Complex vocal learning and three-dimensional mating environments

Human caregivers interacting with children typically modify their speech in ways that promote attention, bonding, and language acquisition. Although this "motherese," or child-directed communication (CDC), occurs in a variety of human cultures, evidence among nonhuman species is very rare. We looked for its occurrence in a nonhuman mammalian species with long-term mother-offspring bonds that is capable of vocal production learning, the bottlenose dolphin (Tursiops truncatus). Dolphin signature whistles provide a unique opportunity to test for CDC in nonhuman animals, because we are able to quantify changes in the same vocalizations produced in the presence or absence of calves. We analyzed recordings made during brief catch-and-release events of wild bottlenose dolphins in waters near Sarasota Bay, Florida, United States, and found that females produced signature whistles with significantly higher maximum frequencies and wider frequency ranges when they were recorded with their own dependent calves vs. not with them. These differences align with the higher fundamental frequencies and wider pitch ranges seen in human CDC. Our results provide evidence in a nonhuman mammal for changes in the same vocalizations when produced in the presence vs. absence of offspring, and thus strongly support convergent evolution of motherese, or CDC, in bottlenose dolphins. CDC may function to enhance attention, bonding, and vocal learning in dolphin calves, as it does in human children. Our data add to the growing body of evidence that dolphins provide a powerful animal model for studying the evolution of vocal learning and language.

Vocal learners such as humans and songbirds can learn to produce elaborate patterns of structurally organized vocalizations, whereas many other vertebrates such as non-human primates and most other bird groups either cannot or do so to a very limited degree. To explain the similarities among humans and vocal-learning birds and the differences with other species, various theories have been proposed. One set of theories are motor theories, which underscore the role of the motor system as an evolutionary substrate for vocal production learning. For instance, the motor theory of speech and song perception proposes enhanced auditory perceptual learning of speech in humans and song in birds, which suggests a considerable level of neurobiological specialization. Another, a motor theory of vocal learning origin, proposes that the brain pathways that control the learning and production of song and speech were derived from adjacent motor brain pathways. Another set of theories are cognitive theories, which address the interface between cognition and the auditory-vocal domains to support language learning in humans. Here we critically review the behavioral and neurobiological evidence for parallels and differences between the so-called vocal learners and vocal non-learners in the context of motor and cognitive theories. In doing so, we note that behaviorally vocal-production learning abilities are more distributed than categorical, as are the auditory-learning abilities of animals. We propose testable hypotheses on the extent of the specializations and cross-species correspondences suggested by motor and cognitive theories. We believe that determining how spoken language evolved is likely to become clearer with concerted efforts in testing comparative data from many non-human animal species.

Experimental Evidence for Synchronization to a Musical Beat in a Nonhuman Animal

Chapter 7 Plasticity of Communication in Nonhuman Primates

Language has been considered by many to be uniquely human. Numerous theories for how it evolved have been proposed but rarely tested. The articles in this theme issue consider the extent to which aspects of language, such as vocal learning, phonology, syntax, semantics, intentionality, cognition and neurobiological adaptations, are shared with other animals. By adopting a comparative approach, insights into the mechanisms and origins of human language can be gained. While points of agreement exist among the authors, conflicting viewpoints are expressed on several issues, such as the presence of proto-syntax in animal communication, the neural basis of the Merge operation, and the neurogenetic changes necessary for vocal learning. Future comparative research in animal communication has the potential to teach us even more about the evolution, neurobiology and cognitive basis of human language. This article is part of the theme issue 'What can animal communication teach us about human language?'

