Disruption of doubly uniparental inheritance of mitochondrial DNA in hybrid mussels (Mytilus edulis × M. galloprovincialis)

Wood, Ann R.; Turner, Gordon; Skibinski, D. O. F.; Beaumont, Andy R.

doi:10.1038/sj.hdy.6800345

Cited by 25 publications

(23 citation statements)

References 31 publications

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“…Hybridization events are known to disrupt the transmission of DUI and result in the appearance of both males lacking an M molecule and in M-positive females (Rawson et al 1996;Wood et al 2003). Successful backcrosses involving F 1 hybrids have the potential to cause the introgression of mtDNA lineages among mussel species that has been previously documented on both historical (Quesada et al 1998a;Rawson and Hilbish 1998) and contemporary time scales (Smietanka et al 2004;see, however, Saavedra et al 1996).…”

Section: Discussionmentioning

confidence: 91%

Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel,Mytilus californianus

Ort

Pogson

2007

Genetics

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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.

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Section: Discussionmentioning

confidence: 91%

Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel,Mytilus californianus

Ort

Pogson

2007

Genetics

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“…Similarly, in some hybrid zones M. edulis FmtDNA asymmetrically introgresses onto M. galloprovincialis and M. trossulus nuclear backgrounds (Saavedra et al 1996;Quesada et al 1998b;Rawson and Hilbish 1998;Comesañ a et al 1999;Quesada et al 1999), but asymmetric MmtDNA introgression has not been observed. Furthermore, in crosses between European M. edulis and M. galloprovincialis, M-mtDNA from M. edulis are disproportionately eliminated (Wood et al 2003).…”

Section: Selective Explanations and Genetic Barriers To Transatlanticmentioning

confidence: 99%

Differential Patterns of Male and Female Mtdna Exchange Across the Atlantic Ocean in the Blue Mussel, Mytilus Edulis

Riginos

Hickerson

Henzler

et al. 2004

Evol

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“…The presence of the M haplotype in hybrid progeny appeared to be largely dependent on the species of the female parent (Wood et al 2003). In heterospecific crosses where M. galloprovincialis was the female parent, the M haplotype was present in 4 to 14% of the progeny, while in crosses where M. edulis was the female parent, M haplotype presence ranged from 82 to 93% (Wood et al 2003). These findings illustrate disruption in DUI in M. galloprovincialis-M. edulis hybrids at far greater frequencies than those reported in Rawson et al (1996b).…”

Section: Introductionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 93%

“…Wood et al (2003) found a large difference in the presence of the M haplotype when comparing 72 h larvae from Mytilus galloprovincialis and M. edulis homospecific (M haplotype presence: 47 to 68%) and heterospecific (M haplotype presence: 4 to 93%) crosses. The presence of the M haplotype in hybrid progeny appeared to be largely dependent on the species of the female parent (Wood et al 2003). In heterospecific crosses where M. galloprovincialis was the female parent, the M haplotype was present in 4 to 14% of the progeny, while in crosses where M. edulis was the female parent, M haplotype presence ranged from 82 to 93% (Wood et al 2003).…”

Section: Introductionmentioning

confidence: 93%

See 1 more Smart Citation

Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation

Brannock¹,

Roberts²,

Hilbish³

2013

Mar. Ecol. Prog. Ser.

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Species within the marine mussel Mytilus edulis complex (M. edulis, M. galloprovincialis, and M. trossulus) have an unusual form of mitochondrial DNA (mtDNA) inheritance commonly referred to as doubly uniparental inheritance (DUI). With DUI, all progeny inherit mtDNA maternally (F), while male progeny also inherit mtDNA paternally (M) through their father's sperm. Therefore, females are normally homoplasmic for the F mtDNA, and males are heteroplasmic for the F and M mtDNA. In this study, we show that the regulation of DUI in populations of blue mussels in northern Japan is severely disrupted; consequently, the majority of individuals (89%) are heteroplasmic for M and F mtDNA. Disruption of DUI is primarily due to the failure of female embryos to exclude the father's M mtDNA from their somatic and germinal tissues. High proportions of heteroplasmic females have only been reported in Japanese mussel populations thus far. We show that this disruption occurs in both parental species (M. trossulus and M. galloprovincialis) as well as hybrids and is independent of geographic location around Hokkaido, Japan. This finding differs from many previous studies, which have shown that disruption in DUI is confined to hybrid zones. In addition, some individuals were heteroplasmic for M or F mtDNA, indicating that DUI disruption is multigenerational. Triplasmic individuals were 3 times more often female and were mostly confined within the hybrid zones; however, a few individuals were found within M. galloprovincialis parental populations.KEY WORDS: Mytilus galloprovincialis · Mytilus trossulus · Doubly uniparental inheritance · Disruption · Heteroplasmy Resale or republication not permitted without written consent of the publisher Editorial responsibility:

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Disruption of doubly uniparental inheritance of mitochondrial DNA in hybrid mussels (Mytilus edulis × M. galloprovincialis)

Cited by 25 publications

References 31 publications

Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel,Mytilus californianus

Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel,Mytilus californianus

Differential Patterns of Male and Female Mtdna Exchange Across the Atlantic Ocean in the Blue Mussel, Mytilus Edulis

Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation

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