Great Apes Research Articles

Humanlike manual activities in Australopithecus

The evolution of the human hand is a topic of great interest in paleoanthropology. As the hand can be involved in a vast array of activities, knowledge regarding how it was used by early hominins can yield crucial information on the factors driving biocultural evolution. Previous research on early hominin hands focused on the overall bone shape. However, while such approaches can inform on mechanical abilities and the evolved efficiency of manipulation, they cannot be used as a definite proxy for individual habitual activity. Accordingly, it is crucial to examine bone structures more responsive to lifetime biomechanical loading, such as muscle attachment sites or internal bone architecture. In this study, we investigate the manual entheseal patterns of Australopithecus afarensis, Australopithecus africanus, and Australopithecus sediba through the application of the validated entheses-based reconstruction of activity method. Using a comparative sample of later Homo and three great ape genera, we analyze the muscle attachment site proportions on the thumb, fifth ray, and third intermediate phalanx to gain insight into the habitual hand use of Australopithecus. We use a novel statistical procedure to account for the effects of interspecies variation in overall size and ray proportions. Our results highlight the importance of certain muscles of the first and fifth digits for humanlike hand use. In humans, these muscles are required for variable in-hand manipulation and are activated during stone-tool production. The entheses of A. sediba suggest muscle activation patterns consistent with a similar suite of habitual manual activities as in later Homo. In contrast, A. africanus and A. afarensis display a mosaic entheseal pattern that combines indications of both humanlike and apelike manipulation. Overall, these findings provide new evidence that some australopith species were already habitually engaging in humanlike manipulation, even if their manual dexterity was likely not as high as in later Homo.

Scoping review of general anaesthesia in non-human great apes

Scoping review of general anaesthesia in non-human great apes

Great ape surveys and the implications of long-term monitoring in the Djéké Triangle, Republic of Congo.

Existing protected areas are anchors for conservation. Safeguarding flora and fauna within their peripheral areas is essential to maintaining their integrity and to potential increases to the area under effective conservation. With the decline in tropical forests, initiatives to increase the area of undisturbed forests under strict protection, particularly those neighboring protected areas, is of critical importance. Applied research has informed such land-management decisions for areas surrounding the Nouabalé-Ndoki National Park (NNNP) in Republic of Congo since the park's inception three decades ago. Here, we present results of the first systematic line transect survey of great ape nests conducted in the Djéké Triangle, a 100 km2 unlogged continuous forest in the Kabo Forestry Management Unit adjacent to the NNNP. Distance sampling methods applied along 26 line transects on two different occasions (2016 and 2018, with total effort of 69.4km) provided density estimates of 0.75 (95% confidence interval (CI) 0.52-1.09) and 0.61 (95% CI 0.40-0.92) chimpanzees/km2 and 2.15 (95% CI 1.36-3.40) and 1.19 (95% CI 0.78-1.82) gorillas/km2 for each of the two surveys, respectively. Estimated ape densities were compared to others across the landscape. The findings provide a unique baseline in an area that supports ongoing behavioral research and future gorilla tourism opportunities in the Djéké Triangle. More importantly, results provided empirical evidence of the environmental value and strategic conservation importance supporting inclusion of the Djéké Triangle into the NNNP in 2023. These long-term monitoring results inform best-practice standards and ape tourism certification.

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.

Instrumental helping motivations of children and chimpanzees

AbstractChimpanzees and other great apes seem to be much less cooperative than humans overall, yet they nevertheless reliably help others in many instrumental circumstances. Although in many contexts the helping behavior of chimpanzees is quite similar to that of human children, recent studies using both behavioral and psychophysiological paradigms have revealed important differences, specifically, in the underlying motivations for prosocial behavior. Here, we provide both a synthesis of recent empirical work and an evolutionary hypothesis that can account for the differences in chimpanzee and human helping motivations.

Temporal lobe evolution in Hominidae and the origin of human lobe proportions.

