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.

Fine-scaled climate variation in equatorial Africa revealed by modern and fossil primate teeth.

Variability in resource availability is hypothesized to be a significant driver of primate adaptation and evolution, but most paleoclimate proxies cannot recover environmental seasonality on the scale of an individual lifespan. Oxygen isotope compositions (δ18O values) sampled at high spatial resolution in the dentitions of modern African primates (n = 2,352 near weekly measurements from 26 teeth) track concurrent seasonal precipitation, regional climatic patterns, discrete meteorological events, and niche partitioning. We leverage these data to contextualize the first δ18O values of two 17 Ma Afropithecus turkanensis individuals from Kalodirr, Kenya, from which we infer variably bimodal wet seasons, supported by rainfall reconstructions in a global Earth system model. Afropithecus' δ18O fluctuations are intermediate in magnitude between those measured at high resolution in baboons (Papio spp.) living across a gradient of aridity and modern forest-dwelling chimpanzees (Pan troglodytes verus). This large-bodied Miocene ape consumed seasonally variable food and water sources enriched in 18O compared to contemporaneous terrestrial fauna (n = 66 fossil specimens). Reliance on fallback foods during documented dry seasons potentially contributed to novel dental features long considered adaptations to hard-object feeding. Developmentally informed microsampling recovers greater ecological complexity than conventional isotope sampling; the two Miocene apes (n = 248 near weekly measurements) evince as great a range of seasonal δ18O variation as more time-averaged bulk measurements from 101 eastern African Plio-Pleistocene hominins and 42 papionins spanning 4 million y. These results reveal unprecedented environmental histories in primate teeth and suggest a framework for evaluating climate change and primate paleoecology throughout the Cenozoic.

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.

A cadaveric study of wrist-joint moments in chimpanzees and orangutans with implications for the evolution of knuckle-walking.

Understanding the mechanism underlying the evolution of knuckle-walking in African great apes but not in humans may provide important implications about the origin and evolution of human bipedal locomotion. In this study, aiming to reveal possible structural adaptations of the chimpanzee's forearm and hand musculature related to knuckle-walking, we measure the passive elastic moment of the chimpanzee's and orangutan's wrist as it was rotated into extension, immobilizing the metacarpophalangeal joint at three different positions: extended (as in knuckle-walking), flexed (as in fist-walking), and an intermediate position. Our findings demonstrate that when the metacarpophalangeal joints are extended, the rigidity of the wrist joint in the extended direction increases. This increased rigidity is attributed to the passive elongation and force generation of digital flexor muscles, which are relatively short in chimpanzees. Consequently, this enhanced wrist-joint rigidity contributes to the stability and energetically efficient transmission of propulsive force to the ground during the stance phase. Overall, our study supports the hypothesis that knuckle-walking is an adaptation to terrestrial locomotion for an ancestor characterized by the restricted capacity for wrist extension owing to the relatively shorter tendons of digital flexor muscles.

The evolutionary origin of human kissing.

A kiss has been a signal of special affection across continents and cultures for millennia. Between times and peoples, social norms invariably prescribe kissing to specific affiliations and contexts, implying deeper biological bases. Why the protruding of the lips and slight suction when touching another? Capuchin monkeys stick their fingers in their friends' eyes as sign of affection, why have humans developed kissing? Here I briefly review proposed hypotheses for the evolution of human kissing. Great ape social behavior suggests that kissing is likely the conserved final mouth-contact stage of a grooming bout when the groomer sucks with protruded lips the fur or skin of the groomed to latch on debris or a parasite. The hygienic relevance of grooming decreased over human evolution due to fur-loss, but shorter sessions would have predictably retained a final "kissing" stage, ultimately, remaining the only vestige of a once ritualistic behavior for signaling and strengthening social and kinship ties in an ancestral ape.

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.

Divergence in bonobo and chimpanzee social life.

New research is shedding light on the nuances and complexity of social relationships in our closest relatives, revealing cooperative intergroup relationships in bonobos, in contrast to lethal intergroup violence in chimpanzees. At the same time, intragroup relationships, at least among males, are characterized by higher frequencies of aggression and lower rates of coalitionary cooperation in bonobos than chimpanzees.

Reassessment of the phylogenetic relationships of the late Miocene apes Hispanopithecus and Rudapithecus based on vestibular morphology.

