scholarly journals Linking paternally inherited mtDNA variants and sperm performance

2019 ◽  
Vol 375 (1790) ◽  
pp. 20190177 ◽  
Author(s):  
Stefano Bettinazzi ◽  
Sugahendni Nadarajah ◽  
Andréanne Dalpé ◽  
Liliana Milani ◽  
Pierre U. Blier ◽  
...  
Keyword(s):  
Fertilization Success ◽  
Direct Selection ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Adaptive Value ◽  
Mitochondrial Genotype ◽  
Mtdna Evolution ◽  
Mtdna Variants ◽  
The Impact ◽  
Energy Pathways

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’.

scholarly journals Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria

2019 ◽  
Vol 286 (1896) ◽  
pp. 20182708 ◽  
Author(s):  
Stefano Bettinazzi ◽  
Enrique Rodríguez ◽  
Liliana Milani ◽  
Pierre U. Blier ◽  
Sophie Breton
Keyword(s):  
Maternal Inheritance ◽  
Direct Selection ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Respiration Rates ◽  
Adaptive Value ◽  
Unique System ◽  
Somatic Tissues ◽  
Nucleotide Divergence ◽  
Strong Control

Mitochondria produce energy through oxidative phosphorylation (OXPHOS), which depends on the expression of both nuclear and mitochondrial DNA (mtDNA). In metazoans, a striking exception from strictly maternal inheritance of mitochondria is doubly uniparental inheritance (DUI). This unique system involves the maintenance of two highly divergent mtDNAs (F- and M-type, 8–40% of nucleotide divergence) associated with gametes, and occasionally coexisting in somatic tissues. To address whether metabolic differences underlie this condition, we characterized the OXPHOS activity of oocytes, spermatozoa, and gills of different species through respirometry. DUI species express different gender-linked mitochondrial phenotypes in gametes and partly in somatic tissues. The M-phenotype is specific to sperm and entails (i) low coupled/uncoupled respiration rates, (ii) a limitation by the phosphorylation system, and (iii) a null excess capacity of the final oxidases, supporting a strong control over the upstream complexes. To our knowledge, this is the first example of a phenotype resulting from direct selection on sperm mitochondria. This metabolic remodelling suggests an adaptive value of mtDNA variations and we propose that bearing sex-linked mitochondria could assure the energetic requirements of different gametes, potentially linking male-energetic adaptation, mitotype preservation and inheritance, as well as resistance to both heteroplasmy and ageing.

Genetics of Mother-Dependent Sex Ratio in Blue Mussels (Mytilus spp.) and Implications for Doubly Uniparental Inheritance of Mitochondrial DNA

Genetics ◽  
2002 ◽  
Vol 161 (4) ◽  
pp. 1579-1588 ◽  
Author(s):  
Ellen Kenchington ◽  
Barry MacDonald ◽  
Liqin Cao ◽  
Defkalion Tsagkarakis ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Sex Ratio ◽  
Female Parent ◽  
Population Level ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Ratio Bias ◽  
Sex Ratio Bias ◽  
Mitochondrial Genotype ◽  
Ratio Determination

Abstract Previous studies have shown that in most pair matings of Mytilus edulis, M. trossulus, and M. galloprovincialis there is a large sex-ratio bias in favor of either males or females. The degree of bias is a characteristic property of the female parent, as matings of the same female with different males produce the same sex ratio, but matings of the same male with different females produce different sex ratios. All three species possess the unusual feature of doubly uniparental inheritance of mitochondrial DNA (mtDNA); i.e., they contain two distinct types of mtDNA, one that is transmitted matrilinearly and one that is transmitted patrilinearly. This coupling of sex and mtDNA transmission raises the possibility that the mechanism of sex-ratio determination in mussels might be under the control of the mtDNA of the female parent. Here we present data from pedigreed crosses that confirm the previous observations that in mussel matings there is a strong sex-ratio bias and that the bias is under the control of the female parent. In addition, these data strongly suggest that this control is exercised by the mother's nuclear rather than mitochondrial genotype. Making use of these findings we develop a model of mother-dependent sex determination and use data from crosses involving wild females to test the model's predictions at the population level.

scholarly journals Bioenergetic consequences of sex-specific mitochondrial DNA evolution

2021 ◽  
Vol 288 (1957) ◽  
pp. 20211585
Author(s):  
Stefano Bettinazzi ◽  
Liliana Milani ◽  
Pierre U. Blier ◽  
Sophie Breton
Keyword(s):  
Mitochondrial Genome ◽  
Acid Metabolism ◽  
Maternal Inheritance ◽  
Tricarboxylic Acid Cycle ◽  
General Rule ◽  
High Energy ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Antioxidant Metabolism ◽  
The Impact

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.

scholarly journals Differential Segregation Patterns of Sperm Mitochondria in Embryos of the Blue Mussel (Mytilus edulis)

Genetics ◽  
2004 ◽  
Vol 166 (2) ◽  
pp. 883-894
Author(s):  
Liqin Cao ◽  
Ellen Kenchington ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Mytilus Edulis ◽  
Blue Mussel ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
Organelle Genomes ◽  
Somatic Tissues ◽  
Tight Linkage ◽  
Mitotracker Green

