Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida)

Abstract

Doubly uniparental inheritance (DUI) describes a mode of mtDNA transmission widespread in gonochoric freshwater mussels (Bivalvia: Palaeoheterodonta: Unionida). In this system, both femaleand male-transmitted mtDNAs, named F and M respectively, coexist in the same species. In unionids, DUI is strictly correlated to gonochorism and to the presence of the atypical open reading frames (ORFans) F-orf and M-orf, respectively inside F and M mtDNAs, which are hypothesized to participate in sex determination. However, DUI is not found in all three Unionida superfamilies (confirmed in Hyrioidea and Unionoidea but not in Etherioidea), raising the question of its origin in these bivalves. To reconstruct the co-evolution of DUI and of ORFans, we sequenced the mtDNAs of four unionids (two gonochoric with DUI, one gonochoric and one hermaphroditic without DUI) and of the related gonochoric species Neotrigonia margaritacea (Palaeoheterodonta: Trigoniida). Our analyses suggest that rearranged mtDNAs appeared early during unionid radiation, and that a duplicated and diverged atp8 gene evolved into the M-orf associated with the paternal transmission route in Hyrioidea and Unionoidea, but not in Etherioidea. We propose that novel mtDNA-encoded genes can deeply influence bivalve sex determining systems and the evolution of the mitogenomes in which they occur.

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

“…As mentioned above, modifications to the cox2 gene is a particular feature often found in DUI species. In unionid mussels, the longest cox2 gene is found in the M mtDNA of Hyridella menziesii (1,380 bp) 22 and is the result of a 3′ extension, as in other DUI unionids 21 . Previous studies indicated an extra-mitochondrial localization of MCOX2 as well as a possible involvement of the protein in reproduction in freshwater mussels 23,24 , further supporting the link between gender and mtDNA transmission patterns.…”

“…Only ORFs encoding proteins with at least one predicted transmembrane domain were retained, because all sex-specific mtORFans characterized to date in DUI species (i.e. those encoding F-ORF in females and M-ORF in males), except for one case, possess at least one transmembrane domain or helix (TMH) 7,8,22,40 . In both S. plana and L. balthica F mtDNAs, only two unassigned regions were susceptible to contain supernumerary ORFs of >150 bp, i.e.…”

Conservation of freshwater bivalves at the global scale: diversity, threats and research needs

“…These tools are particularly important owing to the fact that many species present hidden cryptic diversity (Froufe et al, 2016b;Pfeiffer et al, 2016). Additionally, nextgeneration sequencing is now allowing for quicker and less expensive robust phylogenies using methods like whole-transcriptome and whole-mitogenome analyses with a wide range of markers (Guerra et al, 2017;Lopes-Lima et al, 2017c). Furthermore, using reduced genome representations or snip analyses, it is now possible to get more information on the phylogeographic patterns of species and on the definition of conservation units (Catchen et al, 2017;Desalle & Amato, 2017).…”

The male and female complete mitochondrial genomes of the threatened freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) (Bivalvia: Margaritiferidae)

“…The M-type and F-type mitochondrial lineages show high levels of divergence within species of Unionida freshwater mussels and even distinct gene order arrangements (Fonseca et al 2016;Froufe et al 2016;Guerra et al 2017). The Margaritiferidae also exhibit a unique M-type and F-type gene order (Lopes-Lima, Fonseca, et al 2017).…”