( A) Diagram of the vocal learning–related brain regions and circuits in oscine songbirds and human. These neural pathways are either absent in vocal nonlearning species or rudimentary in many species according to a continuum hypothesis of vocal learning ( Wild et al. The shared neural pathways consist of a cortico-striato-thalamo-cortical loop essential for learning and a motor cortex direct projection from the forebrain vocal motor control regions to the brainstem vocal motor neurons ( Fig. 1997 Petkov and Jarvis 2012) and specialized gene expression in the brain regions comprising the neural pathways ( Hara et al. 2010 Petkov and Jarvis 2012) specialized neural pathways that control the vocal organs (syrinx in birds, larynx in mammals) ( Wild et al. Vocal learning species share a number of characteristic traits not found in vocal nonlearning species including: critical periods for learned imitation of new sounds infant babbling deafness induced deterioration of vocalization dialects ( Doupe and Kuhl 1999 Bolhuis et al.
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Vocal learning evolved independently in humans and at least four nonhuman mammalian lineages (cetaceans, bats, elephants, and pinnipeds) and three avian lineages (oscine songbirds, parrots, and hummingbirds) ( Petkov and Jarvis 2012). Vocal learning is a critical component of spoken language in humans, but understanding of the molecular mechanisms underlying vocal learning and human speech development remains incomplete. These findings reveal strong candidate noncoding regions near genes for the evolutionary adaptations that distinguish vocal learning species from their close vocal nonlearning relatives and provide further evidence of molecular convergence between birdsong and human spoken language. We also found enrichment near the SFARI class S genes associated with syndromic vocal communication forms of autism spectrum disorders.
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We found avian vocal learner-specific ARs, and they were enriched in noncoding regions near genes with known speech functions or brain gene expression specializations in humans and vocal learning birds, including FOXP2, NEUROD6, ZEB2, and MEF2C, and near genes with major neurodevelopmental functions, including NR2F1, NRP2, and BCL11B. To understand the evolutionary basis of vocal learning gene specializations and convergence, we searched for and identified accelerated genomic regions (ARs), a marker of positive selection, specific to vocal learning birds. Humans and each of these three bird clades exhibit specialized behavioral, neuroanatomical, and brain gene expression convergence related to vocal learning, speech, and song.
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Vocal learning, the ability to imitate sounds from conspecifics and the environment, is a key component of human spoken language and learned song in three independently evolved avian groups-oscine songbirds, parrots, and hummingbirds.