Evidence of doubly uniparental inheritance of the mitochondrial DNA in Polititapes rhomboides (Bivalvia,Veneridae): Evolutionary and population genetic analysis of F and M mitotypes

Doubly uniparental inheritance (DUI) is a particular mitochondrial DNA inheritance mode reported in a number of bivalves. DUI species show two types of mtDNA, one transmitted from females to daughters and sons (F mitotype) and another one from males to sons (M mitotype). In Veneridae, the existence of DUI has been investigated in several species but it was found in only two of them. In this study, we obtained partial sequences of rrnL, cytb and cox1 genes of males and females of Polititapes rhomboides from NW Spain and we demonstrated the existence of heteroplasmy in males, as expected under DUI. F and M mitotypes showed a taxon-specific phylogenetic pattern and similar evolutionary rates. We focused on cox1 for population genetic analysis, examining separately F and M mitotypes, but also F mitotypes from females (F_♀) and males (F_♂). In all cases, cox1 bears signs of strong purifying selection, with no apparent evidence of relaxed selection in the M genome, while the divergence between F and M genomes is in agreement with the neutral model of evolution. The cox1 polymorphism, higher at the M than at the F genome, also shows clear footprints of genetic hitchhiking with favourable mutations at other mtDNA loci, except for F_♂. In terms of population structure, results suggest that the pattern depends on the examined mitotype (F, F_♀, F_♂ or M).     

Pyganodon (Bivalvia: Unionoida: Unionidae) phylogenetics: a male- and female-transmitted mitochondrial DNA perspective

Species boundaries, evolutionary relationships and geographic distributions of many unionoid bivalve species, like those in the genus Pyganodon, remain unresolved in Eastern North America. Because unionoid bivalves are one of the most imperiled groups of animals in the world, understanding the genetic variation within and among populations as well as among species is crucial for effective conservation planning. Conservation of unionoid species is indispensable from a freshwater habitat perspective but also because they possess a unique mitochondrial inheritance system where distinct gender-associated mitochondrial DNA lineages coexist: a female-transmitted (F) mt genome and a male-transmitted (M) mt genome that are involved in the maintenance of separate sexes (=dioecy). In this study, 42 populations of Pyganodon sp. were sampled across a large geographical range and fragments of two mitochondrial genes (cox1 and cox2) were sequenced from both the M- and F-transmitted mtDNA genomes. Our results support the recency of the divergence between P. cataracta and P. fragilis. We also found two relatively divergent F and M lineages within P. grandis. Surprisingly, the relationships among the P. grandis specimens in the F and M sequence trees are not congruent. We found that a single haplotype in P. lacustris has recently swept throughout the M genotype space leading to an unexpectedly low diversity in the M lineage in that species. Our survey put forward some challenging results that force us to rethink hybridization and species boundaries in the genus Pyganodon. As the M and F genomes do not always display the same phylogeographic story in each species, we also discuss the importance of being careful in the interpretation of molecular data based solely on maternal transmitted mtDNA genomes. The involvement of F and M genomes in unionoid bivalve sex determination likely played a role in the genesis of the unorthodox phylogeographic patterns reported herein.     

Early replication dynamics of sex-linked mitochondrial DNAs in the doubly uniparental inheritance species Ruditapes philippinarum (Bivalvia Veneridae)

Mitochondrial homoplasmy, which is maintained by strictly maternal inheritance and a series of bottlenecks, is thought to be an adaptive condition for metazoans. Doubly uniparental inheritance (DUI) is a unique mode of mitochondrial transmission found in bivalve species, in which two distinct mitochondrial genome (mtDNA) lines are present, one inherited through eggs (F) and one through sperm (M). During development, the two lines segregate in a sex- and tissue-specific manner: females lose M during embryogenesis, whereas males actively segregate it in the germ line. These two pivotal events are still poorly characterized. Here we investigated mtDNA replication dynamics during embryogenesis and pre-adulthood of the venerid Ruditapes philippinarum using real-time quantitative PCR. We found that both mtDNAs do not detectably replicate during early embryogenesis, and that the M line might be lost from females around 24 h of age. A rise in mtDNA copy number was observed before the first reproductive season in both sexes, with the M mitochondrial genome replicating more than the F in males, and we associate these boosts to the early phase of gonad production. As evidence indicates that DUI relies on the same molecular machine of mitochondrial maternal inheritance that is common in most animals, our data are relevant not only to DUI but also to shed light on how differential segregations of mtDNA variants, in the same nuclear background, may be controlled during development.     

