Detailed mapping of the complex fiber structure and white matter pathways of the chimpanzee brain.

Long-standing questions about human brain evolution may only be resolved through comparisons with close living evolutionary relatives, such as chimpanzees. This applies in particular to structural white matter (WM) connectivity, which continuously expanded throughout evolution. However, due to legal restrictions on chimpanzee research, neuroscience research currently relies largely on data with limited detail or on comparisons with evolutionarily distant monkeys. Here, we present a detailed magnetic resonance imaging resource to study structural WM connectivity in the chimpanzee. This open-access resource contains (1) WM reconstructions of a postmortem chimpanzee brain, using the highest-quality diffusion magnetic resonance imaging data yet acquired from great apes; (2) an optimized and validated method for high-quality fiber orientation reconstructions; and (3) major fiber tract segmentations for cross-species morphological comparisons. This dataset enabled us to identify phylogenetically relevant details of the chimpanzee connectome, and we anticipate that it will substantially contribute to understanding human brain evolution.

Protracted development of stick tool use skills extends into adulthood in wild western chimpanzees.

Tool use is considered a driving force behind the evolution of brain expansion and prolonged juvenile dependency in the hominin lineage. However, it remains rare across animals, possibly due to inherent constraints related to manual dexterity and cognitive abilities. In our study, we investigated the ontogeny of tool use in chimpanzees (Pan troglodytes), a species known for its extensive and flexible tool use behavior. We observed 70 wild chimpanzees across all ages and analyzed 1,460 stick use events filmed in the Taï National Park, Côte d'Ivoire during the chimpanzee attempts to retrieve high-nutrient, but difficult-to-access, foods. We found that chimpanzees increasingly utilized hand grips employing more than 1 independent digit as they matured. Such hand grips emerged at the age of 2, became predominant and fully functional at the age of 6, and ubiquitous at the age of 15, enhancing task accuracy. Adults adjusted their hand grip based on the specific task at hand, favoring power grips for pounding actions and intermediate grips that combine power and precision, for others. Highly protracted development of suitable actions to acquire hidden (i.e., larvae) compared to non-hidden (i.e., nut kernel) food was evident, with adult skill levels achieved only after 15 years, suggesting a pronounced cognitive learning component to task success. The prolonged time required for cognitive assimilation compared to neuromotor control points to selection pressure favoring the retention of learning capacities into adulthood.

Selective deforestation and exposure of African wildlife to bat-borne viruses.

Proposed mechanisms of zoonotic virus spillover often posit that wildlife transmission and amplification precede human outbreaks. Between 2006 and 2012, the palm Raphia farinifera, a rich source of dietary minerals for wildlife, was nearly extirpated from Budongo Forest, Uganda. Since then, chimpanzees, black-and-white colobus, and red duiker were observed feeding on bat guano, a behavior not previously observed. Here we show that guano consumption may be a response to dietary mineral scarcity and may expose wildlife to bat-borne viruses. Videos from 2017-2019 recorded 839 instances of guano consumption by the aforementioned species. Nutritional analysis of the guano revealed high concentrations of sodium, potassium, magnesium and phosphorus. Metagenomic analyses of the guano identified 27 eukaryotic viruses, including a novel betacoronavirus. Our findings illustrate how "upstream" drivers such as socioeconomics and resource extraction can initiate elaborate chains of causation, ultimately increasing virus spillover risk.

Chaos and COSMOS-Considerations on QSM methods with multiple and single orientations and effects from local anisotropy.

PURPOSE: Field-to-susceptibility inversion in quantitative susceptibility mapping (QSM) is ill-posed and needs numerical stabilization through either regularization or oversampling by acquiring data at three or more object orientations. Calculation Of Susceptibility through Multiple Orientations Sampling (COSMOS) is an established oversampling approach and regarded as QSM gold standard. It achieves a well-conditioned inverse problem, requiring rotations by 0°, 60° and 120° in the yz-plane. However, this is impractical in vivo, where head rotations are typically restricted to a range of ±25°. Non-ideal sampling degrades the conditioning with residual streaking artifacts whose mitigation needs further regularization. Moreover, susceptibility anisotropy in white matter is not considered in the COSMOS model, which may introduce additional bias. The current work presents a thorough investigation of these effects in primate brain. METHODS: Gradient-recalled echo (GRE) data of an entire fixed chimpanzee brain were acquired at 7 T (350 µm resolution, 10 orientations) including ideal COSMOS sampling and realistic rotations in vivo. Comparisons of the results included ideal COSMOS, in-vivo feasible acquisitions with 3-8 orientations and single-orientation iLSQR QSM. RESULTS: In-vivo feasible and optimal COSMOS yielded high-quality susceptibility maps with increased SNR resulting from averaging multiple acquisitions. COSMOS reconstructions from non-ideal rotations about a single axis required additional L2-regularization to mitigate residual streaking artifacts. CONCLUSION: In view of unconsidered anisotropy effects, added complexity of the reconstruction, and the general challenge of multi-orientation acquisitions, advantages of sub-optimal COSMOS schemes over regularized single-orientation QSM appear limited in in-vivo settings.

