Molecular population genetics of the male and female mitochondrial DNA molecules of the California sea mussel, Mytilus californianus

Abstract

The presence of two gender-associated mitochondrial genomes in marine mussels provides a unique opportunity to investigate the dynamics of mtDNA evolution without complications inherent in interspecific comparisons. Here, we assess the relative importance of selection, mutation, and differential constraint in shaping the patterns of polymorphism within and divergence between the male (M) and female (F) mitochondrial genomes of the California sea mussel, Mytilus californianus. Partial sequences were obtained from homologous regions of four genes (nad2, cox1, atp6, and nad5) totaling 2307 bp in length. The M and F mtDNA molecules of M. californianus exhibited extensive levels of nucleotide polymorphism and were more highly diverged than observed in other mytilids (overall Tamura-Nei distances >40%). Consistent with previous studies, the M molecule had significantly higher levels of silent and replacement polymorphism relative to F. Both genomes possessed large numbers of singleton and low-frequency mutations that gave rise to significantly negative Tajima's D values. Mutation-rate scalars estimated for silent and replacement mutations were elevated in the M genome but were not sufficient to account for its higher level of polymorphism. McDonald-Kreitman tests were highly significant at all loci due to excess numbers of fixed replacement mutations between molecules. Strong purifying selection was evident in both genomes in keeping the majority of replacement mutations at low population frequencies but appeared to be slightly relaxed in M. Our results suggest that a reduction in selective constraint acting on the M genome remains the best explanation for its greater levels of polymorphism and faster rate of evolution.

Figure 1.—

Bayesian consensus trees for the (a) F mtDNA sequences, (b) M mtDNA sequences, and (c) the combined F and M data.

Figure 2.—

Comparison of silent and replacement nucleotide diversities in the M and F mtDNA molecules.

Figure 3.—

Estimates of mutation-rate scalars for (a) silent mutations and (b) replacement mutations in the F (dotted lines) and M genomes (solid lines) relative to an anonymous nuclear gene (Mca125; dashed lines). Mutation rates were estimated by coalescent simulations using the IM program of Nielsen and Wakeley (2001) assuming a single panmictic population (i.e., constraining t, m₁, and m₂ to equal zero and θ₁ = θ₂ = θ_A).

Figure 4.—

Relationships between the allele frequencies and Grantham scores of amino acid replacement mutations in the (a) M and (b) F genomes.