MBE Advance Access originally published online on December 4, 2008
Molecular Biology and Evolution 2009 26(3):579-589; doi:10.1093/molbev/msn279
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Research Articles |
Near Neutrality, Rate Heterogeneity, and Linkage Govern Mitochondrial Genome Evolution in Atlantic Cod (Gadus morhua) and Other Gadine Fish
Genetics, Evolution, and Molecular Systematics Laboratory, Department of Biology, Memorial University of Newfoundland, St John's, Newfoundland and Labrador, Canada
E-mail: scarr{at}mun.ca.
Accepted for publication November 29, 2008.
The mitochondrial DNA (mtDNA) genome figures prominently in evolutionary investigations of vertebrate animals due to a suite of characteristics that include absence of Darwinian selection, high mutation rate, and inheritance as a single linkage group. Given complete linkage and selective neutrality, mtDNA gene trees are expected to correspond to intraspecific phylogenies, and mtDNA diversity will reflect population size. The validity of these assumptions is, however, rarely tested on a genome-wide scale. Here, we analyze rates and patterns of molecular evolution among 32 whole mitochondrial genomes of Atlantic Cod (Gadus morhua) as compared with its sister taxon, the walleye pollock (Gadus [Theragra] chalcogrammus), and genomes of seven other gadine codfish. We evaluate selection within G. morhua, between sister species, and among species and intraspecific measures of linkage disequilibrium and recombination within G. morhua. Strong rate heterogeneity occurs among sites and genes at all levels of hierarchical comparison, consistent with variation in mutation rates across the genome. Neutrality indices (dN/dS) are significantly greater than unity among G. morhua genomes and between sister species, which suggests that polymorphisms within species are slightly deleterious, as expected under the nearly neutral theory of molecular evolution. Among species of gadines, dN/dS ratios are heterogeneous among genes, consistent with purifying selection and variation in functional constraint among genes rather than positive selection. The dN/dS ratio for ND4L is anomalously high across all hierarchical levels. There is no evidence for recombination within G. morhua. These patterns contrast strongly with those reported for humans: genome-wide patterns in other vertebrates should be investigated to elucidate the complex patterns of mtDNA molecular evolution.
Key Words: mitogenomics • rate heterogeneity • nonsynonymous-to-synonymous ratio • recombination • Gadus morhua • gadine fishes • slightly deleterious polymorphisms
David Irwin, Associate Editor