The reconstructed cranium of Pierolapithecus and the evolution of the great ape face.

Pierolapithecus catalaunicus (~12 million years ago, northeastern Spain) is key to understanding the mosaic nature of hominid (great ape and human) evolution. Notably, its skeleton indicates that an orthograde (upright) body plan preceded suspensory adaptations in hominid evolution. However, there is ongoing debate about this species, partly because the sole known cranium, preserving a nearly complete face, suffers from taphonomic damage. We 1) carried out a micro computerized tomography (CT) based virtual reconstruction of the Pierolapithecus cranium, 2) assessed its morphological affinities using a series of two-dimensional (2D) and three-dimensional (3D) morphometric analyses, and 3) modeled the evolution of key aspects of ape face form. The reconstruction clarifies many aspects of the facial morphology of Pierolapithecus. Our results indicate that it is most similar to great apes (fossil and extant) in overall face shape and size and is morphologically distinct from other Middle Miocene apes. Crown great apes can be distinguished from other taxa in several facial metrics (e.g., low midfacial prognathism, relatively tall faces) and only some of these features are found in Pierolapithecus, which is most consistent with a stem (basal) hominid position. The inferred morphology at all ancestral nodes within the hominoid (ape and human) tree is closer to great apes than to hylobatids (gibbons and siamangs), which are convergent with other smaller anthropoids. Our analyses support a hominid ancestor that was distinct from all extant and fossil hominids in overall facial shape and shared many features with Pierolapithecus. This reconstructed ancestral morphotype represents a testable hypothesis that can be reevaluated as new fossils are discovered.

Life of p: A consonant older than speech.

Which sounds composed the first spoken languages? Archetypal sounds are not phylogenetically or archeologically recoverable, but comparative linguistics and primatology provide an alternative approach. Labial articulations are the most common speech sound, being virtually universal across the world's languages. Of all labials, the plosive 'p' sound, as in 'Pablo Picasso', transcribed /p/, is the most predominant voiceless sound globally and one of the first sounds to emerge in human infant canonical babbling. Global omnipresence and ontogenetic precocity imply that /p/-like sounds could predate the first major linguistic diversification event(s) in humans. Indeed, great ape vocal data support this view, namely, the only cultural sound shared across all great ape genera is articulatorily homologous to a rolling or trilled /p/, the 'raspberry'. /p/-like labial sounds represent an 'articulatory attractor' among living hominids and are likely among the oldest phonological features to have ever emerged in linguistic systems.

Comparative Genomic Analysis Identifies Great-Ape-Specific Structural Variants and Their Evolutionary Relevance.

During the origin of great apes about 14 million years ago, a series of phenotypic innovations emerged, such as the increased body size, the enlarged brain volume, the improved cognitive skill, and the diversified diet. Yet, the genomic basis of these evolutionary changes remains unclear. Utilizing the high-quality genome assemblies of great apes (including human), gibbon, and macaque, we conducted comparative genome analyses and identified 15,885 great ape-specific structural variants (GSSVs), including eight coding GSSVs resulting in the creation of novel proteins (e.g., ACAN and CMYA5). Functional annotations of the GSSV-related genes revealed the enrichment of genes involved in development and morphogenesis, especially neurogenesis and neural network formation, suggesting the potential role of GSSVs in shaping the great ape-shared traits. Further dissection of the brain-related GSSVs shows great ape-specific changes of enhancer activities and gene expression in the brain, involving a group of GSSV-regulated genes (such as NOL3) that potentially contribute to the altered brain development and function in great apes. The presented data highlight the evolutionary role of structural variants in the phenotypic innovations during the origin of the great ape lineage.

An overview of nutritional factors in the aetiopathogenesis of myocardial fibrosis in great apes.

