Coevolution of vocal communication and sociality in primates (original) (raw)
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Social complexity parallels vocal complexity: a comparison of three non-human primate species
Frontiers in Psychology, 2013
Social factors play a key role in the structuring of vocal repertoires at the individual level, notably in non-human primates. Some authors suggested that, at the species level too, social life may have driven the evolution of communicative complexity, but this has rarely been empirically tested. Here, we use a comparative approach to address this issue. We investigated vocal variability, at both the call type and the repertoire levels, in three forest-dwelling species of Cercopithecinae presenting striking differences in their social systems, in terms of social organization as well as social structure. We collected female call recordings from twelve De Brazza's monkeys (Cercopithecus neglectus), six Campbell's monkeys (Cercopithecus campbelli) and seven red-capped mangabeys (Cercocebus torquatus) housed in similar conditions. First, we noted that the level of acoustic variability and individual distinctiveness found in several call types was related to their importance in social functioning. Contact calls, essential to intra-group cohesion, were the most individually distinctive regardless of the species, while threat calls were more structurally variable in mangabeys, the most "despotic" of our three species. Second, we found a parallel between the degree of complexity of the species' social structure and the size, diversity, and usage of its vocal repertoire. Mangabeys (most complex social structure) called twice as often as guenons and displayed the largest and most complex repertoire. De Brazza's monkeys (simplest social structure) displayed the smallest and simplest repertoire. Campbell's monkeys displayed an intermediate pattern.
Social bonding drives vocal exchanges in Bonobos
Scientific Reports
the origin of human speech is still a hotly debated topic in science. evidence of socially-guided acoustic flexibility and proto-conversational rules has been found in several monkey species, but is lacking in social and cooperative great apes. Here we investigated spontaneous vocal interactions within a peaceful context in captive bonobos to reveal that vocal interactions obey temporally and social rules. Dyadic vocal interactions were characterized by call overlap avoidance and short inter-call intervals. Bonobos preferentially responded to conspecifics with whom they maintained close bonds. We also found that vocal sharing rate (production rate of shared acoustic variants within each given dyad) was mostly explained by the age difference of callers, as other individual characteristics (sex, kinship) and social parameters (affinity in spatial proximity and in vocal interactions) were not. Our results show that great apes spontaneously display primitive conversation rules guided by social bonds. The demonstration that such coordinated vocal interactions are shared between monkeys, apes and humans fills a significant gap in our knowledge of vocal communication within the primate phylogeny and highlights the universal feature of social influence in vocal interactions. The evolutionary origins of language and speech remains a fundamental question in science. In particular, whether clues to the origins of speech are present in nonhuman primate communication remains a hotly debated topic 1-4. Despite the diversity of social cultures and languages in humans, universal features in conversations are found across all languages, such as the avoidance of overlapping and a minimum gap between turns 5-8. Orderly vocal exchanges (antiphony between two or more animals or duets within male-female pairs 9) have been found across the primate order: from lemurs 10 , to New World monkeys 11-15 , Old World monkeys 16 and lesser apes 17,18. Vocal turn-taking appears to be associated with social life and cooperation capacities 1,2,5,9,19-21. It is thought to maintain and reinforce social bonds between individuals (e.g. in non-human primates 10,22), enable the extraction of information in the absence of overlap (e.g. 23 but see 24) and reduce stress as in the case of social grooming 25. Vocal exchange is "a characteristic communication style in which a sender produces a vocalization to address a receiver, and the receiver emits a call in response within a brief interval" (cited from 26). Vocal exchange patterns are influenced by social factors in non-human primates. 'Interlocutors' are not randomly selected, and preference is given to elders 11,27-29 , social allies 12,14,22 or dominant individuals 30,31. The attention of the audience also influences vocal outputs leading to persistence (repetition of calls) and elaboration (changes in the acoustic structure of calls) in situations where no response has been received 32,33. Shared primitive forms of vocal turn-taking within non-human primate species might suggest an ancient evolutionary origin 1,34. Surprisingly, however, studies based on great apes are scarce and controversial. No evidence of spontaneous vocal coordinated exchanges has been found in wild chimpanzees 35 , who display complex social interactions and cooperative abilities 36. Indeed, Arcadi 35 found that chimpanzees do not "respond" to the majority of calls they heard (within 5 sec), and that instead, bonded males tend to chorus together, matching each-other's pant hoots 37,38. Nevertheless, a recent study in great apes found for the first time that captive gorillas display some rule-governed call exchanges 31. Relying on our current knowledge, vocal turn-taking is thus reported across phylogenetically distant species (monkeys and more generally in some social mammals such as African elephants 39 , bottlenose dolphins 40 , bats 41,42 , naked mole-rats 43) but with some apparent discontinuities among great apes. More investigations among great ape species, our closest, highly social, relatives, are thus necessary in order to ascertain if vocal-turn taking behavior is as a result of convergent evolution (analogies as adaptations to similar social requirements) or is shared ancestry (homologies which are inheritance behaviours) 34 .
Social learning of vocal structure in a nonhuman primate?
