Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

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 higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.     

A micro-geography of fear: learning to eavesdrop on alarm calls of neighbouring heterospecifics

Many vertebrates eavesdrop on alarm calls of other species, which is a remarkable ability, given geographical variation in community composition and call diversity within and among species. We used micro-geographical variation in community composition to test whether individuals recognize heterospecific alarm calls by: (i) responding to acoustic features shared among alarm calls; (ii) having innate responses to particular heterospecific calls; or (iii) learning specific alarm calls. We found that superb fairy-wrens (Malurus cyaneus) fled to cover to playback of noisy miner (Manorina melanocephala) aerial predator alarm calls only in locations where miners were present, suggesting that learning rather than acoustic structure determines response. Sites with and without miners were well within the dispersal distance of fairy-wrens, and philopatric males and dispersing females showed the same pattern, so that local genetic adaptation is extremely unlikely. Furthermore, where miners were present, fairy-wrens responded appropriately to different miner calls, implying eavesdropping on their signalling system rather than fleeing from miners themselves. Learned eavesdropping on alarm calls enables individuals to harvest ecologically relevant information from heterospecifics on an astonishingly fine spatial scale. Such phenotypic plasticity is valuable in a changing world, where individuals can be exposed to new species.     

Social learning of a communicative signal in captive chimpanzees

The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother-as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.     

Contact calls of common marmosets (Callithrix jacchus): influence of age of caller on antiphonal calling and other vocal responses

Marmosets, as do many other primates, live in forest environments, are group living and constantly at risk of predation. Retaining contact with one another is therefore a matter of survival. We ask here whether their contact calls (phee and twitter vocalizations) are in some way ordered acoustically by sex or age and whether the calls of older marmosets elicit different responses than those of younger marmosets. In our study, marmosets (2–14 years) were visually isolated from conspecifics and the vocal responses to each isolated caller by other marmosets in the colony were recorded. Vocal responses to phee calls largely consisted of phee calls and, less commonly, twitter calls. No differences between the responses to calls by males and females were apparent. However, we found a strong positive and significant correlation between the caller's age and the percentage of its phee calls receiving a phee response, and a significant negative correlation between the caller's age and the percentage of its phee calls receiving a twitter response. The older the marmoset, the more antiphonal calling occurred. Two‐syllable phee calls were emitted more often by older marmosets (10–14 years) than by younger ones (2–6 years). Hence, we have found age‐dependent differences in phee‐call production and a consistent change in the response received across the adult life‐span. This age‐dependent effect was independent of kinship relations. This is the first evidence that marmosets distinguish age by vocal parameters alone and make social decisions based on age. Am. J. Primatol. 71:165–170, 2009. © 2008 Wiley‐Liss, Inc.     

Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wright's (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.     

Female Social Feedback Reveals Non-imitative Mechanisms of Vocal Learning in Zebra Finches

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Stability and change in the vocal signatures of common marmoset mobbing calls

Alarm calls that carry information about the identity of the caller may help the receiver decide how to react. We recorded the tsik calls of six captive adult marmosets (Callithrix jacchus) in two different social groups in response to snake models at two time points (summer 2014 and January 2015). We measured eight acoustic variables including duration, inter-call interval, minimum and maximum frequency, and starting, maximum and ending peak frequency. Discriminant function analyses (DFA) confirmed that calls were individually distinct at both time periods (78.88 and 79.89% correctly classified at time one and time two, respectively). Stability of the vocal signatures was assessed using the DFA model for summer 2014 to classify calls elicited in January 2015. Although the classification rates were lower in 2015, calls were still classified more than would be expected by chance (64.50%). This suggests that acoustic signatures of common marmoset tsik calls remain fairly stable over time and therefore remain recognizable by their groupmates. However, during that six-month period, at least three (out of seven) acoustic parameters changed such that they were significantly higher or lower in all six marmosets; in two marmosets six out of seven parameters changed. Changes to individual ‘voices’ of animals, despite overall stability reflected in above-chance matching of calls over time in a DFA analysis, may have implications for acoustic research.     

