Transcriptional neoteny in the human brain

doi:10.1073/pnas.0900544106

Transcriptional neoteny in the human brain

^aPartner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China;
^bMax Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany;
^cMax Planck Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany;
^dInstitute of Biotechnology, University of Cambridge, Cambridge CB2 1TN, United Kingdom;
^eStanley Medical Research Institute, 9800 Medical Center Drive, Rockville, MD 20850; and
^fMacquarie Group Foundation Chair of Schizophrenia Research, Schizophrenia Research Institute, Prince of Wales Medical Research Institute, University of New South Wales, Sydney, NSW 2052, Australia

Edited by Morris Goodman, Wayne State University, School of Medicine, Detroit, MI, and approved February 18, 2009
↵²M.L., S.P., and P.K. contributed equally as supervisors of this study. (received for review January 16, 2009)

Abstract

In development, timing is of the utmost importance, and the timing of developmental processes often changes as organisms evolve. In human evolution, developmental retardation, or neoteny, has been proposed as a possible mechanism that contributed to the rise of many human-specific features, including an increase in brain size and the emergence of human-specific cognitive traits. We analyzed mRNA expression in the prefrontal cortex of humans, chimpanzees, and rhesus macaques to determine whether human-specific neotenic changes are present at the gene expression level. We show that the brain transcriptome is dramatically remodeled during postnatal development and that developmental changes in the human brain are indeed delayed relative to other primates. This delay is not uniform across the human transcriptome but affects a specific subset of genes that play a potential role in neural development.

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Footnotes

¹To whom correspondence may be addressed. E-mail: somel{at}eva.mpg.de or khaitovich{at}eva.mpg.de
Author contributions: S.B., M.J.W., C.S.W., M.L., S.P., and P.K. designed research; H.F., Z.Y., A.L., and B.N. performed research; A.L., S.G., T.G., J.K., M.D., S.B., M.J.W., and C.S.W. contributed new reagents/analytic tools; M.S., M.L., and P.K. analyzed data; and M.S., M.L., S.P., and P.K. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (GEO accession nos. GSE11528, GSE11512, and GSE15163).
This article contains supporting information online at www.pnas.org/cgi/content/full/0900544106/DCSupplemental.
Freely available online through the PNAS open access option.