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.

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.

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.

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.

Chimpanzees produce diverse vocal sequences with ordered and recombinatorial properties.

The origins of human language remains a major question in evolutionary science. Unique to human language is the capacity to flexibly recombine a limited sound set into words and hierarchical sequences, generating endlessly new sentences. In contrast, sequence production of other animals appears limited, stunting meaning generation potential. However, studies have rarely quantified flexibility and structure of vocal sequence production across the whole repertoire. Here, we used such an approach to examine the structure of vocal sequences in chimpanzees, known to combine calls used singly into longer sequences. Focusing on the structure of vocal sequences, we analysed 4826 recordings of 46 wild adult chimpanzees from Taï National Park. Chimpanzees produced 390 unique vocal sequences. Most vocal units emitted singly were also emitted in two-unit sequences (bigrams), which in turn were embedded into three-unit sequences (trigrams). Bigrams showed positional and transitional regularities within trigrams with certain bigrams predictably occurring in either head or tail positions in trigrams, and predictably co-occurring with specific other units. From a purely structural perspective, the capacity to organize single units into structured sequences offers a versatile system potentially suitable for expansive meaning generation. Further research must show to what extent these structural sequences signal predictable meanings.

Chimpanzee vowel-like sounds and voice quality suggest formant space expansion through the hominoid lineage.

The origins of human speech are obscure; it is still unclear what aspects are unique to our species or shared with our evolutionary cousins, in part due to a lack of a common framework for comparison. We asked what chimpanzee and human vocal production acoustics have in common. We examined visible supra-laryngeal articulators of four major chimpanzee vocalizations (hoos, grunts, barks, screams) and their associated acoustic structures, using techniques from human phonetic and animal communication analysis. Data were collected from wild adult chimpanzees, Taï National Park, Ivory Coast. Both discriminant and principal component classification procedures revealed classification of call types. Discriminating acoustic features include voice quality and formant structure, mirroring phonetic features in human speech. Chimpanzee lip and jaw articulation variables also offered similar discrimination of call types. Formant maps distinguished call types with different vowel-like sounds. Comparing our results with published primate data, humans show less F1-F2 correlation and further expansion of the vowel space, particularly for [i] sounds. Unlike recent studies suggesting monkeys achieve human vowel space, we conclude from our results that supra-laryngeal articulatory capacities show moderate evolutionary change, with vowel space expansion continuing through hominoid evolution. Studies on more primate species will be required to substantiate this. This article is part of the theme issue 'Voice modulation: from origin and mechanism to social impact (Part II)'.

Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees.

Here we show that sexual signaling affects patterns of female spatial association differently in chimpanzees and bonobos, indicating its relevance in shaping the respective social systems. Generally, spatial association between females often mirrors patterns and strength of social relationships and cooperation within groups. While testing for proposed differences in female-female associations underlying female coalition formation in the species of the genus Pan, we find only limited evidence for a higher female-female gregariousness in bonobos. While bonobo females exhibited a slightly higher average number of females in their parties, there is neither a species difference in the time females spent alone, nor in the number of female party members in the absence of sexually attractive females. We find that the more frequent presence of maximally tumescent females in bonobos is associated with a significantly stronger increase in the number of female party members, independent of variation in a behavioural proxy for food abundance. This indicates the need to look beyond ecology when explaining species differences in female sociality as it refutes the idea that the higher gregariousness among bonobo females is driven by ecological factors alone and highlights that the temporal distribution of female sexual receptivity is an important factor to consider when studying mammalian sociality.

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees.

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

Non-invasive assessment of metabolic responses to food restriction using urinary triiodothyronine and cortisol measurement in macaques.

