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http://dx.doi.org/10.1371/journal.pbio.0050013
* Published December 26, 2006 - RESEARCH ARTICLE
Rate of Evolution in Brain-Expressed Genes in Humans and Other Primates
Wang HY, Chien HC, Osada N, Hashimoto K, Sugano S, et al.
PLoS Biology Vol. 5, No. 2, e13 doi:10.1371/journal.pbio.0050013
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Rate of Evolution in Brain-Expressed Genes in Humans and Other Primates
Hurng-Yi Wang1,2?, Huan-Chieh Chien1, Naoki Osada3, Katsuyuki Hashimoto4,
Sumio Sugano5, Takashi Gojobori6, Chen-Kung Chou7, Shih-Feng Tsai8, Chung-I
Wu2*, C.-K. James Shen1*
1 Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan, 2
Department of Ecology and Evolution, University of Chicago, Chicago,
Illinois, United States of America, 3 Division of Biomedical Research
Resources, National Institute of Biomedical Innovation, Osaka, Japan, 4
Division of Genetic Resources, National Institute of Infectious Diseases,
Tokyo, Japan, 5 Laboratory of Functional Genomics, Department of Medical
Genome Sciences, Graduate School of Frontier Sciences, University of Tokyo,
Tokyo, Japan, 6 Center of Information Biology, National Institute of
Genetics, Mishima, Japan, 7 Department of Life Science, Chang Gung
University, Tao-Yuan, Taiwan, 8 Division of Molecular and Genomic Medicine,
National Health Research Institute, Miaoli, Taiwan
Brain-expressed genes are known to evolve slowly in mammals. Nevertheless,
since brains of higher primates have evolved rapidly, one might expect
acceleration in DNA sequence evolution in their brain-expressed genes. In
this study, we carried out full-length cDNA sequencing on the brain
transcriptome of an Old World monkey (OWM) and then conducted three-way
comparisons among (i) mouse, OWM, and human, and (ii) OWM, chimpanzee, and
human. Although brain-expressed genes indeed appear to evolve more rapidly in
species with more advanced brains (apes > OWM > mouse), a similar lineage
effect is observable for most other genes. The broad inclusion of genes in
the reference set to represent the genomic average is therefore critical to
this type of analysis. Calibrated against the genomic average, the rate of
evolution among brain-expressed genes is probably lower (or at most equal) in
humans than in chimpanzee and OWM. Interestingly, the trend of slow evolution
in coding sequence is no less pronounced among brain-specific genes,
vis-a`-vis brain-expressed genes in general. The human brain may thus differ
from those of our close relatives in two opposite directions: (i) faster
evolution in gene expression, and (ii) a likely slowdown in the evolution of
protein sequences. Possible explanations and hypotheses are discussed.
Funding. This research was supported by the Academia Sinica and the National
Science Council, Taiwan; the Ministry of the Health and Welfare, Japan; and
US Public of Health (NIH) Grants.
Competing interests. The authors have declared that no competing interests
exist.
Academic Editor: Kenneth Wolfe, University of Dublin, Ireland
Citation: Wang HY, Chien HC, Osada N, Hashimoto K, Sugano S, et al. (2007)
Rate of Evolution in Brain-Expressed Genes in Humans and Other Primates. PLoS
Biol 5(2): e13 DOI: 10.1371/journal.pbio.0050013
Received: May 23, 2006; Accepted: November 10, 2006; Published: December 26,
2006
Copyright: (c) 2007 Wang et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.
Abbreviations: CDS, coding sequence; Consortium, Chimpanzee Sequencing and
Analysis Consortium; Ka, number of substitutions per site for nonsynonymous
sites; Ks, number of substitutions per site for synonymous sites; OWM, Old
World monkey
* To whom correspondence should be addressed. E-mail: ciwu@uchicago.edu
(CIW); ckshen@ccvax.sinica.edu.tw (CKJS)
? Current address: Graduate Institute of Clinical Medicine, National Taiwan
University, Taipei, Taiwan
Author Summary
Whether comparing morphology or cognitive ability, it is clear that the human
brain has evolved rapidly relative to that of other primates. But the extent
to which genes expressed in the brain also reflect this overall pattern is
unclear. To address this question, it's necessary to measure any variations
in the DNA sequences of these genes between human and chimpanzee. And, to do
this as accurately as possible, it's also important to require an appropriate
reference group to act as a benchmark against which the differences can be
measured. We therefore compared publicly available genomic sequences of
chimps and humans with complementary DNA sequences of several thousand genes
expressed in the brain of another closely related primate—the macaque, an
Old World monkey—as well as the more distantly related mouse. Our analyses
of the rates of protein evolution in these species suggest that genes
expressed in the human brain have in fact slowed down in their evolution
since the split between human and chimpanzee, contrary to some previously
published reports. We suggest that advanced brains are driven primarily by
the increasing complexity in the network of gene interactions. As a result,
brain-expressed genes are constrained in their sequence evolution, although
their expression levels may change rapidly.
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