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.     

High diversity at PRDM9 in chimpanzees and bonobos

Background

The PRDM9 locus in mammals has increasingly attracted research attention due to its role in mediating chromosomal recombination and possible involvement in hybrid sterility and hence speciation processes. The aim of this study was to characterize sequence variation at the PRDM9 locus in a sample of our closest living relatives, the chimpanzees and bonobos.

Methodology/Principal Findings

PRDM9 contains a highly variable and repetitive zinc finger array. We amplified this domain using long-range PCR and determined the DNA sequences using conventional Sanger sequencing. From 17 chimpanzees representing three subspecies and five bonobos we obtained a total of 12 alleles differing at the nucleotide level. Based on a data set consisting of our data and recently published Pan PRDM9 sequences, we found that at the subspecies level, diversity levels did not differ among chimpanzee subspecies or between chimpanzee subspecies and bonobos. In contrast, the sample of chimpanzees harbors significantly more diversity at PRDM9 than samples of humans. Pan PRDM9 shows signs of rapid evolution including no alleles or ZnFs in common with humans as well as signals of positive selection in the residues responsible for DNA binding.

Conclusions and Significance

The high number of alleles specific to the genus Pan, signs of positive selection in the DNA binding residues, and reported lack of conservation of recombination hotspots between chimpanzees and humans suggest that PRDM9 could be active in hotspot recruitment in the genus Pan. Chimpanzees and bonobos are considered separate species and do not have overlapping ranges in the wild, making the presence of shared alleles at the amino acid level between the chimpanzee and bonobo species interesting in view of the hypothesis that PRDM9 plays a universal role in interspecific hybrid sterility.     

The Human Semicircular Canals Orientation Is More Similar to the Bonobos than to the Chimpanzees

For some traits, the human genome is more closely related to either the bonobo or the chimpanzee genome than they are to each other. Therefore, it becomes crucial to understand whether and how morphostructural differences between humans, chimpanzees and bonobos reflect the well known phylogeny. Here we comparatively investigated intra and extra labyrinthine semicircular canals orientation using 260 computed tomography scans of extant humans (Homo sapiens), bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Humans and bonobos proved more similarities between themselves than with chimpanzees. This finding did not fit with the well established chimpanzee – bonobo monophyly. One hypothesis was convergent evolution in which bonobos and humans produce independently similar phenotypes possibly in response to similar selective pressures that may be associated with postural adaptations. Another possibility was convergence following a “random walk” (Brownian motion) evolutionary model. A more parsimonious explanation was that the bonobo-human labyrinthine shared morphology more closely retained the ancestral condition with chimpanzees being subsequently derived. Finally, these results might be a consequence of genetic diversity and incomplete lineage sorting. The remarkable symmetry of the Semicircular Canals was the second major finding of this article with possible applications in taphonomy. It has the potential to investigate altered fossils, inferring the probability of post-mortem deformation which can lead to difficulties in understanding taxonomic variation, phylogenetic relationships, and functional morphology.     

Analysis of chimpanzee history based on genome sequence alignments

Population geneticists often study small numbers of carefully chosen loci, but it has become possible to obtain orders of magnitude for more data from overlaps of genome sequences. Here, we generate tens of millions of base pairs of multiple sequence alignments from combinations of three western chimpanzees, three central chimpanzees, an eastern chimpanzee, a bonobo, a human, an orangutan, and a macaque. Analysis provides a more precise understanding of demographic history than was previously available. We show that bonobos and common chimpanzees were separated ~1,290,000 years ago, western and other common chimpanzees ~510,000 years ago, and eastern and central chimpanzees at least 50,000 years ago. We infer that the central chimpanzee population size increased by at least a factor of 4 since its separation from western chimpanzees, while the western chimpanzee effective population size decreased. Surprisingly, in about one percent of the genome, the genetic relationships between humans, chimpanzees, and bonobos appear to be different from the species relationships. We used PCR-based resequencing to confirm 11 regions where chimpanzees and bonobos are not most closely related. Study of such loci should provide information about the period of time 5–7 million years ago when the ancestors of humans separated from those of the chimpanzees.     

