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Molecular phylogenetic analysis of tropical freshwater mussels (Mollusca: Bivalvia: Unionoida) resolves the position of Coelatura and supports a monophyletic Unionidae

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Abstract

In previous molecular phylogenetic analyses of the freshwater mussel family Unionidae (Bivalvia: Unionoida), the Afrotropical genus Coelatura had been recovered in various positions, generally indicating a paraphyletic Unionidae. However that result was typically poorly supported and in conflict with morphology-based analyses. We set out to test the phylogenetic position of Coelatura by sampling tropical lineages omitted from previous studies. Forty-one partial 28S nuclear rDNA and partial COI mtDNA sequences (1130 total aligned nucleotides) were analyzed separately and in combination under both maximum parsimony and likelihood, as well as Bayesian inference. There was significant phylogenetic incongruence between the character sets (partition homogeneity test, p<0.01), but a novel heuristic for comparing bootstrap values among character sets analyzed separately and in combination illustrated that the observed conflict was due to homoplasy rather than separate gene histories. Phylogenetic analyses robustly supported a monophyletic Unionidae, with Coelatura recovered as part of a well-supported Africa-India clade (=Parreysiinae). The implications of this result are discussed in the context of Afrotropical freshwater mussel evolution and the classification of the family Unionidae.

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... However, considering that the calculated formation temperatures were lower and consistent with that of the hydrothermally modified titanite, EMPA data have shown low concentrations of La in the analysed titanite samples (Table 5), which is commonly related to late hydrothermal activity [50], and our samples can be recognized as products of magmatic hydrothermal conversion [27,51,52]. ...
... Furthermore, the body of modern geological, tectonic, paleomagnetic, and paleontological research indicates that the Burma Terrane most likely represents a Gondwanan fragment that rafted to Asia together with the Indian Plate or as a part of a Trans-Tethyan island arc 38,40,41,[46][47][48][49][50] . However, it is still unclear whether the continental drift could explain the biogeographic patterns in freshwater mussel distribution throughout the Oriental and Afrotropical regions and whether the disjunctive range of several Unionidae clades could reflect Mesozoic tectonic events 19,31,51,52 . While our knowledge on the taxonomy and evolutionary biogeography of freshwater mussels from tropical Africa, Western Indochina, and Sundaland has largely been improved during the last decade 2,19,[22][23][24][25][26][27][28]31,35,51,[53][54][55][56] , the Unionidae fauna of the Indian Subcontinent 57,58 is still waiting for an integrative taxonomic research and thorough biogeographic modeling. ...
... and they generally exhibit the properties of medium-high potassium metaluminous series calc-alkaline rocks (Figure 4c,d). [50]; (b) QAP normative composition diagram [51] for the classification of the Nanpo diorite pluton; (c) A/NK vs. A/CNK diagram after [51]; (d) SiO2 vs. K2O diagram [52]. Abbreviations: IAG-Island arc granitoids, CAG-Continental arc granitoids, CCG-Continental collision granitoids, POG-Post-orogenic granitoids, RRG-Granitoids related to rifts, CEUG-Granitoids related to continental uplift, OP-Oceanic plagioclase granite. ...
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... Freshwater bivalves of the family Unionidae, which contains at least 620 extant species (Bogan and Roe, 2008;Graf and Cummings, 2019), are among the most endangered of freshwater biota (Lydeard et al., 2004;Lopes-Lima et al., 2017) The material used for this study was obtained from the Systematics and Biodiversity Collection of the Justus Liebig University (UGSB), the Natural History Museum London (NHMUK) and the Museum d'Histoire Naturelle de Genève (MHNG), together with data from previous studies (Whelan et al., 2011;Graf et al., 2014;Pfeiffer and Graf, 2015;Bolotov et al., 2017) and almost a decade of fieldwork (between 2006 and 2015). We obtained samples from all 8 genera that supposedly belong to Coelaturini-in this respect Unio caffer, which is widely distributed in southern Africa, was not included in our study because it belongs to Unioninae (see Whelan et al., 2011). ...
