Mandibular Shape, Ontogeny and Dental Development in Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

The postnatal ontogenetic patterns and processes that underlie species differences in African ape adult mandibular morphology are not well understood and there is ongoing debate about whether African ape faces and mandibles develop via divergent or parallel trajectories of shape change. Using three-dimensional (3D) morphometric data, we first tested when in postnatal development differences in mandibular shape are initially evident between sister species Pan troglodytes and P. paniscus. Next, we tested whether each species has a distinct and non-parallel trajectory of mandibular development. Mandibles sampled across a broad developmental range of wildshot bonobos (n = 44) and chimpanzees (n = 59) were radiographed and aged from their dental development. We then collected 3D landmark surface data from all the mandibles. A geometric morphometric analysis of size-corrected 3D data found that bonobos and chimpanzees had parallel and linear ontogenetic trajectories of mandibular shape change. In contrast, mandibular shape was statistically different between P. paniscus and P. troglodytes as early as infancy, suggesting that species shape differences are already established near or before birth. A linear and stable trajectory of shape change suggests that mandibular ontogeny in these apes is unimpacted by non-linear variation in tooth developmental timing.     

External body dimensions ofPan paniscus andPan troglodytes chimpanzees

Postcranial skeletal studies have demonstrated thatPan paniscus is a more gracile animal thanPan troglodytes, with different arm to leg proportions. Published data on external body dimensions are extremely rare forPan paniscus, however. We present here a series of such measures for a sample ofpaniscus, and we compare these to similar measures forPan troglodytes. This comparison further clarifies the morphological distinctions between the two chimpanzee species, and indicates that bonobos have longer legs and smaller chest girths relative to overall body height than doPan troglodytes chimpanzees.     

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.     

Patterns of microsatellite polymorphism in the range-restricted bonobo (Pan paniscus): considerations for interspecific comparison with chimpanzees (P. troglodytes)

The endangered great ape, Pan paniscus (bonobo) has the smallest range of the African apes. Virtually nothing is known about the genetic diversity or genetic structure of this species, while substantial amounts of polymorphism have been reported for the bonobo’s widespread congener, the chimpanzee (P. troglodytes). Given its restricted range, what is the extent of genetic variation in the bonobo relative to the chimpanzee, and is the bonobo genetically depauperate? To investigate patterns of genetic polymorphism, bonobos of wild origin were genotyped for 28 microsatellite loci. The mean number of alleles per locus (5.2) and the mean observed heterozygosity (0.52) in bonobos were similar to variation observed in a wild chimpanzee community (P. t. schweinfurthii). The rarer bonobo is not genetically depauperate and may have genetic diversity comparable to the eastern chimpanzee subspecies. Bonobos have approximately 55% of the allelic diversity and 66% of the observed heterozygosity exhibited by all three chimpanzee subspecies sampled across equatorial Africa. Resampling techniques were used to quantify the effects of sample size differences and number and choice of loci between bonobos and chimpanzees. The examination of these variables underscores their importance in accurately interpreting interspecific comparisons of diversity estimates.     

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. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

The behavior of a group of captive pygmy chimpanzees (Pan paniscus)

A group of captive pygmy chimpanzees (Pan paniscus) was studied in the San Diego Zoological Gardens. The behavior patterns that these animals exhibit are described. Each of these behavior patterns is compared to those described for wild and captive common chimpanzees (P. troglodytes). Differences in behavior between these two species are attributed to specialization of the pygmy chimpanzee to a rain forest habitat and to a monogamous social system.     

Male-male relationships among wild bonobos (Pan paniscus) at Wamba,Republic of Zaire

Male-male relationships among wild bonobos (Pan paniscus) in two adjacent unitgroups (E1 and E2 groups), which were formed by division of the E group, were studied at Wamba, in the Central Zaire Basin, by analyzing the proximity and social interactions among males. Dominant-subordinate relationships between a male-male dyad were easily recognized from the directions of individual agonistic interactions. Male bonobos rarely joined forces in aggression. Clear differences in social status existed between adult and adolescent male bonobos in both groups, as reported in the case of chimpanzees (Pan troglodytes). The presence of mothers in the unit-group greatly influenced the dominant-subordinate relationships among males through strong mother-son bonds in both groups. However, the extent of the mother-son bonds differed between the groups. Males in the E2 group participated more frequently in agonistic or affinitive interactions than did males in the E1 group. Males in the E1 group were divided spatially into several clusters, while there were cohesive relationships among the adult males in the E2 group. The difference in intensities of mother-son bonds between the groups may be explained by the distribution of males at the time of the division of the E group. Differences in male-male relationships between bonobos and chimpanzees seem to be related to differences in intra- and inter-unit-group competition among males between the two species. Male chimpanzees may achieve coexistence by manipulating ambivalent relationships that are caused by intra- and inter-unit-group competition among them, while male bonobos may achieve coexistence by decreasing intra- and inter-unit-group competition among them.     

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.     

