Complete Paternal And Maternal Mitochondrial Genomes Of The Freshwater Mussel Genus Solenaia (Unionidae: Gonideinae) In China And Mitochondrial Phylogenomics Of Unionoida

Freshwater mussels (Bivalvia: Unionoida) are one of the most important faunasin freshwater ecosystems. They are distributed broadly on all continents exceptAntarctica. In China, the middle and lower reaches of the Yangtze River have themost diverse freshwater mussel fauna. Identification and classification of unionoidbivalves are usually based on adult shell morphology, resulting in taxonomicconfusions and controversies about validities of certain unionids.Doubly Uniparental Inheritance (DUI) is an exception to the typical maternalinheritance of mitochondrial DNA in Metazoa, and found only in some bivalves. Inspecies with DUI, there are two highly divergent gender-associated mt genomes:maternal (F) and paternal (M), which transmit independently and show differenttissue localization. Analysis based on complete mitochondrial genome sequence datacould enhance resolution and statistical confidence of inferred phylogenetic trees, andcould be applied to different taxonomic levels.Solenaia is found throughout southeastern Asia. Solenaia species are directlytargeted by local people as food. Meanwhile, anthropogenic events in the watershedgreatly threaten the survival of these species. For conservation purposes, we need toaccurately identify unionoid bivalves and estimate genetic diversity in wildpopulations. Nevertheless, the taxonomy of Solenaia based on shell morphology isconfusing, and the subfamilial placement of this genus remains unclear. In addition,little is known about their genetic information.In order to clarify the taxonomic status of Solenaia and discuss the phylogeneticrelationships within order Unionoida, the entire maternal and paternal mitogenomesof three Chinese Solenaia species (i.e. S. carinatus, S. oleivorus, and S. rivularis)were sequenced and compared with mitogenomes of diverse freshwater musselspecies. Additionally, ML and BI trees were inferred together with the publishedmitogenomes data of unionoids, expecting the classification of unionoids couldreflect natural relationships with robust molecular evidence. Main results are asfollows: 1. The maternal and paternal mitochondrial genomes of S. carinatus, S. oleivorus,and S. rivularis vary in size from16392bp to17550bp. Length differences mainlyresult from the non-coding region. In addition, M mitogenomes possess a uniquecoding3’ extension of cox2that typically yields an~80%increase in gene lengthover that in the corresponding F mitogenomes.2. Gene arrangements of maternal and paternal mitogenomes in Solenaia arenotably different from each other. No gene rearrangement was observed within thesame type mitochondrial genome. Compared with other unionoid mitogenomes inGenbank, paternal mitogenomes show a congruent gene structure. In maternalmitogenomes, however, gene rearrangements are found. The transposition of trnEcontributes to the difference of F mtDNA in Margaritiferidae and typical (i.e.unionids from subfamily Unioniae, Anodontinae and Ambleminae) F mtDNA inUnionidae. The rearrangement between cox2and rrnS is responsible for theremarkable structural difference between Gonideinae F mtDNA and typicalUnionidae F mtDNA. This F genome cox2-rrnS gene rearrangement is asynapomorphy for the female lineage of the subfamily Gonideinae, and the relativeposition between nad2and nad3could be used as a characteristic to accuratelyidentify certain morphologically similar species or genus.3. In three Solenaia species, the nucleotide divergence and amino aciddivergence between the F and M mitogenomes are all over40%(pDnt) and47%(pDaa)respectively, which considerably surpass intra-or inter-species values. Nucleotideand amino acid sequence divergences between all pair of F mitogenomes are lowerthan between M pairs. When it comes to singular protein coding gene, the mostconserved gene is cox1, while the least conserved one is atp8. Overall, genesencoding the cytochrome carriers (COX, CYTB) are more conservative than thoseencoding proteins of the NADH dehydrogenase subunits.4. From maternal and paternal mtDNA perspectives, BI and ML phylogeneticanalyses of Unionoida indicate that Solenaia belongs to Gonideinae, and shares closerrelationships with the Asian unionoid Ptychorhynchus pfisteri, Lamprotula leai,Hyriopsis cumingii, H.schlegelii, and Pronodularia japanensis. The F and M cladesin freshwater mussels are reciprocal monophyly. M genomes evolve faster than F genomes. The phylogenetic trees advocate the classification of sampled Unionidaespecies into four subfamilies: Gonideinae, Ambleminae, Anodontinae, andUnioninae.5. To compensate for the lack of taxon sampling density based on completemitochondrial genome,16S and ND1sequence data were also used for thephylogenetic analyses. We found that the western North American Gonidea angulate,which is morphologically and anatomically more similar to freshwater mussels ofSoutheast Asia than that of North America, have the affinity with Asian Solenaia andPtychorhynchus. They share a more recent common ancestor.