Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

Wild bonobo and chimpanzee females exhibit broadly similar patterns of behavioral maturation but some evidence for divergence.

OBJECTIVES: Primates exhibit variation in rates of growth and development. Variation in female growth and development across ape species appears to be explained by the Ecological Risk Aversion Hypothesis (ERAH). Indeed, existing data on variation in somatic growth and reproductive maturation between humans' closest living ape relatives, bonobos and chimpanzees, appear to be consistent with this hypothesis. However, existing data on behavioral maturation between the two species appear to contradict this hypothesis. We present novel behavioral data on infant and juvenile females from wild populations of both species in order to further evaluate predictions of the ERAH as it relates to the speed of behavioral maturation. MATERIALS AND METHODS: We analyzed 3 years of behavioral data on 17 female bonobos (<8 years of age) from LuiKotale, Democratic Republic of the Congo and 40 years of behavioral data on 30 age-matched female chimpanzees from Gombe, Tanzania. We compared the timing of (a) the attainment of independence from mothers and (b) the development of social skills using the following proxies: proximity between females and their mothers and the time that females spent engaged in eating, suckling, social play, social grooming, and riding on their mothers. RESULTS: We did not find species differences in the proportion of time that females spent in contact with their mothers or engaged in eating, suckling, social play, or social grooming. Female bonobos spent more time riding on their mothers than did female chimpanzees. Female bonobos spent more time at distances greater than 5 m from their mothers during the ages of 3-8 years, but females did not differ during the ages of 0-3 years. DISCUSSION: Behavioral maturation is largely similar between females of the two species based on the ages and proxies considered herein. We propose alternative explanations for the differences that we found in proximity and riding that do not invoke differences in underlying rates of maturation.

Ontogenetic insights into the significance of mandibular corpus shape variation in hominoids: Developmental covariation between M2 crypt formation and corpus shape.

OBJECTIVES: Here, we quantify and compare the cross-sectional shape of the mandibular corpus between M1 and M2 during growth in Pan paniscus, Pan troglodytes, and Pongo pygmaeus. The goal is to assess the hypothesis that the shape of the corpus is influenced by the development of permanent molars in their crypts, by examining ontogenetic changes in corpus shape and investigating covariation between corpus shape and M2 and M3 molar crypt forms. MATERIALS AND METHODS: Ontogenetic changes in mandibular corpus shape were assessed using landmarks and semilandmarks, and measurements of length, width, and height were used to quantify molar crypts (M2 and M3 ). Ontogenetic changes in corpus growth from the eruption of M1 to the eruption of M3 were evaluated for each species through generalized Procrustes analysis and principal components analysis in shape-space and form-space. The relationship between corpus shape and molar crypt form was investigated at three different developmental stages using two-block partial least squares (2B-PLS) analysis. RESULTS: The results show clear differences in growth patterns among all three species and provide evidence that species-level differences in mandibular corpus growth occur prior to the emergence of M1 . The results of the 2B-PLS analysis reveal that significant covariance between corpus shape and molar crypt form is limited to the developmental stage marked by the emergence of M1 , with covariance between corpus shape and M2 crypt width. Corpora that are relatively narrower in the inferior portion of the cross section covary with relatively narrower M2 crypts. CONCLUSIONS: These results have important implications for understanding the taxonomic and phylogenetic significance of mandibular corpus shape variation in the hominoid fossil record.

Heterochrony in chimpanzee and bonobo spatial memory development.

OBJECTIVES: The emergence of human-unique cognitive abilities has been linked to our species' extended juvenile period. Comparisons of cognitive development across species can provide new insights into the evolutionary mechanisms shaping cognition. This study examined the development of different components of spatial memory, cognitive mechanisms that support complex foraging, by comparing two species with similar life history that vary in wild ecology: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). MATERIALS AND METHODS: Spatial memory development was assessed using a cross-sectional experimental design comparing apes ranging from infancy to adulthood. Study 1 tested 73 sanctuary-living apes on a task examining recall of a single location after a 1-week delay, compared to an earlier session. Study 2 tested their ability to recall multiple locations within a complex environment. Study 3 examined a subset of individuals from Study 2 on a motivational control task. RESULTS: In Study 1, younger bonobos and chimpanzees of all ages exhibited improved performance in the test session compared to their initial learning experience. Older bonobos, in contrast, did not exhibit a memory boost in performance after the delay. In Study 2, older chimpanzees exhibited an improved ability to recall multiple locations, whereas bonobos did not exhibit any age-related differences. In Study 3, both species were similarly motivated to search for food in the absence of memory demands. DISCUSSION: These results indicate that closely related species with similar life history characteristics can exhibit divergent patterns of cognitive development, and suggests a role of socioecological niche in shaping patterns of cognition in Pan.

