Revisiting the North American freshwater mussel genus Quadrula sensu lato (Bivalvia Unionidae): phylogeny, taxonomy and species delineation

© 2019 Royal Swedish Academy of Sciences Freshwater mussels (Bivalvia, Unionidae) have suffered strong declines over the last century. High morphological plasticity of Unionidae causes disturbances in their systematics and taxonomy, hampering conservation efforts. Species that have historically been placed under the North American genus Quadrula have suffered from numerous taxonomic and species delineation problems since its inception. Four genera are presently recognized within Quadrula sensu lato, that is, Cyclonaias, Quadrula, Theliderma and Tritogonia, but their phylogenetic basis remains incompletely tested. In the present study, we reconstructed several two-marker (mtDNA cytochrome c oxidase subunit I—COI and NADH dehydrogenase subunit 1—ND1) phylogenies with newly collected specimens and all previously available sequences covering most species within this group. We then delineated the species within the group using an integrative approach with the application of molecular statistical methods, morphometric (Fourier Shape) analyses and geographic distribution data. Four clades corresponding to these genera were consistently recovered in all phylogenies. To validate the generic status of these clades, molecular analyses were complemented with morphological, anatomical and ecological data compiled from the literature. Several revisions are here proposed to the current systematics and taxonomy of these genera, including the synonymization of Cyclonaias asperata under Cyclonaias kieneriana; the inclusion of Quadrula apiculata and Quadrula rumphiana under Quadrula quadrula; the placement of Quadrula nobilis under Tritogonia; and finally the separation of the Mobile River basin populations of Theliderma metanevra as a new species, that is, Theliderma johnsoni n. sp. The conservation implications of the proposed changes are then discussed

Phylogeny of European Anodontini (Bivalvia: Unionidae) with a redescription of Anodonta exulcerata

Freshwater bivalves are highly threatened and globally declining due to multiple anthropogenic impacts, making them important conservation targets. Because conservation policies and actions generally occur at the species level, accurate species identification and delimitation is critical. A recent phylogenetic study of Italian mussel populations revalidated an Anodonta species bringing the number of known European Anodontini from three to four species. The current study contributes to the clarification of the taxonomy and systematics of European Anodontini, using a combination of molecular, morphological and anatomical data, and constructs phylogenies based on complete mitogenomes. A redescription of A. exulcerata and a comparative analysis of morphological and anatomical characters with respect to the other two species of Anodonta present in the area are provided. No reliable diagnostic character has emerged from comparative analysis of the morphometric characters of 109 specimens from 16 sites across the Italian peninsula. In fact, the discriminant analysis resulted in a greater probability of correct assignment to the site of origin than to the species. This confirms the difficulties of an uncritical application of visual characters for the delimitation of species, especially for Anodontinae.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 - European Regional Development Fund and by FCT - Fundação para a Ciência e a Tecnologia, through national funds (UID/Multi/04423/2019). FCT also supported Manuel Lopes-Lima (SFRH/BD/115728/2016).info:eu-repo/semantics/publishedVersio

Complete mitochondrial genomes of the freshwater mussels Amblema plicata (Say, 1817), Pleurobema oviforme (Conrad, 1834), and Popenaias popeii (Lea, 1857) (Bivalvia: Unionidae: Ambleminae)

Freshwater mussels are a critically imperiled group of mollusks that play key ecological roles and provide important services to humans. The Ambleminae is the only subfamily of these mussels, endemic to North America. Complete mitogenomes have only been sequenced for two of five tribes of the subfamily. Pleurobema oviforme, Amblema plicata, and Popenaias popeii each belong to tribes Pleurobemini, Amblemini, and Popenaidini, respectively, and have not had published mitogenomes. Thus, this study aims to present the complete mitogenomes for these species, to provide a phylogeny of the Ambleminae and confirm the gene arrangements with representation from each of its tribes. The newly sequenced mitogenomes range from 15,852 to 15,993 nucleotides, are composed of 13 PCGs, 22 tRNAs, and two rRNAs and all share the same (UF1) gene order.This work was supported by Portuguese Foundation for Science and Technology (FCT) [grant number ConBioMics/BI-Lic/2019-037 (JTT), grant number SFRH/BD/137935/2018 (AGS)]; COMPETE 2020, Portugal 2020 and the European Union through the ERDF, and by Portuguese Foundation for Science and Technology (FCT) through national funds [UID/Multi/04423/2019] under project ConBiomics: the missing approach for the Conservation of Bivalves Project, and [project number NORTE-01- 0145-FEDER-030286]. Fieldwork in Texas was funded by the U.S. Fish and Wildlife Service, and Texas Parks and Wildlife Department (TPWD) as a Joint Traditional Section 6 Project 407348.info:eu-repo/semantics/publishedVersio

A mitochondrial genome assembly of the opal chimaera, Chimaera opalescens Luchetti, Iglésias et Sellos 2011, using PacBio HiFi long reads

