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.

The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: Implications for the operation of doubly uniparental inheritance of mitochondrial DNA

Genome ◽  
1998 ◽  
Vol 41 (6) ◽  
pp. 818-824 ◽  
Author(s):  
Manuel A Garrido-Ramos ◽  
Donald T Stewart ◽  
Brent W Sutherland ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Blue Mussel ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Dominant Type ◽  
Blue Mussels ◽  
Somatic Tissues ◽  
Dna Types ◽  
M Genome

We have examined the mitochondrial DNA (mtDNA) content of several somatic tissues from male and female individuals of the blue mussel, Mytilus edulis. As expected from the mode of doubly uniparental inheritance (DUI) of mtDNA that is characteristic of this genus, the dominant type of mtDNA in male gonads was the male-transmitted M type. In contrast, all male somatic tissues were dominated by the female-transmitted F type. The M type could occasionally be detected in one or another tissue of a few female individuals. The findings have several implications for the operation of doubly uniparental inheritance of mitochondrial DNA, among which the most important are (i) the M genome does not have an unconditional replicative advantage over the F genome, and (ii) in contrast to "masculinization" (the process by which an F molecule assumes the role of the M genome) "feminization" (the process by which an M molecule assumes the role of the F genome) might be a rare but not impossible phenomenon.Key words: mitochondrial DNA inheritance, mitochondrial DNA tissue distribution, blue mussels, gender-specific mtDNA, doubly uniparental inheritance of mtDNA, Mytilus.

Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae)

Genome ◽  
2002 ◽  
Vol 45 (2) ◽  
pp. 348-355 ◽  
Author(s):  
Anne C Dalziel ◽  
Donald T Stewart
Keyword(s):  
Mitochondrial Dna ◽  
Molecular Evolution ◽  
Uniparental Inheritance ◽  
Rt Pcr ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
Specific Expression ◽  
Somatic Tissues ◽  
Selective Forces ◽  
Rates Of Molecular Evolution

Mytilus and other bivalves exhibit an unusual system of mitochondrial DNA (mtDNA) transmission termed doubly uniparental inheritance (DUI). Specifically, males transmit the mtDNA they have received from their fathers to their sons. Females transmit their mother's mtDNA to both sons and daughters. Males are normally heteroplasmic and females are normally homoplasmic, but not exclusively. This system is associated with an unusual pattern of molecular evolution. Male-transmitted mtDNA (M type) evolves faster than female-transmitted (F type) mtDNA. Relatively relaxed selection on the M type has been proposed as an explanation for this phenomenon. To further evaluate the selective forces acting upon the M-type genome, we used RT-PCR to determine where it is expressed. M-type mtDNA expression was detected in all gonad samples and in 50% of somatic tissues of males, and in a single female tissue. F-type mtDNA expression was detected in all female tissues, all male somatic tissues, and all but one male gonad sample. We argue that the expression of M-type mtDNA in male somatic and male gonad tissues has implications for the strength of selection acting upon it.Key words: gender-associated mitochondrial DNA, doubly uniparental inheritance of mtDNA, Mytilus edulis, molecular evolution.

scholarly journals Distribution and frequency of mitochondrial DNA polymorphisms in blue mussel (Mytilus edulis) populations of southwestern Nova Scotia (Canada)

2018 ◽  
Vol 96 (6) ◽  
pp. 608-613 ◽  
Author(s):  
Donald T. Stewart ◽  
Marion Sinclair-Waters ◽  
Alexandra Rice ◽  
Ryan A. Bunker ◽  
Brent M. Robicheau ◽  
...  
Keyword(s):  
Nova Scotia ◽  
Mytilus Edulis ◽  
Blue Mussel ◽  
Phylogenetic Analyses ◽  
Role Reversal ◽  
Dna Polymorphisms ◽  
Swimming Velocity ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Mt Genome

The Atlantic blue mussel (Mytilus edulis Linnaeus, 1758) exhibits doubly uniparental inheritance of mitochondrial (mt) DNA. Females are usually homoplasmic for a female-transmitted mt genome (the F type) and males are heteroplasmic for an F type and a male-transmitted mt genome (the M type). F types can undergo “role-reversal” events, resulting in new male-transmitted mtDNA genomes known as recently masculinized (RM) types that co-occur in populations with evolutionarily older standard-male (SM) types. Phylogenetic analyses have shown that RM types periodically replace SM types. It has also been shown that sperm with RM mtDNA have greater swimming velocity and more efficient components of the electron transport chain compared to sperm with SM mtDNA, thus leading to the hypothesis that RM sperm may have a selective advantage over SM sperm. The present study examines the distribution of RM and SM mitotypes in male M. edulis (n = 225) from 13 localities in southwestern Nova Scotia (Canada). The SM type was more common in all populations, with the proportion of RM types ranging from 0% to 24.1%. The highest proportion of RM types was observed in an aquaculture operation. Analyses of additional populations are required to evaluate the selective pressures affecting the geographic distribution of RM and SM mitotypes in M. edulis.