Doubly uniparental inheritance of mitochondrial DNA in freshwater mussels: History and status of the European species

Doubly uniparental inheritance (DUI) is a mode of inheriting mitochondrial DNA that is distinct from strictly maternal inheritance. It has been described in nine and three families of marine and freshwater mussels, respectively, including the European margaritiferids and unionids. Among the 16 freshwater species of Unionida inhabiting Europe, DUI has been described in 9 species of dioecious mussels and was absent from a single hermaphroditic species and from secondary hermaphroditic specimens. The DUI freshwater mussels include two vastly genetically different mitochondrial genomes: maternal (F genome) and paternal (M genome), which coexist within the same specimen but in different tissues. The F genome is present in all female tissues and somatic male tissues. It is inherited in the typical, maternal, manner. Conversely, the M genome is located primarily in the male gonads and generative cells, and is inherited paternally. Dioecious Unionidae display unique characteristics that have been interrelated for over 200 million years: a high fidelity of the transmission of the F and M genomes in DUI and two paths of spermatogenesis–the typical path that produces sperm cells containing mitochondria with the F genome and the atypical path that produces sperm cells with the M genome. The mitogenomes of freshwater mussels display unique features that are not present in any other animal, that is, an additional, gender-specific gene and an elongated cox2 gene occurring exclusively in the M genome. These features mean that the mitochondria, in addition to their basic function of producing energy, also may take part in determining sex in these dioecious organisms.     

The Complete Maternally and Paternally Inherited Mitochondrial Genomes of the Endangered Freshwater Mussel Solenaia carinatus (Bivalvia: Unionidae) and Implications for Unionidae Taxonomy

Doubly uniparental inheritance (DUI) is an exception to the typical maternal inheritance of mitochondrial (mt) DNA in Metazoa, and found only in some bivalves. In species with DUI, there are two highly divergent gender-associated mt genomes: maternal (F) and paternal (M), which transmit independently and show different tissue localization. Solenaia carinatus is an endangered freshwater mussel species exclusive to Poyang Lake basin, China. Anthropogenic events in the watershed greatly threaten the survival of this species. Nevertheless, the taxonomy of S. carinatus based on shell morphology is confusing, and the subfamilial placement of the genus Solenaia remains unclear. In order to clarify the taxonomic status and discuss the phylogenetic implications of family Unionidae, the entire F and M mt genomes of S. carinatus were sequenced and compared with the mt genomes of diverse freshwater mussel species. The complete F and M mt genomes of S. carinatus are 16716 bp and 17102 bp in size, respectively. The F and M mt genomes of S. carinatus diverge by about 40% in nucleotide sequence and 48% in amino acid sequence. Compared to F counterparts, the M genome shows a more compact structure. Different gene arrangements are found in these two gender-associated mt genomes. Among these, the F genome cox2-rrnS gene order is considered to be a genome-level synapomorphy for female lineage of the subfamily Gonideinae. From maternal and paternal mtDNA perspectives, the phylogenetic analyses of Unionoida indicate that S. carinatus belongs to Gonideinae. The F and M clades in freshwater mussels are reciprocal monophyly. The phylogenetic trees advocate the classification of sampled Unionidae species into four subfamilies: Gonideinae, Ambleminae, Anodontinae, and Unioninae, which is supported by the morphological characteristics of glochidia.     

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.     

Evidence for extreme sequence divergence between the male‐ and female‐transmitted mitochondrial genomes in the bivalve mollusc,Modiolus modiolus (Mytilidae)

