Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic

A number of studies have claimed that recombination occurs in animal mtDNA, although this evidence is controversial. Ladoukakis and Zouros (2001) provided strong evidence for mtDNA recombination in the COIII gene in gonadal tissue in the marine mussel Mytilus galloprovincialis from the Black Sea. The recombinant molecules they reported had not however become established in the population from which experimental animals were sampled. In the present study, we provide further evidence of the generality of mtDNA recombination in Mytilus by reporting recombinant mtDNA molecules in a related mussel species, Mytilus trossulus, from the Baltic. The mtDNA region studied begins in the 16S rRNA gene and terminates in the cytochrome b gene and includes a major noncoding region that may be analogous to the D-loop region observed in other animals. Many bivalve species, including some Mytilus species, are unusual in that they have two mtDNA genomes, one of which is inherited maternally (F genome) the other inherited paternally (M genome). Two recombinant variants reported in the present study have population frequencies of 5% and 36% and appear to be mosaic for F-like and M-like sequences. However, both variants have the noncoding region from the M genome, and both are transmitted to sperm like the M genome. We speculate that acquisition of the noncoding region by the recombinant molecules has conferred a paternal role on mtDNA genomes that otherwise resemble the F genome in sequence.     

Complete sequences of mitochondrial genomes from the Baltic mussel Mytilus trossulus

Marine mussels Mytilus possess two mitochondrial (mt) genomes, which undergo doubly uniparental inheritance (DUI). Female (F) and male (M) genomes are usually highly diverged at the sequence level. Both genomes contain the same set of metazoan genes (for 12 proteins, 2 rRNAs and 23 tRNAs), both lack the atp8 gene and have two tRNAs for methionine. However, recently recombination between those variants has been reported. Both original F and M mt genomes of M. trossulus were replaced by M. edulis mtDNA in the Baltic populations. Highly diverged M genome occurs rarely in the Baltic mussels. Full sequences of the M genome identified in males (sperm) and F genome in females (eggs) were obtained. Both genomes were diverged by 24% in nucleotide sequence, but had similar nucleotide composition and codon usage bias. Constant domain (CD) of the control region (CR), the tRNA and rRNA genes were the most conserved. The most diverged was the variable domain 1 (VD1) of the control region. The F genome was longer than M by 147 bp. and the main difference was localised in the VD1 region. No recombination was observed in whole mtDNA of both studied variants. Nuclear mitochondrial pseudogenes (numts) have not been found by hybridisation with probes complementary to several fragments of the Baltic M. trossulus mtDNA.     

Evidence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.)

Both the maternal (F-type) and paternal (M-type) mitochondrial genomes of the Mytilus species complex M. edulis/galloprovincialis contain a noncoding sequence between the l-rRNA and the tRNA(Tyr) genes, here called the large unassigned region (LUR). The LUR, which is shorter in M genomes, is capable of forming secondary structures and contains motifs of significant sequence similarity with elements known to have specific functions in the sea urchin and the mammalian control region. Such features are not present in other noncoding regions of the F or M Mytilus mtDNA. The LUR can be divided on the basis of indels and nucleotide variation in three domains, which is reminiscent of the tripartite structure of the mammalian control region. These features suggest that the LUR is the main control region of the Mytilus mitochondrial genome. The middle domain has diverged by only 1.5% between F and M genomes, while the average divergence over the whole molecule is approximately 20%. In contrast, the first domain is among the most divergent parts of the genome. This suggests that different parts of the LUR are under different selection constraints that are also different from those acting on the coding parts of the molecule.     

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

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.     

The Control Region of Maternally and Paternally Inherited Mitochondrial Genomes of Three Species of the Sea Mussel Genus Mytilus

