Variation in vocal production learning across songbirds

Songbirds as a whole are considered to be vocal production learners, meaning that they modify the structure of their vocalizations as a result of experience with the vocalizations of others. The more than 4000 species of songbirds, however, vary greatly in crucial features of song development. Variable features include: (i) the normality of the songs of early-deafened birds, reflecting the importance of innate motor programmes in song development; (ii) the normality of the songs of isolation-reared birds, reflecting the combined importance of innate auditory templates and motor programmes; (iii) the degree of selectivity in choice of external models; (iv) the accuracy of copying from external models; and (v) whether or not learning from external models continues into adulthood. We suggest that because of this variability, some songbird species, specifically those that are able to develop songs in the normal range without exposure to external models, can be classified as limited vocal learners. Those species that require exposure to external models to develop songs in the normal range can be considered complex vocal learners. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Effects of domestication on neophobia: A comparison between the domesticated Bengalese finch (Lonchura striata var. domestica) and its wild ancestor, the white-rumped munia (Lonchura striata)

Bengalese finches (Lonchura striata var. domestica) have more complex song traits than their wild ancestors, white-rumped munias (Lonchura striata). Domesticated finches are likely able to allocate more resources to song development rather than allocating resources to mechanisms aimed at coping with predation, which are no longer needed under domesticated conditions. Here, we aimed to examine the effects of changes in selection pressure due to domestication on the behaviour of Bengalese finches and to contemplate the possible evolutionary mechanisms underlying these changes. To do so, we compared neophobic responses to novel-object conditions as an assessment of reactions to potential predators. We studied groups of Bengalese finches and white-rumped munias and found that Bengalese finches were more likely to eat the food provided to them under novel-object conditions. Bengalese finches had a shorter latency time to eat, and this latency time was less affected by the novel object in the case of Bengalese finches compared to white-rumped munias. Therefore, Bengalese finches have reduced neophobic responses due to domestication. The behavioural strategies of white-rumped munias appear to be more suitable for natural environments, which include unpredictable risks, whereas Bengalese finches have likely adapted their behaviour to the conditions of artificial selection.

Addition of new neurons and the emergence of a local neural circuit for precise timing

During development, neurons arrive at local brain areas in an extended period of time, but how they form local neural circuits is unknown. Here we computationally model the emergence of a network for precise timing in the premotor nucleus HVC in songbird. We show that new projection neurons, added to HVC post hatch at early stages of song development, are recruited to the end of a growing feedforward network. High spontaneous activity of the new neurons makes them the prime targets for recruitment in a self-organized process via synaptic plasticity. Once recruited, the new neurons fire readily at precise times, and they become mature. Neurons that are not recruited become silent and replaced by new immature neurons. Our model incorporates realistic HVC features such as interneurons, spatial distributions of neurons, and distributed axonal delays. The model predicts that the birth order of the projection neurons correlates with their burst timing during the song.

Born to sing! Song development in a singing primate

In animal vocal communication, the development of adult-like vocalization is fundamental to interact appropriately with conspecifics. However, the factors that guide ontogenetic changes in the acoustic features remains poorly understood. In contrast with a historical view of nonhuman primate vocal production as substantially innate, recent research suggests that inheritance and physiological modification can only explain some of the developmental changes in call structure during growth. A particular case of acoustic communication is the indris' singing behavior, a peculiar case among Strepsirrhine primates. Thanks to a decade of intense data collection, this work provides the first long-term quantitative analysis on song development in a singing primate. To understand the ontogeny of such a complex vocal output, we investigated juvenile and sub-adult indris' vocal behaviour, and we found that young individuals started participating in the chorus years earlier than previously reported. Our results indicated that spectro-temporal song parameters underwent essential changes during growth. In particular, the age and sex of the emitter influenced the indris' vocal activity. We found that frequency parameters showed consistent changes across the sexes, but the temporal features showed different developmental trajectories for males and females. Given the low level of morphological sexual dimorphism and the marked differences in vocal behavior, we hypothesize that factors like social influences and auditory feedback may affect songs' features, resulting in high vocal flexibility in juvenile indris. This trait may be pivotal in a species that engages in choruses with rapid vocal turn-taking.

Singing-related reorganization of the song motor circuit is accompanied by a shift in hormonal modulation of song

Sex hormones are essential modulators of birdsong. Testosterone, and its active androgenic and estrogenic metabolites, 5α-dihydrotestosterone (DHT) and estradiol, can re-shape the brain circuits responsible for song learning and production. The differential mechanisms of action of these different hormones during song development and song maintenance are, nonetheless, not fully understood. Here we demonstrate that unlike testosterone, DHT treatment does not induce singing behavior in naïve adult female canaries that have never previously produced song. However, in birds with previous testosterone-induced singing experience, DHT alone is enough to promote the re-acquisition of high quality songs, even after months of silence. In addition, we show that the synaptic reorganization that accompanies vocal motor skill development requires more than DHT-induced androgen receptor activation. These results indicate that vocal motor practice will persistently modify the hormone-sensitive brain circuit responsible for song production, suggesting a mechanistic differentiation in the hormone-dependent regulation of the initial vocal motor skill acquisition and later re-acquisition.

Zebra finches go wild! Experimental cultural evolution of birdsong

Vocal learning in songbirds is guided by experience and experience-independent factors. Previously, lineages of zebra finches founded by isolate-reared tutors showed cultural evolution to wild-type song. This suggests that experience-independent biases affect song development even in the absence of wild-type song. We hypothesized that cultural evolution of song depends on both experience-independent biases and tutor songs available. We predicted that songs more distant from wild-type would take longer to culturally evolve toward wild-type features. We bred zebra finches in three groups of lineages in which offspring of each generation served as tutors for the next. Lineages were founded with males singing wild-type song, isolate song, or heterospecific song. The two experimental lineages exhibited rapid cultural evolution of song with many temporal and spectral features converging to wild-type within two generations. However the rate of change differed depending on song features measured, and took longer for lineages founded with heterospecific song.