Abstract In Mytilus, females carry predominantly maternal mitochondrial DNA (mtDNA) but males carry maternal mtDNA in their somatic tissues and paternal mtDNA in their gonads. This phenomenon, known as doubly uniparental inheritance (DUI) of mtDNA, presents a major departure from the uniparental transmission of organelle genomes. Eggs of Mytilus edulis from females that produce exclusively daughters and from females that produce mostly sons were fertilized with sperm stained with MitoTracker Green FM, allowing observation of sperm mitochondria in the embryo by epifluorescent and confocal microscopy. In embryos from females that produce only daughters, sperm mitochondria are randomly dispersed among blastomeres. In embryos from females that produce mostly sons, sperm mitochondria tend to aggregate and end up in one blastomere in the two- and four-cell stages. We postulate that the aggregate eventually ends up in the first germ cells, thus accounting for the presence of paternal mtDNA in the male gonad. This is the first evidence for different behaviors of sperm mitochondria in developing embryos that may explain the tight linkage between gender and inheritance of paternal mitochondrial DNA in species with DUI.

A proposed method for analyzing molecular signatures to detect hermaphroditism in freshwater mussels: a case study using the Eastern Floater (Pyganodon cataracta)

2021 ◽  
Author(s):  
Donald T. Stewart ◽  
Chloe M. Stephenson ◽  
Ljiljana M. Stanton ◽  
Emily E. Chase ◽  
Brent M. Robicheau ◽  
...  
Keyword(s):  
Freshwater Mussels ◽  
Uniparental Inheritance ◽  
Molecular Signatures ◽  
Doubly Uniparental Inheritance ◽  
Hydrophobic Properties ◽  
Mt Dna ◽  
Reading Frame ◽  
Mt Genome ◽  
Primary Nucleotide Sequence

Many freshwater mussels (Order Unionida) have an unusual system of doubly uniparental inheritance (DUI) of mitochondrial (mt) DNA. In species with DUI, males possess a female-transmitted (F-type) mt genome and a male-transmitted (M-type) mt genome. These genomes contain non-canonical open reading frame (orf) genes referred to as f-orf and m-orf, present in F and M mt genomes, respectively. These genes have been implicated in sexual development in Unionida. When gonochoric species become hermaphroditic, which has happened several times in Unionida, they lose their M-type mt genome, and f-orf genes evolve dramatically. Resulting F-ORF proteins are highly divergent in terms of primary nucleotide sequence, inferred amino acids, and hydrophobic properties; these genes (and proteins) are referred to as hermaphroditic orfs or h-orfs (and H-ORFs). We investigated patterns of hydrophobicity divergence for H-ORF proteins in hermaphrodites versus F-ORF proteins in closely related gonochoric species against cytochrome c oxidase subunit 1 (cox1) divergences. This approach was used to assess whether cryptic hermaphrodites can be detected. Although we did not detect evidence for the recent transition of any populations of Eastern Floaters, Pyganodon cataracta (Say, 1817) to hermaphroditism, our analyses demonstrate that molecular signatures in mtDNA can be used to detect hermaphroditism in freshwater mussels.

scholarly journals Size-selective mortality fosters ontogenetic changes in collective risk-taking behaviour in zebrafish, Danio rerio

2021 ◽  
Author(s):  
Tamal Roy ◽  
Robert Arlinghaus
Keyword(s):  
Danio Rerio ◽  
Risk Taking ◽  
Direct Selection ◽  
Small Fish ◽  
Control Line ◽  
Selective Mortality ◽  
Predation Threat ◽  
Size Selection ◽  
Risk Of Predation ◽  
The Impact

AbstractSize-selective mortality is common in fish populations and can operate either in a positive size-selective fashion or be negatively size-selective. Through various mechanisms (like genetic correlations among behaviour and life-history traits or direct selection on behaviour co-varying with growth rate or size-at-maturation), both positive- and negative size-selection can result in evolutionary changes in behavioural traits. Theory suggests that size-selection alone favours boldness, but little experimental evidence exists about whether and to what extent size-selection can trigger its evolution. Here we investigated the impact of size-selective mortality on boldness across ontogeny using three experimental lines of zebrafish (Danio rerio) generated through positive (large-harvested), negative (small-harvested) and random (control line) size-selective mortality for five generations. We measured risk-taking during feeding (boldness) under simulated aerial predation threat and in presence of a live cichlid. We found that boldness decreased with ontogenetic age under aerial predation threat, and the small-harvested line was consistently bolder than controls. Collective personality emerged post larval stages among the selection lines. In presence of a cichlid, the large-harvested line was bolder at the highest risk of predation. The large-harvested line showed higher variability and plasticity in boldness across life stages and predation risks. Collectively, our results demonstrate that size-selective harvesting may evolutionarily alter risk-taking tendency. Size-selection alone favours boldness when selection acts on small fish. Selection typical of fisheries operating on large fish favours boldness at the highest risk of predation and increases behavioural variability and plasticity. There was no evidence for positive size-selection favouring evolution of shyness.

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