Species of the mussel genus Mytilus possess maternally and paternally transmitted mitochondrial genomes. In the interbreeding taxa Mytilus edulis and M. galloprovincialis, several genomes of both types have been fully sequenced. The genome consists of the coding part (which, in addition to protein and RNA genes, contains several small noncoding sequences) and the main control region (CR), which in turn consists of three distinct parts: the first variable (VD1), the conserved (CD), and the second variable (VD2) domain. The maternal and paternal genomes are very similar in gene content and organization, even though they differ by >20% in primary sequence. They differ even more at VD1 and VD2, yet they are remarkably similar at CD. The complete sequence of a genome from the closely related species M. trossulus was previously reported and found to consist of a maternal-like coding part and a paternal-like and a maternal-like CR. From this and from the fact that it was extracted from a male individual, it was inferred that this is a genome that switched from maternal to paternal transmission. Here we provide clear evidence that this genome is the maternal genome of M. trossulus. We have found that in this genome the tRNA^Gln in the coding region is apparently defective and that an intact copy of this tRNA occurs in the CR, that one of the two conserved domains is missing essential motifs, and that one of the two first variable domains has a high rate of divergence. These features may explain the large size and mosaic structure of the CR of the maternal genome of M. trossulus. We have also obtained CR sequences of the maternal and paternal genomes of M. californianus, a more distantly related species. We compare the control regions from all three species, focusing on the divergence among genomes of different species origin and among genomes of different transmission routes.     

A mitochondrial genome with a reversed transmission route in the Mediterranean mussel Mytilus galloprovincialis

Species of the marine mussel genus Mytilus are known to contain two mitochondrial genomes, one transmitted maternally (the F genome) and the other paternally (the M genome). The two genomes have diverged by more than 20% in DNA sequence. Here we present the complete sequence of a third genome, genome C, which we found in the sperm of a Mytilus galloprovincialis male. The coding part of the new genome resembles in sequence the F genome, from which it differs by about 2% on average, but differs from the M genome by as much as the F from the M. Its major control region (CR) is more than three times larger than that of the F or the M genome and consists of repeated sequence domains of the CR of the M genome flanked by domains of the CR of the F genome. We present a sequence of events that reconstruct most parsimoniously the derivation of the C genome from the F and M genomes. The sequence consists of a duplication of CR elements of the M genome and subsequent insertion of these tandemly repeated elements in the F genome by recombination. The fact that the C genome was found as the only mitochondrial genome in the sperm of the male from which it was extracted suggests that it is transmitted paternally.     

Comparative Genomics of Marine Mussels (Mytilus spp.) Gender Associated mtDNA: Rapidly Evolving atp8

The unusual mode of mitochondrial DNA inheritance, with two separate: maternal (F) and paternal (M) lineages, gives unique opportunities to study the evolution of the mitochondrial genome. This system was first discovered in the marine mussels Mytilus. The three related species: Mytilus edulis, Mytilus galloprovincialis and Mytilus trossulus form a complex in which the divergence of M and F lineages pre-dates the speciation. The complete mitochondrial genomes of both lineages were known for all species except Pacific M. trossulus. Here we report, for the first time, the complete sequences of both mitochondrial genomes of Pacific M. trossulus, filling the gap. While the reported M and F genomes are highly diverged (26%), they have similar organisation. The only difference is the translocation of one tRNA gene into the long, mosaic control region of the F genome. Consistent presence of an ORF which most likely represents the atp8 gene was confirmed in both genomes. The predicted protein has characteristics expected of the functional atp8 even though the M and F versions are markedly different in length. Comparative analysis involving all three species led to the conclusion that the cause of a faster evolution of atp8 and Mytilus mtDNA in general is most likely the Compensation-Draft Feedback process coupled with relatively relaxed selection in the M lineage. Thus, we postulate that the adaptive changes may have played a role in the emergence of highly diverged, barely recognizable atp8 in Mytilus mussels.     

Molecular variability in the Celleporella hyalina (Bryozoa; Cheilostomata) species complex: evidence for cryptic speciation from complete mitochondrial genomes

