A brief history of primate research in the Ndoki forest.

The Nouabalé-Ndoki National Park (NNNP) in Republic of Congo has become a beacon for conservation in Central Africa. This manuscript documents the arrival of primatologists, the establishment of field stations and major discoveries in primate behavior and ecology. Field stations were strategically established to study primate behavior in a variety of different contexts from stationary platforms to forest follows of habituated groups. The implementation of new technologies and analyses have also been a hallmark of research at Ndoki. Scientists are shaping a new era in primatology at NNNP by building on past successes and promoting the next generation of Congolese conservationists to address environmental challenges. Results have proven crucial in discussions with government and industry and led to conservation gains such as the inclusion of the intact forests of the Goualougo and Djéké Triangles into the NNNP. The research stations have also become essential for developing a long-term certified sustainable international gorilla tourism program. Despite the many advancements for conservation such as increased protection of forests, development of internationally recognized protocols and large-scale capacity building initiatives, there are reasons for considerable concern in the near- and long-term for primates and their forest habitats in the Ndoki landscape. To address these concerns, we emphasize the long history of forming partnerships with local communities. We also discuss shared overlap featuring multicultural and environmental use of forest resources that is likely to be crucial in championing the conservation of the Ndoki forests for the next 25 years and beyond.

Sequence-based machine learning reveals 3D genome differences between bonobos and chimpanzees.

The 3D structure of the genome is an important mediator of gene expression. As phenotypic divergence is largely driven by gene regulatory variation, comparing genome 3D contacts across species can further understanding of the molecular basis of species differences. However, while experimental data on genome 3D contacts in humans is increasingly abundant, only a handful of 3D genome contact maps exist for other species. Here, we demonstrate that human experimental data can be used to close this data gap. We apply a machine learning model that predicts 3D genome contacts from DNA sequence to the genomes from 56 bonobos and chimpanzees and identify species-specific patterns of genome folding. We estimated 3D divergence between individuals from the resulting contact maps in 4,420 1 Mb genomic windows, of which ∼17% were substantially divergent in predicted genome contacts. Bonobos and chimpanzees diverged at 89 windows, overlapping genes associated with multiple traits implicated in Pan phenotypic divergence. We discovered 51 bonobo-specific variants that individually produce the observed bonobo contact pattern in bonobo-chimpanzee divergent windows. Our results demonstrate that machine learning methods can leverage human data to fill in data gaps across species, offering the first look at population-level 3D genome variation in non-human primates. We also identify loci where changes in 3D folding may contribute to phenotypic differences in our closest living relatives.

Neuro-evolutionary evidence for a universal fractal primate brain shape.

The cerebral cortex displays a bewildering diversity of shapes and sizes across and within species. Despite this diversity, we present a universal multi-scale description of primate cortices. We show that all cortical shapes can be described as a set of nested folds of different sizes. As neighbouring folds are gradually merged, the cortices of 11 primate species follow a common scale-free morphometric trajectory, that also overlaps with over 70 other mammalian species. Our results indicate that all cerebral cortices are approximations of the same archetypal fractal shape with a fractal dimension of df = 2.5. Importantly, this new understanding enables a more precise quantification of brain morphology as a function of scale. To demonstrate the importance of this new understanding, we show a scale-dependent effect of ageing on brain morphology. We observe a more than fourfold increase in effect size (from two standard deviations to eight standard deviations) at a spatial scale of approximately 2 mm compared to standard morphological analyses. Our new understanding may, therefore, generate superior biomarkers for a range of conditions in the future.