Bonobos have a more human-like second-to-fourth finger length ratio (2D:4D) than chimpanzees: a hypothesized indication of lower prenatal androgens

The ratio of the second-to-fourth finger lengths (2D:4D) has been proposed as an indicator of prenatal sex differentiation. However, 2D:4D has not been studied in the closest living human relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). We report the results from 79 chimpanzees and 39 bonobos of both sexes, including infants, juveniles, and adults. We observed the expected sex difference in 2D:4D, and substantially higher, more human-like, 2D:4D in bonobos than chimpanzees. Previous research indicates that sex differences in 2D:4D result from differences in prenatal sex hormone levels. We hypothesize that the species difference in 2D:4D between bonobos and chimpanzees suggests a possible role for early exposure to sex hormones in the development of behavioral differences between the two species.     

A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest,Zaire, and Pan troglodytes in the Kibale Forest,Uganda

Differences in the social organization and dental morphology of Pan paniscus (bonobos) and Pan troglodytes (chimpanzees) have been related to differences in the spatiotemporal availability of food and its exploitation. The presence of abundant terrestrial herbaceous vegetation (THV) in the bonobo's habitat and the apparent greater reliance on herbs for food has been used to explain differences in party size and, by extension, social organization. Using fecal analysis, we assess quantitatively the amount of herbaceous foods consumed by Pan paniscus in the Lomako Forest, Zaire, compared to similar data for Pan troglodytes in the Kibale Forest, Uganda. We examine this data in the context of spatiotemporal patterns of availability of herbaceous foods and fruit, as well as their nutritional content. The results support the suggestion that bonobos consume more herbaceous food than do the Kibale chimpanzees and that these foods are more prevalent in the bonobo's habitat than in the Kibale Forest. However, temporal changes in fruit availability and herb consumption, along with nutritional analyses, suggest that chimpanzees consume herbs as a fallback source of carbohydrates, whereas bonobos consume herbs as a source of protein regardless of season or fruit abundance. Available data suggest that party size while feeding on terrestrial herbs is restricted at both sites, but a determination of the relative strength of this constraint is not possible at this time. Difficulties in methods used for data collection are discussed and areas where more information is needed are highlighted. © 1994 Wiley-Liss, Inc.     

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Plant foods consumed by Pan: Exploring the variation of nutritional ecology across Africa

It has been shown that differences in resource density and nutrient supply affect variation in ranging patterns, habitat use, and sociality. Among nonhuman primates, chimpanzees (Pan troglodytes) and bonobos (P. paniscus) have often been used as models for the link between social system and habitat ecology. Field reports suggest that resource density is higher in habitats occupied by bonobos (compared to chimpanzee habitats), and in the West (compared to the East) of the range of chimpanzees. In this study we compared diet quality at the level of species and populations using information from nutritional analyses of fruit and leaves consumed by chimpanzees (three) and bonobos (one population). Quality of plant foods was assessed on the basis of a) the concentration of macronutrients, fiber, and anti‐feedants, and b) associations of different nutrient components. Overall plant samples collected at each site differed in terms of macronutrient content. However, nutritious quality and gross energy content of food samples were similar suggesting that dietary quality reflects selectivity rather than habitat ecology. The quality of plant foods consumed by bonobos was within the range of chimpanzees and the quality of plant foods consumed by western chimpanzees was not higher than that of eastern chimpanzees. While the results showed significant variation across forests inhabited by Pan, they did not match with geographical patterns between and within Pan species as proposed in previous studies. This suggests that the nutritional quality of the habitat is not always a reliable predictor of the quality of the diet. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Discrimination of extant Pan species and subspecies using the enamel–dentine junction morphology of lower molars

Previous research has demonstrated that species and subspecies of extant chimpanzees and bonobos can be distinguished on the basis of the shape of their molar crowns. Thus, there is potential for fossil taxa, particularly fossil hominins, to be distinguished at similar taxonomic levels using molar crown morphology. Unfortunately, due to occlusal attrition, the original crown morphology is often absent in fossil teeth, and this has limited the amount of shape information used to discriminate hominin molars. The enamel–dentine junction (EDJ) of molar teeth preserves considerable shape information, particularly in regard to the original shape of the crown, and remains present through the early stages of attrition. In this study, we investigate whether the shape of the EDJ of lower first and second molars can distinguish species and subspecies of extant Pan. Micro‐computed tomography was employed to non‐destructively image the EDJ, and geometric morphometric analytical methods were used to compare EDJ shape among samples of Pan paniscus (N = 17), Pan troglodytes troglodytes (N = 13), and Pan troglodytes verus (N = 18). Discriminant analysis indicates that EDJ morphology distinguishes among extant Pan species and subspecies with a high degree of reliability. The morphological differences in EDJ shape among the taxa are subtle and relate to the relative height and position of the dentine horns, the height of the dentine crown, and the shape of the crown base, but their existence supports the inclusion of EDJ shape (particularly those aspects of shape in the vertical dimension) in the systematic analysis of fossil hominin lower molars. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.     

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.     