The main cause of mortality in great apes in zoological settings is cardiovascular disease (CVD), affecting all four taxa: chimpanzee (Pan troglodytes), bonobo (Pan paniscus), gorilla (Gorilla spp.) and orangutan (Pongo spp.). Myocardial fibrosis, the most typical histological characterisation of CVD in great apes, is non-specific, making it challenging to understand the aetiopathogenesis. A multifactorial origin of disease is assumed whereby many potential causative factors are directly or indirectly related to the diet, which in wild-living great apes mainly consists of high-fibre, low-carbohydrate and very low-sodium components. Diets of great apes housed in zoological settings are often different compared with the situation in the wild. Moreover, low circulating vitamin D levels have recently been recognised in great apes housed in more northern regions. Evaluation of current supplementation guidelines shows that, despite implementation of different dietary strategies, animals stay vitamin D insufficient. Therefore, recent hypotheses designate vitamin D deficiency as a potential underlying factor in the pathogenesis of myocardial fibrosis. The aim of this literature review is to: (i) examine important differences in nutritional factors between zoological and wild great ape populations; (ii) explain the potential detrimental effects of the highlighted dietary discrepancies on cardiovascular function in great apes; and (iii) elucidate specific nutrition-related pathophysiological mechanisms that may underlie the development of myocardial fibrosis. This information may contribute to understanding the aetiopathogenesis of myocardial fibrosis in great apes and pave the way for future clinical studies and a more preventive approach to great ape CVD management.

Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species.

Traces of dietary patterns in saliva of hominids: Profiling salivary amino acid fingerprints in great apes and humans.

Herbivorous animals that regularly consume tannin-rich food are known to secrete certain tannin-binding salivary proteins (TBSPs), especially proline-rich proteins and histidine-rich proteins, as an effective measure to counteract the antinutritive effects of dietary tannins. Due to their high binding capacity, TBSPs complex with tannins in the oral cavity, and thereby protect dietary proteins and digestive enzymes. Although the natural diet of great apes (Hominidae) is biased toward ripe fruits, analyses of food plants revealed that their natural diet contains considerable amounts of tannins, which is raising the question of possible counter-measures to cope with dietary tannins. In our study, we investigated the salivary amino acid profiles of zoo-housed Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii, and compared their results with corresponding data from Homo sapiens. Individual saliva samples of 42 apes and 17 humans were collected and quantitated by amino acid analysis, using cation-exchange chromatography with postcolumn derivatization, following acid hydrolysis. We found species-specific differences in the salivary amino acid profiles with average total salivary protein concentration ranging from 308.8 mg/dL in Po. abelii to 1165.6 mg/dL in G. gorilla. Total salivary protein was consistently higher in ape than in human saliva samples (174 mg/dL). All apes had on average also higher relative proline levels than humans did. Histidine levels had the highest concentration in the samples from Po. abelii followed by P. paniscus. In all ape species, the high salivary concentrations of proline and histidine are considered to be indicative of high concentrations of TBSPs in hominids. Given that the species differences in salivary composition obtained in this study correspond with overall patterns of secondary compound content in the diet of wild populations, we assume that salivary composition is resilient to acute and long-lasting changes in diet composition in general and tannin content in particular.

Social cognition and metacognition in great apes: a theory.

Twenty-five years ago, at the founding of this journal, there existed only a few conflicting findings about great apes' social-cognitive skills (theory of mind). In the 2 ½ decades since, we have discovered that great apes understand the goals, intentions, perceptions, and knowledge of others, and they use this knowledge to their advantage in competitive interactions. Twenty-five years ago there existed basically no studies on great apes' metacognitive skills. In the 2 ½ decades since, we have discovered that great apes monitor their uncertainty and base their decisions on that, or else decide to gather more information to make better decisions. The current paper reviews the past 25 years of research on great ape social cognition and metacognition and proposes a theory about how the two are evolutionarily related.

Specimens as individuals: Four interventions and recommendations for great ape skeletal collections research and curation.

Extensive discourse surrounds the ethics of human skeletal research and curation, but there has yet to be a similar discussion of the treatment of great ape skeletal remains, despite the clear interest in their ethical treatment when alive. Here we trace the history of apes who were killed and collected for natural history museums during the early 20th century and showcase how the guiding research questions of the colonial era continue to influence scholarship. We discuss best practices for improving industry and academic standards of research on, and the curation of, ape remains. The suggested interventions involve restoring individual identity and narrative to great apes while engaging with contextual reflexivity and decolonial theory. The resulting recommendations include contextualizing the individual, piecing individuals back together, challenging/questioning the captive-wild dichotomy, and collaborative international conversations. Our objective is to encourage a conversation regarding ethical and theoretical considerations in great ape skeletal remains research.