Many of the brain's essential functions ­ from decision-making to movement ­ take place in its outer layer known as the cerebral cortex. The shape of the cerebral cortex varies significantly between species. For instance, in humans, it is folded in to grooves and ridges, whereas in other animals, including mice, it is completely smooth. The structure of the cortex can also differ within a species, and be altered by aging and certain diseases. This vast variation can make it difficult it to characterize and compare the structure of the cortex between different species, ages and diseases. To address this, Wang et al. developed a new mathematical model for describing the shape of the cortex. The model uses a method known as coarse graining to erase, or 'melt away', any cortical folds or structures smaller than a given threshold size. As this threshold increases, the cortex becomes progressively smoother. The relationship between surface areas and threshold sizes indicates the fractal dimension ­ that is, how fragmented the cortex is across different scales. Wang et al. applied their model to the brain scans of eleven primates, including humans, and found the fractal dimension of the cortex was almost exactly 2.5 for all eleven species. This suggests that the cortices of the different primates follow a single fractal shape, which means the folds of each cortex have a similar branching pattern. Although there were distinctions between the species, they were mainly due to the different ranges of fold sizes in each cortex. The model revealed that the broader the range of fold sizes, the more folded the brain ­ but the fractal pattern remains the same. The brain melting method created by Wang et al. provides a new way to characterise cortical shape. Besides revealing a hitherto hidden regularity of nature, they hope that in the future their new method will be useful in assessing brain changes during human development and ageing, and in diseases like Alzheimer's and epilepsy.

Ecological correlates of chimpanzee termite fishing behavior in Mbam & Djerem National Park, Cameroon.

Chimpanzee insectivory is seasonally variable, with pronounced peaks or set seasonal periods of consumption observed in most chimpanzee communities. This variation is interesting given that chimpanzees invest considerable effort into complex tool-using behaviors to acquire insect prey. Evidence suggests this seasonal variation is related to insect behavior, but few studies have been done to empirically examine this relationship. In this study, we assessed whether a seasonal pattern of termite fishing by Nigeria-Cameroon chimpanzees (Pan troglodytes ellioti) in Mbam & Djerem National Park, Cameroon was driven by termite behavior. We measured termite presence and termite foraging activity monthly at seven termite mounds near Ganga Research Station from April 2022 to April 2023. Macroscopic fecal analysis and camera traps placed at each mound demonstrated termite fishing in this community occurred from March to June, with a rare smaller period of termite fishing in October 2021. Average monthly rainfall, average monthly temperature, and average monthly fruit availability were used to examine potential environmental factors that could impact termite fishing seasonality. Termite presence was significantly different between months with and without chimpanzee termite fishing (t-test, -6.569, p < .001). Termite presence was also significantly associated with average monthly rainfall (ANOVA, F = 13.9, p = .002, R 2 = .775). Termites in this region appear to respond to the transition from dry to wet seasons by moving closer to the soil surface. This corresponds with greater chimpanzee termite fishing, suggesting that termite accessibility may be driving seasonal variation in this behavior.

Comparative analysis of the chimpanzee and human brain superficial structural connectivities.

Diffusion MRI tractography (dMRI) has fundamentally transformed our ability to investigate white matter pathways in the human brain. While long-range connections have extensively been studied, superficial white matter bundles (SWMBs) have remained a relatively underexplored aspect of brain connectivity. This study undertakes a comprehensive examination of SWMB connectivity in both the human and chimpanzee brains, employing a novel combination of empirical and geometric methodologies to classify SWMB morphology in an objective manner. Leveraging two anatomical atlases, the Ginkgo Chauvel chimpanzee atlas and the Ginkgo Chauvel human atlas, comprising respectively 844 and 1375 superficial bundles, this research focuses on sparse representations of the morphology of SWMBs to explore the little-understood superficial connectivity of the chimpanzee brain and facilitate a deeper understanding of the variability in shape of these bundles. While similar, already well-known in human U-shape fibers were observed in both species, other shapes with more complex geometry such as 6 and J shapes were encountered. The localisation of the different bundle morphologies, putatively reflecting the brain gyrification process, was different between humans and chimpanzees using an isomap-based shape analysis approach. Ultimately, the analysis aims to uncover both commonalities and disparities in SWMBs between chimpanzees and humans, shedding light on the evolution and organization of these crucial neural structures.

Novel Evolution of Mineralocorticoid Receptor in Humans Compared to Chimpanzees, Gorillas, and Orangutans.

