The Complete Maternally and Paternally Inherited Mitochondrial Genomes of the Endangered Freshwater Mussel Solenaia carinatus (Bivalvia: Unionidae) and Implications for Unionidae Taxonomy

Abstract

Doubly uniparental inheritance (DUI) is an exception to the typical maternal inheritance of mitochondrial (mt) DNA in Metazoa, and found only in some bivalves. In species with DUI, there are two highly divergent gender-associated mt genomes: maternal (F) and paternal (M), which transmit independently and show different tissue localization. Solenaia carinatus is an endangered freshwater mussel species exclusive to Poyang Lake basin, China. Anthropogenic events in the watershed greatly threaten the survival of this species. Nevertheless, the taxonomy of S. carinatus based on shell morphology is confusing, and the subfamilial placement of the genus Solenaia remains unclear. In order to clarify the taxonomic status and discuss the phylogenetic implications of family Unionidae, the entire F and M mt genomes of S. carinatus were sequenced and compared with the mt genomes of diverse freshwater mussel species. The complete F and M mt genomes of S. carinatus are 16716 bp and 17102 bp in size, respectively. The F and M mt genomes of S. carinatus diverge by about 40% in nucleotide sequence and 48% in amino acid sequence. Compared to F counterparts, the M genome shows a more compact structure. Different gene arrangements are found in these two gender-associated mt genomes. Among these, the F genome cox2-rrnS gene order is considered to be a genome-level synapomorphy for female lineage of the subfamily Gonideinae. From maternal and paternal mtDNA perspectives, the phylogenetic analyses of Unionoida indicate that S. carinatus belongs to Gonideinae. The F and M clades in freshwater mussels are reciprocal monophyly. The phylogenetic trees advocate the classification of sampled Unionidae species into four subfamilies: Gonideinae, Ambleminae, Anodontinae, and Unioninae, which is supported by the morphological characteristics of glochidia.

Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes

“…Subsequent studies demoted Anodontinae to a tribe within Unioninae due to the shared hooked type and subtriangular external shape of the glochidia Carter et al, 2011;Graf, 2002;Graf and Cummings, 2007). However, the rank change of Anodontinae into Anodontini has been recently disputed based on morphology discrepancies in glochidia morphology (Huang et al, 2013). Anodontinae and Unioninae are here recovered as sister clades and due to the ancient divergence of the two clades are herein considered as subfamilies, in accordance with traditional classifications.…”

“…Many species have been assigned to Sinanodonta, primarily by the Russian school of nomenclature (Graf, 2007;Haas, 1969a), but validity of these placements should be tested using molecular tools. Sinanodonta lucida was first described as Anodonta lucida and then assigned to Sinanodonta (Ð ng et al, 1980) but both generic attributions are still being used (e.g., Huang et al, 2013;Pfeiffer and Graf, 2013). Additionally, recent studies based on morphological data consider S. lucida as a synonym of S. woodiana (Graf and Cummings, 2016;He and Zhuang, 2013).…”

The female and male mitochondrial genomes of Unio delphinus and the phylogeny of freshwater mussels (Bivalvia: Unionida)

“…Of the few published phylogenies using the whole mtDNA within the Unionida, only two of the six families are represented, Unionidae and Margaritiferidae (e.g. Huang et al 2013;Froufe et al 2016b). Therefore, most of the published Unionida phylogenies use a combination of two out of three mtDNA genes: Cytochrome c oxidase subunit 1 (COX1), 16S ribosomal RNA (16S-rRNA) and NADH ubiquinone oxidoreductase core subunit 1 (ND1) (e.g.…”

“…The most likely control-region, among all predicted in this study (data supplied on request) is located after ND5 (plus tRNA-H in the M-type) and before the cluster of tRNA genes (tRNA-Q, tRNA-C, tRNA-I, tRNA-V, and tRNA-L) as: (i) it is among the largest non-coding regions, (ii) it is shared by both gender-specific U. delphinus mitogenomes, (iii) it contains sequences with the ability to form stable hairpin structures and direct repeats (Ftype), (iv) which are located in a region where the AT proportion is among the highest (AT% around 68%). Additionally, this region was identified as the control-region in other unionid mtDNAs (Breton et al 2009;Huang et al 2013).…”

The male and female complete mitochondrial genome sequences of the Endangered freshwater mussel Potomida littoralis (Cuvier, 1798) (Bivalvia: Unionidae)

“…Unionid bivalves, such as several other bivalve families, possess an interesting mitochondrial inheritance, called doubly uniparental inheritance (DUI), in which the male gonad tissue contains (M) mitochondria inherited from the fathers, the male somatic tissue contains (F) mitochondria inherited from the mothers, and females inherit their (F) mitochondria through ordinary single uniparental inheritance (Hoeh et al, 1996). The M and F mitochondrial lineages are highly divergent within each animal and have distinct gene order arrangements (Huang et al, 2013).…”