The bryozoan Celleporella has been shown to be composed of multiple, often cryptic, lineages. We sequenced two complete mitochondrial (mt) genomes of the Celleporella hyalina species complex from Wales, UK and Norway (i) to determine genetic divergence at the complete mt genome level, and (ii) to design new molecular markers for examining the interrelationships amongst the major lineages. In addressing (i), we estimated genetic divergence at three levels: (a) nucleotide diversity (π), (b) genome size, and (c) gene order. Genes nad4L, nad6, and atp8 showed the highest levels of divergence, and rrnL, rrnS, and cox1 showed the lowest levels. Inter-genome nucleotide divergence of protein-coding and ribosomal RNA genes, measured as π, was 0.21. The two genomes differed substantially in size, with the Norwegian genome being 2,573 base pairs (bp) longer than the Welsh genome, 17,265 and 14,692 bp, respectively. This difference in size is attributable to long non-coding regions present in the Norwegian genome. Both genomes exhibit similar gene orders, except for the translocation of one transfer RNA (trnA). Considering the high nucleotide diversity, genome size difference and change in gene order, these mt genomes are considered sufficiently divergent to have originated from two distinct species. In addressing (ii) we designed PCR primers that flank the most conserved regions of the genome: 1,300 bp of cox1 and a contiguous 2,000 bp fragment of rrnL + rrnS. The primers have yielded products for tissue from Wales, Norway, New Zealand, Alaska and Chile and should provide useful tools in establishing species- and population-level diversity within the Celleporella complex.     

Patterns of polymorphism and gene flow of gender-associated mitochondrial DNA lineages in European mussel populations

Mussels of the genus Mytilus have two types of mitochondrial DNA (mtDNA). The M type is transmitted paternally and the F type is transmitted maternally. RFLP analysis is used to assess phylogenetic relationships and nucleotide diversity and divergence for both mtDNA genomes in European populations of M. edulis and Atlantic and Mediterranean forms of M. galloprovincialis. Ten restriction endonucleases were used to assay variation in regions of the ND2 and COIII genes for a total of 77 individuals. F and M genomes show a concordant phylogenetic split into two major divergent clades, one specific to Mediterranean M. galloprovincialis and the other containing haplotypes from the three taxa. For both genomes, the geographical distribution of mtDNA variation suggests: (i) extensive levels of mtDNA introgression; (ii) asymmetric mtDNA gene flow from Atlantic to Mediterranean populations; and (iii) recurrent historical hybridization events. Significantly higher mtDNA diversity and divergence are observed for the M than F genome in all three Mytilus taxa, although the evolutionary forces responsible for these differences cannot be resolved. The extensive mtDNA gene flow between European Mytilus taxa conflicts with the restricted mtDNA introgression observed in American mussels , implying geographical variation in the nature of nuclear/mtDNA interactions regulating biparental inheritance.     

Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.)

Marine mussels of the genus Mytilus have an unusual mode of mitochondrial DNA (mtDNA) transmission termed doubly uniparental inheritance (DUI). Female mussels are homoplasmic for the F mitotype, which is inherited maternally, while males are usually heteroplasmic, carrying a mixture of the maternal F mitotype and the paternally inherited M genome. Two classes of M genomes have been observed: "standard" M genomes and "recently masculinized" M genomes. The latter are more similar to F genomes at the sequence level but are transmitted paternally like standard M genomes. In this study we report the complete sequences of two standard male M. edulis and one recently masculinized male M. trossulus mitochondrial genome. A comparative analysis, including the previously sequenced M. edulis F and M. galloprovincialis F and M mtDNAs, reveals that these genomes are identical in gene order, but highly divergent in nucleotide and amino acid sequence. The large amount (>20%) of nucleotide substitutions that fall in coding regions implies that there are several amino acid replacements between the F and M genomes, which likely have an impact on the structural and functional properties of the mitochondrial proteome. Correlation of the divergence rate of different protein-coding genes indicates that mtDNA-encoded proteins of the M genome are still under selective constraints, although less highly than genes of the F genome. The mosaic F/M control region of the masculinized F genome provides evidence for lineage-specific sequences that may be responsible for the different mode of transmission genetics. This analysis shows the value of comparative genomics to better understand the mechanisms of maintenance and segregation of mtDNA sequence variants in mytilid mussels.     

Biparental Inheritance Through Uniparental Transmission: The Doubly Uniparental Inheritance (DUI) of Mitochondrial DNA