... Freshwater bivalves of the family Unionidae, which contains at least 620 extant species (Bogan and Roe, 2008;Graf and Cummings, 2019), are among the most endangered of freshwater biota (Lydeard et al., 2004;Lopes-Lima et al., 2017) The material used for this study was obtained from the Systematics and Biodiversity Collection of the Justus Liebig University (UGSB), the Natural History Museum London (NHMUK) and the Museum d'Histoire Naturelle de Genève (MHNG), together with data from previous studies (Whelan et al., 2011;Graf et al., 2014;Pfeiffer and Graf, 2015;Bolotov et al., 2017) and almost a decade of fieldwork (between 2006 and 2015). We obtained samples from all 8 genera that supposedly belong to Coelaturini-in this respect Unio caffer, which is widely distributed in southern Africa, was not included in our study because it belongs to Unioninae (see Whelan et al., 2011). For Brazzaea only historic material was available, however, and because the extracted DNA was of very poor quantity and quality, this taxon is not further considered here. ...
... We used an extensive set of Asian Parreysiinae from previous studies (Whelan et al., 2011;Graf et al., 2014;Pfeiffer and Graf, 2015;Bolotov et al., 2017) as outgroup, including specimens of Indonaia Prashad, 1918, Radiatula Simpson, 1900, Indochinella Bolotov, Pfeiffer, Vikhrev & Konopleva, 2018 and Parreysia tavoyensis (Gould, 1843) (see Table S1). ...
... Lopes-Lima et al. revised the taxonomy of the Unionidae, separated the primary monophyletic clades and mapped the distribution range of each clade 27 . However, the evolutionary biogeographic patterns of unionids are almost unknown, with only a few reports published 37 . The Oriental naiads are poorly studied by means of a molecular approach 27,[37][38][39][40][41][42] . ...
... However, the evolutionary biogeographic patterns of unionids are almost unknown, with only a few reports published 37 . The Oriental naiads are poorly studied by means of a molecular approach 27,[37][38][39][40][41][42] . The morphology-based taxonomic concept suggests that there are many widespread species, which ranged across a plethora of river systems from the Greater Sunda Archipelago and the Malay Peninsula to Indo-China and India [42][43][44][45] , although recent molecular studies reveal possible cryptic taxa 41 . ...
... Examples of such forms are caecilians 55 , frogs 56,57 and freshwater crabs 58 . The origin of the African Coelaturini clade and its sister relationships with Oriental taxa have been under long-term discussions in light of two primary hypotheses: "Into Africa" and "Out of Africa" 32,37,59,60 . With respect to the "Into Africa" hypothesis, the presence of the Unionidae in the Indian subcontinent and Africa can be explained by an invasion of the same Asiatic lineage when these continents contacted Eurasia during the Eocene (India) and Miocene (Africa) 37,59,60 . ...
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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.
... The Oriental fauna is the second richest unionid fauna in the world after the Nearctic Region (Graf, 2013) and includes a variety of endangered endemic taxa, many of which may be on the brink of extinction due to rapid environmental changes and habitat degradation (Bogan, 1993(Bogan, , 2008Bolotov et al., 2014). Such a unique fauna have been poorly studied using a molecular phylogenetic approach (Graf, 2013) but several recent studies have dramatically improved our understanding of the higher-level classification and evolution of mussels in the region (Graf & Cummings, 2007;Whelan, Geneva, & Graf, 2011). However, today, we are still far from having a complete picture of species diversity of the Indotropical Unionidae and our understanding of the generic-and species-level diversity in the region remains very poorly understood. ...
... Our current understanding is mainly based on publications from the 19th and 20th centuries that utilize foremost a morphological approach for studying the systematics of the family (Graf, 2013;K€ ohler et al., 2012). Additionally, a few recent taxonomic studies based on the application of molecular or cytotaxonomic approaches are available (Kongim, Sutcharit, & Panha, 2015;Vannarattanarat et al., 2014;Whelan et al., 2011). ...
... The best substitution model was selected for each gene separately based on the corrected Akaike Information Coelatura aegyptiaca (Cailliaud, 1827) JN243894 KP795045 JN243872 ANSP:416304 Egypt Whelan et al., 2011) Oxynaia pugio (Benson, 1862) JN243899 KP795046 JN243879 UA:20739.1/UMMZ 304644 Burma Whelan et al., 2011) Radiatula bonneaudii (Eydoux, 1838) JN243898 KP795047 JN243878 UA:20714.2/UMMZ ...