Chondrichthyans (sharks, rays and chimeras) are a fascinating and highly vulnerable group of early branching gnathostomes. However, they remain comparatively poorly sampled from the point of view of molecular resources, with deep water taxa being particularly data deficient. The development of long-read sequencing technologies enables the analysis of phylogenetic relationships through a precise and reliable assembly of complete mtDNA genomes. The sequencing and characterization of the complete mitogenome of the opal chimera Chimera opalescens Luchetti, Iglésias et Sellos 2011, using the long-read technique PacBio HiFi is presented. The entire mitogenome was 23,411 bp long and shows the same overall content, i.e. 13 protein-coding genes, 22 transfer RNA and 2 ribosomal RNA genes, as all other examined Chondrichthyan mitogenomes. Phylogenetic reconstructions using all available Chondrichthyan mitogenomes, including 11 Holocephali (chimeras and ratfishes), places C. opalescens within the Chimaeridae family. Furthermore, the results reinforce previous findings, showing the genus Chimera as paraphyletic and thus highlighting the need to expand molecular approaches in this group of cartilaginous fishes

Shedding light on the Holocephali taxonomy, the mitogenome of Chimaera opalescens

Cartilaginous fish (Chondrichthyes), i.e. sharks, rays, and chimaeras, are extremely interesting from a biological perspective as they represent one of the oldest and most ecologically diverse groups of jawed vertebrates. Their K-selective reproductive traits, make them vulnerable to overfishing. Chimaerid are also a frequent by-catch of deep-water fisheries. Holocephalans comprise a single surviving order, the Chimaeriformes, and are allocated into three different families: Callorhinchidae, Rhinochimaeridae and Chimaeridae (Weigmann 2016). Furthermore, the family Chimaeridae only includes two genera: Chimera and Hydrolagus. Recently, several new species have been described (Iglesias et al., 2022), including Chimera opalescens from deep-sea assemblages (Luchetti et al., 2011). However, previous records of C. opalescens were erroneously classified as Chimera monstrosa (Luchetti et al., 2011; Catarino et al., 2020), due to the similar morphology (Luchetti et al., 2011), which highlights the critical importance of molecular approaches to support species identification. Mitogenomes have been a powerful tool used to elucidate phylogenetic relationships, both at deep and at shallow evolutionary nodes. The development of long-read sequencing technologies a precise and reliable assembly of complete mtDNA genomes. The sequencing and characterization of the complete mitogenome of the opal chimera Chimera opalescens (Luchetti, Iglesias et al., 2011) was carried out, using the long-read technique PacBio HiFi. The entire mitogenome was 23,411 bp long and shows the same overall content, i.e. 13 protein-coding genes, 22 transfer RNA and 2 ribosomal RNA genes, as all other examined chondrichthyan mitogenomes. Phylogenetic reconstructions using all available Chondrichthyan mitogenomes, including 11 Holocephali (chimeras and ratfishes), places C. opalescens within the Chimaeridae family. Furthermore, the results reinforce previous findings, showing the genus Chimera as paraphyletic and thus highlighting the need to expand molecular approaches in this group of cartilaginous fishes

Review of the globally invasive freshwater mussels in the genus Sinanodonta Modell, 1945

In this review, we synthesize the current knowledge of the biology, ecology, and impact of Sinanodonta freshwater mussels (Bivalvia, Unionidae), native to East Asia, that have successfully invaded Europe, Central America, North Africa, and several Asian regions. The main introduction pathways of Sinanodonta were reconstructed based on DNA sequence data and distribution records. We show that invasive lineages of Sinanodonta belong to three species, namely, S. woodiana s. str. (“temperate invasive” lineage), S. pacifica (“tropical invasive” lineage), and S. lauta. Their generalist fish-dispersed larvae, short life span, high fecundity, use by humans for multiple purposes, and ability to establish populations in anthropogenically disturbed conditions were identified as crucial traits driving their invasions. Information on the consequences is scarcer, but Sinanodonta can impact native species through larval parasitism, host fish/food competition, and parasite transmission. In addition, ecosystem effects through their filtration—biodeposition—excretion activity and the occurrence of massive die-offs were detected. Ecosystem services and disservices have not yet been quantified, even at local scales, and management methods in the invasive range are understudied. A better understanding of Sinanodonta ecology, impacts, and management options is urgently needed to make informed decisions and set realistic and impactful restoration goals

Diversity, biogeography and conservation of freshwater mussels (Bivalvia: Unionida) in East and Southeast Asia

