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PLoS Biol. 2014 May 27;12(5):e1001871. doi: 10.1371/journal.pbio.1001871. eCollection 2014 May.

Exceptional evolutionary divergence of human muscle and brain metabolomes parallels human cognitive and physical uniqueness.

Author information

1
CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China; Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
2
CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China; Graduate School of Chinese Academy of Sciences, Beijing, China.
3
CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China.
4
Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata, Japan.
5
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
6
Department of Anthropology, The George Washington University, Washington DC, United States of America.
7
Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, United States of America.
8
Alamogordo Primate Facility, Holloman AFB, Alamogordo, New Mexico, United States of America.
9
Max Planck Institute for Molecular Plant Physiology, Potsdam, Germany.
10
Department of Exercise and Sport Sciences, Section of Human Physiology, University of Copenhagen, Copenhagen, Denmark.
11
Department of Clinical Sciences, Lund University, Malmö University Hospital, Malmö, Sweden.

Abstract

Metabolite concentrations reflect the physiological states of tissues and cells. However, the role of metabolic changes in species evolution is currently unknown. Here, we present a study of metabolome evolution conducted in three brain regions and two non-neural tissues from humans, chimpanzees, macaque monkeys, and mice based on over 10,000 hydrophilic compounds. While chimpanzee, macaque, and mouse metabolomes diverge following the genetic distances among species, we detect remarkable acceleration of metabolome evolution in human prefrontal cortex and skeletal muscle affecting neural and energy metabolism pathways. These metabolic changes could not be attributed to environmental conditions and were confirmed against the expression of their corresponding enzymes. We further conducted muscle strength tests in humans, chimpanzees, and macaques. The results suggest that, while humans are characterized by superior cognition, their muscular performance might be markedly inferior to that of chimpanzees and macaque monkeys.

PMID:
24866127
PMCID:
PMC4035273
DOI:
10.1371/journal.pbio.1001871
[Indexed for MEDLINE]
Free PMC Article

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