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By identifying homogeneity in bone and soft tissue covariation patterns in living hominids, it is possible to produce facial approximation methods with interspecies compatibility. These methods may be useful for producing facial approximations of fossil hominids that are more realistic than currently possible. In this study, we conducted an interspecific comparison of the nasomaxillary region in chimpanzees and modern humans with the aim of producing a method for predicting the positions of the nasal tips of Plio-Pleistocene hominids. We addressed this aim by first collecting and performing regression analyses of linear and angular measurements of nasal cavity length and inclination in modern humans (Homo sapiens; n = 72) and chimpanzees (Pan troglodytes; n = 19), and then performing a set of out-of-group tests. The first test was performed on four subjects that belonged to the same genus as the training sample, i.e., Homo (n = 2) and Pan (n = 2), and the second test, which functioned as an interspecies compatibility test, was performed on Pan paniscus (n = 1), Gorilla gorilla (n = 3), Pongo pygmaeus (n = 1), Pongo abelli (n = 1), Symphalangus syndactylus (n = 3), and Papio hamadryas (n = 3). We identified statistically significant correlations in both humans and chimpanzees with slopes that displayed homogeneity of covariation. Prediction formulae combining these data were found to be compatible with humans and chimpanzees as well as all other African great apes, i.e., bonobos and gorillas. The main conclusion that can be drawn from this study is that our set of regression models for approximating the position of the nasal tip are homogenous among humans and African apes, and can thus be reasonably extended to ancestors leading to these clades., Competing Interests: The authors have declared that no competing interests exist.

Although naturally occurring catalytic RNA molecules-ribozymes-have attracted a great deal of research interest, very few have been identified in humans. Here, we developed a genome-wide approach to discovering self-cleaving ribozymes and identified a naturally occurring ribozyme in humans. The secondary structure and biochemical properties of this ribozyme indicate that it belongs to an unidentified class of small, self-cleaving ribozymes. The sequence of the ribozyme exhibits a clear evolutionary path, from its appearance between ~130 and ~65 million years ago (Ma), to acquiring self-cleavage activity very recently, ~13-10 Ma, in the common ancestors of humans, chimpanzees and gorillas. The ribozyme appears to be functional in vivo and is embedded within a long noncoding RNA belonging to a class of very long intergenic noncoding RNAs. The presence of a catalytic RNA enzyme in lncRNA creates the possibility that these transcripts could function by carrying catalytic RNA domains.

Common chimpanzees (Pan troglodytes) experienced a selective sweep, probably caused by a SIV-like virus, which targeted their MHC class I repertoire. Based on MHC class I intron 2 data analyses, this selective sweep took place about 2-3 million years ago. As a consequence, common chimpanzees have a skewed MHC class I repertoire that is enriched for allotypes that are able to recognise conserved regions of the SIV proteome. The bonobo (Pan paniscus) shared an ancestor with common chimpanzees approximately 1.5 to 2 million years ago. To investigate whether the signature of this selective sweep is also detectable in bonobos, the MHC class I gene repertoire of two bonobo panels comprising in total 29 animals was investigated by Sanger sequencing. We identified 14 Papa-A, 20 Papa-B and 11 Papa-C alleles, of which eight, five and eight alleles, respectively, have not been reported previously. Within this pool of MHC class I variation, we recovered only 2 Papa-A, 3 Papa-B and 6 Papa-C intron 2 sequences. As compared to humans, bonobos appear to have an even more diminished MHC class I intron 2 lineage repertoire than common chimpanzees. This supports the notion that the selective sweep may have predated the speciation of common chimpanzees and bonobos. The further reduction of the MHC class I intron 2 lineage repertoire observed in bonobos as compared to the common chimpanzee may be explained by a founding effect or other subsequent selective processes.

Major histocompatibility complex (MHC) class I genes are critically involved in the defense against intracellular pathogens. MHC diversity comparisons among samples of closely related taxa may reveal traces of past or ongoing selective processes. The bonobo and chimpanzee are the closest living evolutionary relatives of humans and last shared a common ancestor some 1 mya. However, little is known concerning MHC class I diversity in bonobos or in central chimpanzees, the most numerous and genetically diverse chimpanzee subspecies. Here, we used a long-read sequencing technology (PacBio) to sequence the classical MHC class I genes A, B, C, and A-like in 20 and 30 wild-born bonobos and chimpanzees, respectively, with a main focus on central chimpanzees to assess and compare diversity in those two species. We describe in total 21 and 42 novel coding region sequences for the two species, respectively. In addition, we found evidence for a reduced MHC class I diversity in bonobos as compared to central chimpanzees as well as to western chimpanzees and humans. The reduced bonobo MHC class I diversity may be the result of a selective process in their evolutionary past since their split from chimpanzees.

