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Expansion and systematics redefinition of the most threatened freshwater mussel family, the Margaritiferidae
Abstract
Two Unionida (freshwater mussel) families are present in the Northern Hemisphere; the Margaritiferidae, representing the most threatened of unionid families, and the Unionidae, which include several genera of unresolved taxonomic placement. The recent reassignment of the poorly studied Lamprotula rochechouartii from the Unionidae to the Margaritiferidae motivated a new search for other potential species of margaritiferids from members of Gibbosula and Lamprotula. Based on molecular and morphological analyses conducted on newly collected specimens from Vietnam, we here assign Gibbosula crassa to the Margaritiferidae. Additionally, we reanalyzed all diagnostic characteristics of the Margaritiferidae and examined museum specimens of Lamprotula and Gibbosula. As a result, two additional species are also moved to the Margaritiferidae, i.e. Gibbosula confragosa and Gibbosula polysticta. We performed a robust five marker phylogeny with all available margaritiferid species and discuss the taxonomy within the family. The present phylogeny reveals the division of Margaritiferidae into four ancient clades with distinct morphological, biogeographical and ecological characteristics that justify the division of the Margaritiferidae in two subfamilies (Gibbosulinae and Margaritiferinae) and four genera (Gibbosula, Cumberlandia, Margaritifera, and Pseudunio). The systematics of the Margaritiferidae family is re-defined as well as their distribution, potential origin and main biogeographic patterns.
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... Early margaritiferid systematics was based on highly variable or homoplastic morphological characters that often produced conflicting classifications (Lopes-Lima et al., 2018). Molecular phylogenetic studies on the group, which have primarily been based on F I G U R E 4 Percentages distributions of the Gene Ontology (GO) Terms main categories count for: (a) All Unioverse probe regions; (b) The Unioverse probe regions used for the final AHE Margaritiferidae samples alignments. ...
... This reinforces the efficiency of the Unioverse AHE probe dataset in isolating the target regions across Margaritiferidae (Pfeiffer et al., 2019). Both AHE and mtDNA phylogenies retrieve the genuslevel groups recently described by Lopes- Lima et al. (2018), corresponding to the four genera and placing the Gibbosula clade sister to all the remaining genera (Figures 1a,b). However, the position of Cumberlandia concerning Margaritifera and Pseudunio differs among the phylogenies (Figures 1a,b). ...
... However, the position of Cumberlandia concerning Margaritifera and Pseudunio differs among the phylogenies (Figures 1a,b). The results of the AHE phylogeny agree with the published works based on combined mitochondrial and nuclear markers Huff et al., 2004;Lopes-Lima et al., 2018). On the other hand, the mitogenome phylogeny is congruent with other mitochondrial makers-based studies (Araujo et al., 2009;Gomes-dos-Santos et al., 2019;Inoue et al., 2014). ...
The proliferation of genomic sequencing approaches has significantly impacted the field of phylogenetics. Target capture approaches provide a cost-effective, fast and easily applied strategy for phylogenetic inference of non-model organisms. However, several existing target capture processing pipelines are incapable of incorporating whole genome sequencing (WGS). Here, we develop a new pipeline for capture and de novo assembly of the targeted regions using whole genome re-sequencing reads. This new pipeline captured targeted loci accurately, and given its unbiased nature, can be used with any target capture probe set. Moreover, due to its low computational demand, this new pipeline may be ideal for users with limited resources and when high-coverage sequencing outputs are required. We demonstrate the utility of our approach by incorporating WGS data into the first comprehensive phylogenomic reconstruction of the freshwater mussel family Margaritiferidae. We also provide a catalogue of well-curated functional annotations of these previously uncharacterized freshwater mussel-specific target regions, representing a complementary tool for scrutinizing phylogenetic inferences while expanding future applications of the probe set.
... Early margaritiferid systematics was based on highly variable or homoplastic morphological characters that often produced conflicting classifications (Lopes-Lima et al., 2018). Molecular phylogenetic studies on the group, which have primarily been based on F I G U R E 4 Percentages distributions of the Gene Ontology (GO) Terms main categories count for: (a) All Unioverse probe regions; (b) The Unioverse probe regions used for the final AHE Margaritiferidae samples alignments. ...
... This reinforces the efficiency of the Unioverse AHE probe dataset in isolating the target regions across Margaritiferidae (Pfeiffer et al., 2019). Both AHE and mtDNA phylogenies retrieve the genuslevel groups recently described by Lopes- Lima et al. (2018), corresponding to the four genera and placing the Gibbosula clade sister to all the remaining genera (Figures 1a,b). However, the position of Cumberlandia concerning Margaritifera and Pseudunio differs among the phylogenies (Figures 1a,b). ...
... However, the position of Cumberlandia concerning Margaritifera and Pseudunio differs among the phylogenies (Figures 1a,b). The results of the AHE phylogeny agree with the published works based on combined mitochondrial and nuclear markers Huff et al., 2004;Lopes-Lima et al., 2018). On the other hand, the mitogenome phylogeny is congruent with other mitochondrial makers-based studies (Araujo et al., 2009;Gomes-dos-Santos et al., 2019;Inoue et al., 2014). ...
The proliferation of genomic sequencing approaches has significantly impacted the field of phylogenetics. Target capture approaches provide a cost-effective, fast, and easily applied strategy for phylogenetic inference of non-model organisms. However, many existing pipelines used to create phylogenomic datasets from target capture data are incapable of incorporating whole genome sequencing data into their workflows. Here, we develop a highly efficient pipeline for capturing and de novo assembly of the targeted regions using whole genome re-sequencing reads. This new pipeline allows capturing targeted loci accurately and efficiently, and given its unbiased nature, can easily be expanded to be used with any other target capture probe set. We demonstrate the utility of our approach by incorporating whole genome sequencing data into a recently developed target capture probe set to reconstruct the evolutionary history of the freshwater mussel family Margaritiferidae, reconstructing supraspecific relationships outside the Unionidae family, providing the first comprehensive multi-loci phylogeny of the Margaritiferidae. We also provide a catalogue of well-curated functional annotations of the targeted regions for the target capture probe set, representing a complementary tool for scrutinizing phylogenetic inferences while expanding future applications of the probe set.
... Early margaritiferid systematics was based on highly variable or homoplastic morphological characters that often produced conflicting classifications (Lopes-Lima et al., 2018). Molecular phylogenetic studies on the group, which have primarily been based on F I G U R E 4 Percentages distributions of the Gene Ontology (GO) Terms main categories count for: (a) All Unioverse probe regions; (b) The Unioverse probe regions used for the final AHE Margaritiferidae samples alignments. ...
... This reinforces the efficiency of the Unioverse AHE probe dataset in isolating the target regions across Margaritiferidae (Pfeiffer et al., 2019). Both AHE and mtDNA phylogenies retrieve the genuslevel groups recently described by Lopes- Lima et al. (2018), corresponding to the four genera and placing the Gibbosula clade sister to all the remaining genera (Figures 1a,b). However, the position of Cumberlandia concerning Margaritifera and Pseudunio differs among the phylogenies (Figures 1a,b). ...
... However, the position of Cumberlandia concerning Margaritifera and Pseudunio differs among the phylogenies (Figures 1a,b). The results of the AHE phylogeny agree with the published works based on combined mitochondrial and nuclear markers Huff et al., 2004;Lopes-Lima et al., 2018). On the other hand, the mitogenome phylogeny is congruent with other mitochondrial makers-based studies (Araujo et al., 2009;Gomes-dos-Santos et al., 2019;Inoue et al., 2014). ...
The proliferation of genomic sequencing approaches has significantly impacted the field of phylogenetics. Target capture approaches provide a cost-effective, fast, and easily applied strategy for phylogenetic inference of non-model organisms. However, many existing pipelines used to create phylogenomic datasets from target capture data are incapable of incorporating whole genome sequencing data into their workflows. Here, we develop a highly efficient pipeline for capturing and de novo assembly of the targeted regions using whole genome re-sequencing reads. This new pipeline allows capturing targeted loci accurately and efficiently, and given its unbiased nature, can easily be expanded to be used with any other target capture probe set. We demonstrate the utility of our approach by incorporating whole genome sequencing data into a recently developed target capture probe set to reconstruct the evolutionary history of the freshwater mussel family Margaritiferidae, reconstructing supraspecific relationships outside the Unionidae family, providing the first comprehensive multi-loci phylogeny of the Margaritiferidae. We also provide a catalogue of well-curated functional annotations of the targeted regions for the target capture probe set, representing a complementary tool for scrutinizing phylogenetic inferences while expanding future applications of the probe set.
... The family Margaritiferidae Henderson, 1929 are threatened freshwater pearl mussels distributed in Northern Hemisphere freshwater systems. It comprises 16 species in four genera that are arranged in two subfamilies according to recent DNA analyses by Lopes-Lima et al. (2018): Gibbosulinae Bogan, Bolotov, Froufe & Lopes-Lima in Lopes-Lima et al., 2018( ve species in Gibbosula Simpson, 1900, and Margaritiferinae (one species in Cumberlandia Ortmann, 1912, seven in Margaritifera Schumacher, 1815, and three in Pseudounio Haas, 1910. ...
... The family Margaritiferidae Henderson, 1929 are threatened freshwater pearl mussels distributed in Northern Hemisphere freshwater systems. It comprises 16 species in four genera that are arranged in two subfamilies according to recent DNA analyses by Lopes-Lima et al. (2018): Gibbosulinae Bogan, Bolotov, Froufe & Lopes-Lima in Lopes-Lima et al., 2018( ve species in Gibbosula Simpson, 1900, and Margaritiferinae (one species in Cumberlandia Ortmann, 1912, seven in Margaritifera Schumacher, 1815, and three in Pseudounio Haas, 1910. ...
... genetic studies carried out by Bolotov et al. (2015Bolotov et al. ( , 2016, Araujo et al. (2017) and Lopes-Lima et al. (2018), and they are identi ed as M. dahurica (Middendorff, 1850) (mainly in the Amur River basin), M. laevis (Sakhalin, Kuril, Hokkaido and Honshu Islands), and M. middendorf (Rośen, 1926) (from the Kamchatka Peninsula to Sakhalin, Kuril, Hokkaido and Honshu Islands). Margaritifera togakushiensis , recently described from Japan, was regarded as a junior synonym of M. middendorf (Bolotov et al., 2016) in their classi cation. ...
Previous taxonomic and molecular studies demonstrated the existence of two distinct
species of the freshwater pearl mussel genus Margaritifera in the Kamchatka–Sakhalin–Kuril–Japan region, but problems remained as to their identi cation. To solve them, shells of nominal types and other voucher specimens were reexamined morphologically in detail and compared with Japanese populations using multivariate analyses. The results recon rmed the importance of the shape of the dorsal edge of the anterior adductor muscle scar, and demonstrated the usefulness of the width of pseudocardinal teeth as a distinguishing character. Based on the results the previously accepted classi cation was revised: M. laevis (Haas, 1910) (Japanese name: Kawa�shinju-gai) is characterized by a rounded dorsal edge of the anterior adductor muscle scar and thin pseudocardinal teeth, and M. kurilensis (Zatravkin & Starobogatov, 1984) (Japanese name: Kogata-kawa-shinju-gai) is characterized by an angulate dorsal edge of the anterior adductor muscle scar and robust pseudocardinal teeth. Margaritifera middendorf (Rosén, 1926), a name often applied to the latter species, is here considered a junior synonym of M. laevis, and M. togakushiensis Kondo & Kobayashi, 2005, often synonymized with M. middendorf , is shown to be a junior synonym of M. kurilensis, judged from the morphology of the primary types.
... 4 However, the global industrialization process introduced stronger threats to the survival of the species. [6][7][8] In fact, M. margaritifera belongs to one of the most threatened taxonomic groups on earth, the Margaritiferidae. 6 The species was once abundant in cool oligotrophic waters throughout most of northwest Europe and northeast North America. ...
... [6][7][8] In fact, M. margaritifera belongs to one of the most threatened taxonomic groups on earth, the Margaritiferidae. 6 The species was once abundant in cool oligotrophic waters throughout most of northwest Europe and northeast North America. [6][7][8] However, habitat degradation, fragmentation, and pollution have resulted in massive population declines. ...
... 6 The species was once abundant in cool oligotrophic waters throughout most of northwest Europe and northeast North America. [6][7][8] However, habitat degradation, fragmentation, and pollution have resulted in massive population declines. 8 Consequently, the Red List of Threatened Species from the International Union for Conservation of Nature has classified M. margaritifera as Endangered globally and Critically Endangered in Europe. ...
Since historical times, the inherent human fascination with pearls turned the freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) into a highly valuable cultural and economic resource. Although pearl harvesting in M. margaritifera is nowadays residual, other human threats have aggravated the species conservation status, especially in Europe. This mussel presents a myriad of rare biological features, e.g. high longevity coupled with low senescence and Doubly Uniparental Inheritance of mitochondrial DNA, for which the underlying molecular mechanisms are poorly known. Here, the first draft genome assembly of M. margaritifera was produced using a combination of Illumina Paired-end and Mate-pair approaches. The genome assembly was 2.4 Gb long, possessing 105,185 scaffolds and a scaffold N50 length of 288,726 bp. The ab initio gene prediction allowed the identification of 35,119 protein-coding genes. This genome represents an essential resource for studying this species' unique biological and evolutionary features and ultimately will help to develop new tools to promote its conservation.
