Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria

International audiencein animals, strictly maternal inheritance (SMi) of mitochondria is the rule, but one exception (doubly uniparental inheritance or DUI), marked by the transmission of sex-specific mitogenomes, has been reported in bivalves. Associated with DUI is a frequent modification of the mitochondrial cox2 gene, as well as additional sex-specific mitochondrial genes not involved in oxidative phosphorylation. With the exception of freshwater mussels (for 3 families of the order Unionida), these DUI-associated features have only been shown in few species [within Mytilidae (order Mytilida) and Veneridae (order Venerida)] because of the few complete sex-specific mitogenomes published for these orders. Here, we present the complete sex-specific mtDNAs of two recently-discovered DUI species in two families of the order Venerida, Scrobicularia plana (Semelidae) and Limecola balthica (tellinidae). these species display the largest differences in genome size between sex-specific mitotypes in DUI species (>10 kb), as well as the highest mtDNA divergences (sometimes reaching >50%). An important in-frame insertion (>3.5 kb) in the male cox2 gene is partly responsible for the differences in genome size. The S. plana cox2 gene is the largest reported so far in the Kingdom Animalia. The mitogenomes may be carrying sex-specific genes, indicating that general mitochondrial features are shared among DUI species. Animal mitochondrial DNA (mtDNA) is typically depicted as a strictly maternally inherited (SMI) circular DNA molecule that is relatively small (~16 kb) and genomically streamlined with almost invariant gene content (13 protein-coding genes and 24 structural RNAs) 1,2. However, important deviations do occur in the mtD-NAs of bivalve molluscs, which not only display dramatic variation in size (67 kb) 3,4 and gene arrangement 5 , but also the presence of additional protein-coding genes not associated with oxidative phospho-rylation 6-9. An even more extreme departure from the norm in bivalve mitochondrial genomes is their mode of doubly uniparental inheritance (DUI)-both egg and sperm mitochondria are transmitted from generation to generation in several bivalve species, but only male offspring retain paternally-transmitted mitochondria (with male or M mtDNA) in their gametes 10-12. Adult females of DUI-exhibiting species usually possess only the female-transmitted mtDNA (F mtDNA) in their soma and gametes whereas males possess F mtDNA in their soma and M mtDNA in their gametes 10-13. The DNA divergence between F and M mtDNAs usually vary from about 8% to 40% depending on the species 12,14. Genetic analyses suggested that both F and M mtDNAs in DUI bivalves evolve at a faster rate than typical metazoan mtDNA, and that M mtDNA evolves faster than F mtDNA 15-17. One factor explaining this observation may be that the M genome is subject to weaker selective pressures than the F genome due to an unequal "division of labor" in the DUI system 16. Typical animal mtDNA functions in gonads and somatic tissues of both sexes whereas under DUI, F mtDNA functions in female gonads and the soma of both sexes, while M mtDNAs functions primarily in spermatozoa of male gonads and only partially in the male soma 13,16,18. As opposed to SMI that promotes homoplasmy, a state in which all mtDNA copies are typically genetically identical in each cell, thus preventing potentially harmful genomic conflicts, DUI is a naturally heter-oplasmic system in which two highly divergent mitochondrial lineages coexist in the same nuclear background, enabling the analysis of the consequences of tissue heteroplamy 13