Regulation of energy allocation and metabolic rate plays an important role in determining behavior and fitness in wild animals, calling for the validation of non-invasive markers of energetic condition. Recently, the thyroid hormone triiodothyronine (T3) has emerged as a promising marker as concentrations decrease to lower the metabolic rate during energetically challenging periods. However, it remains largely unclear whether T3 merely represents an alternative or provides additional information compared to other compounds involved in the regulation of energy acquisition and allocation, like cortisol and C-peptide, as few joint measurements have been conducted to date in non-invasively collected samples. We aimed to validate the non-invasive measurement of immunoreactive urinary total T3 (uTT3), in comparison to urinary cortisol (uCort) and urinary C-peptide (uCP), as a marker of metabolic response to variation in food intake in macaques, and to address a number of issues regarding the collection, storage and processing of samples which are important for application of uTT3 measurements under field conditions. We used daily samples and body mass measures from a prior food restriction-refeeding experiment over 4 weeks with six captive macaques and analyzed concentrations of uTT3 and uCort in samples collected prior to (fasting) and after morning feeding (non-fasting). Concentrations of uTT3 decreased in response to restriction in food supply and were also lower during weeks of food restriction compared to weeks of refeeding. Variation in uTT3 also correlated positively with variation in body mass and concentrations of uCP. As expected, uCort showed the reverse pattern, increasing during food restriction and decreasing following refeeding, but was not associated with variation in body mass. Generally, compared to fasting samples, concentrations were higher in post-morning feeding, i.e. non-fasting, samples for uTT3 but not uCort. Contamination of urine samples with fecal matter, but not soil, and exposure to UV light led to a decrease in uTT3. uTT3 was largely unaffected by repeated freeze-thaw cycles and by refrigeration for medium-term storage (2 days) but degraded substantially when stored at ambient temperature for the same period. In conclusion, uTT3 measurements inform on the effect of food intake and its associated metabolic response to variation in energetic status. Since uTT3 is reasonably robust to many issues associated with collection and storage of urine samples under field conditions, it is a promising biomarker for studies of energetic condition and basal metabolic rate in wild macaques.

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition.

Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The 'interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the 'social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.

Sex-specific association patterns in bonobos and chimpanzees reflect species differences in cooperation.

In several group-living species, individuals' social preferences are thought to be influenced by cooperation. For some societies with fission-fusion dynamics, sex-specific association patterns reflect sex differences in cooperation in within- and between-group contexts. In our study, we investigated this hypothesis further by comparing sex-specific association patterns in two closely related species, chimpanzees and bonobos, which differ in the level of between-group competition and in the degree to which sex and kinship influence dyadic cooperation. Here, we used long-term party composition data collected on five chimpanzee and two bonobo communities and assessed, for each individual of 10 years and older, the sex of its top associate and of all conspecifics with whom it associated more frequently than expected by chance. We found clear species differences in association patterns. While in all chimpanzee communities males and females associated more with same-sex partners, in bonobos males and females tended to associate preferentially with females, but the female association preference for other females is lower than in chimpanzees. Our results also show that, for bonobos (but not for chimpanzees), association patterns were predominantly driven by mother-offspring relationships. These species differences in association patterns reflect the high levels of male-male cooperation in chimpanzees and of mother-son cooperation in bonobos. Finally, female chimpanzees showed intense association with a few other females, and male chimpanzees showed more uniform association across males. In bonobos, the most differentiated associations were from males towards females. Chimpanzee male association patterns mirror fundamental human male social traits and, as in humans, may have evolved as a response to strong between-group competition. The lack of such a pattern in a closely related species with a lower degree of between-group competition further supports this notion.

Comparison of male conflict behavior in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), with specific regard to coalition and post-conflict behavior.