... The distribution of terrestrial organisms across the Mediterranean led to the classification of Northern Africa and Eurasia as the Palaearctic bioregion (Holt et al. 2013;Husemann et al. 2014). This bioregionalisation has also been described for freshwater groups like molluscs (Lopes-Lima et al. 2018), amphipods (Bauzà-Ribot et al. 2012;Stokkan et al. 2018) or fish (Casal-López and Doadrio 2018). While the Mediterranean Sea is today a geographical barrier for nonmarine European and North African species, in the past, land connections allowed for organism dispersal/isolation events between the two continents. ...
... Molecular data and phylogenetic methods comprise a new toolbox to test these biogeographic hypotheses on freshwater groups showing Iberian-Maghrebian distributions. Biogeography has more often been inferred from fish (Almada et al. 2009;Casal-López and Doadrio 2018;Doadrio and Perdices 2005;Machordom and Doadrio 2001;Perea et al. 2010), lizards (Carranza et al. 2006b;Fonseca et al. 2009;Pinho et al. 2008) or planarians (Lázaro et al. 2009) and, until recently, other freshwater groups such as molluscs have received less attention (Araujo et al. 2017;Boulaassafer et al. 2018;Lopes-Lima et al. 2018;Sands et al. 2019;Sousa et al. 2019). Recent phylogenetic studies of freshwater bivalves show sister relationships between species endemic to either side of the Strait of Gibraltar. ...
... These findings raise the known biodiversity of this genus to 24 species and the number of genera of Hydrobiidae sensu stricto in Morocco to 13 (i.e. Corrosella, Mercuria (Boulaassafer et al. 2018;Glöer et al. 2015), Pseudamnicola Ghamizi et al. 1997), Islamia Radoman, 1973and Aghbalia Glöer et al., 2020a(Glöer et al. 2020a), Ifrania Glöer et al., 2020band Fessia Glöer et al., 2020b(Glöer et al. 2020b, Heideella Backhuys and Boeters, 1974, Atebbania Ghamizi et al., 1999 (Froufe et al. 2016b) and Pseudunio Haas, 1910(Lopes-Lima et al. 2018Sousa et al. 2019). However, most of these taxa show broader geographic ranges than Corrosella, and their species are found in a wider range of habitat types. ...
Despite the high species richness of freshwater gastropods in the western Mediterranean, the evolutionary patterns of the North African taxa are poorly understood. In a recent survey of spring habitats in the Atlas Mountains of Morocco (western Maghreb), we discovered ten snail populations anatomically resembling the genus Corrosella (family Hydrobiidae), which was supposedly endemic to the Iberian Peninsula and southern France. Through morphological and molecular investigations, we assessed the taxonomic status of these populations and their evolutionary origins. Molecular phylogenies based on three gene fragments (COI, 16S rRNA and 28S rRNA) from snails of the newly collected populations and 12 additional congeners distributed across the Iberian Peninsula and southern France clustered together the Moroccan populations within Corrosella in a well-supported clade comprising six putative species: two previously identified as Hydrobia marocana and Pseudamnicola pallaryi and four unknown lineages here described as species new to science. According to a molecular clock analysis calibrated with an external rate, the Moroccan clade originated ca. 7.6 million years ago (Mya) (11–4.5 Mya) and its divergence from the southern Iberia lineages likely occurred 8.4 Mya (12.5–5.5 Mya). This suggests that the biogeography of Corrosella in the western Maghreb has been shaped by old vicariance events likely associated with the Late Miocene-Pliocene geological setting of the region and their interplay with the isolation conditions of springs. Our findings considerably expand knowledge of the diversity and geographic range of Corrosella and provide new insight into faunal relationships between North Africa and Europe.
... Some years ago, several scientific works reported occurrences of the freshwater pearl mussel Margaritifera margaritifera (Margaritiferidae) from tropical areas, that is, West Africa and the Philippines (Akindele et al., 2018;Echem et al., 2016;Joaquino et al., 2017;Ukam et al., 2018). This species is distributed in eastern North America and Western Europe, prefers oligotrophic cold-water rivers and streams and generally uses Atlantic salmon Salmo salar and brown trout Salmo trutta as larval host (Boon et al., 2019;Geist, 2010;Lopes-Lima et al., 2018;Taeubert & Geist, 2017). It is clear that the astonishing records of M. margaritifera from tropical environments were other mussel species and had been misidentified. ...
... Nigeria belongs to the Western Subregion, the fauna of which contains 18 native mussel species . Although representatives of the family Margaritiferidae are undoubtedly absent as noted in recent faunas of sub-Saharan Africa (Lopes-Lima et al., 2018), several authors have reported records of margaritiferids from Nigeria (Appendix A). All these records are based on misidentified samples of native African species belonging to other families (Iridinidae and Etheriidae). ...
1. Freshwater mussels (order Unionida) are a popular group for a wide array of non-taxonomic research driven by questions related to their functions in ecosystems, to relationships among species, to biogeochemical and morphometric patterns of certain species and others. Valid taxonomy and correct species identification are key requirements for all of these aspects. However, species-level identification of representatives from this group is a rather complicated task and should be based on an integrative approach, combining DNA sequences, morphological and anatomical investigation and biogeographical estimates.
2. This article reconsiders a selection of non-taxonomic scientific works (N = 25), containing misidentified occurrences of freshwater mussel species. The dataset contains records of the endangered Margaritifera margaritifera (endemic to eastern North America and Europe) from the Philippines and West Africa, as well as occurrences of the Nearctic Gonidea angulata from West Africa and the Middle East. Several Palearctic and Nearctic unionid species were erroneously reported from the Indus River, Pakistan. Subfossil shells of the native Simpsonella sp. from a prehistoric site in the Philippines were misidentified as the invasive Sinanodonta woodiana that was introduced to the islands in the 20th century. Samples of the tropical lineage of S. woodiana from Indonesia were mistaken for the native Pilsbryoconcha exilis, and vice versa. Salinity tolerance and morphometric characteristics of the estuarine clam Geloina sp. (Cyrenidae) from Sumatra were examined, but these data were published as belonging to the strictly freshwater S. woodiana.
3. It is clear that this information, being reused by researchers, conservationists and stakeholders, will lead to incorrect conclusions on the range, status, biogeochemistry, morphometry and ecological tolerance of certain freshwater mussel taxa, including invasive and endangered species (the so-called ‘error cascades’ in biological sciences caused by ‘bad taxonomy’).
4. To reduce the growing body of literature containing misidentifications of the Unionida taxa, practical recommendations are proposed for researchers, who include freshwater mussels in non-taxonomic surveys, as well as for journal editors dealing with articles that focus on these animals.
... The origin of Pseudunio is still a matter of debate. Lopes-Lima et al. (2018) considered Hauterivian-Barremian Unio idubedae Palacios & Sánchez, 1885 from Spain the earliest crown group member of the Pseudunio clade and assigned it to Paraheudeana Starobogatov, 1970. Barremian Unio valdensis Mantell, 1844 from southern England, which is the type species of Paraheudeana, has well-developed posterior lateral teeth. ...
... In the literature, Pseudunio has been variably treated as a valid genus, a junior subjective synonym of Margaritifera Schumacher, 1815, or a subgenus of the latter. The most recent phylogeny of the Margaritiferidae byLopes-Lima et al. (2018) re-established the validity of Pseudunio as a genus. Unio sinuatus Lamarck, 1819 is a junior subjective synonym of Pseudunio auricularius(Spengler, 1793). ...
... These ecosystem services are expected to occur in large mussel communities, where the semi-infaunal adults display important burrowing and biofiltration functions in the riverbeds (Boeker et al., 2016;Vaughn and Hakenkamp, 2001;Vaughn et al., 2008). Nevertheless, freshwater mussels in the Northern Hemisphere are one of the largest and most threatened freshwater taxa worldwide (Lopes- Lima et al., 2018Lima et al., , 2017a. In Europe, Margaritifera margaritifera (Linnaeus, 1758) is listed as critically endangered (Lopes- Lima et al., 2018Lima et al., , 2017b, and most of the populations lack recent recruitment due to the loss of the habitat required by the young mussels (Geist and Auerswald, 2007). ...
... Nevertheless, freshwater mussels in the Northern Hemisphere are one of the largest and most threatened freshwater taxa worldwide (Lopes- Lima et al., 2018Lima et al., , 2017a. In Europe, Margaritifera margaritifera (Linnaeus, 1758) is listed as critically endangered (Lopes- Lima et al., 2018Lima et al., , 2017b, and most of the populations lack recent recruitment due to the loss of the habitat required by the young mussels (Geist and Auerswald, 2007). ...
The larval development of the endangered freshwater mussel Margaritifera margaritifera (L.) represents one of the most unique parasitism among naiads, in which larva parasite the fish gills for several months. Despite the importance of this parasitic phase to successfully culture the freshwater mussel, the larval morphogenesis remains understudied. To describe the parasitic larval development and metamorphosis, Atlantic salmon (Salmo salar L.) were exposed to glochidia, sampled periodically to visualize the gills by stereomicroscopy and light microscopy and results were summarized throughout three developmental stages. Once attached to the fish gills, glochidia changed their morphology within the first days and acquired an intermediate stage termed mushroom larva due to the presence of the mushroom body and the zip membrane, both structures are transitory and distinctive of this long-lasting parasitism. The zip membrane, located at the valve cleft, may play a unique role in the isolation and acquisition of non-particulate nutrients from the fish, while the mushroom body of the mantle accumulates abundant intracytoplasmic lipid droplets. After 200 days, a successful metamorphosis was evidenced by the formation of a complete set of post-larval organs, pointing to the acquisition of different functionality, which will be essential for the settlement and deposit-feeding into the riverbed. Among the post-larval organs, the byssal complex of the post-larval foot was described for the first time at the end of the parasitic stage of naiads. In conclusion, this study provides an overview of the larval morphogenesis of M. margaritifera, from glochidium to post-larva, essential for understanding the parasitic interaction between the freshwater mussel larva and the fish host. Moreover, the morphological techniques and the hallmarks described might be applicable to optimize and monitor the larval developmental status during one of the most critical stages of the captive breeding programmes of endangered freshwater mussels.
... Given their high sensitivity to habitat disturbance and complex life cycle, and the continuing degradation of freshwater habitats, freshwater mussels have been declining rapidly worldwide in recent decades (Lydeard et al., 2004;Strayer et al., 2004;Geist, 2010;Vaughn, 2018). Globally, Considering these grim assessments, freshwater mussels are considered one of the most threatened groups of freshwater organisms in the world (Strayer et al., 2004;Bogan, 2008;Johnson et al., 2013;Lopes-Lima et al., 2018;Lopes-Lima et al., 2021). ...
... Given that the filtration rates of freshwater mussels are highly dependent on temperature, oxygen and nutrients, climate change is also likely to have a pronounced effect on the ecosystem services they provide by changing their ability to filter water (Malish & Woolnough, 2019). Extreme climatic events are also predicted to become more frequent and intense in the future (Liu et al., 2017b;Lopes-Lima et al., 2018). Droughts and floods have already contributed to massive die-offs of Chinese freshwater mussels (Shu et al., 2009;Zhang et al., 2013;Liu et al., 2017b;Lopes-Lima et al., 2017). ...
1. Freshwater mussels (Mollusca: Bivalvia: Unionida) have a broad global distribution on every continent except Antarctica. However, due to human activities, the diversity of freshwater mussels is seriously globally threatened. China is an important global biodiversity hotspot for this fauna.
2. Here, we comprehensively review the 99 currently recognized species in China, collating for the first time their systematics, distribution, life-history traits, habitat preferences, conservation status, and main threats to suggest future management actions.
3. Our review showed that the taxonomic status and species validity of many freshwater mussels is still not well resolved. The freshwater mussel diversity in the Yangtze River Basin is higher than that in other freshwater habitats of China. Life history characteristics and habitat preferences are poorly known for most species.
4. Only half of the total number of species in China have been assessed for their conservation status. Among those assessed, around half of them are threatened with extinction with more than 10% being considered as Data Deficient.
5. The key threats identified as potentially related to species declines were pollution, habitat loss and fragmentation, loss of access to host fishes, and overharvesting of mussels or their host fishes.
6. We also show that there is a strong geographic bias in the amount of knowledge available for freshwater mussels with most of the available data being concentrated in the middle and lower reaches of the Yangtze basin region. Almost no data are available for these taxa north of the Yellow River basin and in the west and southwest regions of China.