We identified five distinct full-length human mineralocorticoid receptor (MR) genes containing either 984 amino acids (MR-984) or 988 amino acids (MR-988), which can be distinguished by the presence or absence of Lys, Cys, Ser, and Trp (KCSW) in their DNA-binding domain (DBD) and mutations at codons 180 and 241 in their amino-terminal domain (NTD). Two human MR-KCSW genes contain either (Val-180, Val-241) or (Ile-180, Val-241) in their NTD, and three human MR-984 genes contain either (Ile-180, Ala-241), (Val-180, Val-241), or (Ile-180, Val-241). Human MR-KCSW with (Ile-180, Ala-241) has not been cloned. In contrast, chimpanzees contain four MRs: two MR-988s with KCSW in their DBD, or two MR-984s without KCSW in their DBD. Chimpanzee MRs only contain (Ile180, Val-241) in their NTD. A chimpanzee MR with either (Val-180, Val-241) or (Ile-180, Ala-241) in the NTD has not been cloned. Gorillas and orangutans each contain one MR-988 with KCSW in the DBD and one MR-984 without KCSW, and these MRs only contain (Ile-180, Val-241) in their NTD. A gorilla MR or orangutan MR with either (Val-180, Val-241) or (Ile-180, Ala-241) in the NTD has not been cloned. Together, these data suggest that human MRs with (Val-180, Val-241) or (Ile-180, Ala-241) in the NTD evolved after humans and chimpanzees diverged from their common ancestor. Considering the multiple functions in human development of the MR in kidney, brain, heart, skin, and lungs, as well as MR activity in interaction with the glucocorticoid receptor, we suggest that the evolution of human MRs that are absent in chimpanzees may have been important in the evolution of humans from chimpanzees. Investigation of the physiological responses to corticosteroids mediated by the MR in humans, chimpanzees, gorillas, and orangutans may provide insights into the evolution of humans and their closest relatives.

Chimpanzees (Pan troglodytes) recognize that their guesses could be wrong and can pass a two-cup disjunctive syllogism task.

When chimpanzees search for hidden food, do they realize that their guesses may not be correct? We applied a post-decision wagering paradigm to a simple two-cup search task, varying whether we gave participants visual access to the baiting and then asking after they had chosen one of the cups whether they would prefer a smaller but certain reward instead of their original choice (experiment 1). Results showed that chimpanzees were more likely to accept the smaller reward in occluded than visible conditions. Experiment 2 found the same effect when we blocked visual access but manipulated the number of hiding locations for the food piece, showing that the effect is not owing to representation type. Experiments 3 and 4 showed that when given information about the contents of the unchosen cup, chimpanzees were able to flexibly update their choice behaviour accordingly. These results suggest that language is not a pre-requisite to solving the disjunctive syllogism and provides a valuable contribution to the debate on logical reasoning in non-human animals.

Origin of the human malaria parasite Plasmodium vivax.

The geographic origin of Plasmodium vivax, a leading cause of human malaria, has been the subject of much speculation. Here we review the evolutionary history of P. vivax and P. vivax-like parasites in humans and non-human primates on three continents, providing overwhelming evidence for an African origin. This conclusion is consistent with recent reports showing that Duffy-negative humans in Africa are, in fact, susceptible to P. vivax, with parasites invading Duffy-antigen-expressing erythroid precursors. Thus, the African origin of P. vivax not only explains the distribution of the Duffy-negative genotype but also provides new insight into the history and status of P. vivax malaria in Africa and efforts geared toward its eradication.

Removing snares is an effective conservation intervention: a case study involving chimpanzees.

Wild chimpanzees (Pan troglodytes) are caught in snares set for other animals and sometimes injure or lose body parts. Snaring can compromise the health, growth, survival, and behavior of chimpanzees and, thus, represents a threat for the conservation of this endangered species. During a long-term study of chimpanzees at Ngogo in Kibale National Park, Uganda, we started a project to remove snares in and around their territory. We compared the number of times chimpanzees were snared during the 12.75 years after the start of this project with the number of times individuals were snared during the previous 14 years. Only one chimpanzee was snared after we began removing snares compared with 12 individuals caught during the period before. This represents a clear reduction in the risk created by snaring at this site and suggests that removing snares can be employed to protect chimpanzees.