Early communicative gestures in human and chimpanzee 1-year-olds observed across diverse socioecological settings.

We investigated the communicative gestures used by chimpanzee and human infants. In contrast to previous studies, we compared the species at the same age (12-14 months) and used multiple groups living in diverse socioecological settings for both species. We recorded gestures produced by infants and those produce by others and directed toward infants. We classified the gestures into the following types: human-usual, chimpanzee-usual, and species-common; and searched for within species and between species differences. We found no significant differences between groups or species in overall rates of infant-produced or infant-received gestures, suggesting that all of these infants produced and received gestures at similar levels. We did find significant differences, however, when we considered the three types of gesture. Chimpanzee infants produced significantly higher rates of chimpanzee-usual gestures, and human infants produced significantly higher rates of human-usual gestures, but there was no significant species difference in the species-common gestures. Reports of species differences in gesturing in young infants, therefore, could be influenced by investigators' choice of gesture type. Interestingly, we found that 1-year-old infants produced the gesture of "hold mutual gaze" and that the chimpanzee infants had a significantly higher rate than the human infants. We did not find strong evidence that the specific types of gestural environment experienced by young infants influenced the types of gestures that infants produce. We suggest that at this point in development (before human infants use lots of speech), nonverbal communicative gestures may be equally important for human and chimpanzee infants.

Surgical placement of implantable cardiac loop recorders in great apes.

Cardiovascular disease is the leading cause of morbidity and mortality in zoologically managed adult great apes, accounting for 29%-77% of adult deaths in the North American population depending on the species. In an effort to better understand the underlying causes of heart disease, implantable loop recorders (ILRs) have been used in some cases to monitor great apes with suspected or known cases of arrhythmia. This is a 10-year review of the Great Ape Heart Project's experience of implanting 21 ILRs in 7 gorillas (Gorilla gorilla gorilla; 9 total ILR devices), 5 chimpanzees (Pan troglodytes, 11 total ILR devices), and 1 orangutan (Pongo abelii, 1 ILR device) in an effort to develop effective methods for surgical implantation and remote collection of the data for analysis.

Evaluating individual biomarkers for predicting health risks in zoo-housed chimpanzees (Pan troglodytes) and bonobos (Pan paniscus).

Although biomarkers are often used for predicting morbidity and mortality in humans, similar data are lacking in our closest relatives. This study analyzed 16 biomarkers in zoo-housed chimpanzees and bonobos from serum samples collected during both routine and nonroutine veterinary immobilizations. Generalized linear and generalized linear mixed models were used to determine the efficacy of each biomarker to predict all-cause morbidity, defined as the presence of at least one chronic condition, or cardiac disease as a subset of all-cause morbidity. Cox proportional hazards models were used to examine associations between biomarkers and mortality risk from any cause. Analyses were conducted using two data sets for each species, one with all values retained (chimpanzees: n = 148; bonobos: n = 33) and the other from samples collected during routine immobilizations only (chimpanzees: n = 95; bonobos: n = 23). Consistent results across both data sets in chimpanzees included associations of higher cortisol with all-cause morbidity risk, lower creatinine with cardiac disease risk, and higher creatinine with mortality risk, and in bonobos were increased cardiac disease risk with higher cortisol and lower dehydroepiandrosterone-sulfate, fructosamine, and triglycerides. However, there were some inconsistencies between data sets, such as tumor necrosis factor-α predicting mortality risk positively in chimpanzees when all values were retained, but negatively for routine values only. Despite the close evolutionary relationships between chimpanzees and bonobos, the only result observed in both species was a negative association between albumin and mortality risk in the all values retained data sets. Thus, data suggest some biomarkers may be useful predictors of future health outcomes, although a better understanding of both individual and species variation in biomarkers and their contribution to health risks is needed.