Coalitions among males during within group conflicts have a strong influence on the competitive and social environment within social groups. To evaluate possible variation in the occurrence of such coalitions in our closest relatives, chimpanzees and bonobos, we compared male aggression and coalitionary behavior in two natural communities, one of each species, with a similar size and composition. Furthermore we compared affiliative behavior that might be related to coalition formation among males. We found higher frequencies of aggression and a greater likelihood to form coalitions during within-group conflicts among wild male chimpanzees at Taï compared to wild male bonobos at LuiKotale. The species differed in the predominant sex of the male coalition partners, with male bonobos forming coalitions more often with females, while male chimpanzees formed coalitions more often with other males. Compared to male bonobos, male chimpanzees showed higher rates of grooming and tended to reconcile more conflicts with other males. Overall our results showed lower frequencies of reconciliation among bonobos than those described in captivity and at artificial feeding sites. These findings add to the evidence that male cooperation and conflict resolution are potentially very different in bonobos and chimpanzees, despite the fact that these two species are closely related, live in multi-male, multi-female communities with a high degree of fission-fusion dynamics and have female-biased migration patterns. Given the correlation between aggressive, cooperative and some affiliative patterns within the species in our study, we hypothesize that the fitness benefits of male relationships are greater in chimpanzees compared to bonobos.

Androgen correlates of male reproductive effort in wild male long-tailed macaques (Macaca fascicularis): A multi-level test of the challenge hypothesis.

The challenge hypothesis (Wingfield et al., 1990) has been broadly utilised as a conceptual framework to study male androgen correlates of reproductive challenges in mammals. These studies mainly assessed male androgen responsiveness to a general degree of challenge over extended periods of time. Short term co-variation between the socio-sexual challenging context and androgen levels remains, however, largely understudied. We thus aim at providing a multi-level test of the challenge hypothesis by investigating the inter- and intra-individual variations in faecal androgen excretion associated to 1) breeding seasonality, 2) dominance rank, 3) mate-guarding activity and 4) value of the guarded female. We studied long-tailed macaques, a species in which males engage in highly challenging monopolisation of females over discreet periods of time. This particularity allows testing specifically the predicted increase from level B to level C in the challenge hypothesis. The study was carried out during two reproductive seasons on three groups of wild long-tailed macaques. We combined behavioural observations and non-invasive measurements of faecal androgen metabolite (fAM) levels. We found that, as predicted by the challenge hypothesis, male long-tailed macaques respond not only to seasonal but also to short term reproductive challenges by adapting their androgen levels. First, males exhibited a seasonal rise in fAM levels during the mating period which may be triggered by fruit availability as shown by our phenological data. Second, males had increased androgen levels when mate-guarding females and, across mate-guarding periods, males had higher fAM levels when monopolising high-ranking parous females than when monopolising low-ranking ones. Finally, high-ranking males had higher fAM levels than low-ranking males year round. Our study confirms that, in species with a high degree of female monopolisability, androgen may be an important physiological fitness enhancing tool for males by increasing female monopolisation efficiency (in particular with highly valuable females) and helping males to respond to rank take-over challenges.

Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): physiological stress and aggression.

Mate-guarding is an important determinant of male reproductive success in a number of species. However, it is known to potentially incur costs. The aim of the present study was to assess the effect of mate-guarding on male physiological stress and aggression in long-tailed macaques, a species in which males mate-guard females to a lesser extent than predicted by the Priority of Access model (PoA). The study was carried out during two mating periods on three groups of wild long-tailed macaques in Indonesia by combining behavioral observations with non-invasive measurements of fecal glucocorticoid (fGC) levels. Mate-guarding was associated with a general rise in male stress hormone levels but, from a certain threshold of mate-guarding onwards, increased vigilance time was associated with a decrease in stress hormone output. Mate-guarding also increased male-male aggression rate and male vigilance time. Overall, alpha males were more physiologically stressed than other males independently of mating competition. Increased glucocorticoid levels during mate-guarding are most likely adaptive since it may help males to mobilize extra-energy required for mate-guarding and ultimately maintain a balanced energetic status. However, repeated exposure to high levels of stress over an extended period is potentially deleterious to the immune system and thus may carry costs. This potential physiological cost together with the cost of increased aggression mate-guarding male face may limit the male's ability to mate-guard females, explaining the deviance from the PoA model observed in long-tailed macaques. Comparing our results to previous findings we discuss how ecological factors, reproductive seasonality and rank achievement may modulate the extent to which costs of mate-guarding limit male monopolization abilities.