Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals

The classic evidence for vocal production learning involves imitation of novel, often anthropogenic sounds. Among mammals, this has been reported for dolphins, elephants, harbor seals, and humans. A broader taxonomic distribution has been reported for vocal convergence, where the acoustic properties of calls from different individuals converge when they are housed together in captivity or form social bonds in the wild. Vocal convergence has been demonstrated for animals as diverse as songbirds, parakeets, hummingbirds, bats, elephants, cetaceans, and primates. For most species, call convergence is thought to reflect a group-distinctive identifier, with shared calls reflecting and strengthening social bonds. A ubiquitous function for vocal production learning that is starting to receive attention involves modifying signals to improve communication in a noisy channel. Pooling data on vocal imitation, vocal convergence, and compensation for noise suggests a wider taxonomic distribution of vocal production learning among mammals than has been generally appreciated. The wide taxonomic distribution of this evidence for vocal production learning suggests that perhaps more of the neural underpinnings for vocal production learning are in place in mammals than is usually recognized.     

Experimental evidence for action imitation in killer whales (Orcinus orca)

Comparative experimental studies of imitative learning have focused mainly on primates and birds. However, cetaceans are promising candidates to display imitative learning as they have evolved in socioecological settings that have selected for large brains, complex sociality, and coordinated predatory tactics. Here we tested imitative learning in killer whales, Orcinus orca. We used a ‘do-as-other-does’ paradigm in which 3 subjects witnessed a conspecific demonstrator’s performance that included 15 familiar and 4 novel behaviours. The three subjects (1) learned the copy command signal ‘Do that’ very quickly, that is, 20 trials on average; (2) copied 100 % of the demonstrator’s familiar and novel actions; (3) achieved full matches in the first attempt for 8–13 familiar behaviours (out of 15) and for the 2 novel behaviours (out of 2) in one subject; and (4) took no longer than 8 trials to accurately copy any familiar behaviour, and no longer than 16 trials to copy any novel behaviour. This study provides experimental evidence for body imitation, including production imitation, in killer whales that is comparable to that observed in dolphins tested under similar conditions. These findings suggest that imitative learning may underpin some of the group-specific traditions reported in killer whales in the field.     

The evolution of speech: a comparative review

The evolution of speech can be studied independently of the evolution of language, with the advantage that most aspects of speech acoustics, physiology and neural control are shared with animals, and thus open to empirical investigation. At least two changes were necessary prerequisites for modern human speech abilities: (1) modification of vocal tract morphology, and (2) development of vocal imitative ability. Despite an extensive literature, attempts to pinpoint the timing of these changes using fossil data have proven inconclusive. However, recent comparative data from nonhuman primates have shed light on the ancestral use of formants (a crucial cue in human speech) to identify individuals and gauge body size. Second, comparative analysis of the diverse vertebrates that have evolved vocal imitation (humans, cetaceans, seals and birds) provides several distinct, testable hypotheses about the adaptive function of vocal mimicry. These developments suggest that, for understanding the evolution of speech, comparative analysis of living species provides a viable alternative to fossil data. However, the neural basis for vocal mimicry and for mimesis in general remains unknown.     

Imitation, pretend play, and childhood: essential elements in the evolution of human culture?

There is much controversy over what is needed for culture to flourish and what has led human culture to be different from "cultural" characteristics of other animals. Here I argue that the emergence of childhood as a step in the life cycle was critical to the evolution of the human cultural mind. My line of reasoning is built around two complementary features of childhood: imitation and play. When children imitate adults they routinely copy unnecessary and arbitrary actions. They will persistently replicate how an object is used, even when doing so interferes with their ability to produce the very outcome those actions are intended to bring about. Though seemingly maladaptive, this behavior provides for the faithful transmission of cultural ideas across generations. When children play together they commonly construct rules and meanings that exist purely because the players agree they "exist." Play thus provides the building blocks with which children rehearse the kinds of institutional realities that typify cultural practices. I argue that these forms of imitation and play represent a foundation upon which human culture flourished and that neither are prevalent in nonhuman animals. In light of these arguments evidence will be assessed suggesting that childhood emerged relatively late in human evolution.     

