Convergent transcriptional specializations in the brains of humans and song-learning birds
Structured Abstract
INTRODUCTION
Vocal learning, the ability to imitate sounds, is a trait that has undergone convergent evolution in several lineages of birds and mammals, including song-learning birds and humans. This behavior requires cortical and striatal vocal brain regions, which form unique connections in vocal-learning species. These regions have been found to have specialized gene expression within some species, but the patterns of specialization across vocal-learning bird and mammal species have not been systematically explored.
RATIONALE
The sequencing of genomes representing all major vocal-learning and vocal-nonlearning avian lineages has allowed us to develop the genomic tools to measure anatomical gene expression across species. Here, we asked whether behavioral and anatomical convergence is associated with gene expression convergence in the brains of vocal-learning birds and humans.
RESULTS
We developed a computational approach that discovers homologous and convergent specialized anatomical gene expression profiles. This includes generating hierarchically organized gene expression specialization trees for each species and a dynamic programming algorithm that finds the optimal alignment between species brain trees. We applied this approach to brain region gene expression databases of thousands of samples and genes that we and others generated from multiple species, including humans and song-learning birds (songbird, parrot, and hummingbird) as well as vocal-nonlearning nonhuman primates (macaque) and birds (dove and quail). Our results confirmed the recently revised understanding of the relationships between avian and mammalian brains. We further found that songbird Area X, a striatal region necessary for vocal learning, was most similar to a part of the human striatum activated during speech production. The RA (robust nucleus of the arcopallium) analog of song-learning birds, necessary for song production, was most similar to laryngeal motor cortex regions in humans that control speech production. More than 50 genes contributed to their convergent specialization and were enriched in motor control and neural connectivity functions. These patterns were not found in vocal nonlearners, but songbird RA was similar to layer 5 of primate motor cortex for another set of genes, supporting previous hypotheses about the similarity of these cell types between bird and mammal brains.
CONCLUSION
Our approach can accurately and quantitatively identify functionally and molecularly analogous brain regions between species separated by as much as 310 million years from a common ancestor. We were able to identify analogous brain regions for song and speech between birds and humans, and broader homologous brain regions in which these specialized song and speech regions are located, for tens to hundreds of genes. These genes now serve as candidates involved in developing and maintaining the unique connectivity and functional properties of vocal-learning brain circuits shared across species. The finding that convergent neural circuits for vocal learning are accompanied by convergent molecular changes of multiple genes in species separated by millions of years from a common ancestor indicates that brain circuits for complex traits may have limited ways in which they could have evolved from that ancestor.
Abstract
Song-learning birds and humans share independently evolved similarities in brain pathways for vocal learning that are essential for song and speech and are not found in most other species. Comparisons of brain transcriptomes of song-learning birds and humans relative to vocal nonlearners identified convergent gene expression specializations in specific song and speech brain regions of avian vocal learners and humans. The strongest shared profiles relate bird motor and striatal song-learning nuclei, respectively, with human laryngeal motor cortex and parts of the striatum that control speech production and learning. Most of the associated genes function in motor control and brain connectivity. Thus, convergent behavior and neural connectivity for a complex trait are associated with convergent specialized expression of multiple genes.
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Supplementary Material
Summary
Materials and Methods
Figs. S1 to S19
Tables S1 to S8
Resources
References and Notes
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Science
Volume 346 | Issue 6215
12 December 2014
12 December 2014
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Copyright © 2014, American Association for the Advancement of Science.
Submission history
Received: 2 June 2014
Accepted: 11 November 2014
Published in print: 12 December 2014
Acknowledgments
We thank H. Dressman and L.-L. Rowlette for microarray hybridizations, the Allen Institute for Brain Science for early access to human microarray data and human brain in situ hybridizations (and the Allen Institute founders, P. G. Allen and J. Allen, for their encouragement of that project), K. Simonyan for her coordinates of meta-analyses for speech regions, and S. Jarvis for help with imaging. Supported by NIH Directors Pioneer Award DP1 OD000448, National Institute on Deafness and Other Communication Disorders grant R01DC007218, and the Howard Hughes Medical Institute (E.D.J.). The brain gene expression atlas (ZEBrA) is supported by National Institute of General Medical Sciences grant R24GM092842 (C.V.M.). Marmoset experiments were supported by the Funding Program for World-leading Innovative R&D on Science and Technology (A.I.). Microarray data are available in the Gene Expression Omnibus (www.ncbi.nlm.nih.gov/geo) under accession numbers GSE33365 and GSE34819 (for songbird Area X), GSE28395 (for avian arcopallium regions), GSE33667 (for avian brainstem regions), and GSE31613 (for macaque brain regions); human microarray data are available from the Allen Human Brain Atlas site (http://human.brain-map.org/static/download). E.D.J., A.R.P., E.H., M.R., and P.R. conceived and designed the project; E.D.J., A.R.P., and A.J.H. wrote the paper; E.D.J., A.J.H., M.A.M., A.I., E.L., and C.V.M. co-supervised parts of the project; A.R.P. conducted most computational analyses; G.G., T.B., E.J.S., and A.J.H. conducted other computational analyses and supervision; E.H., M.R., O.W., and J.T.H. collected avian samples and performed microarray experiments; J.M., M.W., P.V.L., E.H., R.W., M.K., A.Bo., A.Be., C.V.M., and E.D.J. performed in situ hybridizations and analyses across species; G.Z., M.T.P.G., and E.D.J. provided genomes; and P.R., M.A.M., J.W.T., and E.J.S. performed proteomic experiments.
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