Strict Maternal Inheritance Research Articles

Support for Y-compensation of mother's curse affecting lifespan in Drosophila melanogaster.

Mother's curse refers to male-biased deleterious mutations that may accumulate on mitochondria due to its strict maternal inheritance. If these mutations persist, males should ideally compensate through mutations on Y-chromosomes given its strict paternal inheritance. Previous work addressed this hypothesis by comparing coevolved and non-coevolved Y-mitochondria pairs placed alongside completely foreign autosomal backgrounds, expecting males with coevolved pairs to exhibit greater fitness due to Y-compensation. To date, no evidence for Y-compensation has been found. That experimental design assumes Y-chromosomes compensate via direct interaction with mitochondria and/or coevolved autosomes are unimportant in its function or elucidation. If Y-chromosomes instead compensate by modifying autosomal targets (or its elucidation requires coevolved autosomes), then this design could fail to detect Y-compensation. Here we address if Y-chromosomes ameliorate mitochondrial mutations affecting male lifespan in Drosophila melanogaster. Using three disparate populations we compared lifespan among males with coevolved and non-coevolved Y-mitochondria pairs placed alongside autosomal backgrounds coevolved with mitochondria. We found coevolved pairs exhibited lower mortality risk relative to non-coevolved pairs. In contrast, no such pattern was observed when coevolved and non-coevolved pairs were placed alongside non-coevolved autosomes, as with previous studies. These data are consistent with Y-compensation and highlight the importance of autosomes in this capacity. However, we cannot fully exclude the possibility that Y-autosomal coevolution independent of mitochondrial mutations contributed to our results. Regardless, modern practices in medicine, conservation, and agriculture that introduce foreign Y-chromosomes into non-coevolved backgrounds should be used with caution, as they may disrupt Y-autosome coadaptation and/or inadvertently unbridle mother's curse.

Paternal Mitochondrial DNA Leakage in Natural Populations of Large-Scale Loach, Paramisgurnus dabryanus.

Animal mitochondrial DNA is usually considered to comply with strict maternal inheritance, and only one mitochondrial DNA haplotype exists in an individual. However, mitochondrial heteroplasmy, the occurrence of more than one mitochondrial haplotype, has recently been reported in some animals, such as mice, mussels, and birds. This study conducted extensive field surveys to obtain representative samples to investigate the existence of paternal inheritance of mitochondrial DNA (mtDNA) in natural fish populations. Evidence of paternal mitochondrial DNA leakage of P. dabryanus was discovered using high-throughput sequencing and bioinformatics methods. Two distinct mitochondrial haplotypes (16,569 bp for haplotype I and 16,646 bp for haplotype II) were observed, differing by 18.83% in nucleotide sequence. Phylogenetic analysis suggests divergence between these haplotypes and potential interspecific hybridization with M. anguillicaudatus, leading to paternal leakage. In natural populations of P. dabryanus along the Yangtze River, both haplotypes are present, with Type I being dominant (75% copy number). Expression analysis shows that Type I has higher expression levels of ND3 and ND6 genes compared to Type II, suggesting Type I's primary role. This discovery of a species with two mitochondrial types provides a model for studying paternal leakage heterogeneity and insights into mitochondrial genome evolution and inheritance.

Investigating the role of mitochondrial membrane potential in paternal inheritance of mitochondria