7. To make future conservation and management more effective we suggest that efforts should be concentrated on: 1) increasing the research on basic ecological and life-history features including growth, life-span, reproductive cycle, host fish identification, and habitat requirements of each species; 2) establishing the interspecific and intraspecific genetic diversity patterns of Chinese freshwater mussels, to clarify their taxonomy, systematics, and phylogeny, and understand the phylogeography and population structure of each species; 3) urgently establish protected areas for fish and mussels in locations of high species richness, like Poyang Lake and Dongting Lake, and also in regions with high levels of endemism or genetic uniqueness, like Guangxi Province, Yunnan Province and Heilongjiang Province. In addition, habitat restoration and the conservation of freshwater mussels have become urgent in China, and an integrated systematic conservation and management plan should be developed and effectively implemented.
... Interestingly, none of Unionicola mites is known to be associated with the family Margaritiferidae. Currently, this freshwater mussel family contains 16 species in two subfamilies (Araujo et al., 2017;Bolotov et al., 2016;Lopes-Lima et al., 2018). We know very little about the patterns of host associations of Unionicola mites that occur with freshwater mussels in tropical areas, although multiple nominal mite taxa were described from Southeast Asia, India, Australasia, Africa, and South America (Lundblad, 1969;Vidrine, 1984Vidrine, , 1985Vidrine, , 1986aVidrine, , 1986bVidrine et al., 2005Vidrine et al., , 2006Vidrine et al., , 2007Viets, 1926Viets, , 1957. ...
... Examples of such hidden phylogenetic lineages were recovered in North American mussel mites (Edwards et al., 2010;Ernsting et al., 2014) and European sponge-associated taxa (Stålstedt et al., 2013). Complete mitochondrial genomes are often used to reconstruct robust phylogenies of various animal taxa (Edwards, 2014;Edwards & Vidrine, 2013;Froufe et al., 2020) but mitogenome sequences were generated only for a few species of the genus, for example, U. (Unionicola) foili Edwards & Vidrine, 1994 and U. (Unionicolides) parkeri Vidrine, 1987(Edwards et al., 2011Ernsting et al., 2009 (Araujo et al., 2017;Bolotov et al., 2016;, and is considered endangered (Bolotov et al., 2014;Lopes-Lima et al., 2018). Alongside with the discovery of a margaritiferid-associated mite, we present the first DNA sequence data on a variety of tropical Unionicola spp. ...
Freshwater pearl mussels (Bivalvia: Margaritiferidae) are among the most imperiled groups of animals globally. While the parasites and symbionts of the Margaritiferidae are rather poorly known, these mussels were thought to be free of parasitic mites (Acari: Unionicolidae: Unionicola). Here, we report on the discovery of a mite species being associated with the endangered freshwater pearl mussel Gibbosula laosensis (Lea, 1863) from Myanmar. This species, Unionicola (Gibbosulicola) sella subgen. & sp. nov., morphologically resembles mites belonging to the subgenera Coelaturicola and Fulleratax ( African and Southeast Asian groups, respectively). Our novel discovery expands the host range of Unionicola mites and reveals that all freshwater mussel families of the order Unionida host these aquatic mites. Our phylogenetic research and available published data reveal that the mussel-associated mite assemblage in Southeast and South Asia contains not less than 17 species and 8 subgenera. Currently, the regional taxonomic richness of this group seems to be largely underestimated. We found that mussel mites from Southeast Asia are narrow host specialists, which are known to occur in a single or a few closely related species belonging to one or two sister genera of freshwater mussels. Finally, our results indicate that mussel mites share generally restricted ranges and that their distribution patterns in Southeast Asia are largely congruent with the boundaries of biogeographic subregions delineated on the basis of phylogenetic studies of freshwater mussels.
... Although over-harvesting represented a serious threat to the species for centuries (mostly in Europe and Russia), there has been a decrease in interest and demand for freshwater pearls in the 20 th century 4 . However, the global industrialization process introduced stronger threats to the survival of the species [6][7][8] . In fact, M. margaritifera belongs to one of the most threatened taxonomic groups on earth, the Margaritiferidae 6 . ...
... Besides being able to produce pearls, M. margaritifera presents many other remarkable biological characteristics, e.g. is among the most longest-living invertebrates, reaching up to 280 years 6,11 ; displays very weak signs of senescence, referred as the concept of "negligible senescence" 12 ; has an obligatory parasitic larval stage on salmonid fishes used for nurturing and dispersion 8,10 ; and, like many other bivalves (see Gusman et al. 13 for a recent enumeration), ...
Since historical times, the inherent human fascination with pearls turned the freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) into a highly valuable cultural and economic resource. Although pearl harvesting in M. margaritifera is nowadays residual, other human threats have aggravated the species conservation status, especially in Europe. This mussel presents a myriad of rare biological features, e.g. high longevity coupled with low senescence and Doubly Uniparental Inheritance of mitochondrial DNA, for which the underlying molecular mechanisms are poorly known. Here, the first draft genome assembly of M. margaritifera was produced using a combination of Illumina Paired-end and Mate-pair approaches. The genome assembly was 2,4 Gb long, possessing 105,185 scaffolds and a scaffold N50 length of 288,726 bp. The ab initio gene prediction allowed the identification of 35,119 protein-coding genes. This genome represents an essential resource for studying this species' unique biological and evolutionary features and ultimately will help to develop new tools to promote its conservation.
... The data obtained in this study allowed to detect populations that can be considered distinct conservation units. However, the used mitochondrial marker system are rather applicable for inferring historical population structure due to the relatively slow mutational substitution rate, especially in the case of such slowly evolving species like M. margaritifera (Bolotov et al. 2016;Lopes-Lima et al. 2018). ...
Freshwater organisms are among the most vulnerable species being impaired by global climate change. Freshwater Pearl Mussel (Margaritifera margaritifera) is a keystone species that facilitates a number of important ecosystem functions in cold water oligotrophic streams, while is currently facing habitat alteration and degradation due to human activities. Global climate change is amplifying these negative impacts. Population decline is directly connected with transformation of population genetic structure and may result in significant loss of genetic diversity. In this study, we identified populations of M. margaritifera for conservation prioritization in the north-eastern part of the species’ range and investigated the potential impact of future climate scenarios on its conservation genetics. We used nine microsatellite loci to examine genetic diversity and differentiation in 17 populations of the species from rivers of the Barents, White, and Baltic Sea basins. To forecast the effects of climatic changes on the dynamics of genetic structure, we applied the Bayesian clustering algorithm. Genetic simulations were conditioned to mean summer temperatures estimated under future carbon emission projections, i.e., representative concentration pathway (RCP) scenarios 4.5 and 8.5. High genetic diversity and low genetic differentiation were found in the studied populations, with individuals being assigned to three genetic clusters. Future climate change will significantly rearrange cluster distribution resulting in lower population differentiation. The only exception were populations of the Baltic Sea basin that keep their genetic uniqueness under current and future climatic conditions. Obtained data allowed us to delineate three conservation units that play critical roles in securing the genetic diversity of the species currently and in the future: (1) populations of the Barents Sea basin with the highest contribution to the overall genetic diversity; (2) populations of northern Karelia which will lose significant part of their diversity under the climate change; and (3) populations of the Baltic Sea basin, with a unique gene pool which is threatened by climate change and other anthropogenic pressures.
... Although glochidial morphology and metrics of shell characters have some value as a tool to help identify some Frontiers in Environmental Science frontiersin.org taxa (e.g., Kennedy and Haag, 2005;Pimpão et al., 2012), and indeed have been used for taxonomic re-arrangements in some instances (e.g., Pimpão et al., 2012;Pfeiffer and Graf, 2015;Cruz and Quesada, 2017;Lopes-Lima et al., 2018;Miyahira et al., 2019;Chernyshev et al., 2020), they are not always sufficiently unique within species or among taxonomic groups, as this study has demonstrated. Yet, this study also showed that for most taxa examined, certain characteristics were common at the subfamily and tribal level. ...
Most freshwater mussels have larvae (glochidia in Unionidae, Margaritiferidae and Hyriidae) that are parasitic on fishes. This study describes and compares the diversity of glochidia among 17 species of Australasian Hyriidae. Here, scanning electron microscopy was used to illustrate shell morphology, while patterns of diversity in size, shape and morphological characteristics were analysed quantitatively and qualitatively with Principal Component, Linear Discriminant, and Multiple Correspondence Analyses to separate species with varying degrees of discrimination. Results showed shell lengths ranged from 50 to 390 μm. Shape varied, from sub-oval to sub-triangular, bilaterally symmetrical to scalene, and hook morphology varied from unicuspid, bicuspid, tricuspid or complex with varying length and structure. Unique observations of this study include the consistent variation in glochidial release mechanisms among Australian subfamilies and New Zealand genera. Hyridellini species and Echyridella aucklandica (Gray and Dieffenbach, 1843) are released either freely or as “mesoconglutinates” (presumed brood lures), whereas Velesunioninae and Echyridella menziesii (Gray and Dieffenbach, 1843) release glochidia in “amorphous mucous conglutinates”. Hyridellini predominantly occur within perennially flowing rivers of coastal south-eastern Australia with generally low turbidity, whereas the Velesunioninae occur more typically in slower flowing, intermittent waters, many prone to extended periods of high turbidity. Thus, where Hyridellini occur, mesoconglutinates as visual brood lures may be a more efficient mechanism for infesting host fishes than the passive infestation strategy typical of velesunionine species frequenting more turbid waters. Finally, this study presents systematic descriptions of glochidia and a provisional key for identification of Australasian hyriid glochidia, making an important contribution to the current understanding of taxonomy and life history traits, both critical for hyriid conservation.
... Bu faktörlerle mücadele için, Avrupa Birliği ve USDA-APHIS (ABD Tarım Departmanı)'in uyguladığı gibi stratejik politikaları uygulayabilir ve tatlı su habitatlarını erken tespit amacıyla izlemeye yönelik kaynaklara ve teknolojilere yatırım yapabiliriz. Ayrıca istilacı tatlı su yumuşakçalarına ilişkin küresel düzeyde bir coğrafi veri tabanı geliştirebilir ve istilacı türlerin popülasyonlarını azaltmak ve geçim kaynaklarını iyileştirmek için yeni kullanımlarını değerlendirebiliriz (Froufe ve ark., 2016;Gürlek ve ark., 2019;Lopes-Lima ve ark., 2017a, 2017b, 2018a, 2018b, 2021, 2024Vikhrev ve ark., 2018). ...
... Integrative taxonomy approaches provide a viable solution to the ongoing debate surrounding morphological species definitions. In recent years, an increasing number of studies have employed integrative taxonomy to clarify the taxonomic validity of freshwater mussels (Ayrat, 2005;Lopes-Lima et al., 2017a, 2018aMalhotra & Thorpe, 2004;Prié & Puillandre, 2014;Sheth & Thaker, 2017). Previous studies have classified Lepidodesma aligera as a variant of Lepidodesma languilati, attributing potential morphological variations to specific habitats (Heude, 1877;Paetel, 1890). ...
Increasingly sophisticated molecular techniques and research tools have greatly advanced the understanding of species diversity and phylogenetic relationships in freshwater mussels. However, malacologists have been puzzled by the taxonomic position and species validity of certain species, particularly those described solely based on conchological characteristics. The genus Lepidodesma is one such group. Here, we integrate shell morphology, soft-body anatomy, and molecular phylog-eny to delimit the species validity of Lepidodesma aligera (Heude in Conchyliologie Fluviatile de la Provoince de Nanking 3:17-24, 1877) and Lepidodesma languilati (Heude in Journal De Conchyliologie 22:112-118, 1874). Comparative morphology reveals that L. aligera can be distinguished from L. languilati by its higher post-dorsal wing covered with scattered nodules, as well as differences in the incurrent aperture, excurrent aperture, and gill. Additionally, the average genetic distance based on DNA barcodes (COI) between both species is 4.0%. Integrative taxonomy supports the distinct species of L. aligera, rather than synonymy for L. languilati. Mitochondrial phylogenomic analyses confirm four monophyletic groups (Ambleminae + (Gonideinae + (Unioninae + Parreysiinae))) within the family Unionidae. L. aligera and L. languilati have a well-supported sister-group relationship and form a basal clade splitting from the rest of Unioninae. Therefore, the genus Lepidodesma should be classified as Lepidodesmini in Unioninae. The molecular clock with fossil calibration indicates that Lepidodesma originated in the Early Cretaceous (~121.30 Mya, 95% HPD = 90.37-156.54 Mya) and diverged in the Middle Neogene (~12.94 Mya, 95% HPD = 6.72-22.13 Mya). This study firstly provides anatomical features and molecular data for L. aligera and demonstrates the species validity and the systematic position of Lepidodesma taxa, which enrich our understanding of this rare group and facilitate its management and conservation.
... Even so, morphological variation is high within habitats and overlaps between them, implying an imperfect predictability to freshwater mussel evolution-a pattern also seen in a few marine bivalve clades Serb et al., 2017). The frequency and degree of morphological convergence in other systems tends to increase with decreasing phylogenetic distance (Ord & Summers, 2015;Stayton, 2008), but these freshwater mussels are not a shallow radiation, with the most recent common ancestor of Margaritiferidae + Unionidae estimated to be ~210-250 Myr (Bolotov et al., 2016;Lopes-Lima et al., 2018). Datasets containing many taxa and few morphological traits, like the one analyzed here, tend to detect greater degrees of convergence (Stayton, 2008). ...