Objectives Evolutionary changes in hominin social complexity have been associated with increases in absolute brain size. The temporal lobes are nestled in the middle cranial fossae (MCF) of the skull, the dimensions of which allow estimation of temporal lobe volume (TLV) in extant and fossil taxa. Materials and Methods The main aim of this study is to determine where along the hominid phylogeny, major temporal lobe size transitions occurred. We used computed tomography (CT) scans of crania, 3D photogrammetry data, and laser surface scans of endocranial casts to measure seven MCF metrics in 11 extant anthropoid taxa using multiple regressions to estimate TLV in 5 extant hominids and 10 fossil hominins. Phylogenetic comparative methods mapped temporal lobe size, brain size, and temporal lobe proportions onto phylogenetic trees broadly for Hominidae and specifically for Hominini. Results Extant Homo sapiens were not an outlier in relative brain size, temporal lobe size, or proportions of the temporal lobes, but some proportions within the lobe were uniquely altered. The most notable changes in relative temporal lobe size and proportions saw a decrease in relative temporal lobe size and proportions in the genus Pan compared to other extant great apes and fossil hominins while there was a relative increase in the temporal lobe width and length in Australopithecus-Paranthropus clade compared to the genus Homo and other extant great apes including modern humans. Discussion We do not find support for the social brain, environmental or functional craniology hypotheses alone but think it prudent to consider the implications of cerebral reorganization between the temporal lobes and other regions of the brain within the context of these hypotheses and with future investigation is warranted.

Young sanctuary-living chimpanzees produce more communicative expressions with artificial objects than with natural objects

In humans, interactions with objects are often embedded in communicative exchanges. Objects offer unique affordances to explore, carry functions and hold cultural relevance, which can shape children’s interactions and communication. Research indicates that the use of artificial objects, such as certain toys, helps promote pre-linguistic communication, consequently impacting language development. Given that chimpanzees use objects extensively compared to other great apes, and considering the differences between chimpanzees and bonobos in intrinsic motivation for tool use and the extended developmental period during which they learn to use objects, it is reasonable to expect that objects may influence chimpanzees’ communication. Here, we examined interactions of 31 immature sanctuary-living chimpanzees with non-novel artificial and natural objects and tested their vocal and facial expressions, applying methods previously designed for children. Our results showed an increase in these expressions associated with artificial objects. These findings provide the first empirical evidence that chimpanzee communicative expressions may be influenced by inherent properties of objects, potentially promoting varied communication, comparable to the impact distinctive objects have on pre-linguistic children. By exploring this connection between object-centric interactions and communication, this study reveals deep phylogenetic roots where objects may have shaped great ape communication and possibly evolutionary foundations of language.

Deep genetic substructure within bonobos.

Establishing the genetic and geographic structure of populations is fundamental, both to understand their evolutionary past and preserve their future. Nevertheless, the patterns of genetic population structure are unknown for most endangered species. This is the case for bonobos (Pan paniscus), which, together with chimpanzees (Pan troglodytes), are humans' closest living relatives. Chimpanzees live across equatorial Africa and are classified into four subspecies,1 with some genetic population substructure even within subspecies. Conversely, bonobos live exclusively in the Democratic Republic of Congo and are considered a homogeneous group with low genetic diversity,2 despite some population structure inferred from mtDNA. Nevertheless, mtDNA aside, their genetic structure remains unknown, hampering our understanding of the species and conservation efforts. Mapping bonobo genetic diversity in space is, however, challenging because, being endangered, only non-invasive sampling is possible for wild individuals. Here, we jointly analyze the exomes and mtDNA from 20 wild-born bonobos, the whole genomes of 10 captive bonobos, and the mtDNA of 136 wild individuals. We identify three genetically distinct bonobo groups of inferred Central, Western, and Far-Western geographic origin within the bonobo range. We estimate the split time between the central and western populations to be ∼145,000 years ago and genetic differentiation to be in the order of that of the closest chimpanzee subspecies. Furthermore, our estimated long-term Ne for Far-West (∼3,000) is among the lowest estimated for any great ape lineage. Our results highlight the need to attend to the bonobo substructure, both in terms of research and conservation.

Global primary predictors of extinction risk in primates.

Identifying the main predictors of species' extinction risk while accounting for the effects of spatial and phylogenetic structures in the data is key to preventing species loss in tropical forests through adequate conservation practices. We recorded 22 705 precise geographical locations of primate occurrence across four major geographic realms (Neotropics, mainland Africa, Madagascar and Asia) to assess predictors of threat status using a novel Bayesian spatio-phylogenetic approach. We estimated the relative contributions of fixed factors (forest amount, body mass, home range, diel activity, locomotion, evolutionary distinctiveness and climatic instability) and random factors (space and phylogeny) to primate extinction risk. Precipitation instability increased the extinction risk in the Neotropics but decreased it in mainland Africa and Madagascar. Forest amount was negatively associated with extinction risk in all realms except Madagascar. Body mass increased the extinction risk in the Neotropics and Madagascar, whereas home range increased the extinction risk in mainland Africa and decreased it in Asia. Evolutionary distinctiveness negatively influenced extinction risk only in mainland Africa. Our findings highlight the importance of climate change mitigation and forest protection strategies. Increasing the protection of large primates and reducing hunting are also essential.

