Evolutionary novelties underlie sound production in baleen whales.

Baleen whales (mysticetes) use vocalizations to mediate their complex social and reproductive behaviours in vast, opaque marine environments1. Adapting to an obligate aquatic lifestyle demanded fundamental physiological changes to efficiently produce sound, including laryngeal specializations2-4. Whereas toothed whales (odontocetes) evolved a nasal vocal organ5, mysticetes have been thought to use the larynx for sound production1,6-8. However, there has been no direct demonstration that the mysticete larynx can phonate, or if it does, how it produces the great diversity of mysticete sounds9. Here we combine experiments on the excised larynx of three mysticete species with detailed anatomy and computational models to show that mysticetes evolved unique laryngeal structures for sound production. These structures allow some of the largest animals that ever lived to efficiently produce frequency-modulated, low-frequency calls. Furthermore, we show that this phonation mechanism is likely to be ancestral to all mysticetes and shares its fundamental physical basis with most terrestrial mammals, including humans10, birds11, and their closest relatives, odontocetes5. However, these laryngeal structures set insurmountable physiological limits to the frequency range and depth of their vocalizations, preventing them from escaping anthropogenic vessel noise12,13 and communicating at great depths14, thereby greatly reducing their active communication range.

The domestication of the larynx: The neural crest connection.

Wolves howl and dogs bark, both are able to produce variants of either vocalization, but we see a distinct difference in usage between wild and domesticate. Other domesticates also show distinct changes to their vocal output: domestic cats retain meows, a distinctly subadult trait in wildcats. Such differences in acoustic output are well-known, but the causal mechanisms remain little-studied. Potential links between domestication and vocal output are intriguing for multiple reasons, and offer a unique opportunity to explore a prominent hypothesis in domestication research: the neural crest/domestication syndrome hypothesis. This hypothesis suggests that in the early stages of domestication, selection for tame individuals decreased neural crest cell (NCCs) proliferation and migration, which led to a downregulation of the sympathetic arousal system, and hence reduced fear and reactive aggression. NCCs are a transitory stem cell population crucial during embryonic development that tie to diverse tissue types and organ systems. One of these neural-crest derived systems is the larynx, the main vocal source in mammals. We argue that this connection between NCCs and the larynx provides a powerful test of the predictions of the neural crest/domestication syndrome hypothesis, discriminating its predictions from those of other current hypotheses concerning domestication.

Rapid evolution of the primate larynx?

Tissue vibrations in the larynx produce most sounds that comprise vocal communication in mammals. Larynx morphology is thus predicted to be a key target for selection, particularly in species with highly developed vocal communication systems. Here, we present a novel database of digitally modeled scanned larynges from 55 different mammalian species, representing a wide range of body sizes in the primate and carnivoran orders. Using phylogenetic comparative methods, we demonstrate that the primate larynx has evolved more rapidly than the carnivoran larynx, resulting in a pattern of larger size and increased deviation from expected allometry with body size. These results imply fundamental differences between primates and carnivorans in the balance of selective forces that constrain larynx size and highlight an evolutionary flexibility in primates that may help explain why we have developed complex and diverse uses of the vocal organ for communication.

Social dynamics impact scolding behaviour in captive groups of common ravens (Corvus corax).

BACKGROUND: Predator avoidance can have immense impacts on fitness, yet individual variation in the expression of anti-predator behaviour remains largely unexplained. Existing research investigating learning of novel predators has focused either on individuals or groups, but not both. Testing in individual settings allows evaluations of learning or personality differences, while testing in group settings makes it impossible to distinguish any such individual differences from social dynamics. In this study, we investigate the effect of social dynamics on individual anti-predator behaviour. We trained 15 captive ravens to recognize and respond to a novel experimental predator and then exposed them to this predator in both group and isolation settings across 1.5 years to tease apart individual differences from social effects and evaluate two hypotheses: (1) weaker anti-predator responses of some individuals in the group occurred, because they failed to recognize the experimental predator as a threat, leading to weak responses when separated, or (2) some individuals had learned the new threat, but their scolding intensity was repressed in the group trials due to social dynamics (such as dominance rank), leading to increased scolding intensity when alone. RESULTS: We found that dominance significantly influences scolding behaviour in the group trials; top-ranked individuals scold more and earlier than lower ranking ones. However, in the separation trials scolding duration is no longer affected by rank. CONCLUSIONS: We speculate that, while top-ranked individuals use their anti-predator responses to signal status in the group, lower-ranking ravens may be suppressed from, or are less capable of, performing intense anti-predator behaviour while in the group. This suggests that, in addition to its recruitment or predator-deterrent effects, alarm calling may serve as a marker of individual quality to conspecifics.