Epiphyseal fusion and dental development in Pan paniscus with comparisons with Pan troglodytes.

OBJECTIVES: Compared with frequent studies of skeletal development in chimpanzees, relatively little is known about bonobo skeletal development. This study seeks to explore the relationship between skeletal and dental development in both species of Pan. New data are presented for fusion sites not previously observed in bonobos. MATERIALS AND METHODS: In a sample of 34 Pan paniscus and 168 Pan troglodytes subadults, state of fusion was recorded for 30 epiphyseal fusion sites using a three-stage system of unfused, midfusion, and complete fusion based on Wintheiser, Clauser, and Tappen. Stage of dental development for permanent mandibular dentition was assessed using the Demrijian, Goldstein, and Tanner method. These data allowed for comparisons of both species of Pan and the two subspecies of P. troglodytes. RESULTS: The sequence of fusion events was generally consistent between the two species, but some exceptions may exist for the knee and ankle. The number of fusion events that occurred after complete dental mineralization was similar in both species. No statistically significant differences were found in the fusion timing for the subspecies of P. troglodytes. DISCUSSION: Bolter and Zihlman suggested that fusion at the acetabulum occurs earlier in Pan paniscus, while fusion of epiphyses at the knee are delayed, compared with P. troglodytes. Our data do not indicate earlier fusion of the acetabulum, but fusion events at the knee may complete later relative to dental mineralization in Pan pansicus. Compared with Homo sapiens, both P. troglodytes and Pan paniscus demonstrate later completion of epiphyseal fusion relative to dental mineralization.

Within arm's reach: Measuring forearm length to assess growth patterns in captive bonobos and chimpanzees.

OBJECTIVES: Bonobos and chimpanzees are known to differ in various morphological traits, a dichotomy that is sometimes used as an analogy for evolutionary splits during human evolution. The aim of our study was to measure the forearm length of immature and adult bonobos and adult chimpanzees to assess the extent of age-related changes of forearm length in bonobos and sex-dimorphism in bonobos and chimpanzees. MATERIALS AND METHODS: As a proxy of somatic growth we measured forearm length of captive bonobos and chimpanzees ranging in age from 1 to 55 years. Measures were taken from subjects inserting their arms into a transparent Plexiglas® tube, a novel technique facilitating repeated measures of nonanesthetized apes in captivity. RESULTS: Measures from adult females (>12 years) showed that bonobos exceed chimpanzees in terms of forearm length and that sexual dimorphism in forearm length is pronounced in chimpanzees, but not in bonobos. Forearm length increased significantly with chronological age in bonobos. Validation tests revealed that the device generates useful data on morphometric dimensions. DISCUSSION: In most primates, sexual dimorphism in body size is male-biased and the differences in forearm length in chimpanzees follow this trend. Given that males of the two species did not differ in forearm length, the absence/presence of sexual dimorphism of this trait must be due to differences in somatic growth in females. Our novel method offers an alternative to obtain morphometric measures and facilitates longitudinal studies on somatic growth. Am J Phys Anthropol 161:37-43, 2016. © 2016 Wiley Periodicals, Inc.

Age-related changes in urinary testosterone levels suggest differences in puberty onset and divergent life history strategies in bonobos and chimpanzees.

Research on age-related changes in morphology, social behavior, and cognition suggests that the development of bonobos (Pan paniscus) is delayed in comparison to chimpanzees (Pan troglodytes). However, there is also evidence for earlier reproductive maturation in bonobos. Since developmental changes such as reproductive maturation are induced by a number of endocrine processes, changes in hormone levels are indicators of different developmental stages. Age-related changes in testosterone excretion are an indirect marker for the onset of puberty in human and non-human primates. In this study we investigated patterns of urinary testosterone levels in male and female bonobos and chimpanzees to determine the onset of puberty. In contrast to other studies, we found that both species experience age-related changes in urinary testosterone levels. Older individuals of both sexes had significantly higher urinary testosterone levels than younger individuals, indicating that bonobos and chimpanzees experience juvenile pause. The males of both species showed a similar pattern of age-related changes in urinary testosterone levels, with a sharp increase in levels around the age of eight years. This suggests that species-differences in aggression and male mate competition evolved independently of developmental changes in testosterone levels. Females showed a similar pattern of age-related urinary testosterone increase. However, in female bonobos the onset was about three years earlier than in female chimpanzees. The earlier rise of urinary testosterone levels in female bonobos is in line with reports of their younger age of dispersal, and suggests that female bonobos experience puberty at a younger age than female chimpanzees.

Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development.

We present information on age related changes of thyroid hormone levels in bonobos (N = 96) and chimpanzees (N = 100) ranging between one and 56 years of age. Fresh urine samples were used for hormone measurements with a commercial competitive total triiodothyronine (T3) ELISA. In both species, immature individuals had higher TT3 levels than adults and there was a marked decrease in TT3 levels between age classes. The two species differed in terms of the timing of TT3 level changes, with chimpanzees experiencing a significant decline in TT3 levels after 10 years of age and bonobos after 20 years of age. The decline of TT3 in chimpanzees appears to coincide with the time when somatic growth terminates while TT3 values in bonobos decrease much later. This temporal asymmetry in urinary thyroid hormone levels indicates heterochrony in the ontogenetic changes of the two sister species and developmental delay in bonobos. The prolongation of high TT3 levels in bonobos, which is characteristic of immatures of both Pan species may affect the behavior of bonobos; namely, the low intensity of aggression they display. Given that developmental studies are often based on post-mortem analyses of skeletons, measures of urinary thyroid hormones offer a non-invasive tool for exploring ontogenetic changes in living wild and captive hominoids.

The ontogenetic ritualization of bonobo gestures.

Great apes communicate with gestures in flexible ways. Based on several lines of evidence, Tomasello and colleagues have posited that many of these gestures are learned via ontogenetic ritualization-a process of mutual anticipation in which particular social behaviors come to function as intentional communicative signals. Recently, Byrne and colleagues have argued that all great ape gestures are basically innate. In the current study, for the first time, we attempted to observe the process of ontogenetic ritualization as it unfolds over time. We focused on one communicative function between bonobo mothers and infants: initiation of "carries" for joint travel. We observed 1,173 carries in ten mother-infant dyads. These were initiated by nine different gesture types, with mothers and infants using many different gestures in ways that reflected their different roles in the carry interaction. There was also a fair amount of variability among the different dyads, including one idiosyncratic gesture used by one infant. This gestural variation could not be attributed to sampling effects alone. These findings suggest that ontogenetic ritualization plays an important role in the origin of at least some great ape gestures.

Permanent tooth mineralization in bonobos (Pan paniscus) and chimpanzees (P. troglodytes).

The timing of tooth mineralization in bonobos (Pan paniscus) is virtually uncharacterized. Analysis of these developmental features in bonobos and the possible differences with its sister species, the chimpanzee (P. troglodytes), is important to properly quantify the normal ranges of dental growth variation in closely related primate species. Understanding this variation among bonobo, chimpanzee and modern human dental development is necessary to better contextualize the life histories of extinct hominins. This study tests whether bonobos and chimpanzees are distinguished from each other by covariance among the relative timing and sequences of tooth crown initiation, mineralization, root extension, and completion. Using multivariate statistical analyses, we compared the relative timing of permanent tooth crypt formation, crown mineralization, and root extension between 34 P. paniscus and 80 P. troglodytes mandibles radiographed in lateral and occlusal views. Covariance among our 12 assigned dental scores failed to statistically distinguish between bonobos and chimpanzees. Rather than clustering by species, individuals clustered by age group (infant, younger or older juvenile, and adult). Dental scores covaried similarly between the incisors, as well as between both premolars. Conversely, covariance among dental scores distinguished the canine and each of the three molars not only from each other, but also from the rest of the anterior teeth. Our study showed no significant differences in the relative timing of permanent tooth crown and root formation between bonobos and chimpanzees.

Chimpanzees and bonobos exhibit divergent spatial memory development.

Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (Studies 1 and 2). We then compared older apes using a matched memory choice paradigm (Study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species' different feeding ecologies. Furthermore, chimpanzees - but not bonobos - showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.

Skeletal development in Pan paniscus with comparisons to Pan troglodytes.

