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Open access funding provided by Projekt DEAL. AM, CC, and RMW were supported by the Max Planck Society; AM was supported by the Wenner Gren Foundation (Grant Number 9095); CC was supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement no. 679787). Research at the Taï Chimpanzee Project has been funded by the Max Planck Society since 1997. ; In many group-living animal species, interactions take place in changing social environments, increasing the information processing necessary to optimize social decision-making. Communities with different levels of spatial and temporal cohesion should differ in the predictability of association patterns. While the focus in this context has been on primate species with high fission-fusion dynamics, little is known about the variability of association patterns in species with large groups and high temporal cohesion, where group size and the environment create unstable subgroups. Here, we use sooty mangabeys as a model species to test predictability on two levels: on the subgroup level and on the dyadic level. Our results show that the entirety of group members surrounding an individual is close to random in sooty mangabeys; making it unlikely that individuals can predict the exact composition of bystanders for any interaction. At the same time, we found predictable dyadic associations based on assortative mixing by age, kinship, reproductive state in females, and dominance rank; potentially providing individuals with the ability to partially predict which dyads can be usually found together. These results indicate that animals living in large cohesive groups face different challenges from those with high fission-fusion dynamics, by having to adapt to fast-changing social contexts, while unable to predict who will be close-by in future interactions. At the same time, entropy measures on their own are unable to capture the predictability of association patterns in these groups. ; Publisher PDF ; Peer reviewed

AbstractThe onset of intentional communication in children's first year of life represents a major milestone in human cognitive development. Similarly, it is well established that our closest living relatives, the great apes, communicate with signals characterized by at least first‐order intentionality. Despite the well‐documented influence of developmental experiences on socio‐cognitive abilities in apes, the developmental trajectory of intentional signal use as well as effects of social exposure remain poorly understood under naturalistic conditions. Here, we addressed these issues by studying the ontogeny of intentional communication in chimpanzee infants of two subspecies (Pan troglodytes schweinfurthii/verus) and communities living in their natural environments. Overall, we found that gestures and bimodal signal combinations were most commonly accompanied by markers of intentional communication: audience checking, persistence to the goal, and sensitivity to recipient's attentional state. Within individuals, the proportion of communicative behaviours associated with goal persistence and sensitivity to attention increased with age. Cross‐sectional comparisons between infants revealed an age effect on the use of audience checking. Context, interaction partner and site affiliation affected the production of specific markers irrespective of infants' age. The present study provided hitherto undocumented evidence for the development of three important markers of intentional communication in great apes. Moreover, our results suggest that social exposure impacts early intentional signal use.

The study was funded by the Leverhulme Trust, the British Academy, the Max Planck Society, the Leakey Foundation, and the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant agreement nos. 679787 and 283871) ; Adjusting communication to take into account information available to one's audience is routine in humans but is assumed absent in other animals, representing a recent development on the lineage leading to humans. This assumption may be premature. Recent studies show changes in primate alarm signaling to threats according to the receivers' risk. However, a classic problem in these and other perspective-taking studies is discerning whether signalers understand the receivers' mental states or simply are responding to their behavior. We designed experiments to exclude concurrent reading of the receivers' behavior by simulating receivers using prerecorded calls of other group members. Specifically, we tested whether wild chimpanzees emitted differing signals in response to a snake model when simulated receivers previously emitted either snake-related calls (indicating knowledge) or acoustically similar non-snake-related calls (indicating ignorance). Signalers showed more vocal and nonvocal signaling and receiver-directed monitoring when simulated receivers had emitted non-snake-related calls. Results were not explained by signaler arousal nor by receiver identity. We conclude that chimpanzees are aware enough of another's perspective to target information toward ignorant group members, suggesting that the integration of signaling and social cognition systems was already emerging in early hominoid lineages before the advent of more language-specific features, such as syntax. ; Publisher PDF ; Peer reviewed

AbstractThe 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.

AbstractPostnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one‐species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter‐individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d'Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter‐individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development.

AM, AP, LS, CC, and RW were supported by the Max Planck Society; AM was supported by the Wenner Gren Foundation (Grant Number 9095) and the British Academy Newton International Fellowship; AP was supported by the Leakey Foundation; LS was supported by the Minerva Foundation; JG was supported by an NSF Graduate Research Fellowship (DGE-1142336), the Canadian Institutes of Health Research's Strategic Training Initiative in Health Research's Systems Biology Training Program, an NSERC Vanier Canada Graduate Scholarship (CGS), and a long-term Research Grant from the German Academic Exchange Service (DAAD-91525837-57048249). CC was supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement no. 679787). RW was supported by DFG Researcher Unit (FOR 2136) Sociality and Health in Primates (WI 2637/3-1). Research at the Taï Chimpanzee Project has been funded by the Max Planck Society since 1997. ; Predictability of social interactions can be an important measure for the social complexity of an animal group. Predictability is partially dependent on how consistent interaction patterns are over time: does the behavior on 1 day explain the behavior on another? We developed a consistency measure that serves two functions: detecting which interaction types in a dataset are so inconsistent that including them in further analyses risks introducing unexplained error; and comparatively quantifying differences in consistency within and between animal groups. We applied the consistency measure to simulated data and field data for one group of sooty mangabeys (Cercocebus atys atys) and to groups of Western chimpanzees (Pan troglodytes verus) in the Taï National Park, Côte d'Ivoire, to test its properties and compare consistency across groups. The consistency measures successfully identified interaction types whose low internal consistency would likely create analytical problems. Species-level differences in consistency were less pronounced than differences within groups: in all groups, aggression and dominance interactions were the most consistent, followed by grooming; spatial proximity at different levels was much less consistent than directed interactions. Our consistency measure can facilitate decision making of researchers wondering whether to include interaction types in their analyses or social networks and allows us to compare interaction types within and between species regarding their predictability. ; Publisher PDF ; Peer reviewed

This research was funded by The European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (Grant Agreement No 679787), awarded to CC and the Research Council of Norway (SFF-III 223257/F50). ; Investigating the repeatability of trait variation between individuals, that is the amount of individual variation in relation to overall phenotypic variation, indicates an upper level of heritability and reveals whether a given trait may be subject to selection. Labile traits are characterized by high levels of flexibility and consequently low trait repeatability is expected. Indeed, research examining glucocorticoid levels in various non-mammal species found low repeatability scores. However, mammals may be different in this respect as (i) differential maternal care early in life has the potential to prime hypothalamic-pituitary-adrenal axis functioning and (ii) allelic variation affecting hypothalamic-pituitary-adrenal axis functioning has been reported. Individuals often differ from each other in average and/or plastic labile trait expression, two aspects that can be described using a reaction norm approach. Both consistent and flexible reaction norm expression has been argued to serve adaptive purposes, depending on the stability and predictability of environmental conditions. Here, we investigated both trait and reaction norm repeatability of urinary cortisol levels in wild adult male chimpanzees. To capture the expression of the circadian urinary cortisol rhythm of individual males over time, urine samples were collected throughout the day. In total data of 30 males collected over a period of 8 years were included in the dataset. No male was sampled over the whole 8-year period however. We found minor levels of trait repeatability but considerable reaction norm repeatability. This implies a minor role of genetic or priming factors on cortisol excretion, but reveals that males differ consistently in average urinary cortisol levels and the shape of the circadian urinary cortisol rhythm. Relating these results to fitness parameters will provide answers to questions on the adaptive value of reaction norm repeatability of this labile hormonal trait in the future. ; Publisher PDF ; Peer reviewed