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ENERGY ENVIRONMENTS AND SUBPOPULATION RADIATION

To understand the radiation of subpopulations of a species, it is necessary to study the intraspecific variation of a single species that occupies a wide range of regional energetic environments. The best studied species in this regard is Homo sapiens.

A striking feature of the radiation of mammalian and primate genomic elements is that mtDNA sequences show a much greater sequence evolution rate than do nDNA sequences (Brown et al., 1982; Neckelmann et al., 1987; Wallace et al., 1987). This rapid mtDNA radiation is reflected in the high degree of functional and regional variation of human mtDNAs (Wallace et al., 2007). The mtDNA genes of all animals encode the core proteins of OXPHOS, so mtDNA mutations directly affect bioenergetic physiology and provide the ideal genetic system for adaptation to changes in regional energy environments.

Mitochondrial Bioenergetics and the mtDNA

The unique capacity of the mtDNA to regulate bioenergetics has its roots in the symbiotic origin of the eukaryotic cell. Current theory postulates that a glycolytic motile microorganism, the proto-nucleus-cytosol, formed an association with an oxidative α-protobacterium, the proto-mitochondrion, about 2 billion years ago, probably in response to the rise in atmospheric oxygen generated by free-living cyanobacteria.

As the symbiosis matured, the two organisms consolidated their metabolic pathways and exchanged genes, natural selection enriching for more efficient forms. During the ensuing intersymbiont reorganization, most of the genes of the mitochondrial genome were transferred to the nDNA to become interspersed among the existing nuclear-cytosol bioenergetic genes. Ultimately, one genetic and metabolic combination was sufficiently energetically efficient to permit the advent of multicellularity. In this proto-multicellular eukaryote, 98% of the protein-coding genes of the mitochondrial genome had been transferred to the nucleus, encompassing all of the polypeptide genes for mitochondrial growth, reproduction, and metabolism plus ≈80 polypeptide genes for OXPHOS (Wallace, 2005, 2007; Wallace et al., 2010).

The mtDNAs of multicellular animals all retained roughly the same 13 OXPHOS polypeptide genes. These include seven (ND1, 2, 3, 4L, 4, 5, and 6) of the 45 subunits of OXPHOS complex I, one [cytochrome b (cytb)] of the 11 subunits of complex III, three (COI, II, and III) of the 13 subunits of complex IV, and two (ATP 6 and 8) of the ≈16 subunits of complex V. Animal mtDNAs also retain the rRNA and tRNA genes for mitochondrial protein synthesis and a control region for regulating mtDNA replication and transcription (Wallace, 2005, 2007; Wallace et al., 2010).



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