Testing for personality consistency across naturally occurring behavioral contexts in sanctuary chimpanzees (Pan troglodytes).

Personality is both a reflection of the bio-behavioral profile of individuals and a summary of how they typically interact with their physical and social world. Personality is usually defined as having distinct behavioral characteristics, which are assumed to be consistent over time and across contexts. Like other mammals, primates have individual differences in personality. Although temporal consistency is sometimes measured in primates, and contextual consistency is sometimes measured across experimental contexts, it is rare to measure both in the same individuals and outside of experimental settings. Here, we aim to measure both temporal and contextual consistency in chimpanzees, assessing their personality with behavioral observations from naturally occurring contexts (i.e., real-life settings). We measured personality-based behaviors in 22 sanctuary chimpanzees, in the contexts of feeding, affiliation, resting, and solitude, across two time periods, spanning 4 years. Of the 22 behaviors recorded, about 64% were consistent across two to four contexts and 50% were consistent over time. Ten behaviors loaded significantly onto three trait components: explorativeness, boldness-sociability, and anxiety-sociability, as revealed by factor analysis. Like others, we documented individual differences in the personality of chimpanzees based on reliably measured observations in real-life contexts. Furthermore, we demonstrated relatively strong, but not absolute, temporal, and contextual consistency in personality-based behaviors. We also found another aspect of individual differences in personality, specifically, the extent to which individual chimpanzees show consistency. Some individuals showed contextual and temporal consistency, whereas others show significant variation across behaviors, contexts, and/or time. We speculate that the relative degree of consistency in personality may vary within chimpanzees. It may be that different primate species vary in the extent to which individuals show consistency of personality traits. Our behavioral-based assessment can be used with wild populations, increasing the validity of personality studies, facilitating comparative studies and potentially being applicable to conservation efforts.

An Analysis of Methylome Evolution in Primates.

Although the investigation of the epigenome becomes increasingly important, still little is known about the long-term evolution of epigenetic marks and systematic investigation strategies are still lacking. Here, we systematically demonstrate the transfer of classic phylogenetic methods such as maximum likelihood based on substitution models, parsimony, and distance-based to interval-scaled epigenetic data. Using a great apes blood data set, we demonstrate that DNA methylation is evolutionarily conserved at the level of individual CpGs in promotors, enhancers, and genic regions. Our analysis also reveals that this epigenomic conservation is significantly correlated with its transcription factor binding density. Binding sites for transcription factors involved in neuron differentiation and components of AP-1 evolve at a significantly higher rate at methylation than at the nucleotide level. Moreover, our models suggest an accelerated epigenomic evolution at binding sites of BRCA1, chromobox homolog protein 2, and factors of the polycomb repressor 2 complex in humans. For most genomic regions, the methylation-based reconstruction of phylogenetic trees is at par with sequence-based reconstruction. Most strikingly, phylogenetic reconstruction using methylation rates in enhancer regions was ineffective independently of the chosen model. We identify a set of phylogenetically uninformative CpG sites enriched in enhancers controlling immune-related genes.

Lineage sorting in apes.

Recombination allows different parts of the genome to have different genealogical histories. When a species splits in two, allelic lineages sort into the two descendant species, and this lineage sorting varies along the genome. If speciation events are close in time, the lineage sorting process may be incomplete at the second speciation event and lead to gene genealogies that do not match the species phylogeny. We review different recent approaches to model lineage sorting along the genome and show how it is possible to learn about population sizes, natural selection, and recombination rates in ancestral species from application of these models to genome alignments of great ape species.

Facial asymmetry tracks genetic diversity among Gorilla subspecies.

