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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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References

  1. Schuchmann, K.-L. in Handbook of the birds of the world: barn-owls to hummingbirds (eds del Hoyo, J., Elliott, A. & Sargatal, J.) 468– 680 (Lynx Ediciones, Barcelona, 1999).

    Google Scholar 

  2. Ventura, D. F. & Takase, E. Ultraviolet color discrimination in the hummingbird. Invest. Ophthalmol. Vis. Sci. 35 , 2168 (1994).

    Google Scholar 

  3. Rehkamper, G., Schuchmann, K. L., Schleicher, A. & Zilles, K. Encephalization in hummingbirds (Trochilidae). Brain Behav. Evol. 37, 85–91 ( 1991).

    Article  CAS  Google Scholar 

  4. Vielliard, J. Catálogo sonográfico dos cantos e piados dos beija-flores do Brasil. Boletim do Museu de Biologia “Mello Leitão” Série Biologia 58, 1–20 (1983).

    Google Scholar 

  5. Nottebohm, F. The origins of vocal learning. Am. Nat. 106, 116–140 (1972).

    Article  Google Scholar 

  6. Baptista, L. F. & Schuchmann, K. L. Song learning in the anna hummingbird (Calypte anna). Ethology 84, 15–26 (1990).

    Article  Google Scholar 

  7. Nottebohm, F., Stokes, T. M. & Leonard, C. M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165, 457– 486 (1976).

    Article  CAS  Google Scholar 

  8. Scharff, C. & Nottebohm, F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11, 2896–2913 (1991).

    Article  CAS  Google Scholar 

  9. Yu, A. C. & Margoliash, D. Temporal hierarchical control of singing in birds. Science 273, 1871– 1875 (1996).

    Article  ADS  CAS  Google Scholar 

  10. Hessler, N. A. & Doupe, A. J. Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. J. Neurosci. 19, 10461– 10481 (1999).

    Article  CAS  Google Scholar 

  11. Durand, S. E., Heaton, J. T., Amateau, S. K. & Brauth, S. E. Vocal control pathways through the anterior forebrain of a parrot (Melopsittacus undulatus). J. Comp. Neurol. 377, 179 –206 (1997).

    Article  CAS  Google Scholar 

  12. Jarvis, E. D., Scharff, C., Grossman, M. R., Ramos, J. A. & Nottebohm, F. For whom the bird sings: context-dependent gene expression. Neuron 21, 775– 788 (1998).

    Article  CAS  Google Scholar 

  13. Jarvis, E. D. & Mello, C. V. Molecular mapping of brain areas involved in parrot vocal communication. J. Comp. Neurol. 419, 1–31 (2000).

    Article  CAS  Google Scholar 

  14. Brenowitz, E. A. Comparative approaches to the avian song system. J. Neurobiol. 33, 517–531 ( 1997).

    Article  CAS  Google Scholar 

  15. Ruschi, A. Hummingbirds of State of Espirito Santo (Rios Editora, São Paulo, 1982).

    Google Scholar 

  16. Chaudhuri, A. Neural activity mapping with inducible transcription factors. Neuroreport 8, 5–9 ( 1997).

    Article  Google Scholar 

  17. Mello, C. V. & Clayton, D. F. Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J. Neurosci. 14, 6652– 6666 (1994).

    Article  CAS  Google Scholar 

  18. Jarvis, E. D., Schwabl, H., Ribeiro, S. & Mello, C. V. Brain gene regulation by territorial singing behavior in freely ranging songbirds. Neuroreport 8, 2073–2077 ( 1997).

    Article  CAS  Google Scholar 

  19. Wild, J. M., Dongfeng, L. & Eagleton, C. Projections of the dorsomedial nucleus of the intercollicular complex (DM) in relation to respiratory-vocal nuclei in the brainstem of pigeon (Columbia livia) and zebra finch (Taeniopygia guttata). J. Comp. Neurol. 377, 392–413 (1997).

    Article  CAS  Google Scholar 

  20. Nottebohm, F., Kelley, D. B. & Paton, J. A. Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207, 344 –357 (1982).

    Article  CAS  Google Scholar 

  21. Lidsky, T. I., Manetto, C. & Schneider, J. S. A consideration of sensory factors involved in motor functions of the basal ganglia. Brain Res. 356, 133–146 (1985).

    Article  CAS  Google Scholar 

  22. Guinee, L. H. & Payne, K. B. Rhyme-like repetitions in songs of humpback whales. Ethology 79, 295– 306 (1988).

    Article  Google Scholar 

  23. Esser, K. H. Audio-vocal learning in a non-human mammal: the lesser spear-nosed bat Phyllostomus discolor. Neuroreport 5, 1718–1720 (1994).

    Article  CAS  Google Scholar 

  24. Sibley, C. G. & Ahlquist, J. E. Phylogeny and Classification of Birds: A Study in Molecular Evolution (Yale Univ. Press, New Haven, 1990).

    Google Scholar 

  25. Kroodsma, D. E. & Konishi, M. A suboscine bird (eastern phoebe, Sayornis phoebe) develops normal song without auditory feedback. Anim. Behav. 42, 477– 487 (1991).

    Article  Google Scholar 

  26. Feduccia, A. Explosive evolution in tertiary birds and mammals. Science 267, 637–638 (1995).

    Article  ADS  CAS  Google Scholar 

  27. Koenig, C. Vocal patterns as interspecific isolating mechanisms in screech owls of the genus Otus (Aves: Strigidae) of southern South America. Stuttg. Beitr. Nat.kd. A Biol. 0(511), 1– 35 (1994).

    Google Scholar 

  28. Payne, R. B. in Current Ornithology (ed. Johnston, R. J.) 87–126 (Plenum, New York, 1986).

  29. Miller, E. H. in Ecology and evolution of acoustic communication in birds (eds Kroodsma, D. E. & Miller, E. H.) 241–257 (Cornell Univ. Press, Ithaca, 1996).

    Google Scholar 

  30. Ellis, D. H., Swengel, S. R., Archibald, G. W. & Kepler, C. B. A sociogram for the cranes of the world. Behav. Processes 43, 125–151 (1998).

    Article  CAS  Google Scholar 

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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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