Many bivalvian mollusks have a sperm-transmitted mitochondrial genome (M), along with the standard egg-transmitted one (F). The phenomenon, known as doubly uniparental inheritance (DUI) of mtDNA, is the only known case in which biparental inheritance of a cytoplasmic genome is the rule rather than the exception. In the mussel Mytilus sperm mitochondria disperse randomly among blastomeres in female embryos, but form an aggregate and stay in the same blastomere in male embryos. In adults, somatic tissues of both sexes are dominated by the F genome. Sperm contains only the M genome and eggs the F (and perhaps traces of M). A female produces mostly daughters, mostly sons, or both sexes in about equal numbers, irrespective of its mate. Thus maleness and M mtDNA fate are tightly linked and under maternal control. Hybridization and triploidization affect the former but not the latter, which suggests that the two are not causally linked. Gene content and arrangement are the same in conspecific F and M genomes, but primary sequence has diverged from 20 % to 40 %, depending on species. The two genomes differ at the control region (CR). Synonymous substitutions accumulate faster in the M than the F genome and non-synonymous even faster. Expression studies indicate that the M genome is active only at spermatogenesis. These observations suggest that the M genome is under a more relaxed selective constraint than the F. Some mytilid species carry, in low frequencies, sperm-transmitted mtDNAs whose primary sequence is of the F type and the CR is an F/M mosaic (“masculinized” genomes). In venerids sperm mitochondria behavior, M genome fate and sex determination are as in mytilids. In unionids the M genome also evolves faster than the F and F/M sequence divergence reaches 50 %. The identification of F-specific and M-specific open reading frames in non-coding regions of unionids and mytilids, in conjunction with the CR’s mosaic structure of masculinized genomes, suggest that the mitochondrial genomes of species with DUI carry sequences that affect their transmission route. A model that incorporates these findings is presented in this review.     

The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa

The complete mitochondrial genome of Flustrellidra hispida (Bryozoa, Ctenostomata, Flustrellidridae) was sequenced using a transposon-mediated approach. All but one of the 36 genes were identified (trnS2). The genome is 13,026 bp long, being one of the smallest metazoan mitochondrial genomes sequenced to date with a unique gene order when compared to other Metazoa. The genome has an overall AT richness of 59.4%. We found seven regions of overlaps between tRNAs and protein-coding genes ranging from 2 to 11 nt, and seven regions of overlap between tRNAs, ranging from 1 to 8 nt, resulting in a total number of 46 overlapping nucleotides. Genes nad4, cox2, atp8, and nad3 are terminated by the abbreviated stop codon T and cytb is suggested to terminate on (ACT)AA; we postulate that mRNA editing is required to remove AC for TAA to be functional in terminating translation. Phylogenetic analysis of nucleotide and amino acid data place Flustrellidra in the Lophotrochozoa. DNA for this study originated from two populations resulting in a contig consisting of multiple haplotypes. Twenty-seven SNP sites were detected, the majority occurring in cox1 and nad5. With cox1 already established as a marker in bryozoan studies, we advocate the further testing of nad5.     

Presence of two mitochondrial genomes in the mytilid Perumytilus purpuratus: Phylogenetic evidence for doubly uniparental inheritance

This study presents evidence, using sequences of ribosomal 16S and COI mtDNA, for the presence of two mitochondrial genomes in Perumytilus purpuratus. This may be considered evidence of doubly uniparental mtDNA inheritance. The presence of the two types of mitochondrial genomes differentiates females from males. The F genome was found in the somatic and gonadal tissues of females and in the somatic tissues of males; the M genome was found in the gonads and mantle of males only. For the mitochondrial 16S region, ten haplotypes were found for the F genome (nucleotide diversity 0.004), and 7 haplotypes for the M genome (nucleotide diversity 0.001), with a distance Dxy of 0.125 and divergence Kxy of 60.33%. For the COI gene 17 haplotypes were found for the F genome (nucleotide diversity 0.009), and 10 haplotypes for the M genome (nucleotide diversity 0.010), with a genetic distance Dxy of 0.184 and divergence Kxy of 99.97%. Our results report the presence of two well-differentiated, sex-specific types of mitochondrial genome (one present in the male gonad, the other in the female gonad), implying the presence of DUI in P. purpuratus. These results indicate that care must be taken in phylogenetic comparisons using mtDNA sequences of P. purpuratus without considering the sex of the individuals.     