Mountain gorillas are particularly inbred compared to other gorillas and even the most inbred human populations. As mountain gorilla skeletal material accumulated during the 1970s, researchers noted their pronounced facial asymmetry and hypothesized that it reflects a population-wide chewing side preference. However, asymmetry has also been linked to environmental and genetic stress in experimental models. Here, we examine facial asymmetry in 114 crania from three Gorilla subspecies using 3D geometric morphometrics. We measure fluctuating asymmetry (FA), defined as random deviations from perfect symmetry, and population-specific patterns of directional asymmetry (DA). Mountain gorillas, with a current population size of about 1000 individuals, have the highest degree of facial FA (explaining 17% of total facial shape variation), followed by Grauer gorillas (9%) and western lowland gorillas (6%), despite the latter experiencing the greatest ecological and dietary variability. DA, while significant in all three taxa, explains relatively less shape variation than FA does. Facial asymmetry correlates neither with tooth wear asymmetry nor increases with age in a mountain gorilla subsample, undermining the hypothesis that facial asymmetry is driven by chewing side preference. An examination of temporal trends shows that stress-induced developmental instability has increased over the last 100 years in these endangered apes.

Great apes and human children rationally monitor their decisions.

Several species can detect when they are uncertain about what decision to make-revealed by opting out of the choice, or by seeking more information before deciding. However, we do not know whether any nonhuman animals recognize when they need more information to make a decision because new evidence contradicts an already-formed belief. Here, we explore this ability in great apes and human children. First, we show that after great apes saw new evidence contradicting their belief about which of two rewards was greater, they stopped to recheck the evidence for their belief before deciding. This indicates the ability to keep track of the reasons for their decisions, or 'rational monitoring' of the decision-making process. Children did the same at 5 years of age, but not at 3 years. In a second study, participants formed a belief about a reward's location, but then a social partner contradicted them, by picking the opposite location. This time even 3-year-old children rechecked the evidence, while apes ignored the disagreement. While apes were sensitive only to the conflict in physical evidence, the youngest children were more sensitive to peer disagreement than conflicting physical evidence.

Calcar femorale variation in extant and fossil hominids: Implications for identifying bipedal locomotion in fossil hominins.

The calcar femorale is an internal bony structure of the proximal femur considered to be functionally related to bipedal locomotion. Among extant primates, the presence of a calcar femorale has been so far documented in extant humans and Pan and, among extinct hominins, in the Late Miocene Orrorin, in a Pliocene Australopithecus, and in a Middle Pleistocene Homo specimen. Using high-resolution microcomputed tomography, we investigated the occurrence and morphology (i.e., shape, location, and size) of the calcar femorale in an adult sample of extant humans, Pan troglodytes, Gorilla gorilla, Pongo sp., and Papio ursinus. We also investigated for the first time the occurrence and morphology of a calcar femorale in the adult proximal femoral remains of a Late Miocene great ape (Rudapithecus) and five Plio-Pleistocene hominins from Southern and Eastern Africa (Australopithecus and Paranthropus). We took four measurements: periosteal-to-tip maximum length, maximum length excluding cortical thickness, maximum vertical height, and the distance between the most anterior and posterior limits of the root. To allow for intergeneric comparisons, estimated body size was used to standardize all measurements. Nine of 10 extant humans have a well-developed calcar femorale. Among the African apes, 6 of 10 Pan and 6 of 10 Gorilla also show a distinct calcar femorale. In Pongo (n = 9), it is only present in one captive individual. None of the five investigated Papio specimens show any trace of this structure. Only calcar femorale height, which is systematically taller and extends into the lower part of the lesser trochanter, discriminates humans from extant great apes, except for one Gorilla. The calcar femorale was absent in one Paranthropus robustus and variably developed in all other investigated fossils. These results indicate that this structure cannot be considered as a diagnostic feature of habitual bipedal locomotion and emphasize the need for further investigations of its functional role.

Spatio-temporal changes in chimpanzee density and abundance in the Greater Mahale Ecosystem, Tanzania.