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

Social learning and evolution: the cultural intelligence hypothesis

If social learning is more efficient than independent individual exploration, animals should learn vital cultural skills exclusively, and routine skills faster, through social learning, provided they actually use social learning preferentially. Animals with opportunities for social learning indeed do so. Moreover, more frequent opportunities for social learning should boost an individual's repertoire of learned skills. This prediction is confirmed by comparisons among wild great ape populations and by social deprivation and enculturation experiments. These findings shaped the cultural intelligence hypothesis, which complements the traditional benefit hypotheses for the evolution of intelligence by specifying the conditions in which these benefits can be reaped. The evolutionary version of the hypothesis argues that species with frequent opportunities for social learning should more readily respond to selection for a greater number of learned skills. Because improved social learning also improves asocial learning, the hypothesis predicts a positive interspecific correlation between social-learning performance and individual learning ability. Variation among primates supports this prediction. The hypothesis also predicts that more heavily cultural species should be more intelligent. Preliminary tests involving birds and mammals support this prediction too. The cultural intelligence hypothesis can also account for the unusual cognitive abilities of humans, as well as our unique mechanisms of skill transfer.     

鸣禽鸣叫学习的神经生物学机制

鸣禽鸣叫具有复杂的神经生理和生化基础,表现为一种复杂的学习过程。鸣啭控制系统是研究神经系统与学习、行为和发育关系的重要模型。而鸣禽鸣叫学习行为与鸣啭控制系统内长时程增强效应、神经元超微结构的改变和神经核团内的电活动、激素水平高低及其周期性变化、神经元再生或改变、即早基因的表达等方面密切相关。对鸣禽鸣叫的神经生物学机制进行了综述。     

Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus

Individualistic contact calls facilitate mother‐offspring reunion after separation. However, in many mammals, both the acoustic structure and individuality of contact calls differ between mother and young. In contrast, in Siberian wapiti Cervus elaphus sibiricus, contact calls are similar in the acoustics between mother and young, whereas effects of this similarity on vocal individuality were not investigated. In this study, we analyzed acoustic differences between closed‐mouth (nasal) and open‐mouth (oral) contact calls and examined individuality of the most usual oral calls of 19 Siberian wapiti (9 hinds and 10 5–6‐month adolescents) emitted in response to mother‐offspring separation. In the oral calls, the values of frequency and power variables were higher than in the nasal calls. Calls of hinds and adolescents did not differ by the maximum fundamental frequency and duration, whereas the peak frequency was higher in the young. Discriminant function analysis (DFA) based on 11 acoustic variables of oral calls accurately classified to individual 92.5% of hind calls and 96.9% of adolescent calls (chi‐square test for differences between hinds and adolescents, p = 0.19). Variables mainly contributing to vocal identity (duration, start, and maximum fundamental frequency) were the same in calls of mothers and adolescents. We conclude that similarities in the acoustics calls of mothers and adolescents mean that they do not differ in their potential for encoding individual identity, suggesting a mutual process of mother‐offspring vocal recognition in Siberian wapiti.     

Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution

Mitochondrial DNA (mtDNA) of multicellular animals (Metazoa) is typically a small ( approximately 16 kbp), circular-mapping molecule that encodes 37 tightly packed genes. The structures of mtDNA-encoded transfer RNAs (tRNAs) and ribosomal RNAs (rRNAs) are usually highly unorthodox, and proteins are translated with multiple deviations from the standard genetic code. In contrast, mtDNA of the choanoflagellate Monosiga brevicollis, the closest unicellular relative of animals, is four times larger, contains 1.5 times as many genes, and lacks mentioned peculiarities of animal mtDNA. To investigate the evolutionary transition that led to the specific organization of metazoan mtDNA, we determined complete mitochondrial sequences from the demosponges Geodia neptuni and Tethya actinia, two representatives of the most basal animal phylum, the Porifera. We found that poriferan mtDNAs resemble those of other animals in their compact organization, lack of introns, and a well-conserved animal-like gene order. Yet, they contain several extra genes, encode bacterial-like rRNAs and tRNAs, and use a minimally derived genetic code. Our findings suggest that the evolution of the typical metazoan mtDNA has been a multistep process in which the compact genome organization and the reduced gene content were established prior to the reduction of tRNA and rRNA structures and the introduction of multiple changes of the translation code.     

