Behaviourally driven gene expression reveals song nuclei in hummingbird brain

Abstract

Hummingbirds have developed a wealth of intriguing features, such as backwards flight, ultraviolet vision, extremely high metabolic rates, nocturnal hibernation, high brain-to-body size ratio and a remarkable species–specific diversity of vocalizations1,2,3,4. Like humans, they have also developed the rare trait of vocal learning, this being the ability to acquire vocalizations through imitation rather than instinct5,6. Here we show, using behaviourally driven gene expression in freely ranging tropical animals, that the forebrain of hummingbirds contains seven discrete structures that are active during singing, providing the first anatomical and functional demonstration of vocal nuclei in hummingbirds. These structures are strikingly similar to seven forebrain regions that are involved in vocal learning and production in songbirds and parrots7,8,9,10,11,12,13—the only other avian orders known to be vocal learners5. This similarity is surprising, as songbirds, parrots and hummingbirds are thought to have evolved vocal learning and associated brain structures independently5,14, and it indicates that strong constraints may influence the evolution of forebrain vocal nuclei.

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Figure 1: Song sonograms (frequency versus time) of the hummingbird species studied: Aphantochroa cirrhochloris and Glaucis hirsuta15.
Figure 2: Identification of vocal control brain areas.
Figure 3: Quantification of ZENK expression.
Figure 4: Comparative brain anatomy of hearing- and vocalizing-induced ZENK expression in avian vocal learners.

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Acknowledgements

We thank the Museu de Biologia Mello Leitão (MBML) in Espírito Santo, Brazil, S. Mendes and D. Loss for providing a natural space and services that made this project possible. We also thank the MBML and A. Ruschi for permission to partially reproduce hummingbird illustrations by E. Demonte; P. Rousselot, K. S. Leon and A. Ferreira for help with recordings, sonograms and behavioural scoring; P. Delgado for histological assistance; S. Baumwell and L. Moore for help in manuscript preparation; S. Durand, R. Mooney and S. Nowicki for comments on the manuscript; L. Katz and N. Cant for use of microscope equipment; J. Ahlquist for discussions on avian evolution; C. Cunningham for assistance with phylogenetic analysis; and F. Nottebohm for his support. This project was approved by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) and Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq); funding was provided by the Kluge Trust Fund and Duke University start-up funds to E.D.J., an NIDCD grant to C.V.M., and personal funds by E.D.J. and C.V.M. We dedicate this paper to the memory of L. Baptista, a pioneer of vocal communication in hummingbirds.

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Correspondence to Claudio V. Mello.

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Jarvis, E., Ribeiro, S., da Silva, M. et al. Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406, 628–632 (2000). https://doi.org/10.1038/35020570

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