Species conservation and management require reliable information about animal distribution and population size. Better management actions within a species' range can be achieved by identifying the location and timing of population changes. In the Greater Mahale Ecosystem (GME), western Tanzania, deforestation due to the expansion of human settlements and agriculture, annual burning, and logging are known threats to wildlife. For one of the most charismatic species, the endangered eastern chimpanzee (Pan troglodytes schweinfurthii), approximately 75% of the individuals are distributed outside national park boundaries, requiring monitoring and protection efforts over a vast landscape of various protection statuses. These efforts are especially challenging when we lack data on trends in density and population size. To predict spatio-temporal chimpanzee density and abundance across the GME, we used density surface modeling, fitting a generalized additive model to a 10-year time-series data set of nest counts based on line-transect surveys. The chimpanzee population declined at an annual rate of 2.41%, including declines of 1.72% in riparian forests (from this point forward, forests), 2.05% in miombo woodlands (from this point forward, woodlands) and 3.45% in nonforests. These population declines were accompanied by ecosystem-wide declines in vegetation types of 1.36% and 0.32% per year for forests and woodlands, respectively; we estimated an annual increase of 1.35% for nonforests. Our model predicted the highest chimpanzee density in forests (0.86 chimpanzees/km2 , 95% confidence intervals (CIs) 0.60-1.23; as of 2020), followed by woodlands (0.19, 95% CI 0.12-0.30) and nonforests (0.18, 95% CI 0.10-1.33). Although forests represent only 6% of the landscape, they support nearly one-quarter of the chimpanzee population (769 chimpanzees, 95% CI 536-1103). Woodlands dominate the landscape (71%) and therefore support more than a half of the chimpanzee population (2294; 95% CI 1420-3707). The remaining quarter of the landscape is represented by nonforests and supports another quarter of the chimpanzee population (750; 95% CI 408-1381). Given the pressures on the remaining suitable habitat in Tanzania, and the need of chimpanzees to access both forest and woodland vegetation to survive, we urge future management actions to increase resources and expand the efforts to protect critical forest and woodland habitat and promote strategies and policies that more effectively prevent irreversible losses. We suggest that regular monitoring programs implement a systematic random design to effectively inform and allocate conservation actions and facilitate interannual comparisons for trend monitoring, measuring conservation success, and guiding adaptive management.

Understanding Language Evolution: Beyond Pan-Centrism.

Language does not fossilize but this does not mean that the language's evolutionary timeline is lost forever. Great apes provide a window back in time on our last prelinguistic ancestor's communication and cognition. Phylogeny and cladistics implicitly conjure Pan (chimpanzees, bonobos) as a superior (often the only) model for language evolution compared with earlier diverging lineages, Gorilla and Pongo (orangutans). Here, in reviewing the literature, it is shown that Pan do not surpass other great apes along genetic, cognitive, ecologic, or vocal traits that are putatively paramount for language onset and evolution. Instead, revived herein is the idea that only by abandoning single-species models and learning about the variation among great apes, there might be a chance to retrieve lost fragments of the evolutionary timeline of language.

Great ape health watch: Enhancing surveillance for emerging infectious diseases in great apes.

Infectious diseases have the potential to extirpate populations of great apes. As the interface between humans and great apes expands, zoonoses pose an increasingly severe threat to already endangered great ape populations. Despite recognition of the threat posed by human pathogens to great apes, health monitoring is only conducted for a small fraction of the world's wild great apes (and mostly those that are habituated) meaning that outbreaks of disease often go unrecognized and therefore unmitigated. This lack of surveillance (even in sites where capacity to conduct surveillance is present) is the most significant limiting factor in our ability to quickly detect and respond to emerging infectious diseases in great apes when they first appear. Accordingly, we must create a surveillance system that links disease outbreaks in humans and great apes in time and space, and enables veterinarians, clinicians, conservation managers, national decision makers, and the global health community to respond quickly to these events. Here, we review existing great ape health surveillance programs in African range habitats to identify successes, gaps, and challenges. We use these findings to argue that standardization of surveillance across sites and geographic scales, that monitors primate health in real-time and generates early warnings of disease outbreaks, is an efficient, low-cost step to conserve great ape populations. Such a surveillance program, which we call "Great Ape Health Watch" would lead to long-term improvements in outbreak preparedness, prevention, detection, and response, while generating valuable data for epidemiological research and sustainable conservation planning. Standardized monitoring of great apes would also make it easier to integrate with human surveillance activities. This approach would empower local stakeholders to link wildlife and human health, allowing for near real-time, bidirectional surveillance at the great ape-human interface.