Abstract The process of oxidative phosphorylation (OXPHOS) in mitochondria depends on an electrochemical gradient known as the mitochondrial membrane potential (Δψm). Reflecting high functionality, elevated Δψm usually depicts healthy mitochondria and contributes to organelle selection. This study investigates whether mitochondrial properties linked with bioenergetics, such as Δψm, play a role in paternal inheritance of mitochondria. More specifically, the study looks at how sperm Δψm responds to egg chemoattractants in bivalves characterized by distinct mitochondrial inheritance patterns: strict maternal inheritance (SMI) and doubly uniparental inheritance (DUI), the latter displaying sex-specific transmission of paternal mitochondrial DNA. Sperm Δψm was examined in four bivalve species: the blue mussel (Mytilus edulis) and the Manila clam (Ruditapes philippinarum) (DUI), plus the hard clam (Mercenaria mercenaria) and the soft-shell clam (Mya arenaria) (SMI). In the absence of egg chemoattractants, sperm Δψm did not vary between the two groups. However, there was a trend of increase in Δψm following egg detection only in sperm bearing paternally derived mitochondria (DUI). This suggests, along with bioenergetic changes, that Δψm modulation might be a specific property of at least some DUI species, possibly implicated in their unique ability to transmit their mitochondria in a sex-specific fashion.

Mitochondrial effects on fertility and longevity in Tigriopus californicus contradict predictions of the mother's curse hypothesis.

Strict maternal inheritance of mitochondria favours the evolutionary accumulation of sex-biased fitness effects, as mitochondrial evolution occurs exclusively in female lineages. The 'mother's curse' hypothesis proposes that male-harming mutations should accumulate in mitochondrial genomes when they have neutral or beneficial effects on female fitness. Rigorous empirical tests have largely focused on Drosophila, where support for the predictions of mother's curse has been mixed. We investigated the impact of mother's curse mutations in Tigriopus californicus, a minute crustacean. Using non-recombinant backcrosses, we introgressed four divergent mitochondrial haplotypes into two nuclear backgrounds and recorded measures of fertility and longevity. We found that the phenotypic effects of mitochondrial mutations were context dependent, being influenced by the nuclear background in which they were expressed, as well as the sex of the individual and rearing temperature. Mitochondrial haplotype effects were greater for fertility than longevity, and temperature effects were greater for longevity. However, in opposition to mother's curse expectations, females had higher mitochondrial genetic variance than males for fertility and longevity, little evidence of sexual antagonism favouring females was found, and the impacts of mitonuclear mismatch harmed females but not males. Together, this indicates that selection on mitochondrial variation has not resulted in the accumulation of male mutation load in Tigriopus californicus.

The complete paternally inherited mitochondrial genomes of three clam species in genus Macridiscus (Bivalvia: Veneridae): A TDRL model of dimer-mitogenome rearrangement of doubly uniparental inheritance

One of the most striking exceptions to strict maternal inheritance of mitochondrial DNA (mtDNA) in the animal kingdom is a system called doubly uniparental inheritance (DUI), which exists in several bivalve species. DUI is characterized by the presence of two distinct sex-associated mitochondrial lineages: one transmitted through eggs (F-type mtDNA) and the other through sperm (M-type mtDNA). Presently, most known species exhibiting DUI belong to the freshwater bivalve order Unionoida. Other groups with species exhibiting DUI include the orders Mytiloida, Veneroida, and Nuculanoida. In Veneroida, the complete M-type mtDNA is available for two species. We report the presence of DUI in three species belonging to genus Macridiscus (Macridiscus melanaegis, Macridiscus multifarious, and Macridiscus semicancellata), in the order Veneroida, further obtaining their complete M-type mitogenomes. The M-type mitogenome sizes for M. melanaegis, M. multifarious, and M. semicancellata were 19,019 bp, 18,694 bp, and 18,726 bp, respectively, and the mean nucleotide difference between M-type and F-type mitogenomes was 21–23%. We compared the M-type and F-type mitogenomes and found that they show roughly the same genome features, except for gene order. In phylogenetic analyses of Veneroida, a “gender-joining” pattern was revealed within Macridiscus, similar to the pattern of “partial” Mytilus complex (except Unionida). This new insight provides novel evidence supporting the theory that Veneroida and Mytiloida have a more similar DUI pattern than Unionida. A large-scale rearrangement between the sex-linked mitogenomes of the three Macridiscus species was reported. From the observed rearrangement patterns, gene rearrangement between the two sex-linked mitogenomes could be explained by the tandem duplication and random loss (TDRL) model of dimer-mitogenome. This is the first report of heterogeneous genomes with two types of large-scale arrangements in the same organism, and may be contribute significantly to the study of mitochondrial recombination mechanisms.

