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Cited by 86Evolution and Genetic DynamicsGenomics and Phylogenetic StudiesEvolution and Paleontology Studies

Molecular evolution of aerobic energy metabolism in primates.

Grossman, Lawrence I., Schmidt, Timothy R., Wildman, Derek E., Goodman, Morris·2001·Molecular Phylogenetics and Evolution
DOI 10.1006/mpev.2000.0890
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Abstract

As part of our goal to reconstruct human evolution at the DNA level, we have been examining changes in the biochemical machinery for aerobic energy metabolism. We find that protein subunits of two of the electron transfer complexes, complex III and complex IV, and cytochrome c, the protein carrier that connects them, have all undergone a period of rapid protein evolution in the anthropoid lineage that ultimately led to humans. Indeed, subunit IV of cytochrome c oxidase (COX; complex IV) provides one of the best examples of positively selected changes of any protein studied. The rate of subunit IV evolution accelerated in our catarrhine ancestors in the period between 40 to 18 million years ago and then decelerated in the descendant hominid lineages, a pattern of rate changes indicative of positive selection of adaptive changes followed by purifying selection acting against further changes. Besides clear evidence that adaptive evolution occurred for cytochrome c and subunits of complexes III (e.g., cytochrome c(1)) and IV (e.g., COX2 and COX4), modest rate accelerations in the lineage that led to humans are seen for other subunits of both complexes. In addition the contractile muscle-specific isoform of COX subunit VIII became a pseudogene in an anthropoid ancestor of humans but appears to be a functional gene in the nonanthropoid primates. These changes in the aerobic energy complexes coincide with the expansion of the energy-dependent neocortex during the emergence of the higher primates. Discovering the biochemical adaptations suggested by molecular evolutionary analysis will be an exciting challenge.

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  • This scenario reconciles human brain metabolism with comparative genetic analyses showing that genes related to cell metabolism are among those with larger changes in human evolution and evidence of evolutionary pressure for high rates of aerobic energy consumption.

    “This scenario reconciles human brain metabolism with comparative genetic analyses that show that genes related to cell metabolism are among those that exhibit the larger changes in human evolution [9], [10], with evidence of evolutionary pressure for high rates of aerobic energy consumption [52].”

    From Scaling of Brain Metabolism with a Fixed Energy Budget per Neuron: Implications for Neuronal Activity, Plasticity and Evolution (2011) · cites this paper as [52]

  • The process of mitochondrial electron transport shows accelerated evolution of multiple subunits of complex III, complex IV, and cytochrome c.

    “Second, the process of mitochondrial electron transport shows accelerated evolution of multiple subunits of complex III, complex IV, and cytochrome c (6, 38), suggesting that the engine of energy generation has been a prominent target of Darwinian positive selection in anthropoid primates.”

    From Evolution of increased glia–neuron ratios in the human frontal cortex (2006) · cites this paper as [38]

  • The engine of energy generation has been a prominent target of Darwinian positive selection in anthropoid primates.

    “Second, the process of mitochondrial electron transport shows accelerated evolution of multiple subunits of complex III, complex IV, and cytochrome c (6, 38), suggesting that the engine of energy generation has been a prominent target of Darwinian positive selection in anthropoid primates.”

    From Evolution of increased glia–neuron ratios in the human frontal cortex (2006) · cites this paper as [38]

  • The biochemical mechanism of generating energy has been under evolutionary selection going back at least to the anthropoid primate stem, presumably to fuel increases in brain size.

    “Indeed, considerable evidence indicates that the biochemical mechanism of generating energy has been under evolutionary selection going back at least to the anthropoid primate stem, presumably to fuel increases in brain size.”

    From Evolution of increased glia–neuron ratios in the human frontal cortex (2006) · cites this paper as [38]

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Authors
Grossman, L. I., Schmidt, T. R., Wildman, D. E., & Goodman, M.
Affiliations
Wayne State University (US)
Corresponding author
Grossman, Lawrence I.
ORCID
Venue
Molecular Phylogenetics and Evolution
Publisher
Elsevier BV
Published
2001-01
Volume
18
Issue
1
Pages
26-36
ISSN
1055-7903 (ISSN-L)
DOI
10.1006/mpev.2000.0890
OpenAlex
W2076710678
Cited by
86
References
74
Citations by year
2026: 1 · 2024: 1 · 2023: 4 · 2022: 2 · 2021: 1 · 2020: 1 · 2018: 1 · 2017: 6 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 6 · 2012: 3
FWCI
3.28
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Molecular Phylogenetics and Evolution (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
Keywords
aerobic metabolism, primate evolution, human evolution, cytochrome c oxidase, cytochrome bc1 complex, cytochrome c, cytochrome c1, positive selection, purifying selection, rate shifts, pseudogenization, neocortex evolution, electron transport chain, anthropoid primates
MeSH terms
Animals, Cytochrome c Group, Electron Transport Complex IV, Electron Transport, Biological Evolution, Humans, Models, Biological, Models, Genetic, Mutation, Phylogeny, Primates, Evolution, Molecular, Protein Isoforms

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