Chimpanzees make tactical use of high elevation in territorial contexts.

Tactical warfare is considered a driver of the evolution of human cognition. One such tactic, considered unique to humans, is collective use of high elevation in territorial conflicts. This enables early detection of rivals and low-risk maneuvers, based on information gathered. Whether other animals use such tactics is unknown. With a unique dataset of 3 years of simultaneous behavioral and ranging data on 2 neighboring groups of western chimpanzees, from the Taï National Park, Côte d'Ivoire, we tested whether chimpanzees make decisions consistent with tactical use of topography to gain an advantage over rivals. We show that chimpanzees are more likely to use high hills when traveling to, rather than away from, the border where conflict typically takes place. Once on border hills, chimpanzees favor activities that facilitate information gathering about rivals. Upon leaving hills, movement decisions conformed with lowest risk engagement, indicating that higher elevation facilitates the detection of rivals presence or absence. Our results support the idea that elevation use facilitated rival information gathering and appropriate tactical maneuvers. Landscape use during territorial maneuvers in natural contexts suggests chimpanzees seek otherwise inaccessible information to adjust their behavior and points to the use of sophisticated cognitive abilities, commensurate with selection for cognition in species where individuals gain benefits from coordinated territorial defense. We advocate territorial contexts as a key paradigm for unpicking complex animal cognition.

Social uncertainty promotes signal complexity during approaches in wild chimpanzees (Pan troglodytes verus) and mangabeys (Cercocebus atys atys).

The social complexity hypothesis for the evolution of communication posits that complex social environments require greater communication complexity for individuals to effectively manage their relationships. We examined how different socially uncertain contexts, reflecting an increased level of social complexity, relate to variation in signalling within and between two species, which display varying levels of fission-fusion dynamics (sympatric-living chimpanzees and sooty mangabeys, Taï National Park, Ivory Coast). Combined signalling may improve message efficacy, notably when involving different perception channels, thus may increase in moments of high social uncertainty. We examined the probability of individuals to emit no signal, single or multisensory or combined (complex) signals, during social approaches which resulted in non-agonistic outcomes. In both species, individuals were more likely to use more combined and multisensory signals in post-conflict approaches with an opponent than in other contexts. The clearest impact of social uncertainty on signalling complexity was observed during chimpanzee fusions, where the likelihood of using complex signals tripled relative to other contexts. Overall, chimpanzees used more multisensory signals than mangabeys. Social uncertainty may shape detected species differences in variation in signalling complexity, thereby supporting the hypothesis that social complexity, particularly associated with high fission-fusion dynamics, promotes signalling complexity.

Chimpanzees show the capacity to communicate about concomitant daily life events.

One universal feature of human language is its versatility in communicating about juxtapositions of everyday events. Versatile combinatorial systems of communication can be selected for if (a) several vocal units are flexibly combined into numerous and long vocal sequences and (b) vocal sequences relate to numerous daily life events. We propose (b) is more likely during simultaneous or serial (concomitant) events than single events. We analyzed 9,391 vocal utterances across the repertoire of wild chimpanzees and their events of production. Chimpanzees used vocal sequences across a range of daily life events and twice as often during concomitant than single events. Also, utterance diversity correlated positively with event diversity. Our results show the potential of chimpanzee vocal sequences to convey combined information about numerous daily life events, a step from which generalized combinatoriality could have evolved.

Comprehension of own and other species' alarm calls in sooty mangabey vocal development.

Abstract: Primates understand the meaning of their own and other species' alarm calls, but little is known about how they acquire such knowledge. Here, we combined direct behavioural observations with playback experiments to investigate two key processes underlying vocal development: comprehension and usage. Especifically, we studied the development of con- and heterospecific alarm call recognition in free-ranging sooty mangabeys, Cercocebus atys, across three age groups: young juveniles (1-2y), old juveniles (3-4y) and adults (> 5y). We observed that, during natural predator encounters, juveniles alarm called to a significantly wider range of species than adults, with evidence of refinement during the first four years of life. In the experiments, we exposed subjects to leopard, eagle and snake alarm calls given by other group members or sympatric Diana monkeys. We found that young juveniles' locomotor and vocal responses were least appropriate and that they engaged in more social referencing (look at adults when hearing an alarm call) than older individuals, suggesting that vocal competence is obtained via social learning. In conclusion, our results suggest that alarm call comprehension is socially learned during the juvenile stage, with comprehension preceding appropriate usage but no difference between learning their own or other species' alarm calls. Significance statement: Under natural conditions, animals do not just interact with members of their own species, but usually operate in a network of associated species. However, ontogenetic research on primate communication frequently ignores this significant element. We studied the development of con- and heterospecific alarm call recognition in wild sooty mangabeys. We found that communicative competence was acquired during the juvenile stages, with alarm call comprehension learning preceding appropriate vocal usage and with no clear difference in learning of con- and heterospecific signals. We also found that, during early stages of life, social referencing, a proactive form of social learning, was key in the acquisition of competent alarm call behaviour. Our results show that primates equally learn to interpret alarm calls from their own and other species during their early stages of life and that this learning process is refined as the animals mature. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-023-03318-6.