A beluga whale socialized with bottlenose dolphins imitates their whistles

The research on imitation in the animal kingdom has more than a century-long history. A specific kind of imitation, auditory–vocal imitation, is well known in birds, especially among songbirds and parrots, but data for mammals are limited to elephants, marine mammals, and humans. Cetaceans are reported to imitate various signals, including species–specific calls, artificial sounds, and even vocalizations from other species if they share the same habitat. Here we describe the changes in the vocal repertoire of a beluga whale that was housed with a group of bottlenose dolphins. Two months after the beluga’s introduction into a new facility, we found that it began to imitate whistles of the dolphins, whereas one type of its own calls seemed to disappear. The case reported here may be considered as an interesting phenomenon of vocal accommodation to new social companions and cross-species socialization in cetaceans.     

Reinforcement of vocalizations through contingent vocal imitation

Maternal vocal imitation of infant vocalizations is highly prevalent during face-to-face interactions of infants and their caregivers. Although maternal vocal imitation has been associated with later verbal development, its potentially reinforcing effect on infant vocalizations has not been explored experimentally. This study examined the reinforcing effect of maternal vocal imitation of infant vocalizations using a reversal probe BAB design. Eleven 3- to 8-month-old infants at high risk for developmental delays experienced contingent maternal vocal imitation during reinforcement conditions. Differential reinforcement of other behavior served as the control condition. The behavior of 10 infants showed evidence of a reinforcement effect. Results indicated that vocal imitations can serve to reinforce early infant vocalizations.     

Vocal group signatures in the goitred gazelle Gazella subgutturosa

The potential for vocal modification in mammals has recently been of great interest. This study focuses on the potential for vocal matching in juvenile and adolescent goitred gazelles Gazella subgutturosa that were group housed as part of an animal management programme. Two groups of animals (16 and 19 unrelated individuals, respectively) were recorded at two different ages, juvenile and adolescent, regarding 20–25 calls per individual per age; each group was evaluated in a separate year. Vocal similarity of group members compared to non-members was prominent in both ages, but higher in juveniles. Individual identity was prominent in both ages and higher in adolescents. The more prominent vocal indicators of group membership in juveniles could be related to their higher social dependence compared to adolescents. The more individualized calls of adolescents could be a mechanistic consequence of more stable growth at older age. Our results suggest vocal plasticity of goitred gazelles under social influences. These data add to recent evidence about domestic goat kids Capra hircus, suggesting that vocalizations of species that are not capable of imitation are more flexible than previously thought.     

Imitative learning by captive western lowland gorillas (Gorilla gorilla gorilla) in a simulated food-processing task

Although field studies have suggested the existence of cultural transmission of foraging techniques in primates, identification of transmission mechanisms has remained elusive. To test experimentally for evidence of imitation in the current study, we exposed gorillas (Gorilla gorilla gorilla) to an artificial fruit foraging task designed by A. Whiten and D. M. Custance (1996). Gorillas (n=6) watched a human model remove a series of 3 defenses around a fruit. Each of the defenses was removed using 1 of 2 alternative techniques. Subsequent video analysis of gorillas' behavior showed a significant tendency to copy the observed technique on 1 of the individual defenses and the direction of removal on another defense. This is the first statistically reliable evidence of imitation in gorillas. Sequence of defense removal was not replicated. The gorillas' responses were most similar to those of chimpanzees.     

Evidence suggests vocal production learning in a cross-fostered Risso’s dolphin (<Emphasis Type="Italic">Grampus</Emphasis><Emphasis Type="Italic">griseus</Emphasis>)

Vocal learning is a rare skill in mammals, and we have limited information about the contexts in which they use it. Previous studies suggested that cetaceans in general are skilled at imitating sounds, but only few species have been studied to date. To expand this investigation to another species and to investigate the possible influence of the social environment on vocal learning, we studied the whistle repertoire of a female Risso’s dolphin (Grampus griseus) that was stranded at an early age and was subsequently raised in a group of bottlenose dolphins (Tursiops truncatus). We show that this cross-fostered animal produced vocal signals more akin to those of its Tursiops poolmates than those of Risso’s dolphins in the wild. This is one of very few systematic cross-fostering studies in cetaceans and the first to suggest vocal production learning in the Risso’s dolphin. Our findings also suggest that social experience is a major factor in the development of the vocal repertoire in this species.     

