Dataset Information

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.

SUBMITTER: Ort BS

PROVIDER: S-EPMC2034615 | biostudies-literature | 2007 Oct

REPOSITORIES: biostudies-literature

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

Ort Brian S BS Pogson Grant H GH

Genetics 20070824 2

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 w ...[more]

PMID: 17720935

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Project description:The doubly uniparental inheritance system allows for the use of two independent mitochondrial genomes for population history investigations. Under this system, two lineages of mitochondrial DNA (mtDNA) exist and males are typically heteroplasmic, having the additional, usually divergent, mitochondrial genome inherited from their male parent. This additional mtDNA typically evolves faster, potentially allowing for insight into more recent events in population history. Few studies did explore this possibility in marine mussels Mytilus showing its usefulness. Recent observations of the Mytilus trossulus mussels who have retained their native mtDNA in European waters posed the question of their origin. Are they part of a population present, but previously undetected, or is this a potentially human mediated, ongoing spread of an invasive species? To tackle this question, we amplified with species-specific primers and sequenced an approximately 1,200-bp-long fragment spanning COIII and ND2 genes from both mitochondrial genomes of mussels sampled at five locations worldwide, covering the whole M. trossulus range. The overall pattern of polymorphisms is compatible with the entirely postglacial history of the whole species, indicating a very deep bottleneck at last glacial maximum, with possible retention of the whole species in a single refugium, and the effective population size of no more than a few thousands. Both analyses of molecular variance and isolation with migration (IM) models point at the West Atlantic as the source of the European M. trossulus mussels, at least the ones who retained their native mtDNA. The hypothesis that this is an ongoing, human-mediated process was considered. To this end, comparison with the well-known case: the introduction of congeneric mussel, Mytilus galloprovincialis, from Mediterranean Sea to Asia was used. This introduction occurred within the last 100 years. The results inferred by the IM model suggest that the timing and structure of transatlantic migration of M. trossulus differs significantly from the M. galloprovincialis case: it is more than 1,000 years old and involves a much larger fraction of the ancestral population. Therefore, most likely, this invasion is not a human-mediated process.

Project description:BackgroundFew exceptions have been described from strict maternal inheritance of mitochondrial DNA in animals, including sea mussels (Mytilidae), clams (Donacidae, Veneridae and Solenidae) and freshwater mussels (Unionoidae) order. In these bivalves mitochondria and their DNA are transferred through two separate routes. The females inherit only the maternal mitochondrial DNA whereas the males inherit maternal as well as paternal mitochondrial DNA, which is usually present only in gonads and sperm. The mechanism controlling this phenomenon is unclear but leads to the existence of two separate mitochondrial DNA lineages in a single species. The lineages are usually well differentiated: up to 20-50% divergence in nucleotide sequence. Occasionally, a maternal mitochondrial DNA can invade the paternal transmission route, eventually replacing the diverged M-type and lowering the divergence. Such role reversal (masculinization) event has happened recently in the Mytilus population of the Baltic Sea which consists of M. edulis × M. trossulus hybrids, but the functional status of the resulting mitochondrial genome was unknown.ResultsIn this paper we sequenced transcripts from one specimen that was identified as male carrying both the female mitochondrial genome and a recently masculinized mitochondrial genome. Additionally, the analysis of the control region has showed that the recently masculinized, recombinant genome, not only has an M-type control region and all coding regions derived from the F-type, but also is transcriptionally active along side the maternally inherited F-type genome. In the comparative analysis, the two genomes exhibit different substitution patterns, typical for the M vs. F genome comparisons. The genetic distances and ratios of non-synonymous substitutions also suggest that one of the genomes is transitioning from the maternal to the paternal inheritance mode, consistent with its recent masculinization.ConclusionWe have shown, for the first time, that the recently masculinized mitochondrial genome is active and that it accumulates excess of non-synonymous substitutions across its coding sequence. This suggests, that, under certain cytonuclear incompatibility conditions, masculinization may serve to restore the endangered functionality of the paternally inherited genome. This is also another example of a mitochondrial genome in which the recombination in the control region predated its transition from paternal to maternal transmission route.

Dataset Information

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

Publications

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

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