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The Oriental Region harbours the second richest fauna of freshwater bivalves in the world, including many endangered endemic taxa. However, the Oriental fauna of the Unionidae have been very poorly studied using an integrative taxonomic approach, which may provide reasonable revisions of complicated (cryptic) taxa based on morphological, molecular, biogeographic and ecological evidence. Here, we present the first example of an integrative taxonomic revision concerning the status of Unio exolescens Gould (1843), a nominal mussel taxon that was accepted as a valid species within the genus Trapezoideus Simpson (1900). Currently, Trapezoideus exolescens is considered the type of the genus as far as the originally designated type species, U. foliaceus Gould (1843), was considered to be a synonym of T. exolescens. Using nucleotide sequences obtained from mitochondrial (COI and 16S rRNA) and nuclear (28S rDNA) genes, we found that the topotypes of Unio exolescens Gould (1843) cluster together with representatives of another mussel genus, Lamellidens Simpson (1900). Based on these results and on morphological data, we transfer Unio exolescens Gould (1843) from Trapezoideus to Lamellidens and propose Lamellidens exolescens (Gould, 1843) comb. nov. In addition, we revisited the status of Unio foliaceus Gould (1843) as a valid species and the type of the genus Trapezoideus based on the morphological study of the type specimen, although a question concerning the true position of this taxon is still open because its molecular sequences are not available. Our findings highlight that an integrative taxonomic approach is an important tool, particularly when dealing with such species-rich Unionidae fauna as those of the Oriental Realm.
... With the advancement of molecular technology, significant progress in developing improved phylogenetic hypotheses for Unionidae has occurred in the past several decades (Graf, 2013;Huang et al., 2013;Klishko et al., 2017;Pavan-Kumar et al., 2022;Whelan et al., 2011;Wu et al., 2019). Specifically, phylogenetic analyses utilizing mitogenomes have the potential to effectively address both deep and shallow-level taxonomic puzzlers (Pfeiffer et al., 2019;Wu et al., 2020Wu et al., , 2022. ...
... Unionidae is the most prevalent group among freshwater mussels (Graf & Cummings, 2007), but the subfamily classification has been discordant due to uncertainties surrounding early evolution and lineage genesis (Bolotov et al., 2017;Lopes-lima et al., 2017a;Pfeiffer & Graf, 2015;Whelan et al., 2011). Recently, Pfeiffer et al. (2019) proposed a taxonomy system of Unionidae consisting of five subfamilies based on genomic data, among which Modellnaiinae was excluded due to the lack of molecular data for Modellnaia siamensis limited to Thailand. ...
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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.
... The Unionidae have frequently been recovered as paraphyletic by phylogenetic analysis throughout the last decade (Graf and Cummings, 2006). However, their findings were unsubstantiated and based on insufficient taxon and character sampling (Whelan et al., 2011); only two molecular character sets had been used to assess Unionoida family-group level associations through COI gene (Whelan et al., 2011), Other Unionidae phylogenetic analysis had relied on specific gene region. While, Lopes-Lima et al. (2017) hypothesized the subfamily's evolutionary connection based on COI. ...
... The Unionidae have frequently been recovered as paraphyletic by phylogenetic analysis throughout the last decade (Graf and Cummings, 2006). However, their findings were unsubstantiated and based on insufficient taxon and character sampling (Whelan et al., 2011); only two molecular character sets had been used to assess Unionoida family-group level associations through COI gene (Whelan et al., 2011), Other Unionidae phylogenetic analysis had relied on specific gene region. While, Lopes-Lima et al. (2017) hypothesized the subfamily's evolutionary connection based on COI. ...