语言如何进化

人类语言具有复杂多变的递归结构,漫长的物种进化过程中唯独人类精通语言。语言的进化始于大约两百万年前的“更新世时期”,语言在当时作为一种认知适应对于人类应对自然界带给人类的挑战（如动物掠食与森林毁坏）有很大帮助。人类进化过程中学习与文化因素形成一种选择压力促使人际交流语法化,人际交流语法化引发大脑容量增加,然而,最初的语言进化与基因无关。学习与文化压力也使交流的媒介依次变为手语模式、表情模式与语言模式。交流媒介的逐渐变化最终导致了FOXP2基因突变,FOXP2基因突变让智人具有了自主的言语能力。与地球上其它的人科动物相比,人类的语言能力使人类在进化中具有明显的优势     

Direct reciprocity in animals: The roles of bonding and affective processes

The presence of direct reciprocity in animals is a debated topic, because, despite its evolutionary plausibility, it is believed to be uncommon. Some authors claim that stable reciprocal exchanges require sophisticated cognition which has acted as a constraint on its evolution across species. In contrast, a more recent trend of research has focused on the possibility that direct reciprocity occurs within long‐term bonds and relies on simple as well as more complex affective mechanisms such as emotional book‐keeping, rudimentary and higher forms of empathy, and inequity aversion, among others. First, we present evidence supporting the occurrence of long‐term reciprocity in the context of existing bonds in social birds and mammals. Second, we discuss the evidence for affective responses which, modulated by bonding, may underlie altruistic behaviours in different species. We conclude that the mechanisms that may underlie reciprocal exchanges are diverse, and that some act in interaction with bonding processes. From simple associative learning in social contexts, through emotional contagion and behavioural mimicry, to empathy and a sense of fairness, widespread and diverse social affective mechanisms may explain why direct reciprocity may not be a rare phenomenon among social vertebrates.     

Vocal learning in birds and humans

Vocal learning is the modification of vocal output by reference to auditory information. It allows for the imitation and improvisation of sounds that otherwise would not occur. The emergence of this skill may have been a primary step in the evolution of human language, but vocal learning is not unique to humans. It also occurs in songbirds, where its biology can be studied with greater ease. What follows is a review of some of the salient anatomical, developmental, and behavioral features of vocal learning, alongside parallels and differences between vocal learning in songbirds and humans.     

Cognitive test batteries in animal cognition research: evaluating the past,present and future of comparative psychometrics

For the past two decades, behavioural ecologists have documented consistent individual differences in behavioural traits within species and found evidence for animal “personality”. It is only relatively recently, however, that increasing numbers of researchers have begun to investigate individual differences in cognitive ability within species. It has been suggested that cognitive test batteries may provide an ideal tool for this growing research endeavour. In fact, cognitive test batteries have now been used to examine the causes, consequences and underlying structure of cognitive performance within and between many species. In this review, we document the existing attempts to develop cognitive test batteries for non-human animals and review the claims that these studies have made in terms of the structure and evolution of cognition. We argue that our current test battery methods could be improved on multiple fronts, from the design of tasks, to the domains targeted and the species tested. Refining and optimising test battery design will provide many benefits. In future, we envisage that well-designed cognitive test batteries may provide answers to a range of exciting questions, including giving us greater insight into the evolution and structure of cognition.     

Evolution of the brain and intelligence

Intelligence has evolved many times independently among vertebrates. Primates, elephants and cetaceans are assumed to be more intelligent than 'lower' mammals, the great apes and humans more than monkeys, and humans more than the great apes. Brain properties assumed to be relevant for intelligence are the (absolute or relative) size of the brain, cortex, prefrontal cortex and degree of encephalization. However, factors that correlate better with intelligence are the number of cortical neurons and conduction velocity, as the basis for information-processing capacity. Humans have more cortical neurons than other mammals, although only marginally more than whales and elephants. The outstanding intelligence of humans appears to result from a combination and enhancement of properties found in non-human primates, such as theory of mind, imitation and language, rather than from 'unique' properties.     

Observational learning of tool use in children: Investigating cultural spread through diffusion chains and learning mechanisms through ghost displays

In the first of two experiments, we demonstrate the spread of a novel form of tool use across 20 “cultural generations” of child-to-child transmission. An experimentally seeded technique spread with 100% fidelity along twice as many “generations” as has been investigated in recent exploratory “diffusion” experiments of this type. This contrasted with only a single child discovering the technique spontaneously in a comparable group tested individually without any model. This study accordingly documents children’s social learning of tool use on a new, population-level scale that characterizes real-world cultural phenomena. In a second experiment, underlying social learning processes were investigated with a focus on the contrast between imitation (defined as copying actions) and emulation (defined as learning from the results of actions only). In two different “ghost” conditions, children were presented with the task used in the first experiment but now operated without sight of an agent performing the task, thereby presenting only the information used in emulation. Children in ghost conditions were less successful than those who had watched a model in action and showed variable matching to what they had seen. These findings suggest the importance of observational learning of complex tool use through imitation rather than only through emulation. Results of the two experiments are compared with those of similar experiments conducted previously with chimpanzees and are discussed in relation to the wider perspective of human culture and the influence of task complexity on social learning.     