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

High angular resolution susceptibility imaging and estimation of fiber orientation distribution functions in primate brain.

Uncovering brain-tissue microstructure including axonal characteristics is a major neuroimaging research focus. Within this scope, anisotropic properties of magnetic susceptibility in white matter have been successfully employed to estimate primary axonal trajectories using mono-tensorial models. However, anisotropic susceptibility has not yet been considered for modeling more complex fiber structures within a voxel, such as intersecting bundles, or an estimation of orientation distribution functions (ODFs). This information is routinely obtained by high angular resolution diffusion imaging (HARDI) techniques. In applications to fixed tissue, however, diffusion-weighted imaging suffers from an inherently low signal-to-noise ratio and limited spatial resolution, leading to high demands on the performance of the gradient system in order to mitigate these limitations. In the current work, high angular resolution susceptibility imaging (HARSI) is proposed as a novel, phase-based methodology to estimate ODFs. A multiple gradient-echo dataset was acquired in an entire fixed chimpanzee brain at 61 orientations by reorienting the specimen in the magnetic field. The constant solid angle method was adapted for estimating phase-based ODFs. HARDI data were also acquired for comparison. HARSI yielded information on whole-brain fiber architecture, including identification of peaks of multiple bundles that resembled features of the HARDI results. Distinct differences between both methods suggest that susceptibility properties may offer complementary microstructural information. These proof-of-concept results indicate a potential to study the axonal organization in post-mortem primate and human brain at high resolution.

Slow development of vocal sequences through ontogeny in wild chimpanzees (Pan troglodytes verus).

The development of the unique, hierarchical, and endless combinatorial capacity in a human language requires neural maturation and learning through childhood. Compared with most non-human primates, where combinatorial capacity seems limited, chimpanzees present a complex vocal system comprising hundreds of vocal sequences. We investigated how such a complex vocal system develops and the processes involved. We recorded 10,929 vocal utterances of 98 wild chimpanzees aged 0-55 years, from Taï National Park, Ivory Coast. We developed customized Generalized non-Linear Models to estimate the ontogenetic trajectory of four structural components of vocal complexity: utterance length, diversity, probability of panting (requiring phonation across inhalation and exhalation), and probability of producing two adjacent panted units. We found chimpanzees need 10 years to reach adult levels of vocal complexity. In three variables, the steepest increase coincided with the age of first non-kin social interactions (2-5 years), and plateaued in sub-adults (8-10 years), as individuals integrate into adult social life. Producing two adjacent panted units may require more neuromuscular coordination of the articulators, as its emergence and steepest increase appear later in development. These results suggest prolonged maturational processes beyond those hitherto thought likely in species that do not learn their vocal repertoire. Our results suggest that multifaceted ontogenetic processes drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation. As humans live in a complex social world, empirical support for the "social complexity hypothesis" may have relevance for theories of language evolution. RESEARCH HIGHLIGHTS: Chimpanzees need around 10 years to develop the vocal structural complexity present in the adult repertoire, way beyond the age of emergence of every single vocal unit. Multifaceted ontogenetic processes may drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation. Non-linear increases in vocal complexity coincide with social developmental milestones. Vocal sequences requiring rapid articulatory change emerge later than other vocal sequences, suggesting neuro-muscular maturational processes continue through the juvenile years.

Brain structure and function: a multidisciplinary pipeline to study hominoid brain evolution.

To decipher the evolution of the hominoid brain and its functions, it is essential to conduct comparative studies in primates, including our closest living relatives. However, strong ethical concerns preclude in vivo neuroimaging of great apes. We propose a responsible and multidisciplinary alternative approach that links behavior to brain anatomy in non-human primates from diverse ecological backgrounds. The brains of primates observed in the wild or in captivity are extracted and fixed shortly after natural death, and then studied using advanced MRI neuroimaging and histology to reveal macro- and microstructures. By linking detailed neuroanatomy with observed behavior within and across primate species, our approach provides new perspectives on brain evolution. Combined with endocranial brain imprints extracted from computed tomographic scans of the skulls these data provide a framework for decoding evolutionary changes in hominin fossils. This approach is poised to become a key resource for investigating the evolution and functional differentiation of hominoid brains.