Exogenous paternal mitochondria rescue hybrid incompatibility and the destiny of exogenous mitochondria

The mitochondria of most organisms follow strict maternal inheritance, and the mechanism of elimination of paternal mitochondria is unclear. Our previous studies showed that the paternal mtDNA presented in the embryo of hybrid Megalobrama Amblycephala (BSB,♀) ​× ​Carassius auratus red var(RCC,♂) (BR) and its reciprocal hybrid (RB), but its expression was quiescent. However, the microinjected mitochondria persisted in the embryo and its mtDNA expressed throughout embryonic development. In addition, the chromosome number of RCC (2n ​= ​100) is much larger than that of BSB (2n ​= ​48). All BR embryos were severely abnormal and ultimately died, while the RB embryos could survive and grow up into adult. It implied that the nuclear-cytoplasm incompatibility may be an important cause of BR abnormality. In this study, exogenous parental mitochondria were microinjected into BR embryos, and it was found that paternal mitochondrial DNA persisted and expressed throughout embryonic development. Meanwhile, the study also found that microinjection of isolated paternal (RCC) mitochondria into BR embryos significantly improved the degree of early embryonic abnormality with some fry swimming normally, comparing to the control embryos. However, injection of maternal (BSB) mitochondria did not improve the development of BR embryos. We safely concluded exogenous mitochondria escape the mechanism of elimination and its DNA persist and express throughout embryonic development. In addition, the expression of paternal mitochondrial genes largely reduces the cyto-nuclear conflict, so that the early BR embryos exhibit less degree of abnormality and enhanced activity.

Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system?

Animal and plant species exhibit an astonishing diversity of sexual systems, including environmental and genetic determinants of sex, with the latter including genetic material in the mitochondrial genome. In several hermaphroditic plants for example, sex is determined by an interaction between mitochondrial cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Specifically, CMS involves aberrant mitochondrial genes that prevent pollen development and specific nuclear genes that restore it, leading to a mixture of female (male-sterile) and hermaphroditic individuals in the population (gynodioecy). Such a mitochondrial-nuclear sex determination system is thought to be rare outside plants. Here, we present one possible case of CMS in animals. We hypothesize that the only exception to the strict maternal mtDNA inheritance in animals, the doubly uniparental inheritance (DUI) system in bivalves, might have originated as a mitochondrial-nuclear sex-determination system. We document and explore similarities that exist between DUI and CMS, and we propose various ways to test our hypothesis.

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Songbirds have one special accessory chromosome, the so-called germline-restricted chromosome (GRC), which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line-like the mitochondria-and is eliminated from the sperm during spermatogenesis. Here, we show that the GRC has the potential to be paternally inherited. Confocal microscopy using GRC-specific fluorescent in situ hybridization probes indicated that a considerable fraction of sperm heads (1 to 19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred male hybrid of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the mitochondria originated from a castanotis mother, whereas the GRC came from a guttata father. Moreover, analyzing GRC haplotypes across nine castanotis matrilines, estimated to have diverged for up to 250,000 y, showed surprisingly little variability among GRCs. This suggests that a single GRC haplotype has spread relatively recently across all examined matrilines. A few diagnostic GRC mutations that arose since this inferred spreading suggest that the GRC has continued to jump across matriline boundaries. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population via occasional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

Relaxed selection on male mitochondrial genes in DUI bivalves eases the need for mitonuclear coevolution

