Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia)

Abstract

Blue mussels of the genus Mytilus have an unusual mode of mitochondrial DNA (mtDNA) transmission: males receive mtDNA from both parents and transmit their paternal mtDNA to their sons; females receive mtDNA only from their mother (Skibinski, Gallagher, and Beynon 1994~2, 1994b; Zouros et al. 1994~2, 1994b). This mode of mtDNA transmission has been termed “doubly uniparental inheritance” (DUI; Zouros et al. 1994a). It is known from the work of Hoffmann, Boore, and Brown (1992) and Boore and Brown (1994) that the gene order of Mytilus mtDNA is much more different from that of vertebrates, insects, or the chiton Katharina (itself a mollusk) than these other mtDNA gene orders are from each other. Here we report another exceptional feature of the Mytilus mtDNA genome, specifically, an accelerated rate of sequence divergence. Based on a comparison of nucleotide and amino acid sequences, we demonstrate that the Mytilus mtDNA is the most divergent metazoan mtDNA known today and that it evolves at a higher rate than is typical for animals. We suggest that the fast rate of mtDNA evolution in Mytilus is causally related to DUI. Nucleotide sequences of both the “female” (F) and “male” (M) mitotypes of Mytilus edulis for cytochrome c oxidase subunits I (COI, 660 bp) and III (COIII, 762 bp) were obtained as described elsewhere (Folmer et al. 1994; Stewart et al. 1995). Ten additional sequences representing major metazoan lineages were either obtained from Genbank or communicated to us. Estimates of sequence divergence and the construction of neighborjoining trees were carried out using MEGA version 1.02 (Kumar, Tamura, and Nei 1993) and were based on the combined COI/COIII data set. Pairwise proportional distances for first and second nucleotide positions and for amino acids are shown in table 1. Given the taxonomic distance of the compared taxa, nucleotide substitutions at third positions were saturated and were excluded from nucleotide distance calculations.