Evidence for the communicative function of human-directed gazing in 6- to 7-week-old dog puppies

In human infants, the ability to show gaze alternations between an object of interest and another individual is considered fundamental to the development of complex social-cognitive abilities. Here we show that well-socialised dog puppies show gaze alternations in two contexts at an early age, 6–7 weeks. Thus, 69.4% of puppies in a novel object test and 45.59% of puppies during an unsolvable task alternated their gaze at least once between a person’s face and the object. In both contexts, the frequency of gaze alternations was positively correlated with the duration of whimpering, supporting the communicative nature of puppies’ gazing. Furthermore, the number of gaze alternations in the two contexts was correlated, indicating an underlying propensity for gazing at humans despite likely different motivations in the two contexts. Similar to humans, and unlike great apes or wolves, domestic dogs show gaze alternations from an early age if they are well-socialised. They appear to have a genetic preparedness to communicate with humans via gaze alternations early in ontogeny, but they may need close contact with humans for this ability to emerge, highlighting the interactive effects of domestication and environmental factors on behavioural development in dogs.

A short natural history of mental time travels: a journey still travelled?

Tulving's introduction of episodic memory and the metaphor of mental time travel has immensely enriched our understanding of human cognition. However, his focus on human psychology, with limited consideration of evolutionary perspectives, led to the entrenched notion that mental time travel is uniquely human. We contend that adopting a phylogenetic perspective offers a deeper insight into cognition, revealing it as a continuous evolutionary process. Adherence to the uniqueness of pre-defined psychological concepts obstructs a more complete understanding. We offer a concise natural history to elucidate how events that occurred hundreds of millions of years ago have been pivotal for our ability to mentally time travel. We discuss how the human brain, utilizing parts with ancient origins in a networked manner, enables mental time travel. This underscores that episodic memories and mental time travel are not isolated mental constructs but integral to our perception and representation of the world. We conclude by examining recent evidence of neuroanatomical correlates found only in great apes, which show great variability, indicating the ongoing evolution of mental time travel in humans.This article is part of the theme issue 'Elements of episodic memory: lessons from 40 years of research'.

Impact and characterization of serial structural variations across humans and great apes

Modern sequencing technology enables the systematic detection of complex structural variation (SV) across genomes. However, extensive DNA rearrangements arising through a series of mutations, a phenomenon we refer to as serial SV (sSV), remain underexplored, posing a challenge for SV discovery. Here, we present NAHRwhals (https://github.com/WHops/NAHRwhals), a method to infer repeat-mediated series of SVs in long-read genomic assemblies. Applying NAHRwhals to haplotype-resolved human genomes from 28 individuals reveals 37 sSV loci of various length and complexity. These sSVs explain otherwise cryptic variation in medically relevant regions such as the TPSAB1 gene, 8p23.1, 22q11 and Sotos syndrome regions. Comparisons with great ape assemblies indicate that most human sSVs formed recently, after the human-ape split, and involved non-repeat-mediated processes in addition to non-allelic homologous recombination. NAHRwhals reliably discovers and characterizes sSVs at scale and independent of species, uncovering their genomic abundance and suggesting broader implications for disease.

Implementation of automated cognitive testing systems for socially housed rhesus (Macaca mulatta) and squirrel (Saimiri spp.) monkeys: Age differences in learning.

Utilizing Automated Cognitive Testing Systems (ACTS) with group-housed nonhuman primates offers a number of advantages over manual testing and computerized testing of singly housed subjects. To date, ACTS usage has been limited to great apes or African monkeys. Here, we detail what we have learned while implementing ACTS with socially housed squirrel monkeys and rhesus macaques and provide information about the training process. In addition, we examined the effects of age on learning acquisition. We found age differences in learning for both squirrel monkeys and rhesus monkeys. Older monkeys were not as proficient as younger monkeys on learning to use the touch screens (squirrel monkeys only), discrimination learning (rhesus monkeys only; note: squirrel monkeys were not trained to criterion on this task), and recognition learning (both species). Overall, ACTS provide a number of advantages for studying cognition in socially living nonhuman primates and can be used to further investigate cognitive decline whether related to natural aging processes or disease pathology. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Epidemiological Consequences of Individual Centrality on Wild Chimpanzees.