Late Miocene great apes are key to reconstructing the ancestral morphotype from which earliest hominins evolved. Despite consensus that the late Miocene dryopith great apes Hispanopithecus laietanus (Spain) and Rudapithecus hungaricus (Hungary) are closely related (Hominidae), ongoing debate on their phylogenetic relationships with extant apes (stem hominids, hominines, or pongines) complicates our understanding of great ape and human evolution. To clarify this question, we rely on the morphology of the inner ear semicircular canals, which has been shown to be phylogenetically informative. Based on microcomputed tomography scans, we describe the vestibular morphology of Hispanopithecus and Rudapithecus, and compare them with extant hominoids using landmark-free deformation-based three-dimensional geometric morphometric analyses. We also provide critical evidence about the evolutionary patterns of the vestibular apparatus in living and fossil hominoids under different phylogenetic assumptions for dryopiths. Our results are consistent with the distinction of Rudapithecus and Hispanopithecus at the genus rank, and further support their allocation to the Hominidae based on their derived semicircular canal volumetric proportions. Compared with extant hominids, the vestibular morphology of Hispanopithecus and Rudapithecus most closely resembles that of African apes, and differs from the derived condition of orangutans. However, the vestibular morphologies reconstructed for the last common ancestors of dryopiths, crown hominines, and crown hominids are very similar, indicating that hominines are plesiomorphic in this regard. Therefore, our results do not conclusively favor a hominine or stem hominid status for the investigated dryopiths.

Positive Selection and Enhancer Evolution Shaped Lifespan and Body Mass in Great Apes.

Within primates, the great apes are outliers both in terms of body size and lifespan, since they include the largest and longest-lived species in the order. Yet, the molecular bases underlying such features are poorly understood. Here, we leveraged an integrated approach to investigate multiple sources of molecular variation across primates, focusing on over 10,000 genes, including approximately 1,500 previously associated with lifespan, and additional approximately 9,000 for which an association with longevity has never been suggested. We analyzed dN/dS rates, positive selection, gene expression (RNA-seq), and gene regulation (ChIP-seq). By analyzing the correlation between dN/dS, maximum lifespan, and body mass, we identified 276 genes whose rate of evolution positively correlates with maximum lifespan in primates. Further, we identified five genes, important for tumor suppression, adaptive immunity, metastasis, and inflammation, under positive selection exclusively in the great ape lineage. RNA-seq data, generated from the liver of six species representing all the primate lineages, revealed that 8% of approximately 1,500 genes previously associated with longevity are differentially expressed in apes relative to other primates. Importantly, by integrating RNA-seq with ChIP-seq for H3K27ac (which marks active enhancers), we show that the differentially expressed longevity genes are significantly more likely than expected to be located near a novel "ape-specific" enhancer. Moreover, these particular ape-specific enhancers are enriched for young transposable elements, and specifically SINE-Vntr-Alus. In summary, we demonstrate that multiple evolutionary forces have contributed to the evolution of lifespan and body size in primates.

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.

Paleoenvironmental inferences on the Late Miocene hominoid-bearing site of Can Llobateres (NE Iberian Peninsula): An ecometric approach based on functional dental traits.

Hispanopithecus laietanus from the Late Miocene (9.8 Ma) of Can Llobateres 1 (CLL1; Vallès-Penedès Basin, NE Iberian Peninsula) represents one of the latest occurrences of fossil apes in Western mainland Europe, where they are last recorded at ∼9.5 Ma. The paleoenvironment of CLL1 is thus relevant for understanding the extinction of European hominoids. To refine paleoenvironmental inferences for CLL1, we apply ecometric models based on functional crown type (FCT) variables-a scoring scheme devised to capture macroscopic functional traits of occlusal shape and wear surfaces of herbivorous large mammal molars. Paleotemperature and paleoprecipitation estimates for CLL1 are provided based on published regional regression models linking average FCT of large herbivorous mammal communities to climatic conditions. A mapping to Whittaker's present-day biome classification is also attempted based on these estimates, as well as a case-based reasoning via canonical variate analysis of FCT variables from five relevant biomes. Estimates of mean annual temperature (25 °C) and mean annual precipitation (881 mm) classify CLL1 as a tropical seasonal forest/savanna, only in partial agreement with the canonical variate analysis results, which classify CLL1 as a tropical rainforest with a higher probability. The former biome agrees better with previous inferences derived from fossil plants and mammals, as well as preliminary isotopic data. The misclassification of CLL1 as a tropical forest is attributed to the mixture of forest-adapted taxa with others adapted to more open environments, given that faunal and plant composition indicates the presence of a dense wetland/riparian forest with more open woodlands nearby. The tested FCT ecometric approaches do not provide unambiguous biome classification for CLL1. Nevertheless, our results are consistent with those from other approaches, thus suggesting that FCT variables are potentially useful to investigate paleoenvironmental changes through time and space-including those that led to the extinction of European Miocene apes.