Frequent and strong morphological convergence suggests that determinism tends to supersede historical contingencies in evolutionary radiations. For many lineages living within the water column of rivers and streams, hydrodynamic forces drive widespread morphological convergence. Living below the sediment-water interface may release organisms from these hydrodynamic pressures, permitting a broad array of morphologies, and thus less convergence. However, we show here that the semi-infaunal freshwater mussels have environmentally determined convergence in shell morphology. Using 3D morphometric data from 715 individuals among 164 Nearctic species, we find that species occurring in rivers with high flow rates have evolved traits that resist dislodgement from their burrowed position in the streambed: thicker shells for their body size, with the thickest sector of the shell being the most deeply buried. Species occurring in low flow environments have evolved thinner and more uniformly thickened shells, corresponding to an alternative adaptation to dislodgement: increased burrowing efficiency. Within species, individuals also show increased shell thickness for their body size at higher flow rates, suggesting that ecophenotypy may, in part, be an important mechanism for establishing populations in new environments and thus evolutionary divergence in this highly imperiledinvertebrate group.
... Freshwater mussels (Order Unionida; hereafter mussels) are among the most endangered groups of organisms in the world (Bogan, 2008;Lopes-Lima et al., 2018;Lopes-Lima et al., 2021). As an example, recent data shows that there is now a total of 540 red-listed species, of which 253 species are considered as globally threatened (IUCN, 2021). ...
The worldwide decline in freshwater biodiversity due to rising anthropogenic pressures is of growing concern. Much evidence reveals that biodiversity loss and taxonomic homogenization results in loss of ecosystem functions. Understanding temporal and spatial patterns of biodiversity is, a major challenge in ecological conservation. Of all groups of threatened aquatic animals, freshwater mussels are responsible for critical trophic and non-trophic functions. Based on published inventories and field surveys, here we aim to evaluate whether freshwater mussel diversity, density and biomass has changed in the last 60 years, as well as the factors driving these patterns in different areas within the Poyang Lake basin, a global biodiversity hotspot in the middle reach of the Yangtze River. Results showed that alpha diversity has declined in the current period (2016-2020) as compared to diversity in the historical (1960-2003) and intermediate periods (2003-2014). Overall species richness declined by 28 percent over 60 years. Density and biomass also declined by 79 and 42 percent, respectively. Population declines led to homogenization of freshwater mussel faunas. Additionally, there was a significant association between pH and alpha and beta diversity, suggesting that acidification related to intensive agriculture development may be one major factor behind mussel declines. In summary, this study provides new insights into the patterns and drivers of freshwater mussel population dynamics in the Poyang Lake basin. The results have implications for the design of freshwater protected areas to slow, and even reverse, current declines.
... Определение моллюсков дается согласно последним ревизионным данным (Клишко, 2014;Bolotov et al., 2016;Lopes-Lima et al., 2018. Описание икры и предличинок рыб, их определение проводили по приводимым в литературе данным (Крыжановский, 1949; Крыжановский и др., 1951; Макеева, 1976; Макеева и др., 2011). ...
The findings of bitterling (Rhodeus sericeus) eggs and larvae in the gill chambers of freshwater bivalve mollusks from Razdolnaya River basin are discussed. Bitterling eggs and larvae were registered in Margaritifera dahurica pearl mussels from Komarovka river, a tributary of Razdolnaya River, on the territory of the Ussuriysky Nature Reserve. Bitterling larvae at different stages of development were also found in Nodularia douglasiae mussels from Razdolnaya River.
... Glochidia morphology and morphometry have proven to be useful in systematics and taxonomy (e.g., Surber 1912;Mansur 1999;Mansur and Silva 1999;Vale et al. 2005;Pimpão et al. 2012;Cruz and Quesada 2017;Lopes-Lima et al. 2018;Miyahira et al. 2019;Chernyshev et al. 2020;Pfeiffer and Graf 2020 ...
Larvae (glochidia) of the freshwater mussel, Westralunio albertisi were obtained from the marsupia of a preserved female at the Western Australian Museum. Glochidial shells of W. albertisi are subtriangular and scalene in shape outline with a convoluted surface dotted with pores and have a protruding ventral apex. Glochidial shells (n = 60) measured 260.0 μm long (L) (±1.11 SE), 233.1 μm high (H) (± 1.32 SE), with a size of 246.6 μm (± 0.99 SE), hinge length (Hg) of 183.6 μm (± 0.99 SE), larval tooth length (LTL) of 53.6 μm (± 0.84 SE) and angle of obliquity (Á) of 12.9° (± 0.28 SE). Larval teeth are singular in each valve, lack microstylets, have convex or concave basal protuberances on opposing valves and terminate as blunt outward facing spoon-like to peg-like cusps. In comparison to Westralunio carteri, W. albertisi is smaller (d.f., 178; P < 0.001) for L (t = 33.85), H (t = 12.80), Size (t = 28.98), Hg (t = 21.32), H/L (t = −15.06) and Hg/L (t = −4.21). Westralunio albertisi also has a more acute Á than W. carteri (d.f., 71; t, 10.17; P < 0.001), but displays no difference in LTL (d.f., 6; t, 0.16, P = 0.44).
... Zotin (2018) also listed several of these manuscript names. In contrast, the European and North American literature has largely made no mention of Woodward's manuscript names (e.g., Huff et al. 2004;Graf & Cummings, 2006;Araujo et al., 2017;Lopes-Lima et al., 2018). The compendium of family-level names in the Bivalvia listed "Promargaritiferinae F.R. Woodward, 1994" as unavailable due to the absence of any description (Bouchet & Rocroi, 2010: 72, 124). ...
This paper supplements the biography of Fred Woodward (1939-2020), by adding 13 overlooked new taxa (10 species, 1 genus, and 2 family-level names) and by adding 51 overlooked publications, for a total of 93 publications. Woodward published primarily on Unionidae, Margaritiferidae, molluscan conservation, and molluscs as archaeological objects.
... Currently, the modern taxonomy of freshwater mussels does not rely on conchological features alone but rather on an integrative approach including other characters such as molecular and anatomical data (e.g. Prié and Puillandre, 2014;Lopes-Lima et al., 2017b, 2018b. Unfortunately, until now, there have been very few surveys and published molecular studies on freshwater mussels from the Eastern Mediterranean countries and the Middle East. ...
Located at the junction between Europe, Africa, and Asia, with distinct evolutionary origins and varied ecological and geographical settings, together with a marked history of changes in orogeny and configuration of the main river basins, turned the Eastern Mediterranean into a region of high diversity and endemism of freshwater taxa.
Freshwater mussels (Bivalvia, Unionidae) from the Western Palearctic have been widely studied in their European range, but little attention has been dedicated to these taxa in the Eastern Mediterranean region and their diversity and phylogeography are still poorly understood.
The present study aims to resolve the diversity, biogeography, and evolutionary relationships of the Eastern Mediterranean freshwater mussels. To that end, we performed multiple field surveys, phylogenetic analyses, and a thorough taxonomic revaluation. We reassessed the systematics of all Unionidae species in the region, including newly collected specimens across Turkey, Israel, and Iran, combining COI + 16S + 28S and COI phylogenies with molecular species delineation methods. Phylogeographical patterns were characterized based on published molecular data, newly sequenced specimens, and species distribution data, as well as ancestral range estimations.
We reveal that Unionidae species richness in the Eastern Mediterranean is over 70% higher than previously assumed, counting 19 species within two subfamilies, the Unioninae (14) and Gonideinae (5). We propose two new species, Anodonta seddoni sp. nov. and Leguminaia anatolica sp. nov. Six additional taxa, Unio delicatus stat. rev., Unio eucirrus stat. rev., Unio hueti stat. rev., Unio sesirmensis stat. rev., Unio terminalis stat. rev. removed from the synonymy of Unio tigridis, as well as Unio damascensis stat. rev. removed from the synonymy of Unio crassus, are re-described. The nominal taxa Unio rothi var. komarowi O. Boettger, 1880 and Unio armeniacus Kobelt, 1911 are proposed as new synonyms of Unio bruguierianus, and Anodonta cyrea Drouët, 1881 and Anodonta cilicica Kobelt & Rolle, 1895 as new synonyms of Anodonta anatina. Also, the presence of Unio tumidus in the Maritza River is confirmed. The phylogeographic patterns described here are interpreted concerning major past geological events.
Conservation needs and implications are presented, together with populations and species conservation priorities.
... This bivalve family evolved in East Asia in the Middle Jurassic [93,94], most probably, simultaneously with Margaritiferidae [95]. Researchers agree that both families had the same ancestor, a representative of the Triassic family Shifangellidae described on the basis of paleontological findings in Eastern China [94]. ...
Analysis of zoogeographic, paleogeographic, and molecular data has shown that the ancestors of many fresh-and brackish-water cold-tolerant hydrobionts of the Mediterranean region and the Danube River basin likely originated in East Asia or Central Asia. The fish genera Gasterosteus, Hucho, Oxynoemacheilus, Salmo, and Schizothorax are examples of these groups among vertebrates, and the genera Magnibursatus (Trematoda), Margaritifera, Potomida, Microcondylaea, Leguminaia, Unio (Mollusca), and Phagocata (Planaria), among invertebrates. There is reason to believe that their ancestors spread to Europe through the Paratethys (or the proto-Paratethys basin that preceded it), where intense speciation took place and new genera of aquatic organisms arose. Some of the forms that originated in the Paratethys colonized the Mediterranean, and overwhelming data indicate that representatives of the genera Salmo, Caspiomyzon, and Ecrobia migrated during the Miocene from the region of the modern Caspian through the Araks Strait, which existed at that time. From the Ponto-Caspian and the Mediterranean regions, noble salmon, three-spined stickleback, European pearl mussel, seals, and mollusks of the genus Ecrobia spread to the Atlantic Ocean and colonized the Subarctic and Arctic regions of Europe and North America. Our study indicates that the area of the former Paratethys retains its significance as a center of origin of new species and genera and that it has been the starting point of migration "corridors" up to the present time.
... a slightly more conservative confidence interval than Froufe et al. Originally, we tried to estimate divergences using fossil calibrations of Margaritiferidae taxa (Bolotov et al., 2016;Lopes-Lima et al., 2018), the sister family to Unionidae. However, the error estimates surrounding divergences within the L. teres species complex were so large the divergence dates were meaningless. ...
Aim
Freshwater mussels share habitat and are parasites of freshwater fishes during the larval life stage. Therefore, models of fish biogeography may also explain the historical biogeography of freshwater mussels. We tested this assumption using predictions of three biogeographic models constructed for northern Gulf of Mexico drainages on a freshwater mussel species complex. Specifically, we tested (1) if speciation was due to vicariant events of fluctuating sea levels that separated lineages east‐west of the Mobile Basin (Central Gulf Coast speciation hypothesis), (2) if the timing of divergences occurred 8.5–3.5 MYA (Gulf Coast allopatric speciation model) and (3) if diversification in Mississippi River populations was recent and for evidence of population increase consistent with range expansion into northern deglaciated regions (Pleistocene glaciation model).
Location
Eastern North America.
Taxon
Freshwater mussels (Bivalvia: Unionidae), Lampsilis teres and L. floridensis.
Methods
We collected 249 specimens from 73 localities across the group's distribution. We used three molecular markers (COI, NDI & ITSI) to conduct time calibrated Bayesian phylogenetic analyses, phylogeographic analyses (AMOVA & SAMOVA) and demographic analyses including Bayesian skyline plots.
Results
Lampsilis teres and L. floridensis are allopatric species whose distributions meet at the eastern edge of the Mobile Basin. Speciation was estimated to occur in the late Miocene. Populations from isolated river systems surrounding the Gulf of Mexico are almost all monophyletic. Mississippi drainage samples formed a shallow clade with recent diversification and showed evidence of recent population expansion.
Main conclusions
The historical biogeography of the L. teres species complex is broadly consistent with tested ichthyofaunal models. The timing of speciation and intraspecific divergences correspond to low sea‐level events suggesting that Gulf Coast sea‐level fluctuations are responsible for dispersal (sea‐level recession) and subsequent cladogenesis (sea‐level inundation). Consistent with numerous other freshwater studies, we found the Mobile Basin to be a suture zone, which may be due to the narrow, offshore continental shelf.
... The neutrality tests and mismatched distributions indicated that lineages A and B have experienced a recent expansion ( Table 2). The EBSP analysis also showed that S. yangtsekiense s.l. has undergone a rapid demographic expansion after the last glacial maximum (~15 kya; Figure 5), similar to that described for other freshwater species found in this region (Horreo et al., 2018;Li et al., 2014;Lopes-Lima et al., 2018;Salvi et al., 2014;Ling et al., 2012). Tajima's D, however, is not significantly negative, indicating that the population has undergone recent expansion after which it was subdivided, undergoing either an extensive migration and expansion and/or contraction (De Queiroz, 2007;Sharma et al., 2014;Wang & Ge, 2010). ...