Disease outbreaks are one of the key threats to great apes and other wildlife. Because the spread of some pathogens (e.g., respiratory viruses, sexually transmitted diseases, ectoparasites) are mediated by social interactions, there is a growing interest in understanding how social networks predict the chain of pathogen transmission. In this study, we built a party network from wild chimpanzees (Pan troglodytes), and used agent-based modeling to test: (i) whether individual attributes (sex, age) predict individual centrality (i.e., whether it is more or less socially connected); (ii) whether individual centrality affects an individual's role in the chain of pathogen transmission; and, (iii) whether the basic reproduction number (R0) and infectious period modulate the influence of centrality on pathogen transmission. We show that sex and age predict individual centrality, with older males presenting many (degree centrality) and strong (strength centrality) relationships. As expected, males are more central than females within their network, and their centrality determines their probability of getting infected during simulated outbreaks. We then demonstrate that direct measures of social interaction (strength centrality), as well as eigenvector centrality, strongly predict disease dynamics in the chimpanzee community. Finally, we show that this predictive power depends on the pathogen's R0 and infectious period: individual centrality was most predictive in simulations with the most transmissible pathogens and long-lasting diseases. These findings highlight the importance of considering animal social networks when investigating disease outbreaks.

Object permanence in rooks (Corvus frugilegus): Individual differences and behavioral considerations.

Piagetian object permanence (OP) refers to the ability to know that an object continues to exist when out of sight: In humans, it develops in six stages. Species of great apes, other mammals, and birds (parrots, corvids, and pigeons) have been shown to possess partial or full OP, which is a prerequisite for more complex physical cognition abilities they may possess. In birds, the greatest variation is in Stage 6 (invisible displacements) and in "A-not-B" errors-incorrectly persevering in searching an empty location rewarded previously. Caching abilities have been invoked as holding explanatory power over results in corvids, for which this error is sometimes completely absent. The rook (Corvus frugilegus), a cognitively advanced, social, caching corvid, has not yet been studied for OP. This study applies tasks of one OP scale commonly adapted for nonhuman animals, Uzgiris and Hunt's Scale 1, as well as later-conceived tasks 16 and S, to a sample of adult, captive rooks. One rook demonstrated full OP (Stage 6b, multiple invisible displacements), whereas other individuals varied, attaining between Stages 5a (single visible displacements) and 6a (single invisible displacements). Like some corvids, a few made transient "A-not-B" errors. Behavioral considerations potentially underlying observed individual variation in results in rooks, including dominance, neophobia, past experiences, and individual idiosyncrasies, are examined. Rooks, like other corvids, possess well-developed OP abilities, and these results support the idea that exertion of executive control is required to avoid "A-not-B" errors, rather than caching abilities or developmental age, as previously suggested.

New perspectives on fighting violence against women.

Gender-based violence (GBV) and, more specifically, violence against women (VAW) are commonly considered a consequence of a patriarchal structure-a social system granting the senior male absolute authority over the family and the community as a whole. Anthropologists have documented that human male dominance is rooted in evolution, with male violent behavior observed among the great apes. Given that evolution is a continuous process, human progress over millennia has modified pre-existing behavior, demonstrating that humans can move beyond ancestral ways of life over time. Precisely because of the imperative to change and improve, at the global international level as well as in individual countries, strong movements are in action to eliminate GBV/VAW. FIGO has been and continues to be at the forefront of the battle for equality, with initiatives that cover many aspects of this, including the imperative to involve men, who-in the majority of cases-are the perpetrators. Since men are often the root of the problem, they must also be at the forefront of the battle to eradicate it. GBV/VAW comprises many facets, including selective female abortion, infanticide, femicide, honor killing, female genital mutilation, and child marriage. These deeply rooted forms of violence continue to perpetuate gender inequalities, remain major obstacles to health and societal progress, and violate the most basic human rights.

Centromeric transposable elements and epigenetic status drive karyotypic variation in the eastern hoolock gibbon.

