vault, but not with size or shape change in the cranial base or face.

Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates.

This study examines statistical correlations between socioecological variables (including measures of group composition, intermale competition, and habitat preference) and the ontogeny of body size sexual dimorphism in anthropoid primates. A regression-based multivariate measure of dimorphism in body weight ontogeny is derived from a sample of 37 species. Quantitative estimates of covariation between socioecological variables and this multivariate measure are evaluated. Statistically significant covariation between the ontogeny of dimorphism and socioecological variables, with the possible exception of habitat preference, is observed. Sex differences in ontogeny are lacking in species that exhibit low levels of intermale competition and are classifiable as species with monogamous/polyandrous mating systems. Among dimorphic species, two modes of dimorphic growth are apparent, which seem to be related to different kinds of group compositions. Multimale/multifemale species tend to become dimorphic through bimaturism (sex differences in duration of growth) with minimal sex differences in growth rate. Single-male/multifemale species tend to attain dimorphism through differences in rate of growth, often with limited bimaturism. Measures of intermale competition may also covary with these modes of dimorphic growth, but the relations among these variables are sometimes ambiguous. Correlations between dimorphic growth and behavioral variables may reflect alternative life history strategies in primates. Specifically, the ways in which risks faced by subadult males are distributed and the relations of these risks to growth rates seem to influence the evolution of size ontogenies. The absence of dimorphic ontogeny in some species can be tied to similar distributions of risk in each sex. In taxa that become dimorphic primarily through rate differences in growth, the lifetime distribution of risks for males may change rapidly. In contrast, males may face a pattern of uniformly changing or stable risk in species that become dimorphic through bimaturism. Finally, much variation recorded by this study remains unexplained, providing additional evidence of the need to specially examine female ontogeny before primate body size dimorphism can be satisfactorily explained.

A re-evaluation of subspecific variation and canine dimorphism in woolly spider monkeys (Brachyteles arachnoides).

A recent study suggests that differing populations of woolly spider monkeys exhibit a substantial degree of morphological, cytogenetic, and behavioral variation. We re-evaluate the differences between populations in the degree of canine tooth height sexual dimorphism and in the frequency of thumbs. Statistical analysis of variation in the degree of canine sexual dimorphism between these populations fails to provide strong evidence for subspecific variation: differences in the degree of canine dimorphism cannot be considered statistically significant. Differences between populations in the frequency of thumbs are, however, statistically significant. The lack of clear distinctions between populations in the degree of canine dimorphism complicates assessments of behavioral variation between these populations. We suggest that the level of geographic variation in woolly spider monkey canine dimorphism is not consistent with subspecific status.

Ontogenetic correlates of diet in anthropoid primates.

This study assesses ontogenetic correlates of diet in anthropoid primates. Associations between body weight growth, adult size, and diet are evaluated for a sample of 42 primate species, of which 8 are classifiable as "folivores." The hypothesis that folivores show a pattern of growth that differs from "nonfolivores" is tested. Ontogenetic variation is summarized through use of parametric and nonparametric regression analysis. Several analytical techniques, including broad interspecific and detailed comparisons among species of similar adult size, are applied. This investigation indicates a clear association between body weight ontogeny and diet: folivorous species grow more rapidly over a shorter duration than comprably sized nonfolivorus species. A positive correlation between adult size and diet is not unambiguously established in this sample. A threshold (at around 1 kg) below which insectivory is very common may adequately characterize the association between adult size and diet in anthropoid primates. Above this threshold, adult size does not appear to covary predictably with diet. Evolutionary correlates of the ontogenetic pattern seen in folivores may include a variety of factors. The distinctive pattern of development in folivores may relate to the profile of ecological and social risks that these species face. Morphophysiological advantages to rapid growth may relate to a need for accelerated alimentary (dental and gut) development. The implications of ontogenetic variation in folivores are discussed.

Effects of annular cranial vault modification on the cranial base and face.