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Freshwater mussels are a guild of stationary, suspended-feeding species; they perform significant ecological functions like nitrogen cycling, bioturbation that gives oxygen and habitat that other creatures need to survive, and increasing water clearance by filtration. Knowledge of the freshwater mussel Unio tigridis Bourguignat, 1852, distribution, and molecular study in Iraq was inadequate. In the current study, this species of freshwater Mussels belonging to the family Unionidae was collected from different locations in the Greater Zab River, from April to August 2022. The average water temperature of the site was arranged between (17.8 to 36.1 C°). All previous studies in the Kurdistan Region and Iraq were based on morphological characters and the current study was the first report of Unio tigridis that was confirmed by molecular genetics and COI gene, analyzed phylogenetically using Maximum Likelihood and Maximum Parsimony Methods.
... In fact, of the six recognized Unionida families (Lopes-Lima et al. 2014), published mitogenomes are essentially restricted to the Unionoidea (Unionidae+Margaritiferidae) with a distribution predominantly within the Northern Hemisphere. While some studies have questioned the monophyly of the Unionoidea (e.g., Combosch et al. 2017;Whelan et al. 2011) the most comprehensive recent studies, using either full mitogenomes (Huang et al. 2019;Wu et al. 2019) or hundreds of nuclear loci (Pfeiffer et al. 2019) support its monophyletic status. Moreover, mitogenome-based Unionida phylogenies reconstructed to date have been based on either F-or M-type mitogenomes Fonseca et al. 2016;Lopes-Lima et al. 2017b). ...
... The first molecular study to include the so-called "problematic" Gonideinae taxa (Graf 2002) only examined the type species, i.e., Gonidea angulata (Lea 1838). Subsequent studies included several additional Gonideinae taxa but the clade Gonideinae was never recovered as monophyletic (Graf and Cummings 2006;Whelan et al. 2011;Pfeiffer and Graf 2013). More recently, multi-marker and mitogenomic approaches have consistently recovered Gonideinae as monophyletic (Huang et al. 2013;Pfeiffer and Graf 2015;Fonseca et al. 2016;Froufe et al. 2016;Lopes-Lima et al. 2017a. ...
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Using a new fossil-calibrated mitogenome-based approach, we identified macroevolutionary shifts in mitochondrial gene order among the freshwater mussels (Unionoidea). We show that the early Mesozoic divergence of the two Unionoidea clades, Margaritiferidae and Unionidae, was accompanied by a synchronous split in the gene arrangement in the female mitogenome (i.e., gene orders MF1 and UF1). Our results suggest that this macroevolutionary jump was completed within a relatively short time interval (95% HPD 201–226 Ma) that coincided with the Triassic–Jurassic mass extinction. Both gene orders have persisted within these clades for ~200 Ma. The monophyly of the so-called “problematic” Gonideinae taxa was supported by all the inferred phylogenies in this study using, for the first time, the M- and F-type mitogenomes either singly or combined. Within Gonideinae, two additional splits in the gene order (UF1 to UF2, UF2 to UF3) occurred in the Mesozoic and have persisted for ~150 and ~100 Ma, respectively. Finally, the mitogenomic results suggest ancient connections between freshwater basins of East Asia and Europe near the Cretaceous–Paleogene boundary, probably via a continuous paleo-river system or along the Tethys coastal line, which are well supported by at least three independent but almost synchronous divergence events.
... Advances in developing improved phylogenetic hypotheses for the Unionidae have occurred in the past several decades (Davis 1984;Lydeard et al. 1996;Nagel and Badino 2001;Hoeh et al. 2001Hoeh et al. , 2002Giribet and Wheeler 2002;Graf 2002;Campbell et al. 2005;Zanatta and Murphy 2006;Graf and Cummings 2007;Campbell and Lydeard 2012a, b;Froufe et al. 2014;Prié and Puillandre 2014;Graf et al. 2015;Pfeiffer and Graf 2015). Most of these studies have focused on North American, Australian, and European taxa, although more recently, African (Whelan et al. 2011;Graf 2013;Elderkin et al. 2016) and Asian (Huang et al. 2002;Zhou et al. 2007;Huang et al. 2013;Bolotov et al. 2017a, b) taxa have been included, and a global phylogenetic framework of the Unionidae has recently been established (Bolotov et al. 2017a;Lopes-Lima et al. 2017a). Despite these advances, the incorporation of Asian taxa into unionid phylogenetic hypotheses, particularly those from China has lagged. ...