Objectives: Female bonobos (Pan paniscus) are characterized as highly affiliative and cooperative, but few studies have quantified the strength and stability of female intra-sexual relationships or explored how variation in social relationships influences cooperation. We measure female social preferences, identify causes of variation in preferences, and test whether variation in social preferences predicts food sharing or coalitionary support., Methods: Data were collected over 3 years from females in the Bompusa community at LuiKotale, DRC. We measured genetic relatedness and constructed social preference indices for party association, proximity, grooming, GG-rubbing and aggression. We identified preferred social partners based on permutation tests and measured stability using Mantel tests. We used factor analysis to identify inter-relationships between preference indices and used LMMs to test whether variation in social preferences was explained by relatedness, rank differences, having dependent young or co-residency time. We used GLMMs to test whether variation in social preferences predicted food sharing or coalitionary support., Results: All females had preferred non-kin partners for proximity, grooming or GG-rubbing, but only grooming preferences were stable across years. Association indices were higher among lactating females, and aggression was lower among females with longer co-residency times. The factor analysis identified one factor, representing proximity and GG-rubbing preferences, labeled behavioral coordination. Dyads with higher levels of behavioral coordination were more likely to share food., Conclusions: Female bonobos exhibit stable, differentiated grooming relationships outside of kinship and philopatry. Females also exhibit flexible proximity and GG-rubbing preferences that may facilitate cooperation with a wider range of social partners., (© 2017 Wiley Periodicals, Inc.)

Common chimps and bonobos are our closest living relatives but almost nothing is known about bonobo internal anatomy. We present the first phylogenetic analysis to include musculoskeletal data obtained from a recent dissection of bonobos. Notably, chimpanzees, and in particular bonobos, provide a remarkable case of evolutionary stasis for since the chimpanzee-human split c.8 Ma among >120 head-neck (HN) and forelimb (FL) muscles there were only four minor changes in the chimpanzee clade, and all were reversions to the ancestral condition. Moreover, since the common chimpanzee-bonobo split c.2 Ma there have been no changes in bonobos, so with respect to HN-FL musculature bonobos are the better model for the last common ancestor (LCA) of chimpanzees/bonobos and humans. Moreover, in the hindlimb there are only two muscle absence/presence differences between common chimpanzees and bonobos. Puzzlingly, there is an evolutionary mosaicism between each of these species and humans. We discuss these data in the context of available genomic information and debates on whether the common chimpanzee-bonobo divergence is linked to heterochrony.

In 2004, an analysis by Lockwood and colleagues of hard-tissue morphology, using geometric morphometrics on the temporal bone, succeeded in recovering the correct phylogeny of living hominids without resorting to potentially problematic methods for transforming continuous shape variables into meristic characters. That work has increased hope that by using modern analytical methods and phylogenetically informative anatomical data we might one day be able to accurately infer the relationships of hominins, including the closest extinct relatives of modern humans. In the present study, using 3D virtually generated models of the hominid temporal bone and a larger suite of geometric morphometric and comparative techniques, we have re-examined the evidence for a Pan-Homo clade. Despite differences in samples, as well as the type of raw data, the effect of measurement error (and especially landmark digitization by a different operator), but also a broader perspective brought in by our diverse set of approaches, our reanalysis largely supports Lockwood and colleagues' original results. However, by focusing not only mainly on shape (as in the original 2004 analysis) but also on size and 'size-corrected' (non-allometric) shape, we demonstrate that the strong phylogenetic signal in the temporal bone is largely related to similarities in size. Thus, with this study, we are not suggesting the use of a single 'character', such as size, for phylogenetic inference, but we do challenge the common view that shape, with its highly complex and multivariate nature, is necessarily more phylogenetically informative than size and that actually size and size-related shape variation (i.e., allometry) confound phylogenetic inference based on morphology. This perspective may in fact be less generalizable than often believed. Thus, while we confirm the original findings by Lockwood et al., we provide a deep reinterpretation of their nature and potential implications for hominid phylogenetics and we show how crucial it is not to overlook size in geometric morphometric analyses., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

