Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

Abstract

BackgroundDoubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata).ResultsCompared to their unionoid F counterparts, the M genomes contain some unique features including a novel localization of the trnH gene, an inversion of the atp8-trnD genes and a unique 3'coding extension of the cytochrome c oxidase subunit II gene. One or more of these unique M genome features could be causally associated with paternal transmission. Unionoid bivalves are characterized by extreme intraspecific sequence divergences between gender-associated mtDNAs with an average of 50% for V. ellipsiformis, 50% for I. japanensis, 51% for P. grandis and 52% for Q. quadrula (uncorrected amino acid p-distances). Phylogenetic analyses of 12 protein-coding genes from 29 bivalve and five outgroup mt genomes robustly indicate bivalve monophyly and the following branching order within the autolamellibranch bivalves: ((Pteriomorphia, Veneroida) Unionoida).ConclusionThe basal nature of the Unionoida within the autolamellibranch bivalves and the previously hypothesized single origin of DUI suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the mitochondrial genome characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition. Descriptions and comparisons presented in this paper are fundamental to a more complete understanding regarding the origins and consequences of DUI.

Mitonuclear interactions: evolutionary consequences over multiple biological scales

“…In this system, heteroplasmy is the norm: a maternal haplotype is transmitted to all offspring, and a paternal haplotype is exclusively transmitted to male offspring. In males, the maternal haplotype is predominant in all somatic tissues, but is outweighed by the paternal haplotype in the gonads, a system that may have evolved in response to asymmetries in functional requirements of reproductive tissues [101,102]. Interestingly, sequence divergence between the two haplotypes can exceed 40%, yet mitochondrial function is maintained, suggesting that mtDNA-encoded components may be matched alongside sex-specific isoforms or duplicates of nuclear-encoded mitochondrial components [101,102].…”

Genetic aspects of mitochondrial genome evolution

“…The doubly uniparental inheritance (DUI) found in all dioecious freshwater mussel species lead to highly differentiated mitogenomes between the two sexes Doucet-Beaupré et al, 2010). The female form has an extra protein coding gene called the F-ORF, while the male form shows some rearrangements of the gene order and features a unique 3'coding extension of the cox2 subunit.…”

Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of unionid mitochondrial DNA

“…Sex-dependent heteroplasmy with two different forms of mtDNA transmitted to the next generations both maternally and paternally was first described in marine bivalves of the genus Mytilus in 1990 and called DUI, doubly uniparental inheritance (FISHER & SKIBINSKI 1990). Besides three species of Mytilus, DUI was detected in a few species representing six bivalve families, and is the most frequent in Unionidae, which have recently been intensely studied in this respect (HOEH et al 1996a, b, LIU et al 1996, PASSAMONTI & SCALI 2001, CUROLE & KOCHER 2002, KREBS 2004, MOCK et al 2004, WALKER et al 2006a, CHAKRABARTI et al 2006, THEOLOGIDIS et al 2008, SOROKA 2008a, b, BRETON et al 2009, DOUCET-BEAUPRÉ et al 2010). …”