The selfish meme & the selflessATMA

The word ‘meme’ was first used by Richard Dawkins (Dawkins, 1976)¹ in the sense of a replicator to introduce the idea of cultural transmission through the process of imitation, just as genes are responsible for the evolution of organisms. Following Dawkins several writers came forth to have a closer look at ‘meme’. The consensus was that this was a fascinating way of explaining cultural evolution and transmission; that meme is the basic unit of (cultural) information whose existence influences events so as to make more copies of itself (Brodie, 1996).² The book which got most attention in this line of literature wasThe Meme Machine (Blackmore, 1993),³ which favours the idea that culture, like biology, evolves through the process of variation, selection and replication. Something striking in Blackmore’s thesis is that emotions and attitudes do not count as memes since they are subjective and never get passed on.     

Primate Culture and Social Learning

The human primate is a deeply cultural species, our cognition being shaped by culture, and cultural transmission amounting to an “epidemic of mental representations” (Sperber, 1996). The architecture of this aspect of human cognition has been shaped by our evolutionary past in ways that we can now begin to discern through comparative studies of other primates. Processes of social learning (learning from others) are important for cognitive science to understand because they are cognitively complex and take many interrelated forms; they shape traditions, cultures and nonsocial aspects of cognition; and in turn they may be shaped by their cultural context. The study of primate social learning and culture has in recent years enjoyed a renaissance, providing a wealth of new findings, key aspects of which are reviewed. The focus is on cognitive issues, including learning about the consequences, sequential structure and hierarchical organization of actions; relating stored knowledge to the assimilation of new social knowledge; feedback guiding the construction of imitations; conceptual grasp of imitation; and the reciprocal relationship between social learning and culture.     

Biology Precedes, Culture Transcends: An Evolutionist's View of Human Nature

I will, first, outline what we currently know about the last 4 million years of human evolutionary history, from bipedal but small-brained Australopithecus to modern Homo sapiens, our species, through the prolific toolmaker Homo habilis and the continent wanderer Homo erectus. I shall then identify anatomical traits that distinguish us from other animals and point out our two kinds of heredity, the biological and the cultural.
Biological inheritance is based on the transmission of genetic information, in humans very much the same as in other sexually reproducing organisms. But cultural inheritance is distinctively human, based on transmission of information by a teaching and learning process that is in principle independent of biological parentage. Cultural inheritance makes possible the cumulative transmission of experience from generation to generation. Cultural heredity is a swifter and more effective (because it can be designed) mode of adaptation to the environment than the biological mode. The advent of cultural heredity ushered in cultural evolution, which transcends biological evolution.
I will, finally, explore ethical behavior as a model case of a distinctive human trait, and seek to ascertain the causal connections between human ethics and human biology. My conclusions are that (1) moral reasoning—that is, the proclivity to make ethical judgments by evaluating actions as either good or evil—is rooted in our biological nature; it is a necessary outcome of our exalted intelligence, but (2) the moral codes that guide our decisions as to which actions are good and which ones are evil are products of culture, including social and religious traditions. This second conclusion contradicts those evolutionists and sociobiologists who claim that the morally good is simply that which is promoted by the process of biological evolution.     

Mouse vocal communication system: Are ultrasounds learned or innate?

Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.     

THE INTERTWINED ROLES OF GENES AND CULTURE IN HUMAN EVOLUTION

This essay critiques dual-inheritance theory as presented in Peter Richerson and Robert Boyd's book Not by Genes Alone: How Culture Transformed Human Evolution (2005). The theory states that culture became prominent in human evolution because it allowed relatively rapid adaptation to changing environments by means of imitation. Imitating the behavior of other members of one's community produces adaptive behaviors more readily than either genetic evolution or individual learning. Imitation follows a number of patterns: imitating high-status individuals, imitating the most common forms of behavior, imitating behaviors perceived to be the most effective solutions to various problems relevant to survival. This process combined with occasional innovations in behavior lead to a process of cultural evolution involving populations of cultural variants. Different local human populations were associated with different local populations of cultural variants, and both the human and the cultural populations evolved over time. Human evolution cannot be understood without taking into account these parallel processes of genetic and cultural evolution. Not by Genes Alone traces the implication of dual-inheritance theory for understanding human evolution and refers to various bodies of evidence relevant to the theory.