The gut microbial communities within great apes have been shown to reflect the phylogenetic history of their hosts, indicating codiversification between great apes and their gut microbiota over evolutionary timescales. But because the great apes examined to date represent geographically isolated populations whose diets derive from different sources, it is unclear whether this pattern of codiversification has resulted from a long history of coadaptation between microbes and hosts (heritable factors) or from the ecological and geographic separation among host species (environmental factors). To evaluate the relative influences of heritable and environmental factors on the evolution of the great ape gut microbiota, we assayed the gut communities of sympatric and allopatric populations of chimpanzees, bonobos, and gorillas residing throughout equatorial Africa. Comparisons of these populations revealed that the gut communities of different host species can always be distinguished from one another but that the gut communities of sympatric chimpanzees and gorillas have converged in terms of community composition, sharing on average 53% more bacterial phylotypes than the gut communities of allopatric hosts. Host environment, independent of host genetics and evolutionary history, shaped the distribution of bacterial phylotypes across the Bacteroidetes, Firmicutes, Proteobacteria, and Actinobacteria, the four most common phyla of gut bacteria. Moreover, the specific patterns of phylotype sharing among hosts suggest that chimpanzees living in sympatry with gorillas have acquired bacteria from gorillas. These results indicate that geographic isolation between host species has promoted the evolutionary differentiation of great ape gut bacterial communities.

Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria-Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

The aim of this research is to determine whether geometric morphometric (GM) techniques can provide insights into how the shape of the mandibular corpus differs between bonobos and chimpanzees and to explore the potential implications of those results for our understanding of hominin evolution. We focused on this region of the mandible because of the relative frequency with which it has been recovered in the hominin fossil record. In addition, no previous study had explored in-depth three-dimensional (3D) mandibular corpus shape differences between adults of the two Pan species using geometric morphometrics. GM methods enable researchers to quantitatively analyze and visualize 3D shape changes in skeletal elements and provide an important compliment to traditional two-dimensional analyses. Eighteen mandibular landmarks were collected using a Microscribe 3DX portable digitizer. Specimen configurations were superimposed using Generalized Procrustes analysis and the projections of the fitted coordinates to tangent space were analyzed using multivariate statistics. The size-adjusted corpus shapes of Pan paniscus and Pan troglodytes could be assigned to species with approximately 93% accuracy and the Procrustes distance between the two species was significant. Analyses of the residuals from a multivariate linear regression of the data on centroid size suggested that much of the shape difference between the species is size-related. Chimpanzee subspecies and a small sample of Australopithecus specimens could be correctly identified to taxon, at best, only 75% of the time, although the Procrustes distances between these taxa were significant. The shape of the mandibular symphysis was identified as especially useful in differentiating Pan species from one another. This suggests that this region of the mandible has the potential to be informative for taxonomic analyses of fossil hominoids, including hominins. The results also have implications for phylogenetic hypotheses of hominoid evolution., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Background: We have analyzed the complete mitochondrial genomes of 22 Pan paniscus (bonobo, pygmy chimpanzee) individuals to assess the detailed mitochondrial DNA (mtDNA) phylogeny of this close relative of Homo sapiens., Results: We identified three major clades among bonobos that separated approximately 540,000 years ago, as suggested by Bayesian analysis. Incidentally, we discovered that the current reference sequence for bonobo likely is a hybrid of the mitochondrial genomes of two distant individuals. When comparing spectra of polymorphic mtDNA sites in bonobos and humans, we observed two major differences: (i) Of all 31 bonobo mtDNA homoplasies, i.e. nucleotide changes that occurred independently on separate branches of the phylogenetic tree, 13 were not homoplasic in humans. This indicates that at least a part of the unstable sites of the mitochondrial genome is species-specific and difficult to be explained on the basis of a mutational hotspot concept. (ii) A comparison of the ratios of non-synonymous to synonymous changes (dN/dS) among polymorphic positions in bonobos and in 4902 Homo sapiens mitochondrial genomes revealed a remarkable difference in the strength of purifying selection in the mitochondrial genes of the F0F1-ATPase complex. While in bonobos this complex showed a similar low value as complexes I and IV, human haplogroups displayed 2.2 to 7.6 times increased dN/dS ratios when compared to bonobos., Conclusions: Some variants of mitochondrially encoded subunits of the ATPase complex in humans very likely decrease the efficiency of energy conversion leading to production of extra heat. Thus, we hypothesize that the species-specific release of evolutionary constraints for the mitochondrial genes of the proton-translocating ATPase is a consequence of altered heat homeostasis in modern humans.