Epidermal patterns of the hands and feet of the pygmy chimpanzee (Pan paniscus)

The characteristics of the epidermal ridge system were studied in a series of eighteen lesser or pygmy chimpanzees (Pan paniscus). The general ridge alignments are very similar to those of the chimpanzee (Pan troglodytes); Biegert ('61). On the average the pattern intensity (P.I.) of the palm configurations is considerably higher in the pygmy chimpanzee than in the chimpanzee, thus representing the highest total palm pattern intensity of all species of the Hominoidea. The sole configurations show parallel main results to those of the palm; however, the decreased sole pattern frequency of the pygmy chimpanzee is of a smaller predominance only as compared to the values of the other species of this superfamily. The preliminary data on the finger tip patterns, translated into P.I. values, are much higher than in chimpanzees and within the range of the mean values of gorillas (Brehme, '73), while those of the toes of pygmy chimpanzees seem to possess the lowest P.I. values of the African apes.     

Brief Communication: Quantitative‐ and molecular‐genetic differentiation in humans and chimpanzees: Implications for the evolutionary processes underlying cranial diversification

Estimates of the amount of genetic differentiation in humans among major geographic regions (e.g., Eastern Asia vs. Europe) from quantitative‐genetic analyses of cranial measurements closely match those from classical‐ and molecular‐genetic markers. Typically, among‐region differences account for ～10% of the total variation. This correspondence is generally interpreted as evidence for the importance of neutral evolutionary processes (e.g., genetic drift) in generating among‐region differences in human cranial form, but it was initially surprising because human cranial diversity was frequently assumed to show a strong signature of natural selection. Is the human degree of similarity of cranial and DNA‐sequence estimates of among‐region genetic differentiation unusual? How do comparisons with other taxa illuminate the evolutionary processes underlying cranial diversification? Chimpanzees provide a useful starting point for placing the human results in a broader comparative context, because common chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are the extant species most closely related to humans. To address these questions, I used 27 cranial measurements collected on a sample of 861 humans and 263 chimpanzees to estimate the amount of genetic differentiation between pairs of groups (between regions for humans and between species or subspecies for chimpanzees). Consistent with previous results, the human cranial estimates are quite similar to published DNA‐sequence estimates. In contrast, the chimpanzee cranial estimates are much smaller than published DNA‐sequence estimates. It appears that cranial differentiation has been limited in chimpanzees relative to humans. Am J Phys Anthropol 154:615–620, 2014. © 2014 Wiley Periodicals, Inc.     

Scapula form and locomotion in chimpanzee evolution

A number of primatologists have followed Coolidge (Am. J. Phys. Anthropol. 18:1–57, 1933) in suggesting that 1) there are significant shape differences in scapula form between pygmy and common chimpanzees, 2) scapulae of P. paniscus resemble those of hylobatids more than do those of P. troglodytes, and 3) therefore pygmy chimpanzees may exhibit a greater component of arm-swinging and other arboreal behaviors than common chimpanzees. In this paper I utilize a comparative analysis of ontogenetic allometries of linear dimensions to determine shape differences in the scapulae of adult pygmy and common chimpanzees and to clarify size-related changes in shape resulting from ontogenetic scaling, i.e., the differential extension of common patterns of growth allometry. Results demonstrate that the scapulae of adult P. paniscus are relatively narrower (in a direction approximately perpendicular to the scapula spine) than those of P. troglodytes, supporting Coolidge's original claim. The allometric analysis further demonstrates, however, that the two chimpanzee species exhibit ontogenetic scaling for all proportions of the scapula examined. Thus, adult pygmy chimpanzees have the scapula proportions observed in small adult and subadult P. troglodytes of comparable scapula size. The implications of this finding for past claims concerning differences in locomotor behavior between the species are discussed. This work lends additional support to previous studies that have demonstrated a high frequency of ontogenetic scaling within the genus Pan and a pedomorphic or juvenilized morphology in the pygmy chimpanzee.     

Evidence for the consumption of arboreal,diurnal primates by bonobos (Pan paniscus)

We present evidence for the consumption of a diurnal, arboreal, group living primate by bonobos. The digit of an immature black mangabey (Lophocebus aterrimus) was found in the fresh feces of a bonobo (Pan paniscus) at the Lui Kotale study site, Democratic Republic of Congo. In close proximity to the fecal sample containing the remains of the digit, we also found a large part of the pelt of a black mangabey. Evidence suggests that the Lui Kotale bonobos consume more meat than other bonobo populations and have greater variation in the mammalian species exploited than previously thought [Hohmann & Fruth, Folia primatologica 79:103–110]. The current finding supports Stanford's argument [Current Anthropology 39:399–420] that some differences in the diet and behavior between chimpanzees (P. troglodytes) and bonobos are an artefact of the limited number of bonobo study populations. If bonobos did obtain the monkey by active hunting, this would challenge current evolutionary models relating the intra‐specific aggression and violence seen in chimpanzees and humans to hunting and meat consumption [Wrangham, Yearbook of Physical Anthropology 42:1–30]. Am. J. Primatol. 71:171–174, 2009. © 2008 Wiley‐Liss, Inc.