Vertebrate DNA in Fecal Samples from Bonobos and Gorillas: Evidence for Meat Consumption or Artefact?

Background: Deciphering the behavioral repertoire of great apes is a challenge for several reasons. First, due to their elusive behavior in dense forest environments, great ape populations are often difficult to observe. Second, members of the genus Pan are known to display a great variety in their behavioral repertoire; thus, observations from one population are not necessarily representative for other populations. For example, bonobos (Pan paniscus) are generally believed to consume almost no vertebrate prey. However, recent observations show that at least some bonobo populations may consume vertebrate prey more commonly than previously believed. We investigated the extent of their meat consumption using PCR amplification of vertebrate mitochondrial DNA (mtDNA) segments from DNA extracted from bonobo feces. As a control we also attempted PCR amplifications from gorilla feces, a species assumed to be strictly herbivorous. Principal Findings: We found evidence for consumption of a variety of mammalian species in about 16% of the samples investigated. Moreover, 40% of the positive DNA amplifications originated from arboreal monkeys. However, we also found duiker and monkey mtDNA in the gorilla feces, albeit in somewhat lower percentages. Notably, the DNA sequences isolated from the two ape species fit best to the species living in the respective regions. This result suggests that the sequences are of regional origin and do not represent laboratory contaminants. Conclusions: Our results allow at least three possible and mutually not exclusive conclusions. First, all results may represent contamination of the feces by vertebrate DNA from the local environment. Thus, studies investigating a species' diet from feces DNA may be unreliable due to the low copy number of DNA originating from diet items. Second, there is some inherent difference between the bonobo and gorilla feces, with only the later ones being contaminated. Third, similar to bonobos, for which the consumption of monkeys has only recently been documented, the gorilla population investigated (for which very little observational data are as yet available) may occasionally consume small vertebrates. Although the last explanation is speculative, it should not be discarded a-priori given that observational studies continue to unravel new behaviors in great ape species

Rapid Evolution of BRCA1 and BRCA2 in Humans and Other Primates

The maintenance of chromosomal integrity is an essential task of every living organism and cellular repair mechanisms exist to guard against insults to DNA. Given the importance of this process, it is expected that DNA repair proteins would be evolutionarily conserved, exhibiting very minimal sequence change over time. However, BRCA1, an essential gene involved in DNA repair, has been reported to be evolving rapidly despite the fact that many protein-altering mutations within this gene convey a significantly elevated risk for breast and ovarian cancers. Results: To obtain a deeper understanding of the evolutionary trajectory of BRCA1, we analyzed complete BRCA1 gene sequences from 23 primate species. We show that specific amino acid sites have experienced repeated selection for amino acid replacement over primate evolution. This selection has been focused specifically on humans and our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). After examining BRCA1 polymorphisms in 7 bonobo, 44 chimpanzee, and 44 rhesus macaque (Macaca mulatta) individuals, we find considerable variation within each of these species and evidence for recent selection in chimpanzee populations. Finally, we also sequenced and analyzed BRCA2 from 24 primate species and find that this gene has also evolved under positive selection. Conclusions: While mutations leading to truncated forms of BRCA1 are clearly linked to cancer phenotypes in humans, there is also an underlying selective pressure in favor of amino acid-altering substitutions in this gene. A hypothesis where viruses are the drivers of this natural selection is discussed.National Institutes of Health R01-GM-093086, 8U42OD011197-13National Science Foundation BCS-07115972Burroughs Wellcome FundMolecular Bioscience

Chimpanzee faces under the magnifying glass: emerging methods reveal cross-species similarities and individuality

Independently, we created descriptive systems to characterize chimpanzee facial behavior, responding to a common need to have an objective, standardized coding system to ask questions about primate facial behaviors. Even with slightly different systems, we arrive at similar outcomes, with convergent conclusions about chimpanzee facial mobility. This convergence is a validation of the importance of the approach, and provides support for the future use of a facial action coding system for chimpanzees,ChimpFACS. Chimpanzees share many facial behaviors with those of humans. Therefore, processes and mechanisms that explain individual differences in facial activity can be compared with the use of a standardized systems such asChimpFACSandFACS. In this chapter we describe our independent methodological approaches, comparing how we arrived at our facial coding categories. We present some Action Descriptors (ADs) from Gaspar’s initial studies, especially focusing on an ethogram of chimpanzee and bonobo facial behavior, based on studies conducted between 1997 and 2004 at three chimpanzee colonies (The Detroit Zoo; Cleveland Metroparks Zoo; and Burger’s Zoo) and two bonobo colonies (The Columbus Zoo and Aquarium; The Milwaukee County Zoo). We discuss the potential significance of arising issues, the minor qualitative species differences that were found, and the larger quantitative differences in particular facial behaviors observed between species, e.g., bonobos expressed more movements containing particular action units (Brow Lowerer, Lip Raiser, Lip Corner Puller) compared with chimpanzees. The substantial interindividual variation in facial behavior within each species was most striking. Considering individual differences and the impact of development, we highlight the flexibility in facial activity of chimpanzees. We discuss the meaning of facial behaviors in nonhuman primates, addressing specifically individual attributes of Social Attraction, facial expressivity, and the connection of facial behavior to emotion. We do not rule out the communicative function of facial behavior, in which case an individual’s properties of facial behavior are seen as influencing his or her social life, but provide strong arguments in support of the role of facial behavior in the expression of internal states

