Abstract
Doubly uniparental inheritance (DUI) describes a mode of mtDNA transmission widespread in gonochoric freshwater mussels (Bivalvia: Palaeoheterodonta: Unionida). In this system, both female- and 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.
Highlights
Doubly uniparental inheritance (DUI) and the ORFans carried by the two mtDNAs have been hypothesized to be part of a sex determination system involving mitochondria, in part because bivalves lack heteromorphic sex chromosomes in their nuclear genomes and because freshwater mussels with DUI that switched from the ancestral gonochoric reproductive mode to a derived hermaphroditism lost the M mt genome in the process[6]
Complete mtDNA sequences have been obtained for N. margaritacea (16,739 bp; putatively the F, if this species has DUI), H. menziesii (F: 16,031 bp; M: 18,140 bp), C. monodonta (F: 16,099 bp; M: 17,575 bp), and M. dubia
The cox[2] genes of N. margaritacea, M. dubia and A. trapesialis do not have a 3′ elongated region. tRNA-Glu is duplicated in C. monodonta F mtDNA
Summary
DUI and the ORFans carried by the two mtDNAs have been hypothesized to be part of a sex determination system involving mitochondria, in part because bivalves lack heteromorphic sex chromosomes in their nuclear genomes and because freshwater mussels with DUI that switched from the ancestral gonochoric reproductive mode to a derived hermaphroditism lost the M mt genome in the process[6]. DUI has been detected in >100 gonochoric bivalve species, with a somewhat scattered phylogenetic distribution[13] The complexity of this system led to the hypothesis that it evolved once in a basal, ancestral lineage of bivalves, followed by subsequent losses in the common ancestor to some modern taxa[1, 14, 15]. In other orders of bivalves, the F and M mtDNAs of a single species are frequently distinct from one another yet they cluster together in a ‘taxon-joining’ pattern[15]. The authors tested for the presence of the M type mtDNA in the trigoniid Neotrigonia margaritacea, but the negative results left uncertain the presence of DUI in the order Trigoniida[14] An update on this question was provided by ref. The sequences obtained, are not publicly available at the time of writing this article, and the low divergence found calls for more in-depth studies to confirm the presence of DUI in N. margaritacea
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