Mitonuclear coevolution is an important prerequisite for efficient energy production in eukaryotes. However, many bivalve taxa experience doubly uniparental inheritance (DUI) and have sex-specific mitochondrial (mt) genomes, providing a challenge for mitonuclear coevolution. We examined possible mechanisms to reconcile mitonuclear coevolution with DUI. No nuclear-encoded, sex-specific OXPHOS paralogs were found in the DUI clam Ruditapes philippinarum, refuting OXPHOS paralogy as a solution in this species. It is also unlikely that mt changes causing disruption of nuclear interactions are strongly selected against because sex-specific mt-residues or those under positive selection in M mt genes were not depleted for contacting nuclear-encoded residues. However, M genomes showed consistently higher dN /dS ratios compared to putatively ancestral F genomes in all mt OXPHOS genes and across all DUI species. Further analyses indicated that this was consistently due to relaxed, not positive selection on M vs. F mt OXPHOS genes. Similarly, selection was relaxed on the F genome of DUI species compared to species with strict maternal inheritance. Coupled with recent physiological and molecular evolution studies, we suggest that relaxed selection on M mt function limits the need to maintain mitonuclear interactions in M genomes compared to F genomes. We discuss our findings with regard to OXPHOS function and the origin of DUI.

Bioenergetic consequences of sex-specific mitochondrial DNA evolution.

Doubly uniparental inheritance (DUI) represents a notable exception to the general rule of strict maternal inheritance (SMI) of mitochondria in metazoans. This system entails the coexistence of two mitochondrial lineages (F- and M-type) transmitted separately through oocytes and sperm, thence providing an unprecedented opportunity for the mitochondrial genome to evolve adaptively for male functions. In this study, we explored the impact of a sex-specific mitochondrial evolution upon gamete bioenergetics of DUI and SMI bivalve species, comparing the activity of key enzymes of glycolysis, fermentation, fatty acid metabolism, tricarboxylic acid cycle, oxidative phosphorylation and antioxidant metabolism. Our findings suggest reorganized bioenergetic pathways in DUI gametes compared to SMI gametes. This generally results in a decreased enzymatic capacity in DUI sperm with respect to DUI oocytes, a limitation especially prominent at the terminus of the electron transport system. This bioenergetic remodelling fits a reproductive strategy that does not require high energy input and could potentially link with the preservation of the paternally transmitted mitochondrial genome in DUI species. Whether this phenotype may derive from positive or relaxed selection acting on DUI sperm is still uncertain.

Expanding the Search for Sperm Transmission Elements in the Mitochondrial Genomes of Bivalve Mollusks.

Doubly uniparental inheritance (DUI) of mitochondrial DNA (mtDNA) in bivalve mollusks is one of the most notable departures from the paradigm of strict maternal inheritance of mtDNA among metazoans. Recently, work on the Mediterranean mussel Mytilus galloprovincialis suggested that a nucleotide motif in the control region of this species, known as the sperm transmission element (STE), helps protect male-transmitted mitochondria from destruction during spermatogenesis. Subsequent studies found similar, yet divergent, STE motifs in other marine mussels. Here, we extend the in silico search for mtDNA signatures resembling known STEs. This search is carried out for the large unassigned regions of 157 complete mitochondrial genomes from within the Mytiloida, Veneroida, Unionoida, and Ostreoida bivalve orders. Based on a sliding window approach, we present evidence that there are additional putative STE signatures in the large unassigned regions of several marine clams and freshwater mussels with DUI. We discuss the implications of this finding for interpreting the origin of doubly uniparental inheritance in ancestral bivalve mollusks, as well as potential future in vitro and in silico studies that could further refine our understanding of the early evolution of this unusual system of mtDNA inheritance.

Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria

In animals, strictly maternal inheritance (SMI) of mitochondria is the rule, but one exception (doubly uniparental inheritance or DUI), marked by the transmission of sex-specific mitogenomes, has been reported in bivalves. Associated with DUI is a frequent modification of the mitochondrial cox2 gene, as well as additional sex-specific mitochondrial genes not involved in oxidative phosphorylation. With the exception of freshwater mussels (for 3 families of the order Unionida), these DUI-associated features have only been shown in few species [within Mytilidae (order Mytilida) and Veneridae (order Venerida)] because of the few complete sex-specific mitogenomes published for these orders. Here, we present the complete sex-specific mtDNAs of two recently-discovered DUI species in two families of the order Venerida, Scrobicularia plana (Semelidae) and Limecola balthica (Tellinidae). These species display the largest differences in genome size between sex-specific mitotypes in DUI species (>10 kb), as well as the highest mtDNA divergences (sometimes reaching >50%). An important in-frame insertion (>3.5 kb) in the male cox2 gene is partly responsible for the differences in genome size. The S. plana cox2 gene is the largest reported so far in the Kingdom Animalia. The mitogenomes may be carrying sex-specific genes, indicating that general mitochondrial features are shared among DUI species.

Linking paternally inherited mtDNA variants and sperm performance.

Providing robust links between mitochondrial genotype and phenotype is of major importance given that mitochondrial DNA (mtDNA) variants can affect reproductive success. Because of the strict maternal inheritance (SMI) of mitochondria in animals, haplotypes that negatively affect male fertility can become fixed in populations. This phenomenon is known as 'mother's curse'. Doubly uniparental inheritance (DUI) of mitochondria is a stable exception in bivalves, which entails two mtDNA lineages that evolve independently and are transmitted separately through oocytes and sperm. This makes the DUI mitochondrial lineages subject to different sex-specific selective sieves during mtDNA evolution, thus DUI is a unique model to evaluate how direct selection on sperm mitochondria could contribute to male reproductive fitness. In this study, we tested the impact of mtDNA variants on sperm performance and bioenergetics in DUI and SMI species. Analyses also involved measures of sperm performance following inhibition of main energy pathways and sperm response to oocyte presence. Compared to SMI, DUI sperm exhibited (i) low speed and linearity, (ii) a strict OXPHOS-dependent strategy of energy production, and (iii) a partial metabolic shift towards fermentation following egg detection. Discussion embraces the adaptive value of mtDNA variation and suggests a link between male-energetic adaptation, fertilization success and paternal mitochondria preservation. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'.

Putative Mitochondrial Sex Determination in the Bivalvia: Insights From a Hybrid Transcriptome Assembly in Freshwater Mussels.

Bivalves exhibit an astonishing diversity of sexual systems, with genetic and environmental determinants of sex, and possibly the only example of mitochondrial genes influencing sex determination pathways in animals. In contrast to all other animal species in which strict maternal inheritance (SMI) of mitochondria is the rule, bivalves possess a system known as doubly uniparental inheritance (DUI) of mitochondria in which maternal and paternal mitochondria (and their corresponding female-transmitted or F mtDNA and male-transmitted or M mtDNA genomes) are transmitted within a species. Species with DUI also possess sex-associated mtDNA-encoded proteins (in addition to the typical set of 13), which have been hypothesized to play a role in sex determination. In this study, we analyzed the sex-biased transcriptome in gonads of two closely-related freshwater mussel species with different reproductive and mitochondrial transmission modes: the gonochoric, DUI species, Utterbackia peninsularis, and the hermaphroditic, SMI species, Utterbackia imbecillis. Through comparative analysis with other DUI and non-DUI bivalve transcriptomes already available, we identify common male and female-specific genes, as well as SMI and DUI-related genes, that are probably involved in sex determination and mitochondrial inheritance in this animal group. Our results contribute to the understanding of what could be the first animal sex determination system involving the mitochondrial genome.