Cardiac differentiation of chimpanzee induced pluripotent stem cell lines with different subspecies backgrounds.

The comparative analysis between humans and non-human primates is an instrumental approach for elucidating the evolutional traits and disease propensity of humans. However, in primates, cross-species analyses of their developmental events have encountered constraints because of the ethical and technical limitations in available sample collection, sequential monitoring, and manipulations. In an endeavor to surmount these challenges, in recent years, induced pluripotent stem cells (iPSCs) have garnered escalating interest as an in vitro tool for cross-species analyses between humans and non-human primates. Meanwhile, compared to humans, there is less information on in vitro differentiation of non-human primate iPSCs, and their genetic diversity including subspecies may cause different eligibility to in vitro differentiation methods. Therefore, antecedent to embarking on a comparative analysis to humans, it is a prerequisite to develop the efficacious methodologies for in vitro differentiation regardless of the intraspecies genetic background in non-human primates. In this study, we executed the in vitro differentiation of cardiomyocytes from four chimpanzee iPSC lines with different subspecies and individual backgrounds. To induce cardiomyocytes from chimpanzee iPSCs, we evaluated our methodology for in vitro cardiac differentiation of human iPSCs. Eventually, with minor alterations, our cardiac differentiation method was applicable to all chimpanzee iPSC lines tested as assessed by the expression of cardiac marker genes and the beating ability. Hence, our in vitro differentiation method will advance iPSC-based research of chimpanzee cardiac development and also hold possible utility to cross-species analyses among primate species.

The expression of empathy in human's closest relatives, bonobos and chimpanzees: current and future directions.

Empathy is a complex, multi-dimensional capacity that facilitates the sharing and understanding of others' emotions. As our closest living relatives, bonobos (Pan paniscus) and chimpanzees (P. troglodytes) provide an opportunity to explore the origins of hominin social cognition, including empathy. Despite certain assumptions that bonobos and chimpanzees may differ empathically, these species appear to overlap considerably in certain socio-emotional responses related to empathy. However, few studies have systematically tested for species variation in Pan empathic or socio-emotional tendencies. To address this, we synthesise the growing literature on Pan empathy to inform our understanding of the selection pressures that may underlie the evolution of hominin empathy, and its expression in our last common ancestor. As bonobos and chimpanzees show overlaps in their expression of complex socio-emotional phenomena such as empathy, we propose that group comparisons may be as or more meaningful than species comparisons when it comes to understanding the evolutionary pressures for such behaviour. Furthermore, key differences, such as how humans and Pan communicate, appear to distinguish how we experience empathy compared to our closest living relatives.

Savanna chimpanzee (Pan troglodytes) crop feeding at Dindefelo, Senegal: challenges and implications for conservation.

Chimpanzees (Pan troglodytes) are categorized as Endangered by the International Union for Conservation of Nature, and habitat loss due to conversion of land for agriculture is one of the major threats to wild populations of this species. This challenging scenario can lead to negative human-chimpanzee interactions, including crop feeding. Chimpanzees consume crops across their geographical range, although little is known about this behavior in savanna habitats. Here we provide new evidence of crop feeding by savanna chimpanzees. We conducted our observations at Dindefelo, a community nature reserve in southeastern Senegal. The chimpanzees were observed to feed on mango (Mangifera indica) and also on baobab (Adansonia digitata), a wild species considered a crop by local people when found in and around villages. Although local people use the fruits of these species for food and income, they tolerated crop-feeding events until recently. In 2023, a case of harassment of a crop-feeding chimpanzee in a mango orchard was witnessed, and four days later a chimpanzee corpse was found at the same place. We conclude that habitat conversion into agricultural fields, uncontrolled bush fires and extraction of wild fruits are the important factors influencing crop-feeding events at Dindefelo. Our findings highlight the need to better understand human-chimpanzee interactions in the anthropogenic landscape of Dindefelo to help mitigate negative attitudes and behaviors towards chimpanzees.

Measuring heart rate in captive chimpanzees without anesthesia.

Heart rate measurements can be useful for the monitoring of both physical and mental condition in humans and nonhuman animals. Yet, information about heart rates in chimpanzees, who are phylogenetically the closest species to humans, is scarce. Existing data on chimpanzee heart rates have mainly been collected from chimpanzees under anesthesia. To address this issue, we conducted electrocardiogram recordings in captive chimpanzees under normal conditions without anesthesia based on positive reinforcement training. We obtained a total of 771 recordings from 35 individuals (22 males and 13 females, 14-53 years old) with no cardiac problems. The females had a higher heart rate than the male chimpanzees, and heart rate decreased as a function of age. In addition, heart rate was lower in the morning and increased during the day. Overall, the mean heart rate of adult males was 86.5 beats/min, and that of female chimpanzees 106.4 beats/min. Our data could serve as a reference point for future research and health-based monitoring of chimpanzee heart rates.

Differences in expression of male aggression between wild bonobos and chimpanzees.

Researchers investigating the evolution of human aggression look to our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), as valuable sources of comparative data.1,2 Males in the two species exhibit contrasting patterns: male chimpanzees sexually coerce females3,4,5,6,7,8 and sometimes kill conspecifics,9,10,11,12 whereas male bonobos exhibit less sexual coercion13,14 and no reported killing.13 Among the various attempts to explain these species differences, the self-domestication hypothesis proposes negative fitness consequences of male aggression in bonobos.2,15,16 Nonetheless, the extent to which these species differ in overall rates of aggression remains unclear due to insufficiently comparable observation methods.17,18,19,20,21,22,23 We used 14 community-years of focal follow data-the gold standard for observational studies24-to compare rates of male aggression in 3 bonobo communities at the Kokolopori Bonobo Reserve, Democratic Republic of Congo, and 2 chimpanzee communities at Gombe National Park, Tanzania. As expected, given that females commonly outrank males, we found that bonobos exhibited lower rates of male-female aggression and higher rates of female-male aggression than chimpanzees. Surprisingly, we found higher rates of male-male aggression among bonobos than chimpanzees even when limiting analyses to contact aggression. In both species, more aggressive males obtained higher mating success. Although our findings indicate that the frequency of male-male aggression does not parallel species difference in its intensity, they support the view that contrary to male chimpanzees, whose reproductive success depends on strong coalitions, male bonobos have more individualistic reproductive strategies.25.

Ape recognition of familiar human faces changed by time and COVID-19 face masks.

Reports of primates being able to recognise familiar humans are rare in the literature and tend to be regarded as anecdotal. The COVID-19 pandemic created two unique conditions facilitating the observation of spontaneous face recognition in zoo apes: i) lengthy gaps in contact with human visitors due to lockdowns and zoo closures, and ii) the wearing of face masks obscuring at least half the face of familiar individuals. Here, I report on the historical context of the familiarity between a primatologist and individual apes of two species, how those apes consistently showed recognition of this particular human over a time span of up to thirty years, how facial recognition was extended to family members, and how recognition persisted even when a significant portion of the face was obscured by a mask. This constitutes, to my knowledge, the first documented cases of recognition of familiar human faces changed by time and COVID-19 face masks in two great ape species. Although based on just two individuals, the documentation of this ability is important because it arose in a more naturalistic and spontaneous context compared to typical face processing research in which primates are tested with experimental stimuli in a laboratory setting. Implications for face processing theory and applications for the therapeutic utility of faces are discussed. These observations provide insight into the evolutionary origins of face recognition and, sitting at the interface of science and society, are of interest to a wide audience.

Minimal Compositionality versus Bird Implicatures: two theories of ABC-D sequences in Japanese tits.