Vocal flexibility in a eusocial rodent.

Vocal production learning-the ability to learn new sounds-is fundamental to human communication and is also seen in many nonhuman species, including birds, bats, elephants, and marine mammals. A new paper in Science may add an unusual rodent species-the naked mole rat-to this list.

Why evolve consciousness? Neural credit and blame allocation as a core function of consciousness.

I concur with Merker and colleague's critiques, suggesting that hypotheses about the evolutionary function of consciousness can help address them. Brains are parallel systems that function to compute possible actions and predict outcomes. I hypothesize that a core function of consciousness per se is the global feedback of information about those actions actually executed, supporting local learning via neuronal updating.

Toward inclusive theories of the evolution of musicality.

We compare and contrast the 60 commentaries by 109 authors on the pair of target articles by Mehr et al. and ourselves. The commentators largely reject Mehr et al.'s fundamental definition of music and their attempts to refute (1) our social bonding hypothesis, (2) byproduct hypotheses, and (3) sexual selection hypotheses for the evolution of musicality. Instead, the commentators generally support our more inclusive proposal that social bonding and credible signaling mechanisms complement one another in explaining cooperation within and competition between groups in a coevolutionary framework (albeit with some confusion regarding terminologies such as "byproduct" and "exaptation"). We discuss the proposed criticisms and extensions, with a focus on moving beyond adaptation/byproduct dichotomies and toward testing of cross-species, cross-cultural, and other empirical predictions.

Dynamic hierarchical cognition: Music and language demand further types of abstracta.

Hierarchical structures are rapidly and flexibly built up in the domains of human language and music. These domains require a tree-building capacity - "dendrophilia" - to dynamically infer hierarchical structures from sensory input (or to hierarchically structure output), based on subunits stored in a lexicon. This dynamic process involves a crucial class of abstracta overlooked in the target article.

Music as a coevolved system for social bonding.

Why do humans make music? Theories of the evolution of musicality have focused mainly on the value of music for specific adaptive contexts such as mate selection, parental care, coalition signaling, and group cohesion. Synthesizing and extending previous proposals, we argue that social bonding is an overarching function that unifies all of these theories, and that musicality enabled social bonding at larger scales than grooming and other bonding mechanisms available in ancestral primate societies. We combine cross-disciplinary evidence from archeology, anthropology, biology, musicology, psychology, and neuroscience into a unified framework that accounts for the biological and cultural evolution of music. We argue that the evolution of musicality involves gene-culture coevolution, through which proto-musical behaviors that initially arose and spread as cultural inventions had feedback effects on biological evolution because of their impact on social bonding. We emphasize the deep links between production, perception, prediction, and social reward arising from repetition, synchronization, and harmonization of rhythms and pitches, and summarize empirical evidence for these links at the levels of brain networks, physiological mechanisms, and behaviors across cultures and across species. Finally, we address potential criticisms and make testable predictions for future research, including neurobiological bases of musicality and relationships between human music, language, animal song, and other domains. The music and social bonding hypothesis provides the most comprehensive theory to date of the biological and cultural evolution of music.

Common marmosets are sensitive to simple dependencies at variable distances in an artificial grammar.

Recognizing that two elements within a sequence of variable length depend on each other is a key ability in understanding the structure of language and music. Perception of such interdependencies has previously been documented in chimpanzees in the visual domain and in human infants and common squirrel monkeys with auditory playback experiments, but it remains unclear whether it typifies primates in general. Here, we investigated the ability of common marmosets (Callithrix jacchus) to recognize and respond to such dependencies. We tested subjects in a familiarization-discrimination playback experiment using stimuli composed of pure tones that either conformed or did not conform to a grammatical rule. After familiarization to sequences with dependencies, marmosets spontaneously discriminated between sequences containing and lacking dependencies ('consistent' and 'inconsistent', respectively), independent of stimulus length. Marmosets looked more often to the sound source when hearing sequences consistent with the familiarization stimuli, as previously found in human infants. Crucially, looks were coded automatically by computer software, avoiding human bias. Our results support the hypothesis that the ability to perceive dependencies at variable distances was already present in the common ancestor of all anthropoid primates (Simiiformes).

Birds have primate-like numbers of neurons in the forebrain.