Aim
The evolutionary importance of paleoclimate regimes has been noted in biogeographic studies. However, little is known about how paleoclimate differences shaped the biogeographic pattern and diversification history of the freshwater fauna in important zoogeographical boundary regions. Here, we aim to investigate how past regional climatic differences have shaped the biogeographic history of the inland aquatic fauna in China using an endemic freshwater crab species complex found on both sides of the Qinling Mountains–Huaihe River Line (QHL), a critical ecological boundary in eastern China, as a model system.
Location
Eastern China, the Qinling Mountains–Huaihe River Line.
Taxon
The Sinopotamon yangtsekiense species complex.
Methods
A total of 482 individuals of Sinopotamon yangtsekiense sensu lato were collected from 34 localities throughout its entire distributional range. The phylogeographic analyses of population structure, morphological and genetic variations, and demographic dynamics were made based on multiple mtDNA and nuDNA loci and on morphological traits. Fine‐tuned ecological niche modeling was used to reconstruct the location of climatically suitable areas that existed during the Last Glacial Maximum.
Results
The divergence of two freshwater crab lineages across the QHL correlated with significant past variations in monsoon intensity and with the location of multiple refuges. The divergence time was broadly consistent with the timing of the critical paleoclimate transition event in the mid‐Pleistocene (95% HPD, 0.48–1.06 Ma). Each freshwater crab lineage has evolved distinct male genital traits associated with their isolation in areas with different precipitation rates and temperatures in the past. The patterns of crab distribution observed today reflect past contractions of the two lineages in response to glacial and interglacial cycles during the Pleistocene, followed by their subsequent rapid expansion after the Last Glacial Maximum (~15 kya).
Main conclusions
Populations of the widespread species Sinopotamon yangtsekiense s.l. experienced a deep division in the past that led to the phylogeographical isolation observed today. The two main drivers of genetic isolation in this taxon were (a) differences in the intensity of the monsoons on each side of the QHL boundary during the mid‐Pleistocene, and (b) isolation of different populations of S. yangtsekiense s.l. in a number of separate refuges during the LGM.
... Margaritifera hembeli, Louisiana Pearlshell (Fig. 1c), is federally threatened under the U.S. Endangered Species Act and is restricted to three tributary drainages of the Red River in central Louisiana (Fig. 1;Smith 1988;Johnson and Brown 1998). Belonging to the family Margaritiferidae, M. hembeli is a morphologically and phylogenetically distinct group of mussels with only five extant North American representatives, much fewer than the 286 mussel species representing the family Unionidae (Bogan 2008;Lopes-Lima et al. 2018a). Margaritifera hembeli individuals are long lived (~ 45-75 years) and inhabit shallow, moderate velocity stream reaches with relatively stable substrates Brown 1998, 2000). ...
Margaritifera hembeli is a federally threatened freshwater mussel species restricted to three central Louisiana drainages. Currently, management efforts are being formulated without an understanding of population-level genetic patterns, which could result in sub-optimal conservation outcomes. In particular, information about riverscape genetic patterns is needed to design effective propagation and reintroduction plans. We apply a genomic approach (RADseq) to assess genetic diversity and structure among four wild populations sampled from across the species range. We also assess the genetic diversity of a captively reared cohort produced from a single female. We recovered population differentiation between individuals sampled to the north and south of the Red River. All sites had similarly low levels of heterogeneity and other measures of genetic diversity. The captive cohort displayed higher levels of genetic diversity than expected and likely represents a case of multiple paternity. Future propagation efforts will likely be able to produce genetically diverse cohorts from a small number of wild-caught females, and we recommend future reintroduction efforts utilize brooders within the sub-drainage closest to the reintroduction effort.
... The systematics of the family was recently redefined byLopes-Lima et al. (2018a). Three of the four margaritiferid species in the MB were reassigned to the genus Pseudunio (Margaritifera auricularia to Pseudunio auricularius, Margaritifera homsensis to Pseudunio homsensis, and Margaritifera marocana to Pseudunio marocanus). ...
• The five global Mediterranean‐climate regions are experiencing alarming rates of freshwater biodiversity loss. Although freshwater mussels are recognized as important functional components in aquatic ecosystems, and are among the most threatened faunal groups globally, there has been no synthesis of the plight of this group within these regions.
• Data from the International Union for Conservation of Nature (IUCN) Red List were reviewed to compare the conservation status, threats, and conservation actions needed for freshwater mussel species occurring in Mediterranean‐climate regions (med‐mussels) with those of other freshwater mussel species globally. The first comprehensive catalogue of med‐mussel species was compiled using existing taxonomic literature.
• There are 41 med‐mussel species, 30 of which occur in the Mediterranean basin. Many regions have just a single species, and regions where multiple species occur generally only have between one and four species per river basin. Med‐mussel species are almost twice as likely to be ‘Imperilled’, are affected by 2.4 times more threats, and require 3.5 times more conservation actions than non‐med mussels. In many cases, the exact threats have not been identified.
• In combination with low species richness, this level of imperilment means that Mediterranean‐climate regions are at risk of losing the benefits that mussels provide to broader ecosystem functioning. The conservation of med‐mussels can be improved by increasing our knowledge of species distributions, including the identification of cryptic species and significant management units, through population genetic work. In addition, recognizing the potential of ‘novel’ habitats and refuge areas could augment the management of this important functional group.
... The Gulf coastal drainages of Mexico south of the Rio Grande are a transition zone between the Nearctic and Neotropic realms and harbor unique assemblages of aquatic biota (Miller & Smith 1986). Freshwater mussels (Bivalvia: Unionida) have high species diversity in the Nearctic and Neotropic regions of North, Central, and South America (Graf & Cummings 2007;Bogan & Roe 2008;Lopes-Lima et al. 2018). The mussel fauna of Central America is highly endemic and is comprised of species in both Unionidae (94 spp.) and Mycetopodidae (8 spp.; Graf & Cummings 2007). ...
The Gulf coastal drainages of central Mexico are a faunal transition zone between North and South America and harbor a unique assemblage of freshwater mussels (Bivalvia: Unionida). However, little information is available regarding the taxonomy, distribution, and evolutionary history of the Mexican mussel fauna due to limited sampling over the last 100 years. To address these knowledge gaps, we evaluated species-level diversity in the genus Popenaias Frierson, 1927, in Mexican Gulf coastal drainages as part of a larger effort to inform conservation efforts for members of this genus both in Mexico and the United States of America. Based on our analyses, we describe Popenaias berezai n. sp. from the Río Valles of the Río Pánuco basin, San Luis Potosí, Mexico. We also provide presumptive distributional range, phylogenetic structure, and molecular and morphological diagnoses of the new species and provide comments on the other species currently in Popenaias. Our findings highlight the high levels of endemism among freshwater mussels in Mexican Gulf coastal drainages and will help guide impending conservation actions for P. popeii, which is listed as "endangered" in the United States.
... The freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) is listed as Critically Endangered in Europe by the IUCN (Moorkens et al., 2017). This bivalve has its taxonomy and evolution well studied (Lopes-Lima et al., 2018) as well as its abiotic tolerances (Varandas et al., 2013). Particular ecological traits and biotic interactions in M. margaritifera are well known since a significant amount of knowledge exists about their peculiar life cycle (i.e. the larva, glochidia, need a fish host to metamorphose into juveniles; Young, 2001, 2003). ...
European freshwater pearl mussel (Margaritifera margaritifera) populations are declining despite a growing effort to conserve them. Here we used a combination of local ecological knowledge (LEK) and field sampling to assess past and current distribution and conservation status of this endangered species in Cávado and Neiva Rivers (Portugal). We performed face-to-face interviews in both rivers and sampled the entire area where the respondents confirmed the historical presence of this species. Abiotic characterization, water quality and fish diversity were also assessed in both rivers. We found that freshwater pearl mussels are now possibly extinct in Cávado River but almost 50% of the respondents confirm its presence in the past, especially elders that lived in villages near its historical distribution. To the contrary, and although the species is still present in Neiva River, only 3.8% of the respondents remembered its presence in the past. In both rivers, respondents suggested pollution as the most important explanation for the freshwater pearl mussels decline. However, nowadays both rivers present excellent water quality and trout Salmo trutta (the freshwater pearl mussel fish host) is still abundant. Since we identified the areas where the species was present in a recent past, this information is vital for possible management actions with the aim of re-introduce or increase the abundance of M. margaritifera populations and/or for the rehabilitation of habitats in both rivers. We also highlight the vital importance of getting LEK, mainly from elders, in order to avoid shifting baseline syndromes and to get qualitative accurate information of past references and/or experience with historical conditions. Results reported here reinforce concern about the conservation status of freshwater pearl mussel populations in Portugal and can be used to guide future research and management initiatives to better conserve this species.
Mainland Southeast Asia, also known as Indochina, is recognized as a global biodiversity hotspot for freshwater mussels, hosting a significant number of species and exhibiting high levels of endemism. Recently, the monotypic genus Songkhlanaia was described from the Songkhla Lake Basin in southern Thailand. In this study, two additional lineages are revealed, S. moreleticomb. nov. and S. songkhramensissp. nov., from the Mekong Basin through an integrative taxonomic approach combining morphological characters and molecular phylogenetic analyses. The multi-locus phylogenetic inference supported the monophyly of the genus and further elucidated the sister relationship between S. moreleti and the new species, and with S. tamodienica positioned as a basal lineage. Pairwise uncorrected COI p-distances among these three species also supported the species validity and ranged from 4.2% to 8.24%. Notably, S. songkhramensissp. nov. and S. moreleti exhibit similarities in shell morphology; however, the new species can be differentiated by more robust pseudocardinal teeth. Both species are distinguishable from S. tamodienica by their approximately twice larger size, more inflated shells, and more prominent, roughened, irregular growth lines on the shell surface. Furthermore, based on the current data, these three species are recognized as endemic and are restricted to disjunct biogeographic areas in Indochina: S. tamodienica in the Songkhla Lake Basin in southern Thailand, S. moreleti in the Tonle Sap and Lower Mekong basins, and S. songkhramensissp. nov. in the Songkhram Basin and its nearby tributaries of the Middle Mekong Basin.
Here, we present a synthesis of the available knowledge on the Giant Freshwater Pearl Mussel Pseudunio auricularius (= Margaritifera auricularia) (Spengler, 1793). We also identify critical knowledge gaps that require attention for effective conservation guidance and species recovery. Pseudunio auricularius is one of Europe’s most endangered invertebrate species, with its range having been reduced by over 90% in the last two centuries. Long thought to be extinct, it was rediscovered in Spain and France in the 1990s–2000s, but these populations are in a very critical situation. Pseudunio auricularius lives in gravelly, stable and well-oxygenated sediments. Larvae (glochidia) attach to fish gills to complete their life cycle. The primary host fish, the Atlantic sturgeon Acipenser sturio, now extinct in European rivers, Salaria fluviatilis in Spain and Petromyzon marinus in France, are threatened. Other stressors are the deterioration of mussel habitats and water quality, climate change and invasive species such as Corbicula spp. The earliest life stages are most vulnerable, further ecological studies are urgently needed. Monitoring and conservation measures such as captive breeding will continue in both countries. Catchment-wide restoration of river morphodynamics and water quality is needed to allow the re-establishment of this emblematic species and its host fishes.
In recent years, the classification system of Unionoida (Margaritiferidae, Unionidae) has undergone major changes from conventional methods by shell morphology, due to breakthroughs in approaches based on molecular phylogenetic analysis. We compared the classification system trends of the Margaritiferidae and Unionidae distributed in Japan, and pointed out that there is a time lag to the classification determinations of the latter. Although the scientific names have been changed, the existence, distribution, and ecological information (ex. host fish for glochidia) of two Japanese margaritiferids have been established, and conservation measures and regulations based on the Red List and laws can be expected. On the other hand, the Unionidae consisted of 3 subfamilies, 11 genera and 15 species has increased to 2 subfamilies, 13 genera and 26 species (excluding alien species) by the new classification system reported in 2020. Therefore, information on the distribution and ecology of many new species must be elucidated. A new classification system will be assumed the further revision, especially for the genus Sinanodonta, and the risk of some local populations extinction increase before clarifying the actual situation of species. We are now proceeding to clarify the early life stage of some Unionoida mussels (ex. parasitic stage, salinity tolerance), but insufficient knowledge of the life cycle of Unionoida has prevented the establishment of complete ex-situ conservation methods. Conversion project of numerous reservoirs are that the most important habitats for Unionidae species pressing forward in Japan. In light of this situation, it is hoped that the new classification system that can serve as a basis for on-site conservation will spread throughout as soon as possible to realize comprehensive conservation.