Rate of change of the phytoplankton community in Itapeva Lake (North Coast of Rio Grande do Sul,Brazil), based on the wind driven hydrodynamic regime

The mussel Mytilus trossulus is an important component of the Baltic brackish water ecosystem. The genetic structure of mussel (M. trossulus) populations was studied in sites along the Polish coast, Southern Baltic for two segments of mitochondrial DNA (mtDNA). The mode of inheritance of Mytilus mtDNA is termed doubly uniparental; two genomes are passed independently down the female (the F genome) and male (the M genome) lines of descent. The M genome has not been detected at high frequency in M. trossulus, thus the present study focuses on the F genome. PCR and RFLP analysis was used to characterise haplotypes in the coding region ND2-COIII; PCR was used to detect length variants in a major noncoding region. Significant differentiation between populations was observed in the frequency of 24 coding region haplotypes and 14 different length variants. For the three most frequent coding region haplotypes, two (I and III) are associated with the length variants, whereas the third (II) is monomorphic for a single variant of short length. It is suggested that variant II is derived by introgression from a related species, M. edulis, and may be resistant to expansion in the noncoding region. In both regions studied, the Ewens–Watterson test reveals significant deviations from neutrality with an excess of rare variants. This might be due to selection against slightly deleterious variants and is consistent with previously published results for Mytilus taxa. The present study also points towards the potential utility of mtDNA length variation in studies of population differentiation of Mytilus.     

Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders

Extensive gene rearrangement is reported in the mitochondrial genomes of lungless salamanders (Plethodontidae). In each genome with a novel gene order, there is evidence that the rearrangement was mediated by duplication of part of the mitochondrial genome, including the presence of both pseudogenes and additional, presumably functional, copies of duplicated genes. All rearrangement-mediating duplications include either the origin of light-strand replication and the nearby tRNA genes or the regions flanking the origin of heavy-strand replication. The latter regions comprise nad6, trnE, cob, trnT, an intergenic spacer between trnT and trnP and, in some genomes, trnP, the control region, trnF, rrnS, trnV, rrnL, trnL1, and nad1. In some cases, two copies of duplicated genes, presumptive regulatory regions, and/or sequences with no assignable function have been retained in the genome following the initial duplication; in other genomes, only one of the duplicated copies has been retained. Both tandem and nontandem duplications are present in these genomes, suggesting different duplication mechanisms. In some of these mitochondrial DNAs, up to 25% of the total length is composed of tandem duplications of noncoding sequence that includes putative regulatory regions and/or pseudogenes of tRNAs and protein-coding genes along with the otherwise unassignable sequences. These data indicate that imprecise initiation and termination of replication, slipped-strand mispairing, and intramolecular recombination may all have played a role in generating repeats during the evolutionary history of plethodontid mitochondrial genomes.     

Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus

Many bivalve species, including mussels of the genus Mytilus, are unusual in having two mtDNA genomes, one inherited maternally (the F genome) and the other inherited paternally (the M genome). The sequence differences between the genomes are usually great, indicating ancient divergence predating speciation events. However, in Mytilus trossulus from the Baltic, both genomes are similar to the F genome from the closely related M. edulis. This study analyzed the mtDNA control region structure in male and female Baltic M. trossulus mussels. We show that a great diversity of structural rearrangements is present in both sexes. Sperm samples are dominated by recombinant haplotypes with M. edulis M-like control region segments, some having large duplications. By contrast, the rearranged haplotypes that dominate in eggs lack segments from this M genome. The rearrangements can be explained by a combination of tandem duplication, deletion, and intermolecular recombination. An evolutionary pathway leading to the recombinant haplotypes is suggested. The data are also considered in relation to the hypothesis that the M. edulis M-like control region sequence is necessary to confer the paternal role on genomes that are otherwise F-like.     

The influence of adjacent nucleotides on the pattern of nucleotide substitution in mitochondrial introns of angiosperms

It has been known that in noncoding regions of the chloroplast genome, the pattern of nucleotide substitution is influenced by the two nucleotides flanking the substitution site. In a GC-rich environment, a bias toward transition was observed, whereas in an AT-rich environment, a bias toward transversion was observed. In this study, the influence of the two adjacent neighbors on the substitution pattern was observed in the first intron of the mitochondrial nad4 gene, although the AT content of this intron is only 48%. The proportion of transversions increases from 0.32 to 0.75 as the A + T content (number of A's + T's) of the two nearest neighbors increases from 0 to 2. This trend was also observed in another mitochondrial group I intron with an AT content of 64%. In addition, a similar, though weaker, effect was observed in vertebrate pseudogenes. So this effect is present in all three types of genomes. Furthermore, in contrast to the situation in the noncoding regions of chloroplast DNA, where most nucleotide substitutions occurred in the categories with an A + T content of either 1 or 2, nucleotide substitutions in the mitochondrial first nad4 intron occurred more evenly in three categories of different A + T contents. This might be due largely to the difference in the AT content (0.48 vs. 0.72) between the mitochondrial first nad4 intron and the chloroplast DNA regions studied.     