The study of non-human animals that are vocal learning, which is the ability to alter the structure of vocalizations, has provided important insights into our understanding of the evolution and development of vocal communication and language. Of particular interest is vocal convergence where individuals learn the vocalizations shared by their social group. Although the development of shared vocalizations has received extensive study across vocal learning species, less attention has been given to the use of these learned signals, especially whether individuals stress the expression of vocalizations that signal high status and deemphasize those that do not. Previous field and captivity studies of Brown-headed Cowbirds (Molothrus ater) show that males 2 years old or older have greater levels of song type sharing than 1 year old males and that females are more sexually stimulated by shared song types than by the non-shared types that occur mostly in the repertoires of yearlings. In this study, we observed males at least 2 years old singing in experimentally paired matches with another male or female conspecific to determine whether they preferentially used some song types in their repertoires and whether preferences were based on shared songs that indicate male age. Data on over 5,000 songs by 12 males showed that males did not use song types randomly. The most frequently used song types directed to both males and females were types shared with the most other males. This was the case whether males or song types were the unit of analysis, clearly demonstrating that this species emphasizes vocalizations that signal high quality (an age of 2 years or more) and therefore optimizes the use of what it has learned. These results support the hypothesis that selection can favor stable presentation of shared vocalizations across social contexts because age-revealing information in vocalizations that require learning significantly improves the accuracy of age assessment, which in many species is typically based on maturational changes that occur with aging.

Karen McComb

Whether brain networks underlying the multimodal processing of language in humans are present in non-human primates is an unresolved question in primate evolution. Conceptual awareness in humans, which is the backbone of verbal and non-verbal semantic elaboration, involves intracerebral connectivity via the inferior fronto-occipital fascicle (IFOF). While non-human primates can communicate through visual information channels, there has been no formal demonstration that they possess a functional homologue of the human IFOF. Therefore, we undertook a post-mortem diffusion MRI tractography study in conjunction with Klingler micro-dissection to search for IFOF fiber tracts in brain of Old-World (vervet) monkeys. We found clear and concordant evidence from both techniques for the existence of bilateral fiber tracts connecting the frontal and occipital lobes. These tracts closely resembled the human IFOF with respect to trajectory, topological organization, and cortical terminal fields. Moreover, these fibers are clearly distinct from other bundles previously described in this region of monkey brain, i.e., the inferior longitudinal and uncinate fascicles, and the external and extreme capsules. This demonstration of an IFOF in brain of a species that diverged from the human lineage some 22millions years ago enhances our comprehension about the evolution of language and social behavior.

Human vocal development is dependent on learning by imitation through social feedback between infants and caregivers. Recent studies have revealed that vocal development is also influenced by parental feedback in marmoset monkeys, suggesting vocal learning mechanisms in nonhuman primates. Marmoset infants that experience more contingent vocal feedback than their littermates develop vocalizations more rapidly, and infant marmosets with limited parental interaction exhibit immature vocal behavior beyond infancy. However, it is yet unclear whether direct parental interaction is an obligate requirement for proper vocal development because all monkeys in the aforementioned studies were able to produce the adult call repertoire after infancy. Using quantitative measures to compare distinct call parameters and vocal sequence structure, we show that social interaction has a direct impact not only on the maturation of the vocal behavior but also on acoustic call structures during vocal development. Monkeys with limited parental interaction during development show systematic differences in call entropy, a measure for maturity, compared with their normally raised siblings. In addition, different call types were occasionally uttered in motif-like sequences similar to those exhibited by vocal learners, such as birds and humans, in early vocal development. These results indicate that a lack of parental interaction leads to long-term disturbances in the acoustic structure of marmoset vocalizations, suggesting an imperative role for social interaction in proper primate vocal development.

The evolution of language has been the subject of much debate and speculation. It is difficult to study in a scientific manner and remains an open research question. This paper proposes an integrated computational framework for investigating possible scenarios of genetic and cultural evolution of language. Specifically, our framework aims to capture cultural evolution to allow for investigation phylogenetic dynamics of language, and at the same time to capture genetic evolution of phenotypic plasticity to allow for investigation of the role of the Baldwin effect in language evolution, while keeping the framework as simple as possible. In our evolutionary experiments and analysis, we discovered a coevolutionary scenario involving biological evolution of phenotypic plasticity, and a cyclic coevolutionary dynamic between genetic and cultural evolution, mediated by phenotypic plasticity.