The basic knowledge of freshwater bivalves in the Unionida in some regions of the world is still limited, hindering potential conservation efforts, including in Vietnam. A subset of these mussels, the freshwater bivalve tribe Anodontini, is especially difficult to properly identify morphologically due to intraspecific shell similarity. This study aims to define the species of Anodontini in Vietnam and describe their evolutionary relationships and distributions by estimating phylogenies and analyzing collected specimens. The Anodontini are represented in Vietnam by five species divided among three genera: Sinanodonta, Cristaria, and Pletholophus. Sinanodonta woodiana, a large species complex, is represented in Vietnam by Sinanodonta jourdyi. Cristaria is confirmed to include the widespread Cristaria plicata and substantiates the validity of Cristaria truncata. Finally, Pletholophus is here recognized as distinct from Cristaria, containing two species in Vietnam, Pletholophus tenuis, and a species new to science. Our study is an important baseline for future studies on Vietnamese freshwater mussels and highlights the importance of surveys, molecular work, and taxonomic expertise to describe the biodiversity of understudied regions.
Contiguous assemblies are fundamental to deciphering the composition of extant genomes. In molluscs, this is considerably challenging owing to the large size of their genomes, heterozygosity, and widespread repetitive content. Consequently, long-read sequencing technologies are
fundamental for high contiguity and quality. The first genome assembly of Margaritifera margaritifera (Linnaeus, 1758) (Mollusca: Bivalvia: Unionida), a culturally relevant, widespread,
and highly threatened species of freshwater mussels, was recently generated. However, the resulting genome is highly fragmented since the assembly relied on short-read approaches. Here, an improved reference genome assembly was generated using a combination of PacBio CLR long reads and Illumina paired-end short reads. This genome assembly is 2.4 Gb long, organized into 1,700 scaffolds with a contig N50 length of 3.4 Mbp. The ab initio gene prediction resulted in 48,314 protein-coding genes. Our new assembly is a substantial improvement and an essential resource for studying this species’ unique biological and evolutionary features, helping promote its conservation.
This Ph.D. Thesis arose with the aim to understand and provide solutions for culturing the endangered Freshwater Pearl Mussel during its parasitic stage in the Atlantic salmon. To optimize the production of young mussels and preserve fish
health, the morphopathological pattern of glochidiosis was characterized during the early and late stages of glochidiosis and related to the larval development and metamorphosis of Margaritifera margaritifera, from glochidium to post-larva. The
results here enclosed contribute to a better understanding of the pathogenesis of glochidiosis that may aid to manage the parasitic stage during the culture of freshwater mussels.
Viruses in the family Rhabdoviridae display remarkable genomic variation and ecological diversity. This plasticity occurs despite the fact that, as negative sense RNA viruses, rhabdoviruses rarely if ever recombine. Here, we describe nonrecombinatorial evolutionary processes leading to genomic diversification in the Rhabdoviridae inferred from two novel rhabdoviruses of freshwater mussels (Mollusca: Bivalvia: Unionida). Killamcar virus 1 (KILLV-1) from a plain pocketbook (Lampsilis cardium) is closely related phylogenetically and transcriptionally to finfish-infecting viruses in the subfamily Alpharhabdovirinae. KILLV-1 offers a novel example of glycoprotein gene duplication, differing from previous examples in that the paralogs overlap. Evolutionary analyses reveal a clear pattern of relaxed selection due to subfunctionalization in rhabdoviral glycoprotein paralogs, which has not previously been described in RNA viruses. Chemarfal virus 1 (CHMFV-1) from a western pearlshell (Margaritifera falcata) is closely related phylogenetically and transcriptionally to viruses in the genus Novirhabdovirus, the sole recognized genus in the subfamily Gammarhabdovirinae, representing the first known gammarhabdovirus of a host other than finfish. The CHMFV-1 G-L noncoding region contains a nontranscribed remnant gene of precisely the same length as the NV gene of most novirhabdoviruses, offering a compelling example of pseudogenization. The unique reproductive strategy of freshwater mussels involves an obligate parasitic stage in which larvae encyst in the tissues of finfish, offering a plausible ecological mechanism for viral host-switching. IMPORTANCE Viruses in the family Rhabdoviridae infect a variety of hosts, including vertebrates, invertebrates, plants and fungi, with important consequences for health and agriculture. This study describes two newly discovered viruses of freshwater mussels from the United States. One virus from a plain pocketbook (Lampsilis cardium) is closely related to fish-infecting viruses in the subfamily Alpharhabdovirinae. The other virus from a western pearlshell (Margaritifera falcata) is closely related to viruses in the subfamily Gammarhabdovirinae, which until now were only known to infect finfish. Genome features of both viruses provide new evidence of how rhabdoviruses evolved their extraordinary variability. Freshwater mussel larvae attach to fish and feed on tissues and blood, which may explain how rhabdoviruses originally jumped between mussels and fish. The significance of this research is that it improves our understanding of rhabdovirus ecology and evolution, shedding new light on these important viruses and the diseases they cause.
Freshwater mussels are essential for the integrity of freshwater ecosystems but numbers of these organisms are declining rapidly at regional and global scales. The phylogenetic and biogeographic aspects of the rich unionoid fauna of the Indo-Burma region are becoming increasingly well understood. Guangxi is part of the Chinese portion of the Indo-Burma biodiversity hotspot but regional studies of the freshwater mussel diversity are scarce. In this study, we report a new genus and species of freshwater mussel from Guangxi, China. Genetic datasets including three genes (COI, 16S rRNA and 28S rRNA) and complete maternal mitogenomes were compiled to infer the phylogenetic history of the group. Molecular phylogenetic analyses showed that the new species formed a monophyletic group and was closely related to Obovalis and Ptychorhynchus in the tribe Gonideini of the subfamily Gonideinae. Morphological and molecular evidence supported that these specimens represent an undescribed genus and species that we describe as Postolata guangxiensisgen. nov., sp. nov. The discovery of this new taxon adds to the known level of endemism of freshwater mussels in Guangxi and a detailed survey of uncharted areas should reveal new diversity in the future. We also suggest that complete mitogenomes or even genome-scale nuclear data should be used for phylogenetic reconstructions when proposing major taxonomic changes.
ZooBank: urn:lsid:zoobank.org:pub:76FC5A1D-7507-4F26-A12C-EC08AB333274
The freshwater mussel Westralunio carteri (Iredale, 1934) has long been considered the sole Westralunio species in Australia, limited to the Southwest and listed as vulnerable on the IUCN Red List and under Australian legislation. Here, we used species delimitation models based on COI mtDNA sequences to confirm existence of three evolutionarily significant units (ESUs) within this taxon and conducted morphometric analyses to investigate whether shell shape differed significantly among these ESUs. “W. carteri” I was found to be significantly larger and more elongated than “W. carteri” II and “W. carteri” II + III combined, but not different from “W. carteri” III alone. We recognise and redescribe “W. carteri” I as Westralunio carteri (Iredale, 1934) from western coastal drainages and describe “W. carteri” II and “W. carteri” III as Westralunio inbisi sp. nov. from southern and lower southwestern drainages. Two subspecies are further delineated: “W. carteri” II is formally described as Westralunio inbisi inbisi subsp. nov. from southern coastal drainages, and “W. carteri” III as Westralunio inbisi meridiemus subsp. nov. from the southwestern corner. Because this study profoundly compresses the range of Westralunio carteri northward and introduces additional southern and southwestern taxa with restricted distributions, new threatened species nominations are necessary.
This paper discusses the life and works of Richard Irwin Johnson (1925-2020), who made significant contributions to our knowledge of the Unionidae (Mollusca: Bivalvia) through his numerous publications and his curation of the sizable collections of freshwater bivalves at the Museum of Comparative Zoology, Harvard University. Johnson also published extensively on the history of malacology, including biographical accounts and museum histories. His 135 publications on mollusks spanned 74 years (from 1941 at age 16 to 2015 at age 90), nearly setting a record for malacology, and his membership in the American Malacological Union / Society for 79 years (1941 to 2020) outlasted any other current or former member. Johnson amassed one of the largest ever private libraries of books and journals on mollusks, and contributed significantly to the growth of the MCZ Malacology Library.
Molluscs are among the most diverse and widespread animal groups in freshwater habitats. Unfortunately, like most freshwater taxa, they are decreasing dramatically and are now among the most threatened animals on Earth, with many species already extinct or on the brink of extinction. Here, we review our current knowledge on the biodiversity and conservation of freshwater molluscs using the concept of knowledge shortfalls. We focus on seven previously proposed key shortfalls to review and analyse existing knowledge gaps relating to (1) taxonomy, the Linnean Shortfall; (2) distribution, the Wallacean Shortfall; (3) abundance and population dynamics, the Prestonian Shortfall: (4) evolution, the Darwinian Shortfall; (5) abiotic tolerances, the Hutchinsonian Shortfall; (6) traits, the Raunkiaeran Shortfall; and (7) biotic interactions, the Eltonian Shortfall. In addition, we address a new shortfall, which relates to the application and effectiveness of conservation measures, including assessments, methods, funding, and policies, the Ostromian Shortfall. Based on our review, we provide recommendations and suggest pathways to overcome these existing shortfalls. This work also introduces the articles in this special issue of Hydrobiologia, which represent key contributions to the First International Freshwater Mollusk Conservation Society Meeting held in Verbania, Italy, in 2018.
The objective of this review is to update our previously published checklist of Recent freshwater mussel species and genera (Graf & Cummings, 2007, J. Molluscan Stud.: 291–314) to reflect the new data and research findings that have accumulated over the last decade. The MUSSEL Project Database was developed to synthesize the available taxonomic nomenclature, species ranges and published taxonomic hypotheses on genus–species combinations and synonymy. We have found 4,988 available species-group level nominal species representing 958 valid species in 192 genera worldwide, an increase of 118 species since 2007. The current patterns of species richness are discussed with regard to both taxonomy and geography, as is the general flux in the number of species recognized over time. A checklist is provided herein, with a bibliography to key faunistic and taxonomic references. The full dataset is maintained and updated on the MUSSEL Project Web Site (http://mussel-project.net/).
Species are a fundamental unit of biology, and defining accurate species boundaries is integral to effective conservation and management of imperiled taxa. Freshwater mussels (Bivalvia: Unionidae) are among the most imperiled groups of organisms in North America, yet species boundaries remain uncertain for many taxa. The False Spike, Fusconaia mitchelli (Simpson in Dall, 1895), is a freshwater mussel considered to be endemic to central Texas (Brazos, Colorado, and Guadalupe drainages). Recent research revealed significant intraspecific genetic variation between geographically separated populations of F. mitchelli, which could be indicative of speciation; however , small sample sizes for several of the populations precluded formal taxonomic revision. Here, we increase taxon sampling and use multilocus DNA sequence data and traditional morphometrics to re-evaluate species boundaries in F. mitchelli. We sequenced three loci: the protein-coding mitochondrial DNA genes cytochrome c oxi-dase subunit 1 and NADH dehydrogenase 1, and the nuclear internal transcribed spacer 1. Phylogenetic analyses depicted deep genetic divergence between F. mitchelli in the Guadalupe and those in the Brazos and Colorado drainages, which was further supported by available biogeographic information. Morphometric analyses and coa-lescent-based species delimitation models integrating both DNA sequence and morphological data provided strong support for the divergence observed between the two geographically isolated clades of F. mitchelli. Based on these results, we revise taxonomy accordingly by elevating the junior synonym Fusconaia iheringi (Wright, 1898) to represent the Brazos and Colorado populations and restrict the distribution of F. mitchelli to the Guadalupe River drainage. Our findings may impact pending management decisions to protect F. mitchelli under the U.S. Endangered Species Act.
Doubly uniparental inheritance (DUI) is a mode of inheriting mitochondrial DNA that is distinct from strictly maternal inheritance. It has been described in nine and three families of marine and freshwater mussels, respectively, including the European margaritiferids and unionids. Among the 16 freshwater species of Unionida inhabiting Europe, DUI has been described in 9 species of dioecious mussels and was absent from a single hermaphroditic species and from secondary hermaphroditic specimens. The DUI freshwater mussels include two vastly genetically different mitochondrial genomes: maternal (F genome) and paternal (M genome), which coexist within the same specimen but in different tissues. The F genome is present in all female tissues and somatic male tissues. It is inherited in the typical, maternal, manner. Conversely, the M genome is located primarily in the male gonads and generative cells, and is inherited paternally. Dioecious Unionidae display unique characteristics that have been interrelated for over 200 million years: a high fidelity of the transmission of the F and M genomes in DUI and two paths of spermatogenesis–the typical path that produces sperm cells containing mitochondria with the F genome and the atypical path that produces sperm cells with the M genome. The mitogenomes of freshwater mussels display unique features that are not present in any other animal, that is, an additional, gender‐specific gene and an elongated cox2 gene occurring exclusively in the M genome. These features mean that the mitochondria, in addition to their basic function of producing energy, also may take part in determining sex in these dioecious organisms.