The location of the mental foramen on the mandibular corpus has figured prominently in debates concerning the taxonomy of fossil hominins and Gorilla gorilla. In this study we quantify the antero/posterior (A/P) position of the mental foramen across great apes, modern humans and Australopithecus. Contrary to most qualitative assessments, we find significant differences between some extant hominoid species in mental foramen A/P position supporting its potential usefulness as a character for taxonomic and phylogenetic analyses of fossil hominoids. Gorilla gorilla, particularly the eastern subspecies, with a comparatively longer dental arcade and fossil and extant hominins with reduced canines and incisors tend to exhibit more anteriorly positioned mental foramina. Conversely, Pan troglodytes exhibits more posteriorly positioned mental foramina. Variation in this character among Gorilla gorilla subspecies supports recent taxonomic assessments that separate eastern and western populations. In all taxa other than Pan troglodytes the A/P position of the mental foramen is positively allometric with respect to dental arcade length. Thus, within each of these species, specimens with longer dental arcades tend to have more posteriorly positioned mental foramina. Those species with greater sexual dimorphism in canine size and dental arcade length (i.e., Gorilla gorilla and Pongo pygmaeus) exhibit more extreme differences between smaller and larger individuals. Moreover, among great apes those individuals with greater anterior convergence of the dental arcade tend to exhibit more posteriorly positioned mental foramina. Dental arcade length, canine crown area and anterior convergence are all significantly associated with mental foramen A/P position, suggesting that these traits may influence taxonomic variation in the A/P position of the mental foramen., ((c) 2010 Wiley-Liss, Inc.)

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.

Previous research has demonstrated that species and subspecies of extant chimpanzees and bonobos can be distinguished on the basis of the shape of enamel-dentine junction of lower molar crowns. Thus, there is potential for fossil taxa, particularly fossil hominins, to be distinguished at similar taxonomic levels using lower molar crown morphology. New imaging techniques allow for the collection of large amounts of shape data, but it is not clear whether taxonomic distinctiveness increases with the inclusion of more and more finely detailed aspects of crown shape. We examine whether increasing the amount of shape data collected will lead to an increase in the accuracy with which enamel-dentine junction (EDJ) shape classifies Pan lower first and second molars at the species and subspecies level. 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, Pan troglodytestroglodytes, and Pan troglodytes verus. The results of discriminant analyses using three landmark sets (number of landmarks=8, 112, and 534 landmarks and semi-landmarks, respectively) indicate a high degree of classification accuracy for each landmark set, with small increases in accuracy as the numbers of landmarks are increased. The morphological differences in EDJ shape among the taxa are subtle, but consistent, and relate to the relative height and position of the dentine horns. Thus, EDJ shape can contribute to taxonomic analyses and the more information that can be included the better., (Copyright (c) 2009 S. Karger AG, Basel.)

Bonobos are large, highly mobile primates living in the relatively undisturbed, contiguous forest south of the Congo River. Accordingly, gene flow among populations is assumed to be extensive, but may be impeded by large, impassable rivers. We examined mitochondrial DNA control region sequence variation in individuals from five distinct localities separated by rivers in order to estimate relative levels of genetic diversity and assess the extent and pattern of population genetic structure in the bonobo. Diversity estimates for the bonobo exceed those for humans, but are less than those found for the chimpanzee. All regions sampled are significantly differentiated from one another, according to genetic distances estimated as pairwise FSTs, with the greatest differentiation existing between region East and each of the two Northern populations (N and NE) and the least differentiation between regions Central and South. The distribution of nucleotide diversity shows a clear signal of population structure, with some 30% of the variance occurring among geographical regions. However, a geographical patterning of the population structure is not obvious. Namely, mitochondrial haplotypes were shared among all regions excepting the most eastern locality and the phylogenetic analysis revealed a tree in which haplotypes were intermixed with little regard to geographical origin, with the notable exception of the close relationships among the haplotypes found in the east. Nonetheless, genetic distances correlated with geographical distances when the intervening distances were measured around rivers presenting effective current-day barriers, but not when straight-line distances were used, suggesting that rivers are indeed a hindrance to gene flow in this species.

Cusp base areas measured from digitized images increase the amount of detailed quantitative information one can collect from post-canine crown morphology. Although this method is gaining wide usage for taxonomic analyses of extant and extinct hominoids, the techniques for digitizing images and taking measurements differ between researchers. The aim of this study was to investigate interobserver error in order to help assess the reliability of cusp base area measurement within extant and extinct hominoid taxa. Two of the authors measured individual cusp base areas and total cusp base area of 23 maxillary first molars (M(1)) of Pan. From these, relative cusp base areas were calculated. No statistically significant interobserver differences were found for either absolute or relative cusp base areas. On average the hypocone and paracone showed the least interobserver error (< 1%) whereas the protocone and metacone showed the most (2.6-4.5%). We suggest that the larger measurement error in the metacone/protocone is due primarily to either weakly defined fissure patterns and/or the presence of accessory occlusal features. Overall, levels of interobserver error are similar to those found for intraobserver error. The results of our study suggest that if certain prescribed standards are employed then cusp and crown base areas measured by different individuals can be pooled into a single database.