Segregation of sperm mitochondria in two- and four-cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA

Genome ◽  
2006 ◽  
Vol 49 (7) ◽  
pp. 799-807 ◽  
Author(s):  
Andrew T Cogswell ◽  
Ellen L.R Kenchington ◽  
Eleftherios Zouros
Keyword(s):  
Mytilus Edulis ◽  
Blue Mussel ◽  
Mitochondrial Genomes ◽  
Uniparental Inheritance ◽  
Cleavage Furrow ◽  
Doubly Uniparental Inheritance ◽  
Developmental Mechanism ◽  
Sex Ratio Bias ◽  
The Family ◽  
Early Developmental

Species of the family Mytilidae have 2 mitochondrial genomes, one that is transmitted through the egg and one that is transmitted through the sperm. In the Mytilus edulis species complex (M. edulis, M. galloprovincialis, and M. trossulus) there is also a strong mother-dependent sex-ratio bias in favor of one or the other sex among progeny from pair matings. In a previous study, we have shown that sperm mitochondria enter the egg and that their behavior during cell division is different depending on whether the egg originated from a female- or male-biased mother. Specifically, in eggs from females that produce mostly or exclusively daughters, sperm mitochondria disperse randomly among cells after egg division. In eggs from females that produce predominantly sons, sperm mitochondria tend to stay together in the same cell. Here, we extend these observations and show that in 2- and 4-cell embryos from male-biased mothers most sperm mitochondria are located near or at the cleavage furrow of the major cell, in contrast to embryos from female-biased mothers where there is no preferential association of sperm mitochondria with the cleavage furrow. This observation provides evidence for an early developmental mechanism through which sperm mitochondria are preferentially channeled into the primordial cells of male embryos, thus making the paternal mitochondrial genome the dominant mtDNA component of the male germ line.Key words: mussels, doubly uniparental inheritance of mtDNA, sperm mitochondria.

scholarly journals The Effects of Natural Hybridization on the Regulation of Doubly Uniparental mtDNA Inheritance in Blue Mussels (Mytilus spp.)

Genetics ◽  
1996 ◽  
Vol 144 (1) ◽  
pp. 241-248 ◽  
Author(s):  
Paul D Ramon ◽  
Carol L Secor ◽  
Thomas J Hilbish
Keyword(s):  
High Frequency ◽  
Blue Mussel ◽  
Natural Hybridization ◽  
F1 Hybrids ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
High Frequencies ◽  
Blue Mussels ◽  
Mtdna Inheritance

Abstract Blue mussels in the Mythilus edulis species complex have a doubly uniparental mode of mtDNA inheritance with separate maternal and paternal mtDNA lineages. Female mussels inherit their mtDNA solely from their mother, while males inherit mtDNA from both parents. In the male gonad the paternal mtDNA is preferentially replicated so that only paternal mtDNA is transmitted from fathers to sons. Hybridization is common among differentiated blue mussel taxa; whenever it involves M. trossulus, doubly uniparental mtDNA inheritance is disrupted. We have found high frequencies of males without and females with paternal mtDNA among hybrid mussels produced by interspecific matings between M. galloprovincialis and M. trossulus. In contrast, hybridization between M. galloprovincialis and M. edulis does not affect doubly uniparental inheritance, indicating a difference in the divergence of the mechanisms regulating mtDNA inheritance among the three blue mussel taxa. Our data indicate a high frequency of disrupted mtDNA transmission in F1 hybrids and suggest that two separate mechanisms, one regulating the transmission of paternal mtDNA to males and another inhibiting the establishment of paternal mtDNAin females, act to regulate doubly uniparental inheritance. We propose a model for the regulation of doubly uniparental inheritance that is consistent with these observations.

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

Genetics ◽  
1997 ◽  
Vol 145 (4) ◽  
pp. 1073-1082 ◽  
Author(s):  
Carlos Saavedra ◽  
María-Isabel Reyero ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Sex Ratio ◽  
Mytilus Galloprovincialis ◽  
Germ Line ◽  
Female Parent ◽  
Female Gonad ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
Male Progeny

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.

Sign in / Sign up

Export Citation Format

Share Document