Fusion of skeletal elements provides markers for timing of growth and is one component of a chimpanzee's physical development. Epiphyseal closure defines bone growth and signals a mature skeleton. Most of what we know about timing of development in chimpanzees derives from dental studies on Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a wild range restricted to central Africa. Here, we report on the timing of skeletal fusion for female captive P. paniscus (n = 5) whose known ages range from 0.83 to age 11.68 years. Observations on the skeletons were made after the individuals were dissected and bones cleaned. Comparisons with 10 female captive P. troglodytes confirm a generally uniform pattern in the sequence of skeletal fusion in the two captive species. We also compared the P. paniscus to a sample of three unknown-aged female wild P. paniscus, and 10 female wild P. troglodytes of known age from the Taï National Park, Côte d'Ivoire. The sequence of teeth emergence to bone fusion is generally consistent between the two species, with slight variations in late juvenile and subadult stages. The direct-age comparisons show that skeletal growth in captive P. paniscus is accelerated compared with both captive and wild P. troglodytes populations. The skeletal data combined with dental stages have implications for estimating the life stage of immature skeletal materials of wild P. paniscus and for more broadly comparing the skeletal growth rates among captive and wild chimpanzees (Pan), Homo sapiens, and fossil hominins.

The right time to happen: play developmental divergence in the two Pan species.

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a 'timing hotspot' for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.

Comparison of the endocranial ontogenies between chimpanzees and bonobos via temporal regression and spatiotemporal registration.

This paper aims at quantifying ontogenetic differences between bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) endocrania, using dental development as a timeline. We utilize a methodology based on smooth and invertible deformations combined with a metric of "currents" that defines a distance between endocranial surfaces and does not rely on correspondence between landmarks. This allows us to perform a temporal surface regression that estimates typical endocranial ontogenetic trajectories separately for bonobos and chimpanzees. We highlight non-linear patterns of endocranial ontogenetic change and significant differences between species at local anatomical levels rather than considering the endocranium as a uniform entity. A spatiotemporal registration permits the quantification of inter-species differences decomposed into a morphological deformation (accounting for size and shape differences independently of age) and a time warp (accounting for changes in the dynamics of development). Our statistical simulations suggest that patterns of endocranial volume (EV) increase may differ significantly between bonobos and chimpanzees, with an earlier phase of a relatively rapid increase (preferentially at some endocranial subdivisions) in the former and a much later phase of relatively rapid increase in the latter. As a consequence, the chimpanzee endocranium appears to reach its adult size later. Moreover, the time warp indicates that juvenile bonobos develop much slower than juvenile chimpanzees, suggesting that inter-specific ontogenetic shifts do not only concern EV increase, but also the rate of shape changes over time. Our method provides, for the first time, a quantitative estimation of inter-specific ontogenetic shifts that appear to differentiate non-linearly.

Bonobo but not chimpanzee infants use socio-sexual contact with peers.

Bonobos have been observed to use socio-sexual behavior at higher frequency than chimpanzees. Little is known about the developmental influences that shape this behavior in bonobos. We compared the social sexual behavior of wild-born bonobo (n = 8) and chimpanzee (n = 16) infants in an experimental feeding test. Subjects of both species were orphans of the bushmeat trade living at sanctuaries in peer groups. During the experiment, chimpanzee infants never had socio-sexual interactions with one another. In contrast, bonobo infants had socio-sexual interactions significantly more than the chimpanzee infants and more often when food was presented. During these socio-sexual interactions, bonobo infants did not show a preference for heterosexual partners or genital-genital positioning that is reproductive in adults (e.g. a dorso-ventral posture). These findings suggest that the socio-sexual behavior previously observed in various captive and wild bonobos is species-typical. Wild-born bonobos originating from a large geographical range develop this behavior long before puberty and without the need for adults initiating such behavior or acting as models for observational learning. Meanwhile, chimpanzee infants of the same age with similar rearing history show no signs of the same socio-sexual behavior. Results are interpreted regarding hypotheses for the evolution of bonobo psychology.

The presence of accessory cusps in chimpanzee lower molars is consistent with a patterning cascade model of development.