A High-Quality Bonobo Genome Refines The Analysis Of Hominid Evolution

The divergence of chimpanzee and bonobo provides one of the few examples of recent hominid speciation(1,2). Here we describe a fully annotated, high-quality bonobo genome assembly, which was constructed without guidance from reference genomes by applying a multiplatform genomics approach. We generate a bonobo genome assembly in which more than 98% of genes are completely annotated and 99% of the gaps are closed, including the resolution of about half of the segmental duplications and almost all of the full-length mobile elements. We compare the bonobo genome to those of other great apes(1,3-5) and identify more than 5,569 fixed structural variants that specifically distinguish the bonobo and chimpanzee lineages. We focus on genes that have been lost, changed in structure or expanded in the last few million years of bonobo evolution. We produce a high-resolution map of incomplete lineage sorting and estimate that around 5.1% of the human genome is genetically closer to chimpanzee or bonobo and that more than 36.5% of the genome shows incomplete lineage sorting if we consider a deeper phylogeny including gorilla and orangutan. We also show that 26% of the segments of incomplete lineage sorting between human and chimpanzee or human and bonobo are non-randomly distributed and that genes within these clustered segments show significant excess of amino acid replacement compared to the rest of the genome

Age-dependent cognitive inflexibility in great apes

The ability to suppress and/or change behaviour on the basis of negative feedback, often conceptualized as cognitive flexibility, has rarely been investigated in nonhuman great apes across a broad age range. In this study, 25 chimpanzees, Pan troglodytes, eight bonobos, Pan paniscus, seven orang-utans, Pongo abelii, and three gorillas, Gorilla gorilla, whose ages ranged from 5 to 48 years, were presented with a transparent Plexiglas rectangular box horizontally attached to their cage mesh. A square container, 7.5 cm2, fixed inside the apparatus contained a food reward (i.e. a grape). While the container rested on its central position the grape was not accessible. To retrieve the grape the subjects needed to grasp the handle connected to the reward container and displace it sideways to reach one of the lateral access windows. Subjects were intensively trained to displace the handle to a specific side (right or left, depending on the group) and then the rewarded side was reversed during the test. Performance in this reversal task did not differ significantly between species. However, a U-shaped relation between age and perseverative responding (i.e. moves to the previously rewarded side) was observed, extending findings with humans to our closest living primate relatives. (C) 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.PostprintPeer reviewe

A high-quality bonobo genome refines the analysis of hominid evolution

The divergence of chimpanzee and bonobo provides one of the few examples of recent hominid speciation1,2. Here we describe a fully annotated, high-quality bonobo genome assembly, which was constructed without guidance from reference genomes by applying a multiplatform genomics approach. We generate a bonobo genome assembly in which more than 98% of genes are completely annotated and 99% of the gaps are closed, including the resolution of about half of the segmental duplications and almost all of the full-length mobile elements. We compare the bonobo genome to those of other great apes1,3,4,5 and identify more than 5,569 fixed structural variants that specifically distinguish the bonobo and chimpanzee lineages. We focus on genes that have been lost, changed in structure or expanded in the last few million years of bonobo evolution. We produce a high-resolution map of incomplete lineage sorting and estimate that around 5.1% of the human genome is genetically closer to chimpanzee or bonobo and that more than 36.5% of the genome shows incomplete lineage sorting if we consider a deeper phylogeny including gorilla and orangutan. We also show that 26% of the segments of incomplete lineage sorting between human and chimpanzee or human and bonobo are non-randomly distributed and that genes within these clustered segments show significant excess of amino acid replacement compared to the rest of the genome

Nest grouping patterns of bonobos (Pan paniscus) in relation to fruit availability in a forest-savannah mosaic

A topic of major interest in socio-ecology is the comparison of chimpanzees and bonobos’ grouping patterns. Numerous studies have highlighted the impact of social and environmental factors on the different evolution in group cohesion seen in these sister species. We are still lacking, however, key information about bonobo social traits across their habitat range, in order to make accurate inter-species comparisons. In this study we investigated bonobo social cohesiveness at nesting sites depending on fruit availability in the forest-savannah mosaic of western Democratic Republic of Congo (DRC), a bonobo habitat which has received little attention from researchers and is characterized by high food resource variation within years. We collected data on two bonobo communities. Nest counts at nesting sites were used as a proxy for night grouping patterns and were analysed with regard to fruit availability. We also modelled bonobo population density at the site in order to investigate yearly variation. We found that one community density varied across the three years of surveys, suggesting that this bonobo community has significant variability in use of its home range. This finding highlights the importance of forest connectivity, a likely prerequisite for the ability of bonobos to adapt their ranging patterns to fruit availability changes. We found no influence of overall fruit availability on bonobo cohesiveness. Only fruit availability at the nesting sites showed a positive influence, indicating that bonobos favour food ‘hot spots’ as sleeping sites. Our findings have confirmed the results obtained from previous studies carried out in the dense tropical forests of DRC. Nevertheless, in order to clarify the impact of environmental variability on bonobo social cohesiveness, we will need to make direct observations of the apes in the forest-savannah mosaic as well as make comparisons across the entirety of the bonobos’ range using systematic methodology

Does the use of the dynamic system approach really help fill in the gap between human and non human primate language ? Commentary to S. Shanker and B. J. King " the Emergence of a New Paradigm in Ape Language Research"

The highly recommended transposition of the dynamic system approach for tackling the question of apes’ linguistic abilities has clearly not led to a demonstration that these primates have acquired language. Fundamental differences related to functional modalities – namely, use of the declarative and the form of engagement between mother and infant –can be observed in the way humans and apes use their communicatory systems

Would humans without language be apes?

The bedrock of comparative psychology of cognition, especially where nonhuman primates are concerned, rests on Darwin's famous account according to which continuity would be the main trait leading from the animal to the human mind. This idea was popularized through the statement in which Darwin postulated only quantitative differences between humans and the other species, namely "the difference in mind between man and the higher animals, great as it is, certainly is one of degree and not of kind" (Darwin, 1871, p. 128)..