Regular Article
Molecular Evolution of Aerobic Energy Metabolism in Primates

https://doi.org/10.1006/mpev.2000.0890Get rights and content

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 c1) 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.

References (71)

  • L.I. Grossman et al.

    Nuclear genes for cytochrome c oxidase

    Biochim. Biophys. Acta

    (1997)
  • L.I. Grossman et al.

    Cloning, sequence analysis, and expression of a mouse cDNA encoding cytochrome c oxidase subunit VIa liver isoform

    Biochim. Biophys. Acta

    (1995)
  • D.L. Gumucio et al.

    Differential phylogenetic footprinting as a means to identify base changes responsible for recruitment of the anthropoid gamma gene to a fetal expression pattern

    J. Biol. Chem.

    (1994)
  • R.P. Herzig et al.

    Sequential serum-dependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c

    J. Biol. Chem.

    (2000)
  • R.M. Johnson et al.

    Fetal globin expression in New World monkeys [published erratum appears in J Biol Chem 1996 Nov 22;271(47):30298]

    J. Biol. Chem.

    (1996)
  • B. Kadenbach et al.

    A second mechanism of respiratory control

    FEBS Lett.

    (1999)
  • B. Kadenbach et al.

    Regulation of mitochondrial energy generation in health and disease

    Biochim. Biophys. Acta

    (1995)
  • B. Kadenbach et al.

    Tissue-specific and species-specific expression of cytochrome c oxidase isozymes in vertebrates

    Biochim. Biophys. Acta

    (1990)
  • D. Linder et al.

    Species-specific expression of cytochrome c oxidase isozymes

    Comp. Biochem. Physiol. B

    (1995)
  • N. Osheroff et al.

    The reaction of primate cytochromes c with cytochrome c oxidase: Analysis of the polarographic assay

    J. Biol. Chem.

    (1983)
  • J.K. Rilling et al.

    The primate neocortex in comparative perspective using magnetic resonance imaging

    J. Hum. Evol.

    (1999)
  • A. Rotig et al.

    Screening human EST database for identification of candidate genes in respiratory chain deficiency

    Mol. Genet. Metab.

    (2000)
  • R.C. Scarpulla et al.

    Isolation and structure of a rat cytochrome c gene

    J. Biol. Chem.

    (1981)
  • M.A. Smith et al.

    Oxidative stress in Alzheimer's disease

    Biochim. Biophys. Acta

    (2000)
  • N.A.E. Steenaart et al.

    Mitochondrial cytochrome c oxidase subunit IV is phosphorylated by an endogenous kinase

    FEBS Lett.

    (1997)
  • D.A. Tagle et al.

    Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus): Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints

    J. Mol. Biol.

    (1988)
  • V. Tiranti et al.

    Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency

    Am. J. Hum. Genet.

    (1998)
  • G. Villani et al.

    Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types

    J. Biol. Chem.

    (1998)
  • W. Wu et al.

    Molecular evolution of cytochrome c oxidase subunit I in primates: Is there co-evolution between mitochondrial and nuclear genomes?

    Mol. Phylogenet. Evol.

    (2000)
  • R.M. Adkins et al.

    Evolution of the primate cytochrome c oxidase subunit II gene

    J. Mol. Evol.

    (1994)
  • T.D. Andrews et al.

    Evolutionary rate acceleration of cytochrome c oxidase subunit I in simian primates

    J. Mol. Evol.

    (2000)
  • T.D. Andrews et al.

    Accelerated evolution of cytochrome b in simian primates: Adaptive evolution in concert with other mitochondrial proteins?

    J. Mol. Evol.

    (1998)
  • S. Arnold et al.

    Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase

    Eur. J. Biochem.

    (1997)
  • M.L. Baba et al.

    Evolution of cytochrome c investigated by the maximum parsimony method

    J. Mol. Evol.

    (1981)
  • L. Banci et al.

    Mitochondrial cytochromes c: A comparative analysis

    J. Biol. Inorg. Chem.

    (1999)
  • Cited by (82)

    • Comparative biochemistry of cytochrome c oxidase in animals

      2018, Comparative Biochemistry and Physiology Part - B: Biochemistry and Molecular Biology
      Citation Excerpt :

      In most cases, the species under study are chosen because of some metabolic exceptionalism. Grossman and colleagues (Grossman et al., 2001; Grossman et al., 2004) have championed a model of positive selection in various COX subunits in relation to hominoid evolution. Early in snake evolution, the entire mitochondrial genome experienced two punctuated bouts of adaptive evolution, where COX1 experienced the highest levels of positive selection (Castoe et al., 2008).

    • Evolution of Large Brain and Body Size in Mammals

      2016, Evolution of Nervous Systems: Second Edition
    View all citing articles on Scopus
    1

    To whom correspondence and reprint requests should be addressed at Center for Molecular Medicine and Genetics, Wayne State University School of Medicine, Detroit, MI 48201. E-mail: [email protected].

    View full text