The function of loud calls (Hoot Series) in wild western gorillas (Gorilla gorilla)

The use of loud vocal signals to reduce distance among separated social partners is well documented in many species; however, the underlying mechanisms by which the reduction of spacing occurs and how they differ across species remain unclear. Western gorillas (Gorilla gorilla) offer an opportunity to investigate these issues because their vocal repertoire includes a loud, long‐distance call (i.e., hoot series) that is potentially used in within‐group communication, whereas mountain gorillas use an identical call exclusively during intergroup encounters. First, we tested whether the hoot series functions as a contact/separation call. Second, we examined which individuals were more likely to reply and which party was more responsible for decreasing distance to identify the underlying mechanisms and cognitive implications of hoot series. We collected behavioral, spatial, and acoustic data on five adult gorillas over 15 months at the Mondika Research Center (Republic of Congo and CAR). Hoot series are individually distinct calls and given by both male and female gorillas when separated from each other. Following hooting, the distance between separated group members decreased significantly; thus we concluded that western gorillas use this call to reestablish group cohesion. The way in which proximity was achieved depended upon listeners replying or not to the caller. Replies may indicate a conflict between callers about intended travel direction, with vocal interchanges serving to negotiate a consensus. Although the acoustic features of vocal signals are highly constrained in closely related species, our results demonstrate that the function and usage of particular calls can be flexible. Am J Phys Anthropol 155:379–391, 2014. © 2014 Wiley Periodicals, Inc.     

Social learning of novel route preferences in adult humans

Non-human animals can acquire novel route preferences by following knowledgeable individuals. Such socially learned route preferences can be stably maintained over multiple transmission episodes, sometimes forming long-lived traditions. In humans, preferences for familiar routes or heavily used worn trails over unfamiliar ones have been described in various contexts. However, social learning of route preferences has not been experimentally demonstrated in humans. Here, we demonstrate that social learning and tradition influence route choice. We led adult male and female participants into a room by one of two routes. Participants followed the demonstrated route choices, and later remembered and preferred this choice even when determinably suboptimal (i.e. longer and not preferred by control participants) or when the choice was indicated as arbitrary (the demonstrator took one route to retrieve a poster that had ostensibly fallen). Moreover, route preferences were stably maintained over multiple transmission episodes. We suggest that simple social learning processes, often neglected in human and primate research, can result in long-lived route preferences that may influence a range of additional behaviour patterns.     

Contact call diversity in natural beluga entrapments in an Arctic estuary: Preliminary evidence of vocal signatures in wild belugas

Broadband, pulsed contact calls have been described for captive and temporarily restrained belugas, but little information exists on their usage in the wild. We examined vocal production during 14 natural beluga entrapments in a shallow channel in Cunningham Inlet, as isolation events offer ideal contexts to study contact calls. Drone footage, overhead photos, and shore‐based photos confirmed the number of individuals and age composition in each entrapment. Contact calls comprised the majority (61%) of vocalizations produced by entrapped whales compared to the free‐ranging herd (10%). We divided contact calls into complex (80%), those with a stereotyped, spectrographically prominent component overlapping the pulse train that characterizes all beluga contact calls, and simple (20%), those with no overlapping component. For each entrapment, we generated a catalogue of complex contact call types, totaling 87 types. Our classification was corroborated both quantitatively and by 55 naïve human judges. Occasional instances of overlapping contact calls of the same type indicated dyadic production. The number of contact call types per entrapment was strongly related to (never exceeding) the number of individuals, excluding neonates. Although this suggests a system of vocal signatures in belugas, consistent with their fission‐fusion society and earlier findings, whether signature identity is encoded individually or shared with related animals remains unknown.     

Ultrasonic vocalizations in mouse models for speech and socio‐cognitive disorders: insights into the evolution of vocal communication

Comparative analyses used to reconstruct the evolution of traits associated with the human language faculty, including its socio‐cognitive underpinnings, highlight the importance of evolutionary constraints limiting vocal learning in non‐human primates. After a brief overview of this field of research and the neural basis of primate vocalizations, we review studies that have addressed the genetic basis of usage and structure of ultrasonic communication in mice, with a focus on the gene FOXP2 involved in specific language impairments and neuroligin genes (NL‐3 and NL‐4) involved in autism spectrum disorders. Knockout of FoxP2 leads to reduced vocal behavior and eventually premature death. Introducing the human variant of FoxP2 protein into mice, in contrast, results in shifts in frequency and modulation of pup ultrasonic vocalizations. Knockout of NL‐3 and NL‐4 in mice diminishes social behavior and vocalizations. Although such studies may provide insights into the molecular and neural basis of social and communicative behavior, the structure of mouse vocalizations is largely innate, limiting the suitability of the mouse model to study human speech, a learned mode of production. Although knockout or replacement of single genes has perceptible effects on behavior, these genes are part of larger networks whose functions remain poorly understood. In humans, for instance, deficiencies in NL‐4 can lead to a broad spectrum of disorders, suggesting that further factors (experiential and/or genetic) contribute to the variation in clinical symptoms. The precise nature as well as the interaction of these factors is yet to be determined.