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Evolutionary origins of vocal mimicry in songbirds.

ABSTRACT: Vocal learning is an important behavior in oscines (songbirds). Some songbird species learn heterospecific sounds as well as conspecific vocalizations. The emergence of vocal mimicry is necessarily tied to the evolution of vocal learning, as mimicry requires the ability to acquire sounds through learning. As such, tracking the evolutionary origins of vocal mimicry may provide insights into the causes of variation in song learning programs among songbirds. We compiled a database of known vocal mimics that comprised 339 species from 43 families. We then traced the evolutionary history of vocal mimicry across the avian phylogeny using ancestral trait reconstruction on a dataset of oscine passerines for which vocalizations have been described. We found that the common ancestor to oscines was unlikely to mimic sounds, suggesting that song learning evolved with mechanisms to constrain learning to conspecific models. Mimicry then evolved repeatedly within the songbird clade, either through relaxation of constraints on conspecific learning or through selection for active vocal mimicry. Vocal mimicry is likely ancestral in only a handful of clades, and we detect many instances of independent origins of mimicry. Our analysis underscores the liability of vocal mimicry in songbirds, and highlights the evolutionary flexibility of song learning mechanisms.

SUBMITTER: Goller M

PROVIDER: S-EPMC6121844 | biostudies-other | 2018 Aug

REPOSITORIES: biostudies-other

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Evolutionary origins of vocal mimicry in songbirds.

Goller Maria M Shizuka Daizaburo D

Evolution letters 20180622 4

Vocal learning is an important behavior in oscines (songbirds). Some songbird species learn heterospecific sounds as well as conspecific vocalizations. The emergence of vocal mimicry is necessarily tied to the evolution of vocal learning, as mimicry requires the ability to acquire sounds through learning. As such, tracking the evolutionary origins of vocal mimicry may provide insights into the causes of variation in song learning programs among songbirds. We compiled a database of known vocal mi ...[more]

PMID: 30283692

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Project description:The development of highly complex vocal skill, like human language and bird songs, is underlain by learning. Vocal learning, even when occurring in adulthood, is thought to largely depend on a sensitive/critical period during postnatal development, and learned vocal patterns emerge gradually as the long-term consequence of vocal practice during this critical period. In this scenario, it is presumed that the effect of vocal practice is thus mainly limited by the intrinsic timing of age-dependent maturation factors that close the critical period and reduce neural plasticity. However, an alternative, as-yet untested hypothesis is that vocal practice itself, independently of age, regulates vocal learning plasticity. Here, we explicitly discriminate between the influences of age and vocal practice using a songbird model system. We prevented zebra finches from singing during the critical period of sensorimotor learning by reversible postural manipulation. This enabled to us to separate lifelong vocal experience from the effects of age. The singing-prevented birds produced juvenile-like immature song and retained sufficient ability to acquire a tutored song even at adulthood when allowed to sing freely. Genome-wide gene expression network analysis revealed that this adult vocal plasticity was accompanied by an intense induction of singing activity-dependent genes, similar to that observed in juvenile birds, rather than of age-dependent genes. The transcriptional changes of activity-dependent genes occurred in the vocal motor robust nucleus of the arcopallium (RA) projection neurons that play a critical role in the production of song phonology. These gene expression changes were accompanied by neuroanatomical changes: dendritic spine pruning in RA projection neurons. These results show that self-motivated practice itself changes the expression dynamics of activity-dependent genes associated with vocal learning plasticity and that this process is not tightly linked to age-dependent maturational factors.

Dataset Information

Evolutionary origins of vocal mimicry in songbirds.

Publications

Evolutionary origins of vocal mimicry in songbirds.

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