Biological predispositions in vocal learning have been proposed to underlie commonalities in vocal sequences, including for speech and birdsong, but cultural propagation could also account for such commonalities [1-4]. Songbirds such as the zebra finch learn the sequencing of their acoustic elements ("syllables") during development [5-8]. Zebra finches are not constrained to learn a specific sequence of syllables, but significant consistencies in the positioning and sequencing of syllables have been observed between individuals within populations and between populations [8-10]. To reveal biological predispositions in vocal sequence learning, we individually tutored juvenile zebra finches with randomized and unbiased sequences of syllables and analyzed the extent to which birds produced common sequences. In support of biological predispositions, birds tutored with randomized sequences produced songs with striking similarities. Birds preferentially started and ended their song sequence with particular syllables, consistently positioned shorter and higher frequency syllables in the middle of their song, and sequenced their syllables such that pitch alternated across adjacent syllables. These patterns are reminiscent of those observed in normally tutored birds, suggesting that birds "creolize" aberrant sequence inputs to produce normal sequence outputs. Similar patterns were also observed for syllables that were not used for tutoring (i.e., unlearned syllables), suggesting that motor biases could contribute to sequence learning biases. Furthermore, zebra finches spontaneously produced acoustic patterns that are commonly observed in speech and music, suggesting that sensorimotor processes that are shared across a wide range of vertebrates could underlie these patterns in humans.

Behavior is critically shaped during sensitive periods in development. Birdsong is a learned vocal behavior that undergoes dramatic plasticity during a sensitive period of sensorimotor learning. During this period, juvenile songbirds engage in vocal practice to shape their vocalizations into relatively stereotyped songs. By the time songbirds reach adulthood, their songs are relatively stable and thought to be "crystallized." Recent studies, however, highlight the potential for adult song plasticity and suggest that adult song could naturally change over time. As such, we investigated the degree to which temporal and spectral features of song changed over time in adult Bengalese finches. We observed that the sequencing and timing of song syllables became more stereotyped over time. Increases in the stereotypy of syllable sequencing were due to the pruning of infrequently produced transitions and, to a lesser extent, increases in the prevalence of frequently produced transitions. Changes in song tempo were driven by decreases in the duration and variability of intersyllable gaps. In contrast to significant changes to temporal song features, we found little evidence that the spectral structure of adult song syllables changed over time. These data highlight differences in the degree to which temporal and spectral features of adult song change over time and support evidence for distinct mechanisms underlying the control of syllable sequencing, timing, and structure. Furthermore, the observed changes to temporal song features are consistent with a Hebbian framework of behavioral plasticity and support the notion that adult song should be considered a form of vocal practice.

Studying the macroevolution of the songs of Passeriformes (perching birds) has proved challenging. The complexity of the task stems not just from the macroevolutionary and macroecological challenge of modeling so many species, but also from the difficulty in collecting and quantifying birdsong itself. Using machine learning techniques, we extracted songs from a large citizen science dataset, and then analyzed the evolution, and biotic and abiotic predictors of variation in birdsong across 578 passerine species. Contrary to expectations, we found few links between life-history traits (monogamy and sexual dimorphism) and the evolution of song pitch (peak frequency) or song complexity (standard deviation of frequency). However, we found significant support for morphological constraints on birdsong, as reflected in a negative correlation between bird size and song pitch. We also found that broad-scale biogeographical and climate factors such as net primary productivity, temperature, and regional species richness were significantly associated with both the evolution and present-day distribution of bird song features. Our analysis integrates comparative and spatial modeling with newly developed data cleaning and curation tools, and suggests that evolutionary history, morphology, and present-day ecological processes shape the distribution of song diversity in these charismatic and important birds.

Understanding the factors that predict and guide variation in behavioral change can lend insight into mechanisms of motor plasticity and individual differences in behavior. The performance of adult birdsong changes with age in a manner that is similar to rapid context-dependent changes to song. To reveal mechanisms of vocal plasticity, we analyzed the degree to which variation in the direction and magnitude of age-dependent changes to Bengalese finch song could be predicted by variation in context-dependent changes. Using a repeated-measures design, we found that variation in age-dependent changes to the timing, sequencing, and structure of vocal elements ("syllables") was significantly predicted by variation in context-dependent changes. In particular, the degree to which the duration of intersyllable gaps, syllable sequencing at branch points, and fundamental frequency of syllables within spontaneous [undirected (UD)] songs changed over time was correlated with the degree to which these features changed from UD song to female-directed (FD) song in young-adult finches (FDyoung). As such, the structure of some temporal features of UD songs converged over time onto the structure of FDyoung songs. This convergence suggested that the FDyoung song could serve as a stable target for vocal motor plasticity. Consequently, we analyzed the stability of FD song and found that the temporal structure of FD song changed significantly over time in a manner similar to UD song. Because FD song is considered a state of heightened performance, these data suggest that age-dependent changes could reflect practice-related improvements in vocal motor performance.

Sensorimotor integration is the process through which the nervous system creates a link between motor commands and associated sensory feedback. This process allows for the acquisition and refinement of many behaviors, including learned communication behaviors such as speech and birdsong. Consequently, it is important to understand fundamental mechanisms of sensorimotor integration, and comparative analyses of this process can provide vital insight. Songbirds offer a powerful comparative model system to study how the nervous system links motor and sensory information for learning and control. This is because the acquisition, maintenance, and control of birdsong critically depend on sensory feedback. Furthermore, there is an incredible diversity of song organizations across songbird species, ranging from songs with simple, stereotyped sequences to songs with complex sequencing of vocal gestures, as well as a wide diversity of song repertoire sizes. Despite this diversity, the neural circuitry for song learning, control, and maintenance remains highly similar across species. Here, we highlight the utility of songbirds for the analysis of sensorimotor integration and the insights about mechanisms of sensorimotor integration gained by comparing different songbird species. Key conclusions from this comparative analysis are that variation in song sequence complexity seems to covary with the strength of feedback signals in sensorimotor circuits and that sensorimotor circuits contain distinct representations of elements in the vocal repertoire, possibly enabling evolutionary variation in repertoire sizes. We conclude our review by highlighting important areas of research that could benefit from increased comparative focus, with particular emphasis on the integration of new technologies.

No abstract

Birdsong is a learned communicative behavior that consists of discrete acoustic elements ("syllables") that are sequenced in a controlled manner. While the learning of the acoustic structure of syllables has been extensively studied, relatively little is known about sequence learning in songbirds. Statistical learning could contribute to the acquisition of vocal sequences, and we investigated the nature and extent of sequence learning at various levels of song organization in the Bengalese finch, Lonchura striata var. domestica. We found that, under semi-natural conditions, pupils (sons) significantly reproduced the sequence statistics of their tutor's (father's) songs at multiple levels of organization (e.g., syllable repertoire, prevalence, and transitions). For example, the probability of syllable transitions at "branch points" (relatively complex sequences that are followed by multiple types of transitions) were significantly correlated between the songs of tutors and pupils. We confirmed the contribution of learning to sequence similarities between fathers and sons by experimentally tutoring juvenile Bengalese finches with the songs of unrelated tutors. We also discovered that the extent and fidelity of sequence similarities between tutors and pupils were significantly predicted by the prevalence of sequences in the tutor's song and that distinct types of sequence modifications (e.g., syllable additions or deletions) followed distinct patterns. Taken together, these data provide compelling support for the role of statistical learning in vocal production learning and identify factors that could modulate the extent of vocal sequence learning.www.nature.com/scientificreports www.nature.com/scientificreports/ syllables. Some studies using experimental tutoring have confirmed the developmental acquisition of vocal sequencing 27-31 , but most of such studies have been conducted on species that produce stereotyped, relatively simple sequences of syllables (e.g., white-crowned sparrows and zebra finches) 26 . Understanding sequence learning in songbird species that produce more complex and variable sequencing is important not only for comparative reasons but also because such species produce syntactic structures that more closely resemble the complexity of syntax in human language 14 .The Bengalese finch (Lonchura striata var. domestica) offers an excellent opportunity to study the acquisition of relatively complex vocal sequences 32 . The songs of individual Bengalese finches consist of a discrete, learned repertoire of syllables that are arranged both in highly stereotyped sequences ("motifs" or "chunks") and in sequences that vary from rendition to rendition ("branch points"; Fig. 1) 26,[33][34][35][36][37][38][39][40] . Previous studies have provided some insight into vocal sequence learning in Bengalese finches by comparing songs between tutors and pupils 41-43 ; for example, Yamashita et al. (2008) analyzed the distribution of three-syllable sequences across two points in an individual's song development and...

Biological predispositions in learning can bias and constrain the cultural evolution of social and 33 communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and 34 cultural "universals". For example, surveys of laboratory and wild populations of zebra finches 35 (Taeniopygia guttata) document consistent patterning of vocal elements ("syllables") with respect to 36 their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are 37 also produced by birds that are experimentally tutored with songs containing randomly sequenced 38 syllables ("tutored birds"). Despite extensive demonstrations of learning biases, much remains to be 39 uncovered about the nature of biological predispositions that bias song learning and production in 40 songbirds. Here we examined the degree to which "innate" auditory templates and/or biases in vocal 41 motor production contribute to vocal learning biases and production in zebra finches. Such 42 contributions can be revealed by examining acoustic patterns in the songs of birds raised without 43 sensory exposure to song ("untutored birds") or of birds that are unable to hear from early in 44 development ("early-deafened birds"). We observed that untutored zebra finches and early-deafened 45 zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) 46 that resemble universal patterns observed in tutored birds. Similar to tutored birds, early-deafened 47 birds also produced song motifs with alternation in acoustic features across adjacent syllables. That 48 universal acoustic patterns are observed in the songs of both untutored and early-deafened birds 49 highlights the contribution motor production biases to the emergence of universals in culturally 50 transmitted behaviors.