Resolving a 150-year-old paternity case in Mormon history using DTC autosomal DNA testing of distant relatives

Although autosomal DNA testing has been available for a number of years, its use to reconstruct genetic profiles of people that lived centuries in the past is relatively recent and there are no published cases where it was employed to verify a kinship relation, likely to be an alleged paternity, that occurred one and a half century ago.DNA testing has already been employed to study the ancestry and posterity of Joseph Smith Jr., founder of the Latter-day Saint (Mormon) movement. Thanks to information found on the paternally inherited Y chromosome, a number of alleged paternities have been disproved, but obviously this analysis is not effective for alleged daughters. Likewise, his reconstructed mitogenome sequence, reported here for the first time, provides information about his maternal ancestry, but is useless in any paternity questions due to the strict maternal inheritance. Among all the children attributed to Joseph Smith Jr., Josephine Lyon, born in 1844, is perhaps the most frequently mentioned.In the current study, 56 individuals, mostly direct descendants of Joseph Smith Jr. and Josephine Lyon, had their autosomal DNA tested to verify Josephine’s biological paternity. Nearly 600,000 autosomal SNPs from each subject were typed and detailed genealogical data were compiled. The absence of shared DNA between Josephine’s grandson and Joseph Smith Jr.’s five great-grandchildren together with various amounts of autosomal DNA shared by the same individual with four other relatives of Windsor Lyon is a clear indication that Josephine was not related to the Smith, but to the Lyon’s family. These inferences were also verified using kinship analyses and likelihood ratio calculations.

Coadaptation of mitochondrial and nuclear genes, and the cost of mother's curse.

Strict maternal inheritance renders the mitochondrial genome susceptible to accumulating mutations that harm males, but are otherwise benign or beneficial for females. This 'mother's curse' effect can degrade male survival and fertility if unopposed by counteracting evolutionary processes. Coadaptation between nuclear and mitochondrial genomes-with nuclear genes evolving to compensate for male-harming mitochondrial substitutions-may ultimately resolve mother's curse. However, males are still expected to incur a transient fitness cost during mito-nuclear coevolution, and it remains unclear how severe such costs should be. We present a population genetic analysis of mito-nuclear coadaptation to resolve mother's curse effects, and show that the magnitude of the 'male mitochondrial load'-the negative impact of mitochondrial substitutions on male fitness components-may be large, even when genetic variation for compensatory evolution is abundant. We also find that the male load is surprisingly sensitive to population size: male fitness costs of mito-nuclear coevolution are particularly pronounced in both small and large populations, and minimized in populations of intermediate size. Our results reveal complex interactions between demography and genetic constraints during the resolution of mother's curse, suggesting potentially widespread species differences in susceptibility to mother's curse effects.

Response to Ghiselli F et al. (2018).

I thank the authors (Ghiselli et al . [1]) for their interesting comments regarding my article [2]. They indeed further clarified some important points regarding both uniparental organelle inheritance (UPI), which we encounter almost exclusively as strictly maternal inheritance (SMI) and doubly uniparental inheritance (DUI) as well as ‘role-reversal' of F-type mitochondrial DNA (mtDNA). Their data again illustrate the fascinating variety in mitochondrial inheritance. The authors critically discuss their data to ask whether these support John Allen's ‘division of labour' hypothesis [3], where male gametes maximize energy production for competitive advantages in motility, thus damaging mtDNA by mutagenic reactive oxygen species (ROS), coming from oxidative phosphorylation (OXPHOS). Non-motile female gametes, on the other hand, repress OXPHOS, keeping their mtDNA pristine. They ‘clarify two discussion points: (i) the exceptions to the strictly maternal inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS.' Before responding to their arguments, it is worthwhile to very briefly summarize a possible …

Mitochondrial activity in gametes and uniparental inheritance: a comment on 'What can we infer about the origin of sex in early eukaryotes?'

