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

Abstract

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:

The detection of sex-linked heteroplasmy inPseudocardium sachalinense(Bivalvia: Mactridae) and its implications for the distribution of doubly uniparental inheritance of mitochondrial DNA

“…), while they are more easily found in Mytilus (Brannock et al. ). Two highly different copies of cox2 gene have been found in unionids (Chakrabarti et al.…”

“…The distribution of DUI in heterodonts Some interesting differences have been found between DUIs of distantly related species, and the discussion about a general model for DUI is ongoing Zouros 2013; and reference therein). The M mitotype is dominant also in the soma of V. philippinarum male individuals , while somatic tissues of male Mytilus specimens contain mainly the F mitotype (Garrido-Ramos et al 1998;Dalziel and Stewart 2002); conversely, heteroplasmic females of V. philippinarum are extremely rare , while they are more easily found in Mytilus (Brannock et al 2013). Two highly different copies of cox2 gene have been found in unionids (Chakrabarti et al 2006(Chakrabarti et al , 2007Doucet-Beaupr e et al 2010), while the same gene is duplicated in M. senhousia males ) and in V. philippinarum females (GenBank accession number NC_003354).…”

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

“…In Mytilus, males without M mtDNA have been obtained artificially by inducing triploidy and/or through interspecific crosses (Kenchington et al, 2009). Natural hybridization among different Mytilus species also appears to induce the retention of the M mtDNA in females (Brannock et al, 2013). However, these two 'unordinary' situations, triploidy and hybridization, can interfere with sex determination and/ or fate of paternal mitochondria in the two sexes.…”

“…Examples for such exceptions are mostly known in the Mytilus species complex (Brannock et al, 2013;Zouros, 2013). In Mytilus, males without M mtDNA have been obtained artificially by inducing triploidy and/or through interspecific crosses (Kenchington et al, 2009).…”

“…Males without M mtDNA, to our knowledge, have never been observed in natural conditions, but have only been produced artificially in Mytilus by chemically induced triploidization (Kenchington et al, 2009). Conversely, heteroplasmy is sometimes observed in female tissues, probably due to the failure of sperm mitochondria degradation Zouros, 2013), hybridization events (reviewed in Brannock et al, 2013) or being even typical of some populations where DUI disruption is frequent (Brannock et al, 2013). Cases of heteroplasmic females are mostly known for Mytilus, but in R. philippinarum they seem to be uncommon so far .…”