Recent research efforts have significantly advanced our knowledge on Asian freshwater mussel (Bivalvia: Unionida) diversity and distribution. Here we provide a modern consensus of the diversity, biogeography and conservation of Unionida in the region comprising East and Southeast Asia (excluding Wallacea) and Asian Russia. A data review confirmed the presence of 228 native and 3 non-native Unionida (98% Unionidae, 2% Margaritiferidae), rendering the region a global hotspot of freshwater mussel diversity. Species richness was highest in China (particularly Yangtze basin) in absolute numbers and Cambodia when correcting for country area, and decreased gradually towards the south and steeply towards the north and east. Six of the seven unionid subfamilies are native to the region, with species richness peaking in Southeast Asia for Rectidentinae, Gonideinae, Parreysiinae and Modellnaiinae, China for Anodontinae and Unioninae, and Asian Russia for Margaritiferidae. Conservation status and data collected after 1980 were not available for 61 and 24% of species, respectively. Dams, deforestation and pollution are likely the major threats to mussels in the region, though data in this respect are scarce. The Philippines, Laos, Indonesia, Myanmar and Malaysia are among the countries with the poorest data availability and urgently require research.AZ was supported by a Postdoctoral Research Fellowship by the School of Environmental and Geographical Sciences, University of Nottingham Malaysia Campus. EF was supported by the Portuguese Foundation for Science and Technology (FCT) under grant SFRH/BPD/ 108445/2015

Mesozoic mitogenome rearrangements and freshwater mussel (Bivalvia: Unionoidea) macroevolution

© 2019, The Author(s), under exclusive licence to The Genetics Society. Using a new fossil-calibrated mitogenome-based approach, we identified macroevolutionary shifts in mitochondrial gene order among the freshwater mussels (Unionoidea). We show that the early Mesozoic divergence of the two Unionoidea clades, Margaritiferidae and Unionidae, was accompanied by a synchronous split in the gene arrangement in the female mitogenome (i.e., gene orders MF1 and UF1). Our results suggest that this macroevolutionary jump was completed within a relatively short time interval (95% HPD 201–226 Ma) that coincided with the Triassic–Jurassic mass extinction. Both gene orders have persisted within these clades for ~200 Ma. The monophyly of the so-called “problematic” Gonideinae taxa was supported by all the inferred phylogenies in this study using, for the first time, the M- and F-type mitogenomes either singly or combined. Within Gonideinae, two additional splits in the gene order (UF1 to UF2, UF2 to UF3) occurred in the Mesozoic and have persisted for ~150 and ~100 Ma, respectively. Finally, the mitogenomic results suggest ancient connections between freshwater basins of East Asia and Europe near the Cretaceous–Paleogene boundary, probably via a continuous paleo-river system or along the Tethys coastal line, which are well supported by at least three independent but almost synchronous divergence events

Conbiomics: the missing approach for the conservation of freshwater bivalves

The decline of freshwater biodiversity hás reached alarming proportions. The extinction rate of freshwater biodiversity is predicted to be five times faster than ali other groups of species. The Unionidae, being the largest of the freshwater bivalve families, is among the most endangered group in the world. They are important providers of aquatic ecosystem services and are characterized by an unusual pattem of mtDNA inheritance. However, phylogeny, population genetic structure and species-level diversity remains unclear for much of the group. With an experienced and well-qualified team, the present proposal aims to define the most important freshwater mussel taxa and most criticai áreas for conservation, at European and Global leveis, to inform the most relevant policy niakers. This will be achieved by integrating a genomics approach with available distribution data, in order to determine and map global species richness, phylogenetic diversity, and weighted endemism. This complementary approach will not only help conserve this vulnerable group but will offer wider benefits to freshwater ecosystems whose billions of people depend globally. Additionally, as these animals have an extraordinary unusual pattern of mtDNA inheritance, they will be used as model-taxa to study the evolution of mtDNA and life in general.This research was developed under Project Nº NORTE-01-0145-FEDER-030286 (ConBiomics: the missing approach for the Conservation of freshwater Bivalves), co-financed by COMPETE 2020, Portugal 2020 and the European Union through the ERDF, and by FCT through national funds.info:eu-repo/semantics/publishedVersio

Invasive fish disrupt host-pathogen dynamics leading to amphibian declines

Sudden disease outbreaks may not necessarily reflect a recent pathogen introduction but may instead arise from the disruption of a host-pathogen equilibrium. Together with invasive species, emerging pathogens pose significant threats to biodiversity. The dynamics of each stressor have been studied separately, yet rarely when interacting. Using a 40-year dataset, we tested the hypothesis that the introduction of an invasive fish leads to such a disruption, manifested by ranavirosis outbreaks on amphibian hosts. MCP sequencing revealed the historical presence of two major Ranavirus clades, with low prevalence. The introduction of fish was not followed by the emergence of new viruses, but rather by an increase in the prevalence of the strains already present, fitting the ‘endemic pathogen hypothesis’. Two decades after the first die-offs, one amphibian species persists in extremely low numbers, but Ranavirus prevalence is closer to the enzootic phase that preceded the outbreaks. Models show that host population collapse and lack of recovery are best explained by the concerted interaction of Ranavirus and invasive fish. We provide robust evidence that invasive species can impact naïve communities by disrupting the host-pathogen balance, exacerbating health threats. This study emphasizes the importance of exploring the historical interactions between multiple stressors to understand population declines.info:eu-repo/semantics/publishedVersio