In his insightful article, Speijer [1] discussed the origin of sex under multiple points of view, providing a comprehensive and balanced overview of different theories and hypotheses. However, we think that the section ‘Higher mutational loads in one gamete type and retention of uniparental mitochondrial inheritance’ (§9) needs some clarification. Speijer [1] elaborates on the correlation between gamete metabolic and physiological differences and their organellar contribution across generations. Specifically, he quotes the ‘division of labour’ hypothesis, which postulates that male gametes maximize energy production for motility by sacrificing mitochondrial DNA (mtDNA) to oxidative phosphorylation (OXPHOS) and its mutagenic by-products, while non-motile female gametes repress OXPHOS, thus being somewhat inactive [2]. Basically, we clarify two discussion points: (i) the exceptions to the strictly maternal inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS. Exceptions to SMI by which bioenergetically active mitochondria are stably inherited through generations might represent a challenge for the division of labour hypothesis. Doubly uniparental inheritance (DUI) is the only known evolutionarily stable exception to the SMI typical of Metazoa. In DUI animals (approx. 100 species of gonochoric bivalve molluscs identified so far [3]), two mitochondrial lineages are inherited, one through eggs (F-type) and the other through sperm (M-type). Eggs are homoplasmic for the F-type, while spermatozoa are homoplasmic for the M-type. These ‘mother-to-daughter’ and ‘father-to-son’ mitochondrial lineages have evolved independently for millions of years (e.g. more than 200 Myr in unionids), accumulating up to 40% of DNA sequence divergence. Since eggs do not transmit the M-type, germ line mitochondria of DUI males are apportioned from the four/five mitochondria of the fertilizing spermatozoon, which carry mtDNA that must be functional and successfully inherited [ …

Lose it or keep it: (how bivalves can provide) insights into mitochondrial inheritance mechanisms.

The strictly maternal inheritance (SMI) is a pattern of mitochondrial inheritance observed across the whole animal kingdom. However, some interesting exceptions are known for the class Bivalvia, in which several species show an unusual pattern called doubly uniparental inheritance (DUI) whose outcome is a heteroplasmic pool of mtDNA in males. Even if DUI has been studied for long, its molecular basis has not been established yet. The aim of this work is to select classes of proteins known to be involved in the maintenance of SMI and to compare their features in two clam species differing for their mitochondrial inheritance mechanism, that is, the SMI species Ruditapes decussatus and the DUI species Ruditapes philippinarum. Data have been obtained from the transcriptomes of male and female ripe gonads of both species. Our analysis focused on nucleases and polymerases, ubiquitination and ubiquitin-like modifier pathways, and proteins involved in autophagy and mitophagy. For each protein group of interest, transcription bias (male or female), annotation, and mitochondrial targeting (when appropriate) were assessed. We did not find evidence supporting a role of nucleases/polymerases or autophagic machinery in the enforcement of SMI in R. decussatus. On the other hand, ubiquitinating enzymes with the expected features have been retrieved, providing us with two alternative testable models for mitochondrial inheritance mechanisms at the molecular level.

The Complete Maternally and Paternally Inherited Mitochondrial Genomes of a Freshwater Mussel Potamilus alatus (Bivalvia: Unionidae).

Doubly uniparental inheritance (DUI) of mitochondrial DNA, found only in some bivalve families and characterized by the existence of gender-associated mtDNA lineages that are inherited through males (M-type) or females (F-type), is one of the very few exceptions to the general rule of strict maternal mtDNA inheritance in animals. M-type sequences are often undetected and hence still underrepresented in the GenBank, which hinders the progress of the understanding of the DUI phenomenon. We have sequenced and analyzed the complete M and F mitogenomes of a freshwater mussel, Potamilus alatus. The M-type was 493 bp longer (M = 16 560, F = 16 067 bp). Gene contents, order and the distribution of genes between L and H strands were typical for unionid mussels. Candidates for the two ORFan genes (forf and morf) were found in respective mitogenomes. Both mitogenomes had a very similar A+T bias: F = 61% and M = 62.2%. The M mitogenome-specific cox2 extension (144 bp) is much shorter than in other sequenced unionid mitogenomes (531–576 bp), which might be characteristic for the Potamilus genus. The overall topology of the phylogenetic tree is in very good agreement with the currently accepted phylogenetic relationships within the Unionidae: both studied sequences were placed within the Ambleminae subfamily clusters in the corresponding M and F clades.