Challenges and perspectives on functional interpretations of australopith postcrania and the reconstruction of hominin locomotion.

In 1994, Hunt published the 'postural feeding hypothesis'-a seminal paper on the origins of hominin bipedalism-founded on the detailed study of chimpanzee positional behavior and the functional inferences derived from the upper and lower limb morphology of the Australopithecus afarensis A.L. 288-1 partial skeleton. Hunt proposed a model for understanding the potential selective pressures on hominins, made robust, testable predictions based on Au. afarensis functional morphology, and presented a hypothesis that aimed to explain the dual functional signals of the Au. afarensis and, more generally, early hominin postcranium. Here we synthesize what we have learned about Au. afarensis functional morphology and the dual functional signals of two new australopith discoveries with relatively complete skeletons (Australopithecus sediba and StW 573 'Australopithecus prometheus'). We follow this with a discussion of three research approaches that have been developed for the purpose of drawing behavioral inferences in early hominins: (1) developments in the study of extant apes as models for understanding hominin origins; (2) novel and continued developments to quantify bipedal gait and locomotor economy in extant primates to infer the locomotor costs from the anatomy of fossil taxa; and (3) novel developments in the study of internal bone structure to extract functional signals from fossil remains. In conclusion of this review, we discuss some of the inherent challenges of the approaches and methodologies adopted to reconstruct the locomotor modes and behavioral repertoires in extinct primate taxa, and notably the assessment of habitual terrestrial bipedalism in early hominins.

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.

Comparison of bone density patterns of the subaxial spine between chimpanzees and gorillas - A case study.

Case study on the bone density pattern of subaxial vertebral column in African apes. INTRODUCTION: African apes have been noted to experience fewer back ailments than humans and to have higher vertebral bone density. Yet, research on the subject is quite limited and has usually included only one or few vertebrae. However, to understand vertebral column as whole and how posture and locomotion might have affected it, we need to know how bone density varies between adjacent vertebrae. MATERIALS AND METHODS: Bone density in the vertebral body was measured for all subaxial vertebrae of five specimens including two Pan troglodytes (1 male and 1 female) and three Gorilla gorilla (2 males and 1 female) using peripheral quantitative computed tomography (pQCT). RESULTS: The results tentatively indicated differences between species, especially in the trabecular density of the cervical segment and support the need for further studies on this subject.

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.

Evolution and molecular interactions of major histocompatibility complex (MHC)-G, -E and -F genes.

Classical HLA (Human Leukocyte Antigen) is the Major Histocompatibility Complex (MHC) in man. HLA genes and disease association has been studied at least since 1967 and no firm pathogenic mechanisms have been established yet. HLA-G immune modulation gene (and also -E and -F) are starting the same arduous way: statistics and allele association are the trending subjects with the same few results obtained by HLA classical genes, i.e., no pathogenesis may be discovered after many years of a great amount of researchers' effort. Thus, we believe that it is necessary to follow different research methodologies: (1) to approach this problem, based on how evolution has worked maintaining together a cluster of immune-related genes (the MHC) in a relatively short chromosome area since amniotes to human at least, i.e., immune regulatory genes (MHC-G, -E and -F), adaptive immune classical class I and II genes, non-adaptive immune genes like (C2, C4 and Bf) (2); in addition to using new in vitro models which explain pathogenetics of HLA and disease associations. In fact, this evolution may be quite reliably studied during about 40 million years by analyzing the evolution of MHC-G, -E, -F, and their receptors (KIR-killer-cell immunoglobulin-like receptor, NKG2-natural killer group 2-, or TCR-T-cell receptor-among others) in the primate evolutionary lineage, where orthology of these molecules is apparently established, although cladistic studies show that MHC-G and MHC-B genes are the ancestral class I genes, and that New World apes MHC-G is paralogous and not orthologous to all other apes and man MHC-G genes. In the present review, we outline past and possible future research topics: co-evolution of adaptive MHC classical (class I and II), non-adaptive (i.e., complement) and modulation (i.e., non-classical class I) immune genes may imply that the study of full or part of MHC haplotypes involving several loci/alleles instead of single alleles is important for uncovering HLA and disease pathogenesis. It would mainly apply to starting research on HLA-G extended haplotypes and disease association and not only using single HLA-G genetic markers.

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.