Doubly Uniparental Inheritance (DUI) represents an outstanding exception to matrilinear inheritance of mitochondria, typical of most Metazoa. Some bivalve mollusks posses two different mitochondrial DNA genomes (M and F mtDNAs) and realize a double mechanism of transmission in which M and F mtDNAs are passed by father to sons and by mother to daughters, respectively. Moreover, DUI has been also related to sex determination, since the presence of M mitocondria in the primordial germ line has been hypothesized to be the masculinization factor of the gonad. Mitochondrial DNA provides an intriguing system for addressing aspects of molecular evolution and intermolecular recombination in both DUI and non-DUI species and studies on DUI bivalves may have a pivotal role in understanding the evolution of the metazoan mitochondrial genome. DUI has been found in a few mussel species (Mytilidae), as well as in several unionids (Unionidae). We started a wide analysis aimed to detect additional DUI systems and, actually, a venerid (Tapes philippinarum) and a mytilid (Musculista senhousia) species showed a mitochondrial heteroplasmy pattern, congruent with a DUI model of mtDNA inheritance. Since T. philippinarum is the first venerid bivalve known to have DUI, our data showed that DUI also occurs in phylogenetically distant families and suggest that it might be widely distributed among bivalves. Furthermore, the T. philippinarum DUI system has been useful to test for selection on mtDNA genes under DUI, as well as for mitochondrial DNA recombination. To address these issues, a large sequence has been analyzed (i.e. a 9.2 kb region of the mitochondrial genome of T. philippinarum, containing 29 genes). Comparisons suggest that the two sex-related mitochondrial genomes do not experience a neutral pattern of divergence, and that selection may act with varying strength on different genes. This pattern of evolution may be related to the long, separate history of M and F genomes within their tissue-specific “arenas”. Moreover, our data suggest that recombinants, although occurring in the soma, may seldom be transmitted to progeny in this species. The DUI system of M. senhousia revealed some unexpected traits, different from any previously known ones. Musculista heteroplasmy pattern is in line with standard DUI, but F haplotypes sequence variability is higher than that of M haplotypes. This is new for a DUI system, and it challenges most of the rationale proposed to account for sex-linked mtDNA evolution. Moreover, the system, tested for F mtDNA variability in somatic tissues, showed that F mitochondrial haplotypes experience a higher mutation rate in males than in females, thus suggesting that there might be some mechanism to keep a low mitochondrial DNA mutation rate in females. This fits well with evolutionary predictions: antioxidant gene complexes, evolved to protect mitochondria from oxidative damages, might be under relaxed selection in males. In phylogenetic trees M and F types clusters together, supporting that M. senhousia may have experienced ‘masculinization’ events in the lineage leading to the taxon. This also suggests that during the evolutionary history ‘masculinization’ might have been present in mytilids, other than Mytilus.
Doubly Uniparental Inheritance, an unusual pattern of mitochondrial DNA transmission in the bivalve mollusks Tapes philippinarum (Veneridae) and Musculista senhousia (Mytilidae).
PASSAMONTI, MARCO;SCALI, VALERIO
2006
Abstract
Doubly Uniparental Inheritance (DUI) represents an outstanding exception to matrilinear inheritance of mitochondria, typical of most Metazoa. Some bivalve mollusks posses two different mitochondrial DNA genomes (M and F mtDNAs) and realize a double mechanism of transmission in which M and F mtDNAs are passed by father to sons and by mother to daughters, respectively. Moreover, DUI has been also related to sex determination, since the presence of M mitocondria in the primordial germ line has been hypothesized to be the masculinization factor of the gonad. Mitochondrial DNA provides an intriguing system for addressing aspects of molecular evolution and intermolecular recombination in both DUI and non-DUI species and studies on DUI bivalves may have a pivotal role in understanding the evolution of the metazoan mitochondrial genome. DUI has been found in a few mussel species (Mytilidae), as well as in several unionids (Unionidae). We started a wide analysis aimed to detect additional DUI systems and, actually, a venerid (Tapes philippinarum) and a mytilid (Musculista senhousia) species showed a mitochondrial heteroplasmy pattern, congruent with a DUI model of mtDNA inheritance. Since T. philippinarum is the first venerid bivalve known to have DUI, our data showed that DUI also occurs in phylogenetically distant families and suggest that it might be widely distributed among bivalves. Furthermore, the T. philippinarum DUI system has been useful to test for selection on mtDNA genes under DUI, as well as for mitochondrial DNA recombination. To address these issues, a large sequence has been analyzed (i.e. a 9.2 kb region of the mitochondrial genome of T. philippinarum, containing 29 genes). Comparisons suggest that the two sex-related mitochondrial genomes do not experience a neutral pattern of divergence, and that selection may act with varying strength on different genes. This pattern of evolution may be related to the long, separate history of M and F genomes within their tissue-specific “arenas”. Moreover, our data suggest that recombinants, although occurring in the soma, may seldom be transmitted to progeny in this species. The DUI system of M. senhousia revealed some unexpected traits, different from any previously known ones. Musculista heteroplasmy pattern is in line with standard DUI, but F haplotypes sequence variability is higher than that of M haplotypes. This is new for a DUI system, and it challenges most of the rationale proposed to account for sex-linked mtDNA evolution. Moreover, the system, tested for F mtDNA variability in somatic tissues, showed that F mitochondrial haplotypes experience a higher mutation rate in males than in females, thus suggesting that there might be some mechanism to keep a low mitochondrial DNA mutation rate in females. This fits well with evolutionary predictions: antioxidant gene complexes, evolved to protect mitochondria from oxidative damages, might be under relaxed selection in males. In phylogenetic trees M and F types clusters together, supporting that M. senhousia may have experienced ‘masculinization’ events in the lineage leading to the taxon. This also suggests that during the evolutionary history ‘masculinization’ might have been present in mytilids, other than Mytilus.I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.