Numerous gene rearrangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthiraptera)

The complete arrangement of genes in the mitochondrial (mt) genome is known for 12 species of insects, and part of the gene arrangement in the mt genome is known for over 300 other species of insects. The arrangement of genes in the mt genome is very conserved in insects studied, since all of the protein-coding and rRNA genes and most of the tRNA genes are arranged in the same way. We sequenced the entire mt genome of the wallaby louse, Heterodoxus macropus, which is 14,670 bp long and has the 37 genes typical of animals and some noncoding regions. The largest noncoding region is 73 bp long (93% A+T), and the second largest is 47 bp long (92% A+T). Both of these noncoding regions seem to be able to form stem-loop structures. The arrangement of genes in the mt genome of this louse is unlike that of any other animal studied. All tRNA genes have moved and/or inverted relative to the ancestral gene arrangement of insects, which is present in the fruit fly Drosophila yakuba. At least nine protein-coding genes (atp6, atp8, cox2, cob, nad1-nad3, nad5, and nad6) have moved; moreover, four of these genes (atp6, atp8, nad1, and nad3) have inverted. The large number of gene rearrangements in the mt genome of H. macropus is unprecedented for an arthropod.     

Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea

We have examined mitochondrial DNA (mtDNA) variation in samples of the mussel Mytilus galloprovincialis from the Black Sea, the Mediterranean and the Spanish Atlantic coast by scoring for presence or absence of cleavage at 20 restriction sites of a fragment of the COIII gene and at four restriction sites of the 16S RNA gene. This species contains two types of mtDNA genomes, one that is transmitted maternally (the F type) and one that is transmitted paternally (the M type). The M genome evolves at a higher rate than the F genome. Normally, females are homoplasmic for an F type and males are heteroplasmic for an F and an M type. Occasionally molecules from the F lineage invade the paternal transmission route, resulting in males that carry two F-type mtDNA genomes. These features of the mussel mtDNA system give rise to a new set of questions when using mtDNA variation in population studies and phylogeny. We show here that the two mtDNA types provide different information with regard to amounts of variation and genetic distances among populations. The F genome exhibits higher degrees of diversity within populations, while the M genome produces higher degrees of differentiation among populations. There is a strong differentiation between the Atlantic and the Black Sea. The Mediterranean samples have intermediate haplotype frequencies, yet are much closer to the Black Sea than to the Atlantic. We conclude that in this species gene flow among the three Seas is restricted and not enough to erase the combined effect of mutation and random drift. In one sample, that from the Black Sea, the majority of males did not contain an M mtDNA type. This suggests that a molecule of the maternal lineage has recently invaded the paternal route and has increased its frequency in the population to the point that the present pool of paternally transmitted mtDNA molecules is highly heterogeneous and cannot be used to read the population's history. This liability of the paternal route means that in species with doubly uniparental inheritance, the maternal lineage provides more reliable information for population and phylogenetic studies.     

Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei

Ctenophores are one of the most basally branching lineages of metazoans with the largest mitochondrial organelles in the animal kingdom. We sequenced the mitochondrial (mtDNA) genome from the Pacific cidipid ctenophore, Pleurobrachia bachei. The circular mitochondrial genome is 11,016 nts, with only 12 genes, and one of the smallest metazoan mtDNA genomes recorded. The protein coding genes are intronless cox1-3, cob, nad1, 3, 4, 4L and 5. The nad2 and 6 genes are represented as short fragments whereas the atp6 gene was found in the nuclear genome. Only the large ribosomal RNA subunit and two tRNAs were present with possibly the small subunit unidentifiable due to extensive fragmentation. The observed unique features of this mitochondrial genome suggest that nuclear and mitochondrial genomes have evolved at very different rates. This reduced mtDNA genome sharply contrasts with the very large sizes of mtDNA found in other basal metazoans including Porifera (sponges), and Placozoa (Trichoplax).