Dataset Information

Disruption of doubly uniparental inheritance of mitochondrial DNA associated with hybridization area of European Mytilus edulis and Mytilus trossulus in Norway.

ABSTRACT: Doubly uniparental inheritance of mitochondria (DUI) is best known in the blue mussel Mytilus. Under this model, two types of mitochondrial DNA exist: female type (F), transmitted from females to offspring of both genders, and male type (M), transmitted exclusively from males to sons. The mitogenomes are usually highly divergent, but an occasional replacement of a typical M genome by a particular F genome has been postulated to explain reduction of this divergence. Disruption of the DUI model has been reported in hybridization areas. Here, we present a new case of DUI disruption in a hybrid M. trossulus/M. edulis population from the North Sea (Norway). No M haplotypes derived from M. trossulus were identified in this population. Typical M haplotypes derived from M. edulis (ME) were rare. Two F-type haplogroups were found: one derived from M. edulis (FE) and the second derived from M. trossulus (FT). Many haplotypes from the FT group were recombinants, with the male CR sequence coming from the M. trossulus genome (FT1 haplogroup) in contrast to M. edulis CR as in the Baltic. FT1 haplotypes were abundant in the studied population, including homoplasmic females. However, males significantly more often carried these haplotypes; therefore, male heteroplasmy involved the original FE and recombinant FT, indicating that the FT genome undergoes masculinization. Structural similarity of FT1 CR with previously reported, masculinized Baltic haplotypes, which were derived from FE/ME recombination, provides further evidence that CR M-F recombination is a prerequisite for masculinization, also in the context of native M. trossulus mtDNA.

SUBMITTER: Smietanka B

PROVIDER: S-EPMC5630648 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Disruption of doubly uniparental inheritance of mitochondrial DNA associated with hybridization area of European Mytilus edulis and Mytilus trossulus in Norway.

Śmietanka Beata B Burzyński Artur A

Marine biology 20171006 11

Doubly uniparental inheritance of mitochondria (DUI) is best known in the blue mussel Mytilus. Under this model, two types of mitochondrial DNA exist: female type (F), transmitted from females to offspring of both genders, and male type (M), transmitted exclusively from males to sons. The mitogenomes are usually highly divergent, but an occasional replacement of a typical M genome by a particular F genome has been postulated to explain reduction of this divergence. Disruption of the DUI m ...[more]

PMID: 29056761

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Project description:BackgroundDoubly Uniparental Inheritance (DUI) of mitochondria occurs when both mothers and fathers are capable of transmitting mitochondria to their offspring, in contrast to the typical Strictly Maternal Inheritance (SMI). DUI was found in some bivalve molluscs, in which two mitochondrial genomes are inherited, one through eggs, the other through sperm. During male embryo development, spermatozoon mitochondria aggregate in proximity of the first cleavage furrow and end up in the primordial germ cells, while they are dispersed in female embryos.Methodology/principal findingsWe used MitoTracker, microtubule staining and transmission electron microscopy to examine the mechanisms of this unusual distribution of sperm mitochondria in the DUI species Ruditapes philippinarum. Our results suggest that in male embryos the midbody deriving from the mitotic spindle of the first division concurs in positioning the aggregate of sperm mitochondria. Furthermore, an immunocytochemical analysis showed that the germ line determinant Vasa segregates close to the first cleavage furrow.Conclusions/significanceIn DUI male embryos, spermatozoon mitochondria aggregate in a stable area on the animal-vegetal axis: in organisms with spiral segmentation this zone is not involved in cleavage, so the aggregation is maintained. Moreover, sperm mitochondria reach the same embryonic area in which also germ plasm is transferred. In 2-blastomere embryos, the segregation of sperm mitochondria in the same region with Vasa suggests their contribution in male germ line formation. In DUI male embryos, M-type mitochondria must be recognized by egg factors to be actively transferred in the germ line, where they become dominant replacing the Balbiani body mitochondria. The typical features of germ line assembly point to a common biological mechanism shared by DUI and SMI organisms. Although the molecular dynamics of the segregation of sperm mitochondria in DUI species are unknown, they could be a variation of the mechanism regulating the mitochondrial bottleneck in all metazoans.

Project description:Two blue mussel lineages of Pliocene origin, Mytilus edulis (ME) and M. trossulus (MT), co-occur and hybridize in several regions on the shores of the North Atlantic. The two species were distinguished from each other by molecular methods in the 1980s, and a large amount of comparative data on them has been accumulated since that time. However, while ME and MT are now routinely distinguished by various genetic markers, they tend to be overlooked in ecological studies since morphological characters for taxonomic identification have been lacking, and no consistent habitat differences between lineages have been reported. Surveying a recently discovered area of ME and MT co-occurrence in the White Sea and employing a set of allozyme markers for identification, we address the issue whether ME and MT are true biological species with distinct ecological characteristics or just virtual genetic entities with no matching morphological and ecological identities. We find that: (1) in the White Sea, the occurrence of MT is largely concentrated in harbors, in line with observations from other subarctic regions of Europe; (2) mixed populations of ME and MT are always dominated by purebred individuals, animals classified as hybrids constituting only ca. 18%; (3) in terms of shell morphology, 80% of MT bear a distinct uninterrupted dark prismatic strip under the ligament while 97% of ME lack this character; (4) at sites of sympatry MT is more common on algal substrates while ME mostly lives directly on the bottom. This segregation by the substrate may contribute to maintaining reproductive isolation and decreasing competition between taxa. We conclude that while ME and MT are not fully reproductively isolated, they do represent clearly distinguishable biological, ecological and morphological entities in the White Sea. It remains to be documented whether the observed morphological and ecological differences are of a local character, or whether they have simply been overlooked in other contact zones.

Dataset Information

Disruption of doubly uniparental inheritance of mitochondrial DNA associated with hybridization area of European Mytilus edulis and Mytilus trossulus in Norway.

Publications

Disruption of doubly uniparental inheritance of mitochondrial DNA associated with hybridization area of European <i>Mytilus edulis</i> and <i>Mytilus trossulus</i> in Norway.

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