Populations of the critically endangered freshwater mussel Pseudunio auricularius (Spengler, 1793) have been suffering sharp declines, particularly in the Ebro basin (Iberian Peninsula). Among other factors, pollution could be responsible for these declines. We conducted, for the first time, acute toxicological tests (96 h) with heavy metals and ammonia on P. auricularius juveniles. The resulting LC50 values, in decreasing order of sensitivity, were: Cd = 38.85 µg/L, Cu = 58.64 µg/L, Ni = 124.60 µg/L, Zn = 267.40 µg/L, Cr(III) > 1000 µg/L, Pb > 2000 µg/L and total ammonia nitrogen (TAN) = 7.53 mg/L. We also report the estimated LC10, NOEC, LOEC and MATC values, which may be used to determine safer habitat conditions. Finally, we compare the obtained LC50 values with the concentrations of the toxicants in natural habitats where the species is present. Overall, the results reported here could be used to implement effective conservation actions, such as relocation of specimens to less-polluted sites or reduction of the concentration of pollutants in disturbed habitats. Considering the lack of ecotoxicological studies on freshwater mussels in Europe, this study may also be useful to establish toxicological reference limits for this imperiled faunal group.
Freshwater ecosystems are the most vulnerable worldwide and freshwater bivalves rank amongst the most threatened animals in the world. Surveying and monitoring freshwater bivalves are difficult tasks: they are difficult to find, hard to identify (taxonomic expertise is needed), and working underwater is technically challenging. It is therefore crucial to find more efficient methods to survey and monitor these species. Here, we present the first metabarcoding approach for freshwater bivalves and compare environmental DNA (eDNA) and traditional surveys. We describe two sets of primers (for Unionida and Venerida) developed for freshwater bivalves eDNA metabarcoding. These primers have been tested in the field, with about 300 studied sites. Results were compared to freshwater bivalves’ surveys using traditional methods, with eDNA always detecting more species than traditional surveys, especially when Sphaerids were taken into account. While our study initially focused on Western Palearctic freshwater bivalve species, our primers were confronted in silico with available sequences and have proven to be effective at a global scale. The results show that eDNA metabarcoding, with our developed primers, is a remarkable tool allowing for non-invasive surveys, detection of rare and inconspicuous species, absence data and overall freshwater bivalves routine monitoring.
Vietnam has the second highest diversity of freshwater mussels (Unionida) in Asia after China. The purpose of this paper is to compile an up-to-date list of the modern unionid fauna of Vietnam and its current conservation status. Unfortunately, there has been relatively little research on this fauna in Vietnam. Fifty-nine species of Unionida have been recorded from Vietnam based on literature, museum records, and our fieldwork. Fifty were assessed in the International Union for Conservation of Nature (IUCN) Red List 2016 in the IUCN categories of Critically Endangered (four species, 6.8%), Endangered (seven species, 12%), Vulnerable (one species, 1.7%), Near Threatened (two species, 3.4%), Least Concern (23 species, 39%), Data Deficient (11 species, 18.6%), and Not Evaluated (11 species, 18.6%). Considering the impacts of pollution, timbering, agriculture, and damming of rivers, research on the diversity and conservation status of freshwater mussels is very urgently needed to propose specific conservation measures for these species in Vietnam. If all taxa listed as Data Deficient are found to be threatened, with around 42% of species threatened, this fauna would be one of the most threatened freshwater molluscan faunas in Asia.
The critically endangered Giant Freshwater Pearl Mussel Margaritifera auricularia was presumed extinct before its rediscovery in Spain in 1985 and France in 2000. Since then, numerous surveys have been set up to search for living populations in France and Spain. This article presents an up-to-date account of species distribution based on available data, i.e. the literature, museum collections and recent field surveys, and provides unpublished molecular data for France. There are still three populations of the Giant Freshwater Pearl Mussel in the Ebro River in Spain, and eight populations in France (two in the Loire watershed, one in the Charente watershed, two in the Garonne watershed and three in the Adour watershed). The biggest population lives in the Charente River with an estimated 100,000 individuals. Recruitment is very scarce in all populations but living specimens estimated to be less than 10 years old have been found in the Ebro in Spain and in the Vienne, Charente, Dronne and Adour rivers in France. The recent rediscovery of populations in France was mainly a result of intensive dedicated surveys including scuba diving. Subsequent advances in knowledge show how large rivers and downstream ecosystems remain a terra incognita for the hydrobiologist.
The Tethys Ocean existed between the continents of Gondwana and Laurasia from the Triassic to the Pliocene. Analyses of multiple biogeographic and phylogenetic histories reveal that the subsequent breakup of the Tethys greatly influenced the distributions of many species. The ancestral Tethyan realm broke into five biogeographic provinces, including the present-day East Pacific, West Atlantic, East Atlantic, Mediterranean Sea, and Indo-West Pacific. Palaeogeographic maps illustrate the Mesozoic Atlantic opening, the Cenozoic closure of the Tethys, the Messinian Salinity Crisis, the mid-Miocene closure of the Central American Seaway, and Quaternary geological changes. Further, we consider Cenozoic sea-level changes and the formation of freshwater habitats. These reconstructions allow assessment of patterns of aquatic diversification for marine and freshwater animals, and comparison of vicariance and dispersal processes. Estimated divergence times indicate that fragmentation of the Tethys was responsible for the vicariant speciation of aquatic animals because these dates are consistent with associated tectonic events. The opening of the Atlantic Ocean during the Cretaceous is responsible for the earliest isolation between the West and East Atlantic. The mid-Miocene closure of the Tethys, which blocked global equatorial currents, appears to have isolated the Atlantic/Mediterranean Sea and Indo-West Pacific. Finally, formation of the Isthmus of Panama isolated East Pacific and West Atlantic marine organisms. Dispersals related to the Messinian Salinity Crisis and Quaternary sea-level changes influenced population structuring. Tethyan changes affected marine habitats, created new freshwater habitats, inland caves and ancient lakes along the Alps and Himalayas, and influenced anchialine caves at the edge of the ancient sea. The extensive new habitats provided opportunities for colonisation and rapid diversification. Future work should focus on testing the biological impact of the series of Tethyan changes.
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.
The freshwater pearl mussel Margaritifera marocana (Pallary, ) is an endemic species of Morocco being listed as critically endangered and it stands among the world's 100 most threatened species. An extensive survey was performed in the Sebou basin (total area of approximately 40,000 km ² ), covering 26 different sites. Margaritifera marocana was found only in four sites limited to a small tributary (Oued (=River) Bouhlou).
This population has a very restricted distribution (no more than 4 km of river length) but appears stable with recent recruitment, since small specimens were found.
Genetic analyses were performed, showing that this population has a similar diversity to that found in the River Laabid (Oum Er Rbia basin), but represents a distinct conservation unit that should be managed independently.
Although this study adds a new population to the current known distribution of M. marocana , urgent conservation measures (e.g. extension of the Tazzekka National Park; better management of river flow; increase of the riparian vegetation in some stretches; establishment of national and international legislation, and engagement of local citizens) are needed given the species' restricted distribution, its rarity, and the numerous threats that impair its future survival.
Since Margaritifera marocana (Pallary, 1918) and M. laosensis (Lea, 1863) were rediscovered, M. homsensis (Lea, 1865) remains the only pearl mussel species known solely based on old shell samples from natural history museums. This is also the last pearl mussel species, which is absent in a phylogeny of the family. Here, we aimed to provide an integrative revision of the taxonomic status of M. homsensis from the Orontes Basin. Using a newly collected specimen from the River Karasu, Hatay Province, southern Turkey, five gene partitions were sequenced, the cytochrome c oxidase subunit I (COI), large ribosomal subunit rRNA (16S), large ribosomal subunit rDNA (28S) and its D3 expansion segment (D3), and small ribosomal subunit rDNA (18S). The multi-gene phylogeny indicates that M. homsensis is a sister taxon of M. auricularia, but both these species are closely related to M. marocana by nuclear genes. The main conchological features, i.e., the shell shape, teeth morphology, and mantle attachment scars, as well as Fourier shell shape analysis have not shown principal differences between M. homsensis and M. auricularia. Based on these data, we concluded that M. homsensis is a valid species that is most closely related to M. auricularia. Special conservation efforts for a population of M. homsensis discovered in Turkey, including the formation of a nature reserve, might contribute to the conservation of the species. Finally, an extensive search for surviving populations in Orontes drainage (southern Turkey, Lebanon, and Syria) and the Nahr-el-Kabir River (Lebanon and Syria) remains necessary to develop a transboundary conservation strategy for this unique taxon.
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.
DAMBE is a comprehensive software workbench for data analysis in molecular biology, phylogenetics and evolution. Several important new functions have been added since version 5 of DAMBE: 1) comprehensive genomic profiling of translation initiation efficiency of different genes in different prokaryotic species, 2) a new index of translation elongation (ITE) that takes into account both tRNA-mediated selection and background mutation on codon-anticodon adaptation, 3) a new and accurate phylogenetic approach based on pairwise alignment only, which is useful for highly divergent sequences from which a reliable multiple sequence alignment is difficult to obtain. Many other functions have been updated and improved including PWM for motif characterization, Gibbs sampler for de novo motif discovery, hidden Markov models for protein secondary structure prediction, self-organizing map for non-linear clustering of transcriptomic data, comprehensive sequence alignment and phylogenetic functions. DAMBE features a graphic, user-friendly and intuitive interface, and is freely available from http://dambe.bio.uottawa.ca.
The unionid family Margaritiferidae, comprising 12 extant species, is widely distributed across the northern hemisphere in North America, Europe and Asia (Bolotov et al., 2016). Most species in this family have dramatically declined over the last century, with nine out of the 12 species assessed as threatened in the most recent IUCN Red List (IUCN, 2016). Among these is the Moroccan pearl mussel Margaritifera marocana (Pallary, 1918), considered one of the 100 most threatened species on the planet (Baillie & Butcher, 2012). This species is now restricted to two small streams in the Oum Er Rbia and Sebou basins and conservation measures are urgently needed (Sousa et al., 2016). Beyond the conservation concern, Unionida are also biologically interesting. They present an unusual mechanism of mitochondrial inheritance called doubly uniparental inheritance (DUI), in which all individuals have the typical maternally transmitted mtDNA (F-type), but the males possess in their germ cells a paternally inherited mtDNA instead (M-type) (Zouros et al., 1994; Breton et al., 2009). So far, DUI has been observed in over 100 species from four bivalve orders (Gusman, Azuelos & Breton, 2017), including three families within Unionida, i.e. Unionidae, Hyriidae and Margaritiferidae (Walker et al., 2006). However, to date, no whole M-type mitogenome has been published for any species belonging to the last two of these families.
The gene arrangement within mitogenomes is highly conserved in many taxonomic groups. For example, most vertebrates share the same gene order (Pereira et al., 2000). In other faunal groups, like Bivalvia, the mitochondrial genome arrangement is more variable, although not many distinct gene orders have been described so far (Serb & Lydeard, 2003). Still, in unionoids, mitogenome rearrangements seem to be rare events that are unlikely to be homoplastic. In this context, mitogenome gene order might be used as an additional character for phylogenetic inference. However, its utility for the Unionida phylogeny has never been tested.
The order Unionida has six recognized families with around 800 species (Lopes-Lima et al., 2014), but the phylogenetic relationships among these families are still not fully resolved (Graf, 2013). This lack of coherence among studies has been consistently attributed to the low number of molecular markers used and insufficient taxon sampling (Bogan & Roe, 2008; Graf, 2013; Fonseca et al., 2016).
Under the above-mentioned assumptions the aims of the present study are to (1) sequence and analyse the whole M- and F-type mitogenomes of Margaritifera marocana, (2) infer the phylogenetic relationships among Unionoidea species using all both the F- and M-type mtDNA sequences publicly available and (3) determine the gene order of all analysed mitogenomes and evaluate its phylogenetic utility.
results of two weeks of fieldwork in northern Vietnam collecting the first live specimens of two species of unionids not seen in several decades.
The family Margaritiferidae is a small but widely distributed group within the Unionoida, or freshwater mussels, whose taxonomy and systematics has been the subject of numerous publications. Despite several efforts, there is no consensus on which characters reliably diagnose this family. Herein, we present the results of a phylogenetic analysis of the most comprehensive data set for Margaritiferidae in terms of taxa and phylogenetic markers assembled to date, including eleven out of the twelve margaritiferid species currently considered valid. In addition, we review the fossil record of the family and attempt to integrate fossil and DNA sequence data to provide a diagnosis of Margaritiferidae, identify its origin and biogeographic patterns, and determine the systematic relationships of its constituent species and their taxonomic affinities. We assembled a molecular data set comprised of five markers: COI, 16S, 28S, 18S and histone 3 for a total of 59 specimens representing eleven species of Margaritifera. Our results indicate that the family Margaritiferidae is a monophyletic group comprised of the single genus Margaritifera, which includes the following 12 species: M. dahurica, M. margaritifera, M. monodonta, M. middendorffi, M. laevis, M. marrianae, M. hembeli, M. falcata, M. laosensis, M. auricularia and M. marocana plus the unstudied M. homsensis. Estimates of divergence times using fossil calibrations or mean substitution rates produced dramatically different results. Divergence estimates based on the fossil calibrations were 10 times higher than those obtained applying the mean substitution rates. The current distribution of the family implies dispersal across marine or brackish waters by their host fish, leaving a fossil record on four continents that dates to the Mesozoic. Margaritiferidae appear to be derived from putative ancestor in the Silesunionidae, with a likely origin in Asia. We suggest that Margaritiferidae had spread along the Tethys margins and crossed the Atlantic already in the Late Triassic or Early Jurassic. Further dispersal events, in the Late Cretaceous or Eocene, may be linked to salinity-depleted coastal waters or freshwater layering.