Great apes have maintained a stable karyotype with few large-scale rearrangements; in contrast, gibbons have undergone a high rate of chromosomal rearrangements coincident with rapid centromere turnover. Here we characterize assembled centromeres in the Eastern hoolock gibbon, Hoolock leuconedys (HLE), finding a diverse group of transposable elements (TEs) that differ from the canonical alpha satellites found across centromeres of other apes. We find that HLE centromeres contain a CpG methylation centromere dip region, providing evidence this epigenetic feature is conserved in the absence of satellite arrays; nevertheless, we report a variety of atypical centromeric features, including protein-coding genes and mismatched replication timing. Further, large structural variations define HLE centromeres and distinguish them from other gibbons. Combined with differentially methylated TEs, topologically associated domain boundaries, and segmental duplications at chromosomal breakpoints, we propose that a "perfect storm" of multiple genomic attributes with propensities for chromosome instability shaped gibbon centromere evolution.

The uniqueness of human vulnerability to brain aging in great ape evolution.

Aging is associated with progressive gray matter loss in the brain. This spatially specific, morphological change over the life span in humans is also found in chimpanzees, and the comparison between these great ape species provides a unique evolutionary perspective on human brain aging. Here, we present a data-driven, comparative framework to explore the relationship between gray matter atrophy with age and recent cerebral expansion in the phylogeny of chimpanzees and humans. In humans, we show a positive relationship between cerebral aging and cortical expansion, whereas no such relationship was found in chimpanzees. This human-specific association between strong aging effects and large relative cortical expansion is particularly present in higher-order cognitive regions of the ventral prefrontal cortex and supports the "last-in-first-out" hypothesis for brain maturation in recent evolutionary development of human faculties.

The origin of great ape gestural forms.

Two views claim to account for the origins of great ape gestural forms. On the Leipzig view, gestural forms are ontogenetically ritualised from action sequences between pairs of individuals. On the St Andrews view, gestures are the product of natural selection for shared gestural forms. The Leipzig view predicts within- and between-group differences between gestural forms that arise as a product of learning in ontogeny. The St Andrews view predicts universal gestural forms comprehensible within and between species that arise because gestural forms were a target of natural selection. We reject both accounts and propose an alternative "recruitment view" of the origins of great ape gestures. According to the recruitment view, great ape gestures recruit features of their existing behavioural repertoire for communicative purposes. Their gestures inherit their communicative functions from visual (and sometimes tactile) presentations of familiar and easily recognisable action schemas and states and parts of the body. To the extent that great ape species possess similar bodies, this predicts mutual comprehensibility within and between species - but without supposing that gestural forms were themselves targets of natural selection. Additionally, we locate great ape gestural communication within a pragmatic framework that is continuous with human communication, and make testable predications for adjudicating between the three alternative views. We propose that the recruitment view best explains existing data, and does so within a mechanistic framework that emphasises continuity between human and non-human great ape communication.

Evolution of the Cytomegalovirus RL11 gene family in Old World monkeys and Great Apes.

Cytomegalovirus (CMV) is a genus of herpesviruses, members of which share a long history of coevolution with their primate hosts including New World monkeys, Old World monkeys (OWMs), and Great Apes (GAs). These viruses are ubiquitous within their host populations and establish lifelong infection in most individuals. Although asymptomatic in healthy individuals, infection poses a significant risk to individuals with a weakened or underdeveloped immune system. The genome of human CMV is the largest among human-infecting viruses and comprises at least 15 separate gene families, which may have arisen by gene duplication. Within human CMV, the RL11 gene family is the largest. RL11 genes are nonessential in vitro but have immune evasion roles that are likely critical to persistence in vivo. These genes demonstrate an extreme level of inter-species and intra-strain sequence diversity, which makes it challenging to deduce the evolutionary relationships within this gene family. Understanding the evolutionary relationships of these genes, especially accurate ortholog identification, is essential for reconstructing ancestral genomes, deciphering gene repertoire and order, and enabling reliable functional analyses across the CMV species, thereby offering insights into evolutionary processes, genetic diversity, and the functional significance of genes. In this work, we combined in silico genome screening with sequence-based and structure-guided phylogenetic analysis to reconstruct the evolutionary history of the RL11 gene family. We confirmed that RL11 genes are unique to OWM and GA CMVs, showing that this gene family was formed by multiple early duplication events and later lineage-specific losses. We identified four main clades of RL11 genes and showed that their expansions were mainly lineage specific and happened independently in CMVs of GAs, African OWMs, and Asian OWMs. We also identified groups of orthologous genes across the CMV tree, showing that some human CMV-specific RL11 genes emerged before the divergence of human and chimpanzee CMVs but were subsequently lost in the latter. The extensive and dynamic species-specific evolution of this gene family suggests that their functions target elements of host immunity that have similarly coevolved during speciation.