BMC Evolutionary Biology, 2011
Background: Non-human primate communication is thought to be fundamentally different from human speech, mainly due to vast differences in vocal control. The lack of these abilities in non-human primates is especially striking if compared to some marine mammals and bird species, which has generated somewhat of an evolutionary conundrum. What are the biological roots and underlying evolutionary pressures of the human ability to voluntarily control sound production and learn the vocal utterances of others? One hypothesis is that this capacity has evolved gradually in humans from an ancestral stage that resembled the vocal behavior of modern primates. Support for this has come from studies that have documented limited vocal flexibility and convergence in different primate species, typically in calls used during social interactions. The mechanisms underlying these patterns, however, are currently unknown. Specifically, it has been difficult to rule out explanations based on genetic relatedness, suggesting that such vocal flexibility may not be the result of social learning. Results: To address this point, we compared the degree of acoustic similarity of contact calls in free-ranging Campbell's monkeys as a function of their social bonds and genetic relatedness. We calculated three different indices to compare the similarities between the calls' frequency contours, the duration of grooming interactions and the microsatellite-based genetic relatedness between partners. We found a significantly positive relation between bond strength and acoustic similarity that was independent of genetic relatedness. Conclusion: Genetic factors determine the general species-specific call repertoire of a primate species, while social factors can influence the fine structure of some the call types. The finding is in line with the more general hypothesis that human speech has evolved gradually from earlier primate-like vocal communication.
Dominance style is a key predictor of vocal use and evolution across nonhuman primates
Royal Society Open Science, 2021
Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from ‘despotic’ to ‘tolerant’). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocali...
Primate Vocal Communication: A Useful Tool for Understanding Human Speech and Language Evolution?
Human Biology, 2011
Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.
Sociality predicts orangutan vocal phenotype
Nature Ecology & Evolution
In humans, individuals’ social setting determines which and how language is acquired. Social seclusion experiments show that sociality also guides vocal development in songbirds and marmoset monkeys, but absence of similar great ape data has been interpreted as support to saltational notions for language origin, even if such laboratorial protocols are unethical with great apes. Here we characterize the repertoire entropy of orangutan individuals and show that in the wild, different degrees of sociality across populations are associated with different ‘vocal personalities’ in the form of distinct regimes of alarm call variants. In high-density populations, individuals are vocally more original and acoustically unpredictable but new call variants are short lived, whereas individuals in low-density populations are more conformative and acoustically consistent but also exhibit more complex call repertoires. Findings provide non-invasive evidence that sociality predicts vocal phenotype i...
Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning
Proceedings of the Royal Society B: Biological Sciences
The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio , ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels ( N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that hi...
Journal of Comparative Psychology, 2004
Although vocal sharing is widespread at several phylogenetic levels, few descriptions concerned primates. The present study involved the dynamics of vocal structures and social organization in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli) at 3-year periods, using precise sound recording and comparison. The authors focused on combined harmonic 6 calls, often involved in vocal exchanges and associated with approaches. Each female produced 1 to 4 variants, shared, or not, between individuals. Changes appeared between years in the form of disappearance, appearance, or transformation of variants. There was a decrease in the global degree of sharing over the years. Greater changes were observed after social disturbance. Sharing would be more important in disturbed than stable groups to advertise bonds. Call or song sharing within groups reflects social affinities in several species of birds (
Social drive and the evolution of primate hearing
Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 2012
The structure and function of primate communication have attracted much attention, and vocal sig- nals, in particular, have been studied in detail. As a general rule, larger social groups emit more types of vocal signals, including those conveying the presence of specific types of predators. The adaptive advantages of receiving and responding to alarm calls are expected to exert a selective pressure on the auditory system. Yet, the comparative biology of primate hearing is limited to select species, and little attention has been paid to the effects of social and vocal complexity on hearing. Here, we use the auditory brainstem response method to generate the largest number of standard- ized audiograms available for any primate radiation. We compared the auditory sensitivities of 11 strepsirrhine species with and without independent contrasts and show that social complexity explains a significant amount of variation in two audiometric parameters—overall sensitivity and high-frequency limit. We verified the generality of this latter result by augmenting our analysis with published data from nine species spanning the primate order. To account for these findings, we develop and test a model of social drive. We hypothesize that social complexity has favoured enhanced hearing sensitivities, especially at higher frequencies.
Nature Communications, 2023
Vocalizations differ substantially between the sexes in many primates, and lowfrequency male vocalizations may be favored by sexual selection because they intimidate rivals and/or attract mates. Sexual dimorphism in fundamental frequency may be more pronounced in species with more intense male mating competition and in those with large group size, where social knowledge is limited and efficient judgment of potential mates and competitors is crucial. These non-mutually exclusive explanations have not been tested simultaneously across primate species. In a sample of vocalizations (n = 1914 recordings) across 37 anthropoid species, we investigated whether fundamental frequency dimorphism evolved in association with increased intensity of mating competition (H1), large group size (H2), multilevel social organization (H3), a trade-off against the intensity of sperm competition (H4), and/or poor acoustic habitats (H5), controlling for phylogeny and body size dimorphism. We show that fundamental frequency dimorphism increased in evolutionary transitions towards larger group size and polygyny. Findings suggest that lowfrequency male vocalizations in primates may have been driven by selection to win mating opportunities by avoiding costly fights and may be more important in larger groups, where limited social knowledge affords advantages to rapid assessment of status and threat potential via conspicuous secondary sexual characteristics. Determining why sex differences evolved and vary among primates is critical to understanding the evolution of mating systems and social organization 1. Sexual dimorphism in body size, skeletal size and shape, dentition, pelage coloration, and ornamentation have been studied extensively 2-6 , but little is known about the evolution of sex differences in primate vocalizations despite the importance of vocal communication 7-9. Comparative studies have focused on acoustic allometry, i.e. the link between an animal's body size and the acoustic properties of its vocalizations 10-13 , as well as adaptive explanations (e.g., acoustic variations in response to the degree of sperm competition 14 and the strength of social bonding 15). However, these studies have conducted analyses at the species level without distinguishing sex, or within one sex only. Primate larynges, including extralaryngeal appendices 16,17 , are also substantially larger in proportion to body size, more variable in size, and have evolved faster than carnivore