Cross-Taxa Similarities in Affect-Induced Changes of Vocal Behavior and Voice in Arboreal Monkeys (original) (raw)
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Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes—Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system.
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.
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...
Coevolution of vocal communication and sociality in primates
Biology Letters, 2005
Understanding the rules that link communication and social behaviour is an essential prerequisite for discerning how a communication system as complex as human language might have evolved. The comparative method offers a powerful tool for investigating the nature of these rules, since it provides a means to examine relationships between changes in communication abilities and changes in key aspects of social behaviour over evolutionary time. Here we present empirical evidence from phylogenetically controlled analyses indicating that evolutionary increases in the size of the vocal repertoire among non-human primate species were associated with increases in both group size and time spent grooming (our measure of extent of social bonding).
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.
The Journal of the Acoustical Society of America, 2011
Although the vocal repertoire of nonhuman primates is strongly constrained by genetic, a growing number of studies evidence socially determined flexibility. According to Snowdon et al. [Social Influences on Vocal Development (University Press, Cambridge, 1997), pp. 234-248], calls with a higher social function (affiliative or agonistic) would be expected to show more flexibility than lesser social calls. Owren and Rendall [Evol. Anthropol., 10, 58-71 (2001)] nuanced this by defending a structure-function relationship. Calls with particular acoustic properties, which directly influence the listener's affect, would be less individually distinctive than calls involved in an affective conditioning process. These hypotheses were tested in Campbell's monkeys using telemetric recordings. This is the first detailed description of female Campbell's monkeys' vocal repertoire emphasizing a possible relationship between social function and flexibility level. The vocal repertoire displayed an "arborescent" organization (call type, subtype, and variants). The highest number of subtypes and the greatest acoustic variability, within and among individuals, were found in calls associated with the highest affiliative social value. However, calls associated with agonism were the most stereotyped, whereas less social alarm calls were intermediate. This only partially validate the hypothesis of Snowdon et al. In accordance with Owren and Rendall's hypotheses, the level of individual distinctiveness was minimum for noisy pulsed calls and maximum for calls involved in affiliative interactions. V
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.
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 .
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...