Linear discriminant analysis (LDA) is frequently used for classification/prediction problems in physical anthropology, but it is unusual to find examples where researchers consider the statistical limitations and assumptions required for this technique. In these instances, it is difficult to know whether the predictions are reliable. This paper considers a nonparametric alternative to predictive LDA: binary, recursive (or classification) trees. This approach has the advantage that data transformation is unnecessary, cases with missing predictor variables do not require special treatment, prediction success is not dependent on data meeting normality conditions or covariance homogeneity, and variable selection is intrinsic to the methodology. Here I compare the efficacy of classification trees with LDA, using typical morphometric data. With data from modern hominoids, the results show that both techniques perform nearly equally. With complete data sets, LDA may be a better choice, as is shown in this example, but with missing observations, classification trees perform outstandingly well, whereas commercial discriminant analysis programs do not predict classifications for cases with incompletely measured predictor variables and generally are not designed to address the problem of missing data. Testing of data prior to analysis is necessary, and classification trees are recommended either as a replacement for LDA or as a supplement whenever data do not meet relevant assumptions. It is highly recommended as an alternative to LDA whenever the data set contains important cases with missing predictor variables., (Copyright 2002 Wiley-Liss, Inc.)

To determine how cellular aging is conserved among primates, we analyzed the replicative potential and telomere shortening in skin fibroblasts of anthropoids and prosimians. The average telomere length of the New World primates Ateles geoffroyi (spider monkey) and Saimiri sciureus (squirrel monkey) and the Old World primates Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), and Pan paniscus (pigmy chimpanzee) ranged from 4 to 16 kb. We found that telomere shortening limits the replicative capacity of anthropoid fibroblasts and that the expression of human telomerase produced telomere elongation and the extension of their in vitro life span. In contrast the prosimian Lemur catta (ring-tailed lemur) had both long and short telomeres and telomere shortening did not provide an absolute barrier to immortalization. Following a transient growth arrest a subset of cells showing a reduced number of chromosomes overgrew the cultures without activation of telomerase. Here we show that the presence of continuous TTAGGG repeats at telomeres and rigorous control of replicative aging by telomere shortening appear to be conserved among anthropoid primates but is less effective in prosimian lemurs., ((c)2001 Elsevier Science.)

Although some mitochondrial, X chromosome, and autosomal sequence diversity data are available for our closest relatives, Pan troglodytes and Pan paniscus, data from the nonrecombining portion of the Y chromosome (NRY) are more limited. We examined approximately 3 kb of NRY DNA from 101 chimpanzees, seven bonobos, and 42 humans to investigate: (i) relative levels of intraspecific diversity; (ii) the degree of paternal lineage sorting among species and subspecies of the genus Pan; and (iii) the date of the chimpanzee/bonobo divergence. We identified 10 informative sequence-tagged sites associated with 23 polymorphisms on the NRY from the genus Pan. Nucleotide diversity was significantly higher on the NRY of chimpanzees and bonobos than on the human NRY. Similar to mtDNA, but unlike X-linked and autosomal loci, lineages defined by mutations on the NRY were not shared among subspecies of P. troglodytes. Comparisons with mtDNA ND2 sequences from some of the same individuals revealed a larger female versus male effective population size for chimpanzees. The NRY-based divergence time between chimpanzees and bonobos was estimated at approximately 1.8 million years ago. In contrast to human populations who appear to have had a low effective size and a recent origin with subsequent population growth, some taxa within the genus Pan may be characterized by large populations of relatively constant size, more ancient origins, and high levels of subdivision.

Although data on nucleotide sequence variation in the human nuclear genome have begun to accumulate, little is known about genomic diversity in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). A 10,154-base pair sequence on the chimpanzee X chromosome is reported, representing all major subspecies and bonobos. Comparison to humans shows the diversity of the chimpanzee sequences to be almost four times as high and the age of the most recent common ancestor three times as great as the corresponding values of humans. Phylogenetic analyses show the sequences from the different chimpanzee subspecies to be intermixed and the distance between some chimpanzee sequences to be greater than the distance between them and the bonobo sequences.