Marine mussels of the family Mytilidae, as well as a number of other bivalves, have a unique system of mitochondrial DNA inheritance called doubly uniparental inheritance (DUI). DUI is characterized by the presence of an ‘F’ mitochondrial genome that is transmitted through mothers to daughters and sons, and an ‘M’ mitochondrial genome that is transmitted only from fathers to sons. In this paper, we demonstrate that DUI exists in the horse mussel, Modiolus modiolus (Linnaeus, 1758) and compare the pattern of molecular evolution of the M and F types in this species. Total DNA was isolated from M. modiolus male and female gonad tissues, as well as from spawned sperm cells. From these DNA samples, partial mitochondrial DNA fragments were amplified from both cytochrome c oxidase subunit I (cox1), and 16S ribosomal RNA (rrnL) genes. Based on cox1 and rrnL sequences, heteroplasmy was observed in M. modiolus and characterized by the resolution of two mitotypes: an F mitotype present in tissues of both males and females, and an M mitotype present in spawned sperm. Using standardized p‐distance and Tamura‐Nei values, M. modiolus is found to display the highest M/F conspecific sequence divergence for any member of the family Mytilidae (i.e. 38% M/F sequence divergence, which is 9% higher than any other intraspecific M/F comparison for the family Mytilidae when standardized using p‐distances across all taxa observed). Sequence analysis also indicated that the M. modiolus M mitotype evolves significantly faster than its conspecific F type. The findings discussed herein broaden the range of mytilid species known to exhibit DUI and they also establish a new threshold for the genetic divergence of male mytilid mitochondrial genomes.     

Nonhomologous Recombination Between the Large Unassigned Region of the Male and Female Mitochondrial Genomes in the Mussel, Mytilus trossulus

Doubly uniparental inheritance of mtDNA (DUI) is commonly observed in several genera of bivalves. Under DUI, female offspring inherit mtDNA from their mothers, while male offspring inherit mtDNA from both parents but preferentially transmit the paternally inherited mtDNA to their sons. Several studies have shown that the female- and male-specific mtDNA lineages in blue mussels, Mytilus spp., vary by upward of 20% at the nucleotide level. In addition to high levels of nucleotide substitution, the present study observed substantial gender-based length polymorphism in the presumptive mitochondrial control region (=large unassigned region; LUR) of North American M. trossulus. In this species, female lineage LUR haplotypes are over 2 kb larger than male lineage LUR haplotypes. Analysis of sequence data for these length variants indicates that the F LUR haplotypes of North American M. trossulus contain sequences similar to the F lineage control region in the congeners M. edulis and M. galloprovincialis. Relative to the F LUR in the latter two species, however, the F lineage LUR haplotypes in M. trossulus contain two large sequence insertions, each nearly 1 kb in size. One of these insertions has high sequence similarity to the male lineage LUR of M. trossulus. The tandem arrangement of F and M control region sequences in the F lineage LUR of M. trossulus is most likely the result of nonhomologous recombination between the male and the female mitochondrial genomes in M. trossulus, a finding that has important implications regarding the transmission and evolution of blue mussel mitochondrial genomes. [Reviewing Editor: Dr. Martin Kreitman]     

An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid <Emphasis Type="Italic">Musculista senhousia</Emphasis> (Mollusca Bivalvia)

Background

Doubly Uniparental Inheritance (DUI) represents the most outstanding exception to matrilinear inheritance of mitochondrial DNA (mtDNA), typical of Metazoa. In a few bivalve mollusks, two sex-linked mtDNAs (the so-called M and F) are inherited in a peculiar way: both daughters and sons receive their F from the mother, whereas sons inherit M from the father (males do not transmit F to their progeny). This realizes a double mechanism of transmission, in which M and F mtDNAs are inherited uniparentally.DUI systems represent a unique experimental model for testing the evolutionary mechanisms that apply to mitochondrial genomes and their transmission patterns as well as to mtDNA recombination.

Results

A new case of DUI is described in Musculista senhousia (Mollusca: Bivalvia: Mytilidae). Its heteroplasmy pattern is in line with standard DUI. Sequence variability analysis evidenced two main results: F haplotypes sequence variability is higher than that of M haplotypes, and F mitochondrial haplotypes experience a higher mutation rate in males' somatic tissues than in females' ones. Phylogenetic analysis revealed also that M. senhousia M and F haplotypes cluster separately from that of the other mytilids.

Conclusion

Sequence variability analysis evidenced some unexpected traits. The inverted variability pattern (the F being more variable than M) was new and it challenges most of the rationales proposed to account for sex-linked mtDNA evolution. We tentatively related this to the history of the Northern Adriatic populations analyzed. Moreover, F sequences evidenced a higher mutation level in male's soma, this variability being produced de novo each generation. This suggests that mechanisms evolved to protect mtDNA in females (f.i. antioxidant gene complexes) might be under relaxed selection in males. Phylogenetic analysis of sex-linked haplotypes confirmed that they have switched their roles during the evolutionary history of mytilids, at variance to what has been observed in unionids. Consequently, reciprocal monophyly of M and F lineages got easily lost because of role-reversals and consequent losses of M lineages, as already observed in Mytilus.