... Our results indicate that the Ambleminae is basal to the other three subfamilies, and its origin is therefore earlier than the other three subfamilies. Globally, eight subfamilies (Anodontinae, Unioninae, Pseudodontinae, Gonideinae, Ambleminae, Rectidentinae, Parreysiinae, and Modellnaiinae) are recognized in the Unionidae (Bolotov et al. 2017a;Lopes-Lima et al. 2017a;Whelan et al. 2011). The lack of mitochondrial genomes for Rectidentinae, Parreysiinae, Modellnaiinae, and Pseudodontinae, precluded their incorporation into this study. ...
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The Yangtze River basin is one of the most species-rich regions for freshwater mussels on Earth, but is gravely threatened by anthropogenic activities. However, conservation planning and management of mussel species has been hindered by a number of taxonomic uncertainties. In order to clarify the taxonomic status and phylogenetic position of these species, mitochondrial genomes of four species ( Acuticostachinensis , Schistodesmuslampreyanus , Cuneopsisheudei and Cuneopsiscapitatus ) were generated and analyzed along with data from 43 other mitogenomes. The complete F-type mitogenomes of A.chinensis , S.lampreyanus , C.heudei , and C.capitatus are 15652 bp, 15855 bp, 15892 bp, and 15844 bp, respectively, and all four F-type mitogenomes have the same pattern of gene arrangement. ML and BI trees based on the mitogenome dataset are completely congruent, and indicate that the included Unionidae belong to three subfamilies with high bootstrap and posterior probabilities, i.e., Unioninae ( Aculamprotula , Cuneopsis , Nodularia , and Schistodesmus ), Anodontinae ( Cristaria , Arconaia , Acuticosta , Lanceolaria , Anemina , and Sinoanodonta ), and Gonideinae ( Ptychorhynchus , Solenaia , Lamprotula , and Sinohyriopsis ). Results also indicate that A.chinensis has affinities with Arconaialanceolata and Lanceolariagrayii and is a member of the subfamily Anodontinae.
... Morphologically, representatives of the genus compare well to the North American genera Obovaria Rafinesque, 1819, and Pleurobema Rafinesque, 1819, which belong to the subfamily Ambleminae Rafinesque, 1820. Extant representatives of this subfamily are deeply split molecularly, and geographically distant from African taxa (Whelan et al., 2011), suggesting that remarkable convergence is the most likely cause of similarity. Also Gonideinae Ortmann, 1916, to which Van Damme and Pickford (2010) attributed Pseudobovaria, is deeply split from Coelaturinae Modell, 1942 (Whelan et al., 2011), and given that good arguments for any subfamily attribution are lacking, I consider the genus' position within Unionidae currently uncertain. ...
... Extant representatives of this subfamily are deeply split molecularly, and geographically distant from African taxa (Whelan et al., 2011), suggesting that remarkable convergence is the most likely cause of similarity. Also Gonideinae Ortmann, 1916, to which Van Damme and Pickford (2010) attributed Pseudobovaria, is deeply split from Coelaturinae Modell, 1942 (Whelan et al., 2011), and given that good arguments for any subfamily attribution are lacking, I consider the genus' position within Unionidae currently uncertain. In any case, the few Pseudobovaria valves that have been obtained from the Kanapoi Formation differ morphologically from previously described Pseudobovaria species in that they are more elongate, with valves and hinges that are less strongly calcified (Fig. 2D). ...