Some birds achieve primate-like levels of cognition, even though their brains tend to be much smaller in absolute size. This poses a fundamental problem in comparative and computational neuroscience, because small brains are expected to have a lower information-processing capacity. Using the isotropic fractionator to determine numbers of neurons in specific brain regions, here we show that the brains of parrots and songbirds contain on average twice as many neurons as primate brains of the same mass, indicating that avian brains have higher neuron packing densities than mammalian brains. Additionally, corvids and parrots have much higher proportions of brain neurons located in the pallial telencephalon compared with primates or other mammals and birds. Thus, large-brained parrots and corvids have forebrain neuron counts equal to or greater than primates with much larger brains. We suggest that the large numbers of neurons concentrated in high densities in the telencephalon substantially contribute to the neural basis of avian intelligence.

Japanese macaque phonatory physiology.

Although the call repertoire and its communicative function are relatively well explored in Japanese macaques (Macaca fuscata), little empirical data are available on the physics and the physiology of this species' vocal production mechanism. Here, a 6 year old female Japanese macaque was trained to phonate under an operant conditioning paradigm. The resulting 'coo' calls and spontaneously uttered 'growl' and 'chirp' calls were recorded with sound pressure level (SPL) calibrated microphones and electroglottography (EGG), a non-invasive method for assessing the dynamics of phonation. A total of 448 calls were recorded, complemented by ex vivo recordings on an excised Japanese macaque larynx. In this novel multidimensional investigative paradigm, in vivo and ex vivo data were matched via comparable EGG waveforms. Subsequent analysis suggests that the vocal range (range of fundamental frequency and SPL) of the macaque was comparable to that of a 7-10 year old human, with the exception of low intensity chirps, the production of which may be facilitated by the species' vocal membranes. In coo calls, redundant control of fundamental frequency in relation to SPL was also comparable to that in humans. EGG data revealed that growls, coos and chirps were produced by distinct laryngeal vibratory mechanisms. EGG further suggested changes in the degree of vocal fold adduction in vivo, resulting in spectral variation within the emitted coo calls, ranging from 'breathy' (including aerodynamic noise components) to 'non-breathy'. This is again analogous to humans, corroborating the notion that phonation in humans and non-human primates is based on universal physical and physiological principles.

A technological framework for running and analyzing animal head turning experiments.

Head turning experiments are widely used to test the cognition of both human infants and non-human animal species. Monitoring head turns allows researchers to non-invasively assess attention to acoustic or visual stimuli. In the majority of head turning experiments, the head direction analyses have been accomplished manually, which is extremely labor intensive and can be affected by subjectivity or other human errors and limitations. In the current study, we introduce an open-source computer program for measuring head directions of freely moving animals including common marmoset monkeys (Callithrix jacchus), American alligators (Alligator mississippiensis), and Mongolian gerbils (Meriones unguiculatus) to reduce human effort and time in video coding. We also illustrate an exemplary framework for an animal head turning experiment with common marmoset monkeys. This framework incorporates computer-aided processes of data acquisition, preprocessing, and analysis using the aforementioned software and additional open-source software and hardware.

Overtone-based pitch selection in hermit thrush song: unexpected convergence with scale construction in human music.

Many human musical scales, including the diatonic major scale prevalent in Western music, are built partially or entirely from intervals (ratios between adjacent frequencies) corresponding to small-integer proportions drawn from the harmonic series. Scientists have long debated the extent to which principles of scale generation in human music are biologically or culturally determined. Data from animal "song" may provide new insights into this discussion. Here, by examining pitch relationships using both a simple linear regression model and a Bayesian generative model, we show that most songs of the hermit thrush (Catharus guttatus) favor simple frequency ratios derived from the harmonic (or overtone) series. Furthermore, we show that this frequency selection results not from physical constraints governing peripheral production mechanisms but from active selection at a central level. These data provide the most rigorous empirical evidence to date of a bird song that makes use of the same mathematical principles that underlie Western and many non-Western musical scales, demonstrating surprising convergence between human and animal "song cultures." Although there is no evidence that the songs of most bird species follow the overtone series, our findings add to a small but growing body of research showing that a preference for small-integer frequency ratios is not unique to humans. These findings thus have important implications for current debates about the origins of human musical systems and may call for a reevaluation of existing theories of musical consonance based on specific human vocal characteristics.

A major blow to primate neonatal imitation and mirror neuron theory.

Keven & Akins' (K&A's) compelling new hypothesis explaining the developmental and neural basis of neonatal tongue protrusion has important implications for current understanding of primate imitation and the explanatory value of mirror neurons. If correct, this hypothesis eliminates a major source of evidence for neonatal imitation. I explore the implications this has for mirror neuron research and the arguments building upon them.

CATOS (Computer Aided Training/Observing System): Automating animal observation and training.

In animal behavioral biology, an automated observing/training system may be useful for several reasons: (a) continuous observation of animals for documentation of specific, irregular events, (b) long-term intensive training of animals in preparation for behavioral experiments, (c) elimination of potential cues and biases induced by humans during training and testing. Here, we describe an open-source-based system named CATOS (Computer Aided Training/Observing System) developed for such situations. There are several notable features in this system. CATOS is flexible and low cost because it is based on free open-source software libraries, common hardware parts, and open-system electronics based on Arduino. Automated video condensation is applied, leading to significantly reduced video data storage compared to the total active hours of the system. A data-viewing utility program helps a user browse recorded data quickly and more efficiently. With these features, CATOS has the potential to be applied to many different animal species in various environments such as laboratories, zoos, or even private homes. Also, an animal's free access to the device without constraint, and a gamified learning process, enhance the animal's welfare and enriches their environment. As a proof of concept, the system was built and tested with two different species. Initially, the system was tested for approximately 10 months with a domesticated cat. The cat was successfully and fully automatically trained to discriminate three different spoken words. Then, in order to test the system's adaptability to other species and hardware components, we used it to train a laboratory rat for 3 weeks.

Honest signaling in domestic piglets (Sus scrofa domesticus): vocal allometry and the information content of grunt calls.

The information conveyed in acoustic signals is a central topic in mammal vocal communication research. Body size is one form of information that can be encoded in calls. Acoustic allometry aims to identify the specific acoustic correlates of body size within the vocalizations of a given species, and formants are often a useful acoustic cue in this context. We conducted a longitudinal investigation of acoustic allometry in domestic piglets (Sus scrofa domesticus), asking whether formants of grunt vocalizations provide information concerning the caller's body size over time. On four occasions, we recorded grunts from 20 kunekune piglets, measured their vocal tract length by means of radiographs (X-rays) and weighed them. Controlling for effects of age and sex, we found that body weight strongly predicts vocal tract length, which in turn determines formant frequencies. We conclude that grunt formant frequencies could allow domestic pigs to assess a signaler's body size as it grows. Further research using playback experiments is needed to determine the perceptual role of formants in domestic pig communication.

Phonological perception by birds: budgerigars can perceive lexical stress.

Metrical phonology is the perceptual "strength" in language of some syllables relative to others. The ability to perceive lexical stress is important, as it can help a listener segment speech and distinguish the meaning of words and sentences. Despite this importance, there has been little comparative work on the perception of lexical stress across species. We used a go/no-go operant paradigm to train human participants and budgerigars (Melopsittacus undulatus) to distinguish trochaic (stress-initial) from iambic (stress-final) two-syllable nonsense words. Once participants learned the task, we presented both novel nonsense words, and familiar nonsense words that had certain cues removed (e.g., pitch, duration, loudness, or vowel quality) to determine which cues were most important in stress perception. Members of both species learned the task and were then able to generalize to novel exemplars, showing categorical learning rather than rote memorization. Tests using reduced stimuli showed that humans could identify stress patterns with amplitude and pitch alone, but not with only duration or vowel quality. Budgerigars required more than one cue to be present and had trouble if vowel quality or amplitude were missing as cues. The results suggest that stress patterns in human speech can be decoded by other species. Further comparative stress-perception research with more species could help to determine what species characteristics predict this ability. In addition, tests with a variety of stimuli could help to determine how much this ability depends on general pattern learning processes versus vocalization-specific cues.

A novel approach to investigate recursion and iteration in visual hierarchical processing.

We describe a new method to explore recursive cognition in the visual domain. We define recursion as the ability to represent multiple hierarchical levels using the same rule, entailing the ability to generate new levels beyond those previously encountered. With this definition recursion can be distinguished from general hierarchical embedding. To investigate this recursion/hierarchy distinction in the visual domain, we developed two novel methods: The Visual Recursion Task (VRT), in which an inferred rule is used to represent new hierarchical levels, and the Embedded Iteration Task (EIT), in which additional elements are added to an existing hierarchical level. We found that adult humans can represent recursion in the visuo-spatial domain, and that this ability is distinct from both general intelligence and the ability to represent iterative processes embedded within hierarchical structures. Compared with embedded iteration, visual recursion correlated positively with other recursive planning tasks (Tower of Hanoi), but not with specific visuo-spatial resources (spatial short-term memory and working memory). We conclude that humans are able to use recursive representations to process complex visuo-spatial hierarchies and that our visual recursion task taps into specific cognitive resources. This method opens exciting opportunities to explore the relationship between visual recursion and language.