     

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.     

Male-Dependent Doubly Uniparental Inheritance of Mitochondrial DNA and Female-Dependent Sex-Ratio in the Mussel Mytilus Galloprovincialis

We have investigated sex ratio and mitochondrial DNA inheritance in pair-matings involving five female and five male individuals of the Mediterranean mussel Mytilus galloprovincialis. The percentage of male progeny varied widely among families and was found to be a characteristic of the female parent and independent of the male to which it was mated. Thus sex-ratio in Mytilus appears to be independent of the nuclear genotype of the sperm. With a few exceptions, doubly uniparental inheritance (DUI) of mtDNA was observed in all families fathered by four of the five males: female and male progeny contained the mother's mtDNA (the F genome), but males contained also the father's paternal mtDNA (the M genome). Two hermaphrodite individuals found among the progeny of these crosses contained the F mitochondrial genome in the female gonad and both the F and M genomes in the male gonad. All four families fathered by the fifth male showed the standard maternal inheritance (SMI) of animal mtDNA: both female and male progeny contained only the maternal mtDNA. These observations illustrate the intimate linkage between sex and mtDNA inheritance in species with DUI and suggest different major roles for each gender. We propose a model according to which development of a male gonad requires the presence in the early germ cells of an agent associated with sperm-derived mitochondria, these mitochondria are endowed with a paternally encoded replicative advantage through which they overcome their original minority in the fertilized egg and this advantage (and, therefore, the chance of an early entrance into the germ line) is countered by a maternally encoded egg factor.     

Evolution of a Unique Mitotype-Specific Protein-Coding Extension of the Cytochrome c Oxidase II Gene in Freshwater Mussels (Bivalvia: Unionoida)

A unique mode of mitochondrial DNA inheritance, designated doubly-uniparental inheritance (DUI), occurs in three bivalve subclasses (Pteriomorpha: Mytiloida, Palaeoheterodonta: Unionoida, Heterodonta: Veneroida), indicating that DUI may be a widespread phenomenon among bivalves. In mytiloids, breakdown of this pattern of inheritance (gender-switching) is observed in natural populations and in a phylogenetic context. In contrast, gender-switching has not occurred during the evolutionary history of unionoids. Here we present sequences for the male (M) and female (F) mitotypes from an additional 8 species of Unionoida. Consistent with previous observations, the M and F mitotypes of all species form reciprocally monophyletic clades supporting the hypothesis of taxon-specific rates of gender-switching. Coinciding with the absence of gender-switching is an ≈185 codon extension of the cytochrome c oxidase II (MTCO2) locus in the male genome. The extension is present in all 12 unionoid species examined, including a representative of the family Margaritiferidae, indicating that this protein-coding polymorphism originated ≥ 200 MYBP. Although the extension is well conserved in length among 11 of the 12 species, one taxon has a significantly shortened extension. Lastly, examination of the rates and patterns of substitution indicate that the extension is evolving under relaxed purging selection, a pattern inconsistent with the conserved nature of MTCO2 or any cytochrome c oxidase locus.[Reviewing Editor: Dr. J. William Ballard]     

Mitochondrial DNA copy number is maintained during spermatogenesis and in the development of male larvae to sustain the doubly uniparental inheritance of mitochondrial DNA system in the blue mussel Mytilus galloprovincialis

Doubly uniparental inheritance (DUI) of mitochondrial (mt) DNA has been reported in the blue mussel Mytilus galloprovincialis. In DUI, males inherit both paternal (M type) and maternal (F type) mtDNA. Here we investigated changes in M type mtDNA copy numbers and mitochondrial mass in testicular cells by real‐time polymerase chain reaction and flow cytometry. The ratios of M type mtDNA copy numbers to nuclear DNA content were not different between haploid (1n), diploid (2n) and tetraploid (4n) spermatogenic cells. The mitochondrial mass decreased gradually during spermatogenesis. These results suggest that mtDNA and mitochondrial mass are maintained during spermatogenesis. We then traced M type mtDNA in larvae after fertilization. M type mtDNA was maintained up to 24 h after fertilization in the male‐biased crosses, but decreased significantly in female‐biased crosses (predicted by Mito Tracker staining pattern). These results are strikingly different from those reported for mammals and fish, where it is well known that the mitochondria and mtDNA are reduced during spermatogenesis and that sperm mitochondria and mtDNA are eliminated soon after fertilization. Thus, the M type mtDNA copy number is maintained during spermatogenesis and in the development of male larvae to sustain the DUI system in the blue mussel.     