Article
The Early Pliocene Kanapoi Formation of the Omo-Turkana Basin consists of two fluvial/deltaic sedimentary sequences with an intermediate lacustrine sequence that was deposited in Paleolake Lonyumun, the earliest large lake in the basin. Overall, the geology and vertebrate paleontology of the Kanapoi Formation are well studied, but its freshwater mollusks, despite being a major component of the benthic ecosystem, have not been subjected to in-depth study. Here I present the first treatment of these mollusks, which have been retrieved mainly from the lacustrine but also from the upper fluvial sediments, with a focus on paleoecological implications. Overall, the freshwater mollusk fauna is reasonably diverse and contains the gastropods Bellamya (Viviparidae), Melanoides (Thiaridae), Cleopatra (Paludomidae) and Gabbiella (Bithyniidae), as well as the unionoid bivalves Coelatura, Pseudobovaria (Unionidae), Aspatharia, Iridina (Iridinidae) and Etheria (Etheriidae). Material is typically recrystallized and lithified and its taphonomy suggests deposition in a system with intermediate energy, such as a beach, with post-depositional deformation and abrasion. The mollusk assemblage is indicative of perennial, fresh and well-oxygenated waters in the Kanapoi region. It suggests that Paleolake Lonyumun had largely open shores with limited vegetation and that swampy or ephemeral backwaters were rare. Overall, these findings support earlier paleoecological interpretations based on the fish assemblage of Paleolake Lonyumun at Kanapoi. Moreover, mollusk assemblages from this lake are very similar across the Omo-Turkana Basin (Nachukui, Usno, Mursi and Koobi Fora Formations) suggesting that the lacustrine paleoecological conditions found in the Kanapoi Formation existed throughout the basin.
... Palaeoheterodonts divide into the marine Trigoniida and the freshwater clade Unionida, as in virtually every published bivalve phylogeny. Resolution within Unionida is, however, not well supported, and recent analyses have found alternative resolutions (e.g., Graf and Cummings, 2007;Whelan et al., 2011). For example, our ML tree supports Hyriidae as the sister group to the remaining families, followed by Unionidae and then by Margaritiferidae, which is sister group to a well-supported clade of Iridinidae, Etheriidae, and Mycetopodidae (Figs. 1a and 3), but our Bayesian analysis supports the latter clade as sister group to a monophyletic Hyriidae + Unionidae + Margaritiferidae (Fig. 2a). ...
... For example, our ML tree supports Hyriidae as the sister group to the remaining families, followed by Unionidae and then by Margaritiferidae, which is sister group to a well-supported clade of Iridinidae, Etheriidae, and Mycetopodidae (Figs. 1a and 3), but our Bayesian analysis supports the latter clade as sister group to a monophyletic Hyriidae + Unionidae + Margaritiferidae (Fig. 2a). Resolution within Unionida seems to be highly sensitive to analytical parameters and methodologies (Whelan et al., 2011) as well as taxon sampling (Graf et al., 2015), and again it appears that additional data will be necessary to resolve this enigmatic Triassic radiation of freshwater bivalves (Bieler et al., 2014). ...
... Given their highly endangered status, modern systematics research is urgently needed to gain a better understanding of mussel evolution and taxonomy. At deep evolutionary timescales, progress has been made in recent years towards understanding phylogenetic relationships among major clades of freshwater mussels (Whelan et al., 2011;Lopes-Lima et al., 2017a;Pfeiffer et al., 2019;Smith et al., 2020). At the species level, molecular phylogenetic data have revealed previously overlooked species diversity or instances of previously recognized species that were not valid (Williams et al., 2017;Johnson et al., 2018;Pfeiffer et al., 2018). ...
Article
Inaccurate taxonomy can lead to species in need of conservation being overlooked, which makes revisionary systematics crucially important for imperilled groups. The freshwater mussel genus Alasmidonta is one such group in need of study. Here, we take a multilocus phylogenetic approach to assess species-level taxonomy of Alasmidonta and test monophyly of this genus. Phylogenetic inference resulted in polyphyly of Alasmidonta. Lasmigona, which was included to test monophyly of Alasmidonta, was also polyphyletic. Species delimitation methods disagreed about whether Alasmidonta arcula, Alasmidonta triangulata and Alasmidonta undulata are distinct species, but all delimitation methods agreed that Alasmidonta harbours an undescribed species that would be considered Alasmidonta varicosa under current taxonomy. Given conflict among species delimitation methods and geographical separation, we maintain the current taxonomy for A. arcula and A. triangulata. The undescribed species is restricted to rivers of the Uwharrie Mountains region in North Carolina, USA that flow into the Pee Dee River from the east and can be distinguished morphologically from A. varciosa by higher and wider placed adductor mussels and a hooked pseudocardinal tooth. We offer insights into how supraspecific taxonomy of subtribe Alasmidontina might be resolved and formally describe the lineage from the Uwharrie Mountains region as Uwharrie elktoe, Alasmidonta uwharriensis sp. nov.
... