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The authors wish to thank the Editor and the three anonymous reviewers for helpful remarks and suggestions that improved the quality of the manuscript. This research was developed under ConBiomics: the missing approach for the Conservation of freshwater Bivalves Project No NORTE-01-0145-FEDER-030286, cofinanced by COMPETE 2020, Portugal 2020 and the European Union through the ERDF, and by FCT through national funds (UID/Multi/04423/2019). FCT also supported MLL (SFRH/BD/115728/2016). The Russian Ministry of Education and Science (project no. 6.2343.2017/4.6), the Federal Agency for Scientific Organizations (project no. 0409-2015-0143), the Presidium of the Russian Academy of Sciences (scientific program no. 52), and the Russian Foundation for Basic Research, RFBR (project no. 17-45-290066) supported INB. Permits for fieldwork and sampling in Malaysia were issued by the Malaysian Ministry of Higher Education (FRGS/1/2015/WAB13/UNIM//1).

The concept of long-lived (ancient) lakes has had a great influence on the development of evolutionary biogeography. According to this insight, a number of lakes on Earth have existed for several million years (e.g., Baikal and Tanganyika) and represent unique evolutionary hotspots with multiple intra-basin radiations. In contrast, rivers are usually considered to be variable systems, and the possibility of their long-term existence during geological epochs has never been tested. In this study, we reconstruct the history of freshwater basin interactions across continents based on the multi-locus fossil-calibrated phylogeny of freshwater mussels (Unionidae). These mussels most likely originated in Southeast and East Asia in the Jurassic, with the earliest expansions into North America and Africa (since the mid-Cretaceous) following the colonization of Europe and India (since the Paleocene). We discovered two ancient monophyletic mussel radiations (mean age ~51–55 Ma) within the paleo-Mekong catchment (i.e., the Mekong, Siam, and Malacca Straits paleo-river drainage basins). Our findings reveal that the Mekong may be considered a long-lived river that has existed throughout the entire Cenozoic epoch.

Background Amidst the escalating loss of global biodiversity, freshwater mussels (family Unionidae) have become one of the most imperiled animal groups. Acquiring more biological and phylogenetic information on understudied taxa constitutes a pivotal aspect of conservation biology. Consequently, a comprehensive examination was conducted on Koreosolenaia , Parvasolenaia , and Sinosolenaia from China encompassing morphology, anatomy, distribution, and molecular systematics to provide theoretical support for future species endangerment assessments and biodiversity conservation. Results The shell characteristics of Koreosolenaia , Parvasolenaia , and Sinosolenaia were clearly distinct, and the soft-body morphology could also be easily distinguished from each other. The papillae of the incurrent aperture of Sinosolenaia iridinea , Sinosolenaia recognita , and Sinosolenaia oleivora , which were previously described as difficult, exhibited significant variations that could be utilized for species diagnosis. Furthermore, both incurrent and excurrent apertures of the Sinosolenaia species had small cysts on their dorsal surfaces which may be unique to this particular group. Comparative analysis of six mitochondrial genomes ( Parvasolenaia rivularis , Koreosolenaia sitgyensis , Sinosolenaia iridinea , Sinosolenaia recognita , Sinosolenaia carinata , and Sinosolenaia oleivora ) revealed a completely consistent gene arrangement pattern. Additionally, there was a high consistency in nucleotide base content and skewness, amino acid usage, and relative synonymous codon usage among the six complete mitochondrial genomes. Mitochondrial phylogenomics of these genomes with additional taxa within Gonideinae robustly supported the generic relationships as follows: ( Inversidens  + (( Microcondylaea  +  Sinosolenaia ) + ( Parvasolenaia  + ( Koreosolenaia  + ( Ptychorhynchus  + ( Postolata  +  Cosmopseudodon ))). Conclusions The present study provided significant data on the shell morphology and soft-body anatomy of Koreosolenaia , Parvasolenaia , and Sinosolenaia , thereby clarifying the diagnostic characteristics for these challenging taxa. Additionally, we established a robust phylogenetic framework at both the generic and species levels based on mitochondrial genomics.

Southeast Asia harbors a unique and diverse freshwater fauna of Mesozoic origin, which is under severe threat of extinction because of rapid economic development and urbanization. The largest freshwater basins of the region are certainly the primary evolutionary hotspots and they attract the most attention as key biodiversity areas for conservation. In contrast, medium-sized rivers are considered low-importance areas with secondary biodiversity, whose faunas originated via founder events from larger basins during the Pleistocene, although such a scenario has never been tested by using a phylogenetic approach. In this investigation, we used freshwater mussels (Unionidae) as a model to estimate the levels of endemism within the Sittaung, a little-known remote basin in Myanmar, compared with the surrounding larger rivers (Irrawaddy, Salween and Mekong). We discovered that the Sittaung represents an exceptional evolutionary hotspot with numerous endemic taxa of freshwater mussels. On the basis of our extensive dataset, we describe two new tribes, two genera, seven species and a subspecies of Unionidae. Our results highlight that medium-sized basins may represent separate evolutionary hotspots that harbor a number of endemic lineages. These basins should therefore be a focus of special conservation efforts alongside the largest Southeast Asian rivers.