Artificial modification of the cranial vault was practiced by a number of prehistoric and protohistoric populations, frequently during an infant's first year of life. We test the hypothesis that, in addition to its direct effects on the cranial vault, annular cranial vault modification has a significant indirect effect on cranial base and facial morphology. Two skeletal series from the Pacific Northwest Coast, which include both nonmodified and modified crania, were used: the Kwakiutl (62 nonmodified, 45 modified) and Nootka (28 nonmodified, 20 modified). Three-dimensional coordinates of 53 landmarks were obtained using a diagraph, and 36 landmarks were used to define nine finite elements in the cranial vault, cranial base, and face. Finite element scaling was used to compare average nonmodified and average modified crania, and the significance of the results were evaluated using a bootstrap test. Annular modification of the cranial vault produces significant effects on the morphology of the cranial base and face. Annular modification in the Kwakiutl resulted in restrictions of the cranial vault in the medial-lateral and superior-inferior dimensions and an increase in anterior-posterior growth. Similar dimensional changes are observed in the cranial base. The Kwakiutl face is increased anterior-posteriorly and reduced anterior-laterally to posterior-medially. Similar effects of modification are observed in the Nootka cranial vault and cranial base, though not in the face. These results demonstrate the developmental interdependence of the cranial vault, cranial base, and face.

Effects of fronto-occipital artificial cranial vault modification on the cranial base and face.

Artificial reshaping of the cranial vault has been practiced by many human groups and provides a natural experiment in which the relationships of neurocranial, cranial base, and facial growth can be investigated. We test the hypothesis that fronto-occipital artificial reshaping of the neurocranial vault results in specific changes in the cranial base and face. Fronto-occipital reshaping results from the application of pads or a cradle board which constrains cranial vault growth, limiting growth between the frontal and occipital and allowing compensatory growth of the parietals in a mediolateral direction. Two skeletal series including both normal and artificially modified crania are analyzed, a prehistoric Peruvian Ancon sample (47 normal, 64 modified crania) and a Songish Indian sample from British Columbia (6 normal, 4 modified). Three-dimensional coordinates of 53 landmarks were measured with a diagraph and used to form 9 finite elements as a prelude to finite element scaling analysis. Finite element scaling was used to compare average normal and modified crania and the results were evaluated for statistical significance using a bootstrap test. Fronto-occipitally reshaped Ancon crania are significantly different from normal in the vault, cranial base, and face. The vault is compressed along an anterior-superior to posterior-inferior axis and expanded along a mediolateral axis in modified individuals. The cranial base is wider and shallower in the modified crania and the face is foreshortened and wider with the anterior orbital rim moving inferior and posterior towards the cranial base. The Songish crania display a different modification of the vault and face, indicating that important differences may exist in the morphological effects of fronto-occipital reshaping from one group to another.

Cranial capacity evolution in Homo erectus and early Homo sapiens.

This paper investigates patterns of cranial capacity evolution in Homo erectus, early Homo sapiens, and in regional subsamples of H. erectus. Specifically, models explaining evolution of cranial capacity in these taxa are evaluated with statistical techniques developed for the analysis of time series data. Regression estimates of rates of evolution in cranial capacity are also obtained. A non-parametric test for trend suggests that cranial capacity in both H. erectus and early H. sapiens may increase significantly through time. Cranial capacity in an Asian subsample of H. erectus (comprised of Chinese and Indonesian specimens) increases significantly through time. Other subsamples of H. erectus (African, Chinese, and Indonesian) do not appear to increase significantly through time. Regression results generally corroborate results of the test for trend. Spatial and temporal variation may characterize evolution of cranial capacity in H. erectus. Different patterns of cranial capacity evolution may distinguish H. erectus from early H. sapiens.

Sexual dimorphism in the baboon facial skeleton.

Baboons exhibit marked sexual dimorphism in many aspects of their morphology. Dimorphism is especially pronounced in the face. We use finite-element analysis to investigate the ontogeny of sexual dimorphism in a cross-sectional sample of baboon (Papio sp.) faces. This method provides detailed quantitative information about size and shape changes at anatomical landmarks in the face during growth. Allometric results suggest that sexual dimorphism in facial size and shape is produced by ontogenetic scaling: males and females share a common ontogenetic trajectory. Analyses of growth in time, which complement allometric analyses, show that female growth slows much earlier than male growth, accounting for the differences between sexes. Local size and local shape follow similar patterns of growth, but changes in these variables are slower in females. Local and global facial size are much more dimorphic than local and global facial shape.