Phylogenetic trees are a central tool for studying language evolution and have wide implications for understanding cultural evolution as a whole. For example, they have been the basis of studies on the evolution of musical instruments, religious beliefs and political complexity. Bayesian phylogenetic methods are transparent regarding the data and assumptions underlying the inference. One of these assumptions—that languages change independently—is incompatible with the reality of language evolution, particularly with language contact. When speakers interact, languages frequently borrow linguistic traits from each other. Phylogenetic methods ignore this issue, which can lead to errors in the reconstruction. More importantly, they neglect the rich history of language contact. A principled way of integrating language contact in phylogenetic methods is sorely missing. We present contacTrees, a Bayesian phylogenetic model with horizontal transfer for language evolution. The model efficiently infers the phylogenetic tree of a language family and contact events between its clades. The implementation is available as a package for the phylogenetics software BEAST 2. We apply contacTrees in a simulation study and a case study on a subset of well-documented Indo-European languages. The simulation study demonstrates that contacTrees correctly reconstructs the history of a simulated language family, including simulated contact events. Moreover, it shows that ignoring contact can lead to systematic errors in the estimated tree height, rate of change and tree topology, which can be avoided with contacTrees. The case study confirms that contacTrees reconstructs known contact events in the history of Indo-European and finds known loanwords, demonstrating its practical potential. The model has a higher statistical fit to the data than a conventional phylogenetic reconstruction, and the reconstructed tree height is significantly closer to well-attested estimates. Our method closes a long-standing gap between the theoretical and empirical models of cultural evolution. The implications are especially relevant for less documented language families, where our knowledge of past contacts and linguistic borrowings is limited. Since linguistic phylogenies have become the backbone of many studies of cultural evolution, the addition of this integral piece of the puzzle is crucial in the endeavour to understand the history of human culture.

In common with human speech, song is culturally inherited in oscine passerine birds ('songbirds'). Intraspecific divergence in birdsong, such as development of local dialects, might be an important early step in the speciation process. It is therefore vital to understand how songs diverge, especially in founding populations. The northward expansion of the Light-vented Bulbul Pycnonotus sinensis (J. F. Gmelin, 1789) into north China in the last 30 years provides an excellent opportunity to study birdsong evolution. We compared ~4400 songs from newly established northern populations with ~2900 songs from southern populations to evaluate song divergence after recent expansion. The total pool of syllables and especially song types was considerably smaller in the north than in the south, indicating 'founder effects' in the new population. The ancestral pattern of mosaic song dialects changed into a pattern of wide geographical sharing of a few song types and syllables, likely the result of fewer geographical barriers to 'meme flow', and the recent spread across a large area in the north. Our results suggest that song evolution and vocal trait shifts can arise rapidly after range expansion, and that in the Light-vented Bulbul 'founder effects', geographical isolation, and recent rapid expansions played important roles in the evolution of song dialects.

Language evolution refers to the origins and development of the human system of communication. Research on language evolution compares aspects of human communication with those of other animals, especially nonhuman primates, and analyzes gestures, multimodal communication, pidgins and creoles, child development, the physiology of the vocal tract, genes and neurons, the brain and brain damage, as well as the fossil record. Theories of language evolution discuss whether human language emerged gradually or abruptly and through which evolutionary adaptations or exaptations, as well as whether there are any key features of human language. Controversies remain but recent research has contributed to a more nuanced picture of differences between humans and nonhumans that may prove to not be qualitative but quantitative.

Animal culture evolves alongside genomes, and the two modes of inheritance-culture and genes-interact in myriad ways. For example, stable geographic variation in culture can act as a reproductive barrier, thereby facilitating genetic divergence between "cultural populations." White-crowned sparrows (Zonotrichia leucophrys) are a well-established model species for bird song learning and cultural evolution, as they have distinct, geographically discrete, and culturally transmitted song types (i.e., song dialects). In this study, we tested the hypothesis that divergence between culturally transmitted songs drives genetic divergence within Nuttall's white-crowned sparrows (Z. l. nuttalli). In accordance with sexual selection theory, we hypothesized that cultural divergence between mating signals both preceded and generated genetic divergence. We characterized the population structure and song variation in the subspecies and found two genetically differentiated populations whose boundary coincides with a major song boundary at Monterey Bay, California. We then conducted a song playback experiment that demonstrated males discriminate between songs based on their degree of divergence from their local dialect. These results support the idea that discrimination against non-local songs is driving genetic divergence between the northern and southern populations. Altogether, this study provides evidence that culturally transmitted bird songs can act as the foundation for speciation by sexual selection.

Limited adult vocal learning maintains call dialects but permits pair-distinctive calls in red crossbills