Tooth crown morphology is of primary importance in fossil primate systematics and understanding the developmental basis of its variation facilitates phenotypic analyses of fossil teeth. Lower molars of species in the chimp/human clade (including fossil hominins) possess between four and seven cusps and this variability has been implicated in alpha taxonomy and phylogenetic systematics. What is known about the developmental basis of variation in cusp number - based primarily on experimental studies of rodent molars - suggests that cusps form under a morphodynamic, patterning cascade model involving the iterative formation of enamel knots. In this study we test whether variation in cusp 6 (C6) presence in common chimpanzee and bonobo lower molars (n = 55) is consistent with predictions derived from the patterning cascade model. Using microcomputed tomography we imaged the enamel-dentine junction of lower molars and used geometric morphometrics to examine shape variation in the molar crown correlated with variation in C6 presence (in particular the size and spacing of the dentine horns). Results indicate that C6 presence is consistent with predictions of a patterning cascade model, with larger molars exhibiting a higher frequency of C6 and with the location and size of later-forming cusps correlated with C6 variation. These results demonstrate that a patterning cascade model is appropriate for interpreting cusp variation in Pan and have implications for cusp nomenclature and the use of accessory cusp morphology in primate systematics.

Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees.

Phenotypic changes between species can occur when evolution shapes development. Here, we tested whether differences in the social behavior and cognition of bonobos and chimpanzees derive from shifts in their ontogeny, looking at behaviors pertaining to feeding competition in particular. We found that as chimpanzees (n = 30) reached adulthood, they became increasingly intolerant of sharing food, whereas adult bonobos (n = 24) maintained high, juvenile levels of food-related tolerance. We also investigated the ontogeny of inhibition during tasks that simulated feeding competition. In two different tests, we found that bonobos (n = 30) exhibited developmental delays relative to chimpanzees (n = 29) in the acquisition of social inhibition, with these differences resulting in less skill among adult bonobos. The results suggest that these social and cognitive differences between two closely related species result from evolutionary changes in brain development.

Behavioral development: timing is everything.

A new study has found that bonobos take longer to reach adult levels of two behaviors than do chimpanzees, providing empirical support for the 'paedomorphism' hypothesis among our closest relatives.

Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a preliminary study.

The dichotomy between the two Pan species, the bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) has been strongly emphasized until very recently. Given that most studies were primarily based on adult individuals, we shifted the "continuity versus discontinuity" discussion to the infant and juvenile stage. Our aim was to test quantitatively, some conflicting statements made in literature considering species differences between immature bonobos and chimpanzees. On one hand it is suggested that infant bonobos show retardation in motor and social development when compared with chimpanzees. Additionally it is expected that the weaning process is more traumatic to chimpanzee than bonobo infants. But on the other hand the development of behaviors is expected to be very similar in both species. We observed eight mother-infant pairs of each species in several European zoos. Our preliminary research partially confirms that immature chimpanzees seem spatially more independent, spending more time at a larger distance from their mother than immature bonobos. However, the other data do not seem to support the hypothesis that bonobo infants show retardation of motor or social development. The development of solitary play, environmental exploration, social play, non-copulatory mounts and aggressive interactions do not differ between the species. Bonobo infants in general even groom other group members more than chimpanzee infants. We also found that older bonobo infants have more nipple contact than same aged chimpanzees and that the weaning process seems to end later for bonobos than for immature chimpanzee. Additionally, although immature bonobos show in general more signs of distress, our data suggest that the weaning period itself is more traumatic for chimpanzees.

Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes.

Heterochrony, the classic framework in which to study ontogeny and phylogeny, in essence relies on a univariate concept of shape. Though principal component (PC) plots of multivariate shape data seem to resemble classical bivariate allometric plots, the language of heterochrony cannot be translated directly into general multivariate methodology. We simulate idealized multivariate ontogenetic trajectories and explore their appearance in PC plots of shape space and size-shape space. Only if the trajectories of two related species lie along exactly the same path in shape space can the classic terminology of heterochrony apply and pure dissociation of size change against shape change be detected. Regional heterochrony--the variation of apparent heterochrony by region--implies a dissociation of local growth fields and cannot be identified in an overall PC analysis. We exemplify a geometric morphometric approach to these issues using adult and subadult crania of 48 Pan paniscus and 47 Pan troglodytes specimens. On each specimen, we digitized 47 landmarks and 144 semilandmarks on facial curves and the external neurocranial surface. We reject the hypothesis of global heterochrony in the cranium of Pan as well as regional heterochrony for the lower face, the upper face, and the neurocranium.