MULTIPLE ORIGINS OF GENDER-ASSOCIATED MITOCHONDRIAL DNA LINEAGES IN BIVALVES (MOLLUSCA: BIVALVIA)

Previous studies have shown that marine mussels (genus Mytilus) and a freshwater mussel (Pyganodon grandis) contain two distinct gender-associated mitotypes, which is a characteristic feature of the phenomenon of doubly uniparental inheritance (DUI) of mitochondrial DNA (mtDNA). Here we present evidence for the presence of distinct male (M) and female (F) mitotypes in three other bivalve species, the mytilid Geukensia demissa, and the unionid species P. fragilis and Fusconaia flava. Nucleotide sequences of a segment of the COI gene from the M and F mitotypes from each of the three mytilid species (M. edulis, M. trossulus, G. demissa) and three unionid species (P. grandis, P. fragilis, F. flava) were used for phylogenetic analysis. The analysis suggests three independent origins of M and F mitotypes for the six species examined; one for the three unionid species, one for the two Mytilus species, and one for Geukensia. The first of these F/M divergence events, while of uncertain age, predates the divergence of the two unionid genera and is likely older than either of the two F/M divergence events in the mytilid taxa. The most parsimonious explanation of multiple F/M divergence events is that they represent independent origins of DUI. Another possibility is that, in a given taxon, an F or M mitotype assumes the role of the opposite mitotype (by virtue of a mechanism that remains to be clarified) and subsequently was fixed within its new gender. The fixation of a mtDNA lineage derived from a mitotype of switched function would reset the divergence of the gender-associated lineages to zero, thereby mimicking a de novo split of F and M lineages from a preexisting mtDNA genome that was not gender specific. Further broad-scale taxonomic studies of the occurrence of distinct M and F mitotypes may allow for the evaluation of the latter hypothesis.     

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 largest unassigned regions of the male- and female-transmitted mitochondrial DNAs in Musculista senhousia (Bivalvia Mytilidae)

Musculista senhousia is a marine mussel with doubly uniparental inheritance (DUI) of mitochondria. In this study we analyzed the largest unassigned region (LUR) of its female- and male-transmitted mitochondrial genomes, described their fine characteristics and searched for shared features. Our results suggest that both LURs contain the control region of their respective mitochondrial genomes. The female-transmitted control region is duplicated in tandem, with the two copies evolving in concert. This makes the F-mtDNA of M. senhousia the first Bivalve mitochondrial genome with this feature. We also compared M. senhousia control regions to that of other Mytilidae, and demonstrated that signals for basic mtDNA functions are retained over evolutionary times even among the fast-evolving mitochondrial genomes of DUI species. Finally, we discussed how similarities between female and male LURs may be explained in the context of DUI evolution and if the duplicated female control region might have influenced the DUI system in this species.     

No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males

Species of the mussel family Mytilidae have a special mitochondrial DNA (mtDNA) transmission system, known as doubly uniparental inheritance (DUI), which consists of a maternally inherited (F) and a paternally inherited (M) mitochondrial genome. Females are normally homoplasmic for the F genome and males are heteroplasmic mosaics, with their somatic tissues dominated by the maternal and their gonads dominated by the paternal genome. Several studies have indicated that the maternal genome may often be present in the male germ line. Here we report the results from the examination of mtDNA in pure sperm from more than 30 males of Mytilus galloprovincialis. In all cases, except one, we detected only the M genome. In the sperm of one male, we detected a paternal genome with an F-like primary sequence that was different from the sequence of the maternal genome in the animal's somatic tissues. We conclude that the male germ line is protected against invasion by the maternal genome. This is important because fidelity of gamete-specific transmission of the two mitochondrial genomes is a basic requirement for the stability of DUI.