Maternal effects on the development of vocal communication in wild chimpanzees.

Early-life experiences, such as maternal care received, influence adult social integration and survival. We examine what changes to social behavior through ontogeny lead to these lifelong effects, particularly whether early-life maternal environment impacts the development of social communication. Chimpanzees experience prolonged social communication development. Focusing on a central communicative trait, the "pant-hoot" contact call used to solicit social engagement, we collected cross-sectional data on wild chimpanzees (52 immatures and 36 mothers). We assessed early-life socioecological impacts on pant-hoot rates across development, specifically: mothers' gregariousness, age, pant-hoot rates and dominance rank, maternal loss, and food availability, controlling for current maternal effects. We found that early-life maternal gregariousness correlated positively with offspring pant-hoot rates, while maternal loss led to reduced pant-hoot rates across development. Males had steeper developmental trajectories in pant-hoot rates than females. We demonstrate the impact of maternal effects on developmental trajectories of a rarely investigated social trait, vocal production.

Patterns and consequences of age-linked change in local relatedness in animal societies.

The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.

Acquisition of predator knowledge from alarm calls via one-trial social learning in monkeys.

How do animals learn to classify the world and what is the role of social learning during this process? Here, we show that young sooty mangabeys, Cercocebus atys, of Taï Forest, Côte d'Ivoire, learn to rapidly classify an unfamiliar predator by attending to others' alarm calls and that such knowledge is retained over long periods. We experimentally exposed subjects to chimeric predator models with both snake- and leopard-like features, combined with playbacks of conspecific snake (N = 12) or leopard alarms (N = 13). Adults classified the chimeras as non-threatening but for juveniles, we found that one single alarm call exposure was sufficient to allocate the chimera to the snake or leopard category, suggesting plausibility judgments in experienced adults. We then retested N = 10 juveniles with the same models more than a year after their first experience and found that they continued to show their original response, indicating long-term retention of socially learned predator categorisation.

Population-specific call order in chimpanzee greeting vocal sequences.

Primates rarely learn new vocalizations, but they can learn to use their vocalizations in different contexts. Such "vocal usage learning," particularly in vocal sequences, is a hallmark of human language, but remains understudied in non-human primates. We assess usage learning in four wild chimpanzee communities of Taï and Budongo Forests by investigating population differences in call ordering of a greeting vocal sequence. Whilst in all groups, these sequences consisted of pant-hoots (long-distance contact call) and pant-grunts (short-distance submissive call), the order of the two calls differed across populations. Taï chimpanzees consistently commenced greetings with pant-hoots, whereas Budongo chimpanzees started with pant-grunts. We discuss different hypotheses to explain this pattern and conclude that higher intra-group aggression in Budongo may have led to a local pattern of individuals signaling submission first. This highlights how within-species variation in social dynamics may lead to flexibility in call order production, possibly acquired via usage learning.

The effect of warning signs on the presence of snare traps in a Ugandan rainforest.

Since chimpanzee (Pan troglodytes) conservation often involves local human populations, conservation strategies must consider psychological factors that impact their behavior. In Budongo Forest, Uganda, for example, local communities commonly engage in snare trap (hereafter: snare) setting for wild meat. This illegal activity posits a substantial threat to wild chimpanzees, causing permanent wounds or death for those who are snared. Despite various schemes previously implemented to address snare setting-an activity that is fueled by poverty, the problem and its detrimental impact on chimpanzees persists. Here, we experimentally tested a novel intervention, a systematic display of specially designed warning signs aimed at local poachers. We monitored the presence of snares before and after introducing these signs over a total period of two years and compared it with that of a similar sized control area with no intervention. Results show that snares were less likely to be present during the "sign" period than during the "non-sign" period in the experimental but not in the control area. We discuss the potential of this cost-effective intervention for limiting illegal activities that pose a severe threat to chimpanzees and other species inhabiting tropical forests.

Dead-infant carrying by chimpanzee mothers in the Budongo Forest.

It has been suggested that non-human primates can respond to deceased conspecifics in ways that suggest they experience psychological states not unlike humans, some of which could indicate they exhibit a notion of death. Here, we report long-term demographic data from two East African chimpanzee groups. During a combined 40-year observation period, we recorded 191 births of which 68 died in infancy, mostly within the first year. We documented the post-mortem behaviour of the mothers and describe nine occasions where Budongo chimpanzee mothers carried infants for 1-3 days after their death, usually until the body started to decompose. We also observed three additional cases of extended carrying lasting for more than 2 weeks, one of which was followed by the unusual extended carrying of an object and another which lasted 3 months. In each case, the corpses mummified. In addition, we report four instances of recurring dead-infant carrying by mothers, three of whom carried the corpse for longer during the second instance. We discuss these observations in view of functional hypotheses of dead-infant carrying in primates and the potential proximate mechanisms involved in this behaviour.