It was argued in a series of experimental studies that Japanese tits (Parus minor) have an ABC call that has an alert function, a D call that has a recruitment function, and an ABC-D call that is compositionally derived from ABC and D, and has a mobbing function. A key conclusion was that ABC-D differs from the combination of separate utterances of ABC and of D (e.g. as played by distinct but close loudspeakers). While the logic of the argument is arguably sound, no explicit rule has been proposed to derive the meaning of ABC-D from that of its parts. We compare two analyses. One posits a limited instance of semantic compositionality ('Minimal Compositionality'); the other does without compositionality, but uses instead a more sophisticated pragmatics ('Bird Implicatures'). Minimal Compositionality takes the composition of ABC and D to deviate only minimally from what would be found with two independent utterances: ABC means that 'there is something that licenses an alert', D means that 'there is something that licenses recruitment', and ABC-D means that 'there is something that licenses both an alert and recruitment'. By contrast, ABC and D as independent utterances yield something weaker, namely: 'there is something that licenses an alert, and there is something that licenses recruitment', without any 'binding' across the two utterances. The second theory, Bird Implicatures, only requires that ABC-D should be more informative than ABC, and/or than D. It builds on the idea, proposed for several monkey species, that a less-informative call competes with a more informative one (the 'Informativity Principle'): when produced alone, ABC and D trigger an inference that ABC-D is false. We explain how both Minimal Compositionality and Bird Implicatures could have evolved, and we compare the predictions of the two theories. Finally, we extend the discussion to some chimpanzee and meerkat sequences that might raise related theoretical problems.

Comprehensive characterization of ERV-K (HML-8) in the chimpanzee genome revealed less genomic activity than humans.

Endogenous retroviruses (ERVs) originate from ancestral germline infections caused by exogenous retroviruses. Throughout evolution, they have become fixed within the genome of the animals into which they were integrated. As ERV elements coevolve with the host, they are normally epigenetically silenced and can become upregulated in a series of physiological and pathological processes. Generally, a detailed ERV profile in the host genome is critical for understanding the evolutionary history and functional performance of the host genome. We previously characterized and cataloged all the ERV-K subtype HML-8 loci in the human genome; however, this has not been done for the chimpanzee, the nearest living relative of humans. In this study, we aimed to catalog and characterize the integration of HML-8 in the chimpanzee genome and compare it with the integration of HML-8 in the human genome. We analyzed the integration of HML-8 and found that HML-8 pervasively invaded the chimpanzee genome. A total of 76 proviral elements were characterized on 23/24 chromosomes, including detailed elements distribution, structure, phylogeny, integration time, and their potential to regulate adjacent genes. The incomplete structure of HML-8 proviral LTRs will undoubtedly affect their activity. Moreover, the results indicated that HML-8 integration occurred before the divergence between humans and chimpanzees. Furthermore, chimpanzees include more HML-8 proviral elements (76 vs. 40) and fewer solo long terminal repeats (LTR) (0 vs. 5) than humans. These results suggested that chimpanzee genome activity is less than the human genome and that humans may have a better ability to shape and screen integrated proviral elements. Our work is informative in both an evolutionary and a functional context for ERVs.

Neuroscience of taste: unlocking the human taste code.

Since antiquity human taste has been divided into 4-5 taste qualities. We realized in the early 1970s that taste qualities vary between species and that the sense of taste in species closer to humans such as primates should show a higher fidelity to human taste qualities than non-primates (Brouwer et al. in J Physiol 337:240, 1983). Here we present summary results of behavioral and single taste fiber recordings from the distant South American marmoset, through the Old World rhesus monkey to chimpanzee, the phylogenetically closest species to humans. Our data show that in these species taste is transmitted in labelled-lines to the CNS, so that when receptors on taste bud cells are stimulated, the cell sends action potentials through single taste nerve fibers to the CNS where they create taste, whose quality depends on the cortical area stimulated. In human, the taste qualites include, but are perhaps not limited to sweet, sour, salty, bitter and umami. Stimulation of cortical taste areas combined with inputs from internal organs, olfaction, vision, memory etc. leads to a choice to accept or reject intake of a compound. The labelled-line organization of taste is another example of Müller's law of specific nerve energy, joining other somatic senses such as vision (Sperry in J Neurophysiol 8:15-28, 1945), olfaction (Ngai et al. in Cell 72:657-666, 1993), touch, temperature and pain to mention a few.