Freshwater mussels of the Order Unionida provide important ecosystem functions and services, yet many of their populations are in decline. We comprehensively review the status of the 16 currently recognized species in Europe, collating for the first time their life-history traits, distribution, conservation status, habitat preferences, and main threats in order to suggest future management actions. In northern, central, and eastern Europe, a relatively homogeneous species composition is found in most basins. In southern Europe, despite the lower species richness, spatially restricted species make these basins a high conservation priority. Information on freshwatermussels in Europe is unevenly distributed with considerable differences in data quality and quantity among countries and species. To make conservation more effective in the future, we suggest greater international cooperation using standardized protocols and methods to monitor and manage European freshwater mussel diversity. Such an approach will not only help conserve this vulnerable group but also, through the protection of these important organisms, will offer wider benefits to freshwater ecosystems.
A total of 209 bivalve generic (subgeneric) and 19 familial (subfamilial) names first proposed by Chinese palaeontologists and published in China are treated herein as an annotated database. The present paper is designed especially for the Treatise on Invertebrate Paleontology Bivalvia revision project, because access to bivalve taxa published by Chinese authors in China has been difficult for non-Chinese researchers. The original diagnoses of these taxa, including the original descriptions and explanation of figures of all the type species, have been translated from Chinese into English, so that non-Chinese colleagues can more easily have access to them.
Bivalves are ubiquitous members of freshwater ecosystems and responsible for important functions and services. The present paper revises freshwater bivalve diversity, conservation status and threats at the global scale and discusses future research needs and management actions. The diversity patterns are uneven across the globe with hotspots in the interior basin in the United States of America (USA), Central America, Indian subcontinent and Southeast Asia. Freshwater bivalves are affected by multiple threats that vary across the globe; however, pollution and natural system (habitat) modifications being consistently found as the most impacting. Freshwater bivalves are among the most threatened groups in the world with 40% of the species being near threatened, threatened or extinct, and among them the order Unionida is the most endangered. We suggest that global cooperation between scientists, managers, politicians and general public, and application of new technologies (new generation sequencing and remote sensing, among others) will strengthen the quality of studies on the natural history and conservation of freshwater bivalves. Finally, we introduce the articles published in this special issue of Hydrobiologia under the scope of the Second International Meeting on Biology and Conservation of Freshwater Bivalves held in 2015 in Buffalo, New York, USA.
The family Margaritiferidae encompasses 12 valid species, which are distributed widely but disjunctively in the Northern Hemisphere. A lack of a well resolved and temporally calibrated phylogenetic framework of Margaritiferidae has made it difficult to discuss the evolutionary pattern and process. Phylogenetic relationships between five major clades, which were revealed in earlier studies, remain elusive and unresolved. Lamprotula rochechouartii has long been classified within the family Unionidae based on shell morphology, but our preliminary molecular study on this species made us hypothesize that it has an affinity with margaritiferids. Hence, five loci (COI, 16S, 18S, 28S and histone H3) were used to investigate the phylogenetic position of L. rochechouartii and intra-familial relationships within Margaritiferidae using various partitioning strategies. Moreover, two mitochondrial genomes were newly obtained to further resolve and validate the five-clade relationships within Margaritiferidae in a broad view of Unionoida evolution. Both five-gene and mitogenome datasets strongly advocated treating Lamprotula rochechouartii as Margaritifera rochechouartiicomb. nov. Maximum likelihood and Bayesian inference analyses using partitioned five-gene dataset resulted in various topologies, but five well-supported clades were obtained. The most probable cladistic relationships generated by five-gene dataset analyses were identical to subsequent whole mitogenome analyses except the position of M. monodonta. M. rochechouartii and M. laosensis had a well-supported sister relationship and formed a basal clade splitting from the rest of the family. Based on six reliable fossils, crown age of the extant Margaritiferidae was estimated during the Late Cretaceous at 88.3 Ma (95% HPD = 66.2-117.4). But we hypothesized a much earlier origin of this family due to the Permian stem age (mean = 257 Ma, 95% HPD = 230.0-296.0) and a high extinction rate in the whole order. Biogeographic scenarios supported a Laurasian origin of extant Margaritiferidae during the Late Cretaceous, and suggested that Asian margaritiferids may have had two origins, having either Asia (M. rochechouartii, M. laosensis) or North America (M. dahurica, M. laevis, and M. middendorffi) as ancestral. The newly added Margaritiferidae species M. rochechouartii expands our recognized distribution range of modern margaritiferids. Our results indicate that whole mitogenome sequences can be used to reconstruct robust phylogenetic relationships for freshwater mussels, especially with the help of adding M-type mitogenomes.
The TethysOcean existed between the continents of Gondwana and Laurasia from the Triassic to the Pliocene. Analyses
of multiple biogeographic and phylogenetic histories reveal that the subsequent breakup of the Tethys greatly influenced
the distributions of many species. The ancestral Tethyan realm broke into five biogeographic provinces, including the
present-day East Pacific, West Atlantic, East Atlantic, Mediterranean Sea, and Indo-West Pacific. Palaeogeographic
maps illustrate the Mesozoic Atlantic opening, the Cenozoic closure of the Tethys, the Messinian Salinity Crisis, the
mid-Miocene closure of the Central American Seaway, and Quaternary geological changes. Further, we consider
Cenozoic sea-level changes and the formation of freshwater habitats. These reconstructions allow assessment of patterns
of aquatic diversification for marine and freshwater animals, and comparison of vicariance and dispersal processes.
Estimated divergence times indicate that fragmentation of the Tethys was responsible for the vicariant speciation of
aquatic animals because these dates are consistent with associated tectonic events. The opening of the Atlantic Ocean
during the Cretaceous is responsible for the earliest isolation between the West and East Atlantic. The mid-Miocene
closure of the Tethys, which blocked global equatorial currents, appears to have isolated the Atlantic/Mediterranean
Sea and Indo-West Pacific. Finally, formation of the Isthmus of Panama isolated East Pacific and West Atlantic marine
organisms. Dispersals related to the Messinian Salinity Crisis and Quaternary sea-level changes influenced population
structuring. Tethyan changes affected marine habitats, created new freshwater habitats, inland caves and ancient lakes
along the Alps and Himalayas, and influenced anchialine caves at the edge of the ancient sea. The extensive new
habitats provided opportunities for colonisation and rapid diversification. Future work should focus on testing the
biological impact of the series of Tethyan changes.
Nearly 200 years ago, a naturalist named Rafinesque stood on the banks of the Ohio River and began to describe the freshwater mussels he found there. Since that time these animals have become the most imperiled animals in North America. Dozens of species have become extinct, and it is estimated that two-thirds of the remaining freshwater mussels face a similar fate. Yet, despite their importance, the mussels of Ohio remain a poorly documented and largely mysterious fauna. The Freshwater Mussels of Ohio by G. Thomas Watters, Michael A. Hoggarth, and David H. Stansbery brings together, for the first time, the most up-to-date research on Ohio’s mussels. Designed for the weekend naturalist and scientist alike, it synthesizes recent work on genetics, biology, and systematics into one book. Each species is illustrated to a degree not found in any other work. Full-page color plates depict shell variation, hinge detail, and beak sculpture. Full-page maps show the distribution of each species based upon the collections of numerous museums (with historical distributions dating from the 1800s). In addition to species accounts, the book has a substantive introduction that includes information on basic biology, human use, and conservation issues. Extensive synonymies, a key to all species, and an illustrated glossary are included as well.
Freshwater mussels of the order Unionida are key elements of freshwater habitats and are responsible for important ecological functions and services. Unfortunately, these bivalves are among the most threatened freshwater taxa in the world. However, conservation planning and management are hindered by taxonomic problems and a lack of detailed ecological data. This highlights the urgent need for advances in the areas of systematics and evolutionary relationships within the Unionida. The present study presents the most comprehensive phylogeny of the most species rich Unionida family, i.e., the Unionidae. The phylogeny is based on a combined dataset of 1032 bp (COI + 28S) of 70 species in 46 genera, with 7 of this genera being sequenced for the first time. The resulting phylogeny divided the Unionidae into 6 supported subfamilies and 18 tribes, three of which are here named for the first time (i.e., Chamberlainiini nomen novum, Cristariini nomen novum and Lanceolariini nomen novum). Molecular analyses were complemented by investigations of selected morphological, anatomical and behavioral characters used in traditional phylogenetic studies. No single morphological, anatomical or behavioral character was diagnostic at the subfamily level and few were useful at the tribe level. However, within subfamilies, many tribes can be recognized based on a subset of these characters. The geographical distribution of each of the subfamilies and tribes is also presented. The present study provides important advances in the systematics of these extraordinary taxa with implications for future ecological and conservation studies.
Three freshwater bivalve taxa are described from the Villar del Arzobispo Formation (Late Jurassic-Early Cretaceous) of Riodeva, Teruel, Spain. The stratigraphic range of the large and geographically widely distributed bivalve Margaritifera, previously recorded from the Early Cretaceous of Spain and southern England, is recognised to extend back probably into the Late Jurassic. This new record extends the palaeogeographic and temporal distribution of the family Margaritiferidae in Europe.
Phylogenies reconstructed from gene sequences can be used to investigate the tempo and mode of species diversification. Here we develop and use new statistical methods to infer past patterns of speciation and extinction from molecular phylogenies. Specifically, we test the null hypothesis that per-lineage speciation and extinction rates have remained constant through time. Rejection of this hypothesis may provide evidence for evolutionary events such as adaptive radiations or key adaptations. In contrast to previous approaches, our methods are robust to incomplete taxon sampling and are conservative with respect to extinction. Using simulation we investigate, first, the adverse effects of failing to take incomplete sampling into account and, second, the power and reliability of our tests. When applied to published phylogenies our tests suggest that, in some cases, speciation rates have decreased through time.
This study focuses on new records of freshwater bivalves from the Late Jurassic Vega, Tereñes and Lastres formations of Asturias, northern Spain. Five new taxa Mujanaia abeuensis gen. et sp. nov., 'Unio' asturianus sp. nov., Margaritifera? lagriega sp. nov., Asturianaia colunghensis gen. et sp. nov. and Asturianaia lastrensis gen. et sp. nov. are described and included in the families Unionidae and Margaritiferidae (Unionida); they are compared and contrasted with other European, Asiatic and North American species. Their discovery constitutes the oldest records of Unionida in Spain, and they provide new palaeogeographical data on the distribution and origin of this group in Europe. These taxa are also an effective tool for the environmental reconstruction of the Jurassic ecosystems of Spain's Dinosaur Coast.
Many doubts still exist about which freshwater mussel Unio species inhabit Northwest Africa. While some authors refer to the presence of Unio delphinus in the Atlantic North African basins of Morocco, a recent IUCN assessment performed on Moroccan Unio species, recognized the existence of a distinct species, U. foucauldianus, with a Critically Endangered conservation status. The present study delivered new genetic, morphological and geographical distribution data on two Unio sp. (i.e., U. delphinus and U. foucauldianus) greatly increasing the almost non-existent data on these taxa. Bayesian phylogenetic analysis revealed two highly supported geographically concordant clades, which diverged by 3.2 ± 0.6% (uncorrected p-distance): the first distributed across Iberia and corresponding to U. delphinus, and the second distributed across Morocco, corresponding to U. foucauldianus. These results were corroborated by the analysis of 10 newly developed microsatellite loci as well as shell morphometry. We suggest that the IUCN critically endangered conservation status of the U. foucauldianus should be revised and probably down-listed since its actual distribution range is much wider than previously described. Phylogenetic relationships with the other Unio sp. were resolved, showing that U. delphinus and U. foucauldianus fall inside the pictorum-lineage. The estimated molecular rate reported herein (0.265 ± 0.06% per million years) represents the first for the Unionida and could be used as a reference in future studies.
This well-illustrated book highlights freshwater mussels fabulous diversity, amazing array of often bizarre ecological adaptations, and their dire conservation plight. Summarizing and synthesizing historical and contemporary information as well as original research and analysis, the book describes the diverse array of mussel life history strategies and builds a cohesive narrative culminating in the development of explicit frameworks to explain pervasive patterns in mussel ecology. The fascinating and colorful role of mussels in human society is also described in detail, including the little-known pearl button industry of the early 1900s and the wild and often violent shell harvest of the 1990s. The final chapter details humans efforts to save these fascinating animals and gives a prognosis for the future of the North American fauna. The book provides the first comprehensive review of mussel ecology and conservation for scientists, natural resource professionals, students, and natural history enthusiasts.