Mitochondrial (mt) function depends critically on optimal interactions between components encoded by mt and nuclear DNAs. mitochondrial DNA (mtDNA) inheritance (SMI) is thought to have evolved in animal species to maintain mito-nuclear complementarity by preventing the spread of selfish mt elements thus typically rendering mtDNA heteroplasmy evolutionarily ephemeral. Here, we show that mtDNA intraorganismal heteroplasmy can have deterministic underpinnings and persist for hundreds of millions of years. We demonstrate that the only exception to SMI in the animal kingdom, that is, the doubly uniparental mtDNA inheritance system in bivalves, with its three-way interactions among egg mt-, sperm mt- and nucleus-encoded gene products, is tightly associated with the maintenance of separate male and female sexes (dioecy) in freshwater mussels. Specifically, this mother-through-daughter and father-through-son mtDNA inheritance system, containing highly differentiated mt genomes, is found in all dioecious freshwater mussel species. Conversely, all hermaphroditic species lack the paternally transmitted mtDNA (=possess SMI) and have heterogeneous macromutations in the recently discovered, novel protein-coding gene (F-orf) in their maternally transmitted mt genomes. Using immunoelectron microscopy, we have localized the F-open reading frame (ORF) protein, likely involved in specifying separate sexes, in mitochondria and in the nucleus. Our results support the hypothesis that proteins coded by the highly divergent maternally and paternally transmitted mt genomes could be directly involved in sex determination in freshwater mussels. Concomitantly, our study demonstrates novel features for animal mt genomes: the existence of additional, lineage-specific, mtDNA-encoded proteins with functional significance and the involvement of mtDNA-encoded proteins in extra-mt functions. Our results open new avenues for the identification, characterization, and functional analyses of ORFs in the intergenic regions, previously defined as “noncoding,” found in a large proportion of animal mt genomes.

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.

Doubly uniparental inheritance (DUI) of mitochondrial DNA, found only in some bivalve families and characterized by the existence of gender-associated mtDNA lineages that are inherited through males (M-type) or females (F-type), is one of the very few exceptions to the general rule of strict maternal mtDNA inheritance in animals. M-type sequences are often undetected and hence still underrepresented in the GenBank, which hinders the progress of the understanding of the DUI phenomenon. We have sequenced and analyzed the complete M and F mitogenomes of a freshwater mussel, Potamilus alatus. The M-type was 493 bp longer (M = 16 560, F = 16 067 bp). Gene contents, order and the distribution of genes between L and H strands were typical for unionid mussels. Candidates for the two ORFan genes (forf and morf) were found in respective mitogenomes. Both mitogenomes had a very similar A+T bias: F = 61% and M = 62.2%. The M mitogenome-specific cox2 extension (144 bp) is much shorter than in other sequenced unionid mitogenomes (531-576 bp), which might be characteristic for the Potamilus genus. The overall topology of the phylogenetic tree is in very good agreement with the currently accepted phylogenetic relationships within the Unionidae: both studied sequences were placed within the Ambleminae subfamily clusters in the corresponding M and F clades.

Five genetically distant groups of mussels possessing high intragroup homogeneity were identified among 65 specimens of 14 East European Unionidae “comparatory species” by genetic analysis of nuclear and mitochondrial markers. By shell morphology other than the shape of the convex contour of the shell, the identified groups correspond to five “taxonomic species” according to Zhadin’s classification. The use of the comparatory method for Unionidae species identification is unjustified.

Between 1997 and 1999, 22 fish species from the rivers Morava and Kyjovka (Czech Republic) and surrounding water pools were examined for the presence of glochidia (gl.). Gl. distribution was studied on 3 common species, Rutilus rutilus, Perca fluviatilis and Rhodeus sericeus. Gl. of two genera, Unio and Anodonta, were found. Anodonta gl. were observed on 10 fish species, Unio gl. on 17 species. Unio gl. were predominantly located on the gills, whereas most Anodonta gl. were found on the fins. Anodonta gl. were predominantly found during winter and spring (November-May), whereas Unio gl. were more abundant during May and June. In perch, the number of gl. was positively correlated with fish length. The highest occurrence of parasites was found on perch, fewer on roach, and in spite of the close relationship between bitterling and unionid mussels, glochidiosis was rare in this species.

Freshwater mussels cannot spread through oceanic barriers and represent a suitable model to test the continental drift patterns. Here, we reconstruct the diversification of Oriental freshwater mussels (Unionidae) and revise their taxonomy. We show that the Indian Subcontinent harbors a rather taxonomically poor fauna, containing 25 freshwater mussel species from one subfamily (Parreysiinae). This subfamily most likely originated in East Gondwana in the Jurassic and its representatives arrived to Asia on two Gondwanan fragments (Indian Plate and Burma Terrane). We propose that the Burma Terrane was connected with the Indian Plate through the Greater India up to the terminal Cretaceous. Later on, during the entire Paleogene epoch, these blocks have served as isolated evolutionary hotspots for freshwater mussels. The Burma Terrane collided with mainland Asia in the Late Eocene, leading to the origin of the Mekong’s Indochinellini radiation. Our findings indicate that the Burma Terrane had played a major role as a Gondwanan “biotic ferry” alongside with the Indian Plate.