Mitochondrial DNA sequences of primates: Tempo and mode of evolution

Abstract

We cloned and sequenced a segment of mitochondrial DNA from human, chimpanzee, gorilla, orangutan, and gibbon. This segment is 896 bp in length, contains the genes for three transfer RNAs and parts of two proteins, and is homologous in all 5 primates. The 5 sequences differ from one another by base substitutions at 283 positions and by a deletion of one base pair. The sequence differences range from 9 to 19% among species, in agreement with estimates from cleavage map comparisons, thus confirming that the rate of mtDNA evolution in primates is 5 to 10 times higher than in nuclear DNA. The most striking new finding to emerge from these comparisons is that transitions greatly outnumber transversions. Ninety-two percent of the differences among the most closely related species (human, chimpanzee, and gorilla) are transitions. For pairs of species with longer divergence times, the observed percentage of transitions falls until, in the case of comparisons between primates and non-primates, it reaches a value of 45. The time dependence is probably due to obliteration of the record of transitions by multiple substitutions at the same nucleotide site. This finding illustrates the importance of choosing closely related species for analysis of evolutionary process. The remarkable bias toward transitions in mtDNA evolution necessitates the revision of equations that correct for multiple substitutions at the same site. With revised equations, we calculated the incidence of silent and replacement substitutions in the two protein-coding genes. The silent substitution rate is 4 to 6 times higher than the replacement rate, indicating strong functional constraints at replacement sites. Moreover, the silent rate for these two genes is about 10% per million years, a value 10 times higher than the silent rate for the nuclear genes studied so far. In addition, the mean substitution rate in the three mitochondrial tRNA genes is at least 100 times higher than in nuclear tRNA genes. Finally, genealogical analysis of the sequence differences supports the view that the human lineage branched off only slightly before the gorilla and chimpanzee lineages diverged and strengthens the hypothesis that humans are more related to gorillas and chimpanzees than is the orangutan.

Phylogenetic analysis using parsimony and likelihood methods

“…Consider the sequence data of the 895-bp segment of the mitochondrial genome (mtDNA) of human (H), chimpanzee (C), gorilla (G), and orangutan (O) (Brown et al 1982). The segment codes for three tRNAs and parts of two proteins.…”

Estimation of the Transition/Transversion Rate Bias and Species Sampling

“…In virtually all DNA sequences from any genome examined, transitions (T↔C, A↔G) have been noted to occur at higher frequencies than transversions (T↔A, T↔G, C↔A, C↔G) (Brown et al 1982;Gojobori et al 1982;Curtis and Clegg 1984;Wakeley 1994Wakeley , 1996. While transition/transversion (ti/tv) bias is known to be a general property of DNA sequence evolution, it is more pronounced in animal mitochondrial DNAs (mtDNAs) than in nuclear or chloroplast DNAs (for a review see Wakeley 1996).…”

“…At levels of 20% divergence or more, the two substitution types show equal frequencies, thereby yielding an apparent ti/tv of approximately 1. Saturation of transitions at high levels of genetic divergence is commonly believed to explain the pattern (e.g., Brown et al 1982;Moritz et al 1987). Thus, it has been suggested that the comparison of closely related sequences may yield more accurate estimates of substitution patterns than will comparisons of more divergent sequences (e.g., Purvis and Bromham 1997).…”

“…A maximum-likelihood approach was used by Hasegawa et al (1990) to estimate the rates of transitions and transversions in primates in an 896-bp segment of mtDNA that contains parts of two proteins (ND4 and ND5) and three tRNA genes (Brown et al 1982;Hayasaka et al 1988). The species sample included the hominoids (human, chimpanzee, gorilla, orangutan, gibbon), four closely related cercopithecoids (Japanese macaque, rhesus macaque, crab-eating macaque, and Barbary macaque), one platyrrhine (common squirrel A-C Counts of sites with transitional (open circles) and transversional (filled circles) differences in pairwise comparisons relative to sequence divergence corrected with the K80 model.…”

A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences

“…Phylogenetic analysis of mitochondrial DNA (mtDNA) is a widely used tool for delineating species relationships (Moritz, 1994) because of its fast rate of sequence evolution and rapid lineage sorting relative to the nuclear genome (Avise, 1989;Brown et al, 1982;Moore, 1995). However, mtDNA can be uninformative if only small portions of the mitogenome are used (Galtier et al, 2009).…”