Gene flow in wild chimpanzee populations: what genetic data tell us about chimpanzee movement over space and time

The isolation of phylogenetically distinct primate immunodeficiency viruses from at least seven wild-born, captive chimpanzees indicates that viruses closely related to HIV-1 may be endemic in some wild chimpanzee populations. The search for the chimpanzee population or populations harbouring these viruses is therefore on. This paper attempts to answer the question of whether or not such populations of chimpanzees are likely to exist at all, and, if so, where they are likely to be found. We summarize what is known about gene flow in wild populations of chimpanzees, both between major phylogeographical subdivisions of the species, and within these subdivisions. Our analysis indicates that hitherto undocumented reproductively isolated chimpanzee populations may in fact exist. This conclusion is based on the observation that, despite limited geographical sampling and limited numbers of genetic loci, conventional notions of the nature and extent of chimpanzee gene flow have recently been substantially revised. Molecular genetic studies using mitochondrial DNA sequences and hypervariable nuclear microsatellite markers have indicated the existence of heretofore undocumented barriers to chimpanzee gene flow. These studies have identified at least one population of chimpanzees genetically distinct enough to be classified into a new subspecies (Pan troglodytes vellerosus). At the same time, they have called into question the long-accepted genetic distinction between eastern chimpanzees (Pan troglodytes schweinfurthii) and western equatorial chimpanzees (Pan troglodytes troglodytes). The same studies have further indicated that gene flow between local populations is more extensive than was previously thought, and follows patterns sometimes inconsistent with those documented through direct behavioural observation. Given the apparently incomplete nature of the current understanding of chimpanzee gene flow in equatorial Africa, it seems reasonable to speculate that a chimpanzee population or populations may exist which both harbour the putative HIV-1 ancestor, and which have remained reproductively isolated from other chimpanzee populations over the time-scale relevant to the evolution of the SIVcpz-HIV-1 complex of viruses. Continued extensive sampling of wild chimpanzee populations, both for their genes and their viruses, should be performed quickly considering the high probability of extinction that many wild chimpanzee populations face today. The history of human-chimpanzee contacts is discussed.     

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.     

Female contributions to the peaceful nature of bonobo society

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are closely related, females of the two species show surprisingly large differences in many behavioral aspects. While female chimpanzees tend to range alone or in small parties during non-estrous periods, female bonobos aggregate even more often than do males. Female chimpanzees do not have frequent social interactions with other females, whereas female bonobos maintain close social associations with one another. Although the ranging patterns of chimpanzee parties are generally led by males, female bonobos often take the initiative in ranging behavior. While female chimpanzees usually do not exhibit estrus during postpartum amenorrhea or pregnancy, female bonobos exhibit a prolonged pseudo-estrus during such non-conceptive periods. Studies of these two species have also shown great differences in agonistic behaviors performed by males. Male chimpanzees frequently fight with other males to compete for estrous females, but male bonobos seldom do so. While there are many records of infanticide by male chimpanzees, there is no confirmed record of such an event among bonobos. Several cases of within-group killing among adult male chimpanzees have been reported, but there is no such record for bonobos. While intergroup conflicts among chimpanzees sometimes involve killing members of the other group, intergroup conflicts among bonobos are considerably more moderate. In some cases, bonobos from two different groups may even range together for several days while engaging in various peaceful interactions. I will address two important questions that arise from these comparisons, exploring why females of such closely related species show such clear differences in behavior and whether or not the behavioral characteristics of female bonobos contribute to the peaceful nature of bonobo society.     

Genetic structure of chimpanzee populations

Little is known about the history and population structure of our closest living relatives, the chimpanzees, in part because of an extremely poor fossil record. To address this, we report the largest genetic study of the chimpanzees to date, examining 310 microsatellites in 84 common chimpanzees and bonobos. We infer three common chimpanzee populations, which correspond to the previously defined labels of “western,” “central,” and “eastern,” and find little evidence of gene flow between them. There is tentative evidence for structure within western chimpanzees, but we do not detect distinct additional populations. The data also provide historical insights, demonstrating that the western chimpanzee population diverged first, and that the eastern and central populations are more closely related in time.     

Are bonobos (Pan paniscus) really more bipedal than chimpanzees (Pan troglodytes)?

Of the living apes, the chimpanzee (Pan troglodytes) and bonobo (Pan paniscus) are often presented as possible models for the evolution of hominid bipedalism. Bipedality in matched pairs of captive bonobos and chimpanzees was analyzed to test hypotheses for the evolution of bipedalism, derived from a direct referential model. There was no overall species difference in rates of bipedal positional behavior, either postural or locomotory. The hominoid species differed in the function or use of bipedality, with bonobos showing more bipedality for carrying and vigilance, and chimpanzees showing more bipedality for display.     

Comparative locomotor behavior of chimpanzees and bonobos: The influence of morphology on locomotion

Results from a 10 month study of adult male and female bonobos (Pan paniscus) in the Lomako Forest, Zaire, and those from a 7 month study of adult male and female chimpanzees in the Tai Forest, Ivory Coast (Pan troglodytes verus), were compared in order to determine whether there are species differences in locomotor behavior and substrate use and, if so, whether these differences support predictions made on the basis of interspecific morphological differences. Results indicate that bonobos are more arboreal than chimpanzees and that male bonobos are more suspensory than their chimpanzee counterpart. This would be predicted on the basis of male bonobo's longer and more narrow scapula. This particular finding is contrary to the prediction that the bonobo is a “scaled reduced version of a chimpanzee” with little or no positional behavior difference as had been suggested. This study provides the behavioral data necessary to untangle contradictory interpretations of the morphological differences between chimpanzees and bonobos, and raises a previously discussed (Fleagle: Size and Scaling in Primate Biology, pp. 1–19, 1985) but frequently overlooked point–that isometry in allometric studies does not necessarily equate with behavioral equivalence. Several researchers have demonstrated that bonobos and chimpanzees follow the same scaling trends for many features, and are in some sense functionally equivalent, since they manage to feed and reproduce. However, as reflected in their morphologies, they do so through different types and frequencies of locomotor behaviors. © 1993 Wiley-Liss, Inc.     

Y-Chromosome variation in hominids: intraspecific variation is limited to the polygamous chimpanzee

Background

We have previously demonstrated that the Y-specific ampliconic fertility genes DAZ (deleted in azoospermia) and CDY (chromodomain protein Y) varied with respect to copy number and position among chimpanzees (Pan troglodytes). In comparison, seven Y-chromosomal lineages of the bonobo (Pan paniscus), the chimpanzee''s closest living relative, showed no variation. We extend our earlier comparative investigation to include an analysis of the intraspecific variation of these genes in gorillas (Gorilla gorilla) and orangutans (Pongo pygmaeus), and examine the resulting patterns in the light of the species'' markedly different social and mating behaviors.

Methodology/Principal Findings

Fluorescence in situ hybridization analysis (FISH) of DAZ and CDY in 12 Y-chromosomal lineages of western lowland gorilla (G. gorilla gorilla) and a single lineage of the eastern lowland gorilla (G. beringei graueri) showed no variation among lineages. Similar findings were noted for the 10 Y-chromosomal lineages examined in the Bornean orangutan (Pongo pygmaeus), and 11 Y-chromosomal lineages of the Sumatran orangutan (P. abelii). We validated the contrasting DAZ and CDY patterns using quantitative real-time polymerase chain reaction (qPCR) in chimpanzee and bonobo.

Conclusion/Significance

High intraspecific variation in copy number and position of the DAZ and CDY genes is seen only in the chimpanzee. We hypothesize that this is best explained by sperm competition that results in the variant DAZ and CDY haplotypes detected in this species. In contrast, bonobos, gorillas and orangutans—species that are not subject to sperm competition—showed no intraspecific variation in DAZ and CDY suggesting that monoandry in gorillas, and preferential female mate choice in bonobos and orangutans, probably permitted the fixation of a single Y variant in each taxon. These data support the notion that the evolutionary history of a primate Y chromosome is not simply encrypted in its DNA sequences, but is also shaped by the social and behavioral circumstances under which the specific species has evolved.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo

Compared to data from chimpanzees, observations on prey capture and meat eating by bonobos (Pan paniscus) are still rare, fragmentary and anecdotal. Here we present new and unpublished information from wild bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Our observations confirm that solitary and terrestrial ungulates are the major prey. However, bonobos at Lui Kotale also consumed other mammalian prey, including other primates. Evidence from direct observations is complemented with information obtained by macroscopic analyses of fresh faeces. Results suggest that bonobos consume meat with frequencies similar to some chimpanzee populations. The data emphasize differences between the two Pan species in terms of prey species selection and prey capture.     

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.     

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.     

Visual Search for Human Gaze Direction by a Chimpanzee (Pan troglodytes)

Background

Humans detect faces with direct gazes among those with averted gazes more efficiently than they detect faces with averted gazes among those with direct gazes. We examined whether this “stare-in-the-crowd” effect occurs in chimpanzees (Pan troglodytes), whose eye morphology differs from that of humans (i.e., low-contrast eyes, dark sclera).

Methodology/Principal Findings

An adult female chimpanzee was trained to search for an odd-item target (front view of a human face) among distractors that differed from the target only with respect to the direction of the eye gaze. During visual-search testing, she performed more efficiently when the target was a direct-gaze face than when it was an averted-gaze face. This direct-gaze superiority was maintained when the faces were inverted and when parts of the face were scrambled. Subsequent tests revealed that gaze perception in the chimpanzee was controlled by the contrast between iris and sclera, as in humans, but that the chimpanzee attended only to the position of the iris in the eye, irrespective of head direction.

Conclusion/Significance

These results suggest that the chimpanzee can discriminate among human gaze directions and are more sensitive to direct gazes. However, limitations in the perception of human gaze by the chimpanzee are suggested by her inability to completely transfer her performance to faces showing a three-quarter view.     

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.     

The Apolipoprotein E (APOE) Gene Appears Functionally Monomorphic in Chimpanzees (Pan troglodytes)

Background

The human apolipoprotein E (APOE) gene is polymorphic, with three primary alleles (E2, E3, E4) that differ at two key non-synonymous sites. These alleles are functionally different in how they bind to lipoproteins, and this genetic variation is associated with phenotypic variation for several medical traits, including cholesterol levels, cardiovascular health, Alzheimer’s disease risk, and longevity. The relative frequencies of these alleles vary across human populations, and the evolution and maintenance of this diversity is much debated. Previous studies comparing human and chimpanzee APOE sequences found that the chimpanzee sequence is most similar to the human E4 allele, although the resulting chimpanzee protein might function like the protein coded for by the human E3 allele. However, these studies have used sequence data from a single chimpanzee and do not consider whether chimpanzees, like humans, show intra-specific and subspecific variation at this locus.

Methodology and Principal Findings

To examine potential intraspecific variation, we sequenced the APOE gene of 32 chimpanzees. This sample included 20 captive individuals representing the western subspecies (P. troglodytes verus) and 12 wild individuals representing the eastern subspecies (P. t. schweinfurthii). Variation in our resulting sequences was limited to one non-coding, intronic SNP, which showed fixed differences between the two subspecies. We also compared APOE sequences for all available ape genera and fossil hominins. The bonobo APOE protein is identical to that of the chimpanzee, and the Denisovan APOE exhibits all four human-specific, non-synonymous changes and appears functionally similar to the human E4 allele.

Conclusions

We found no coding variation within and between chimpanzee populations, suggesting that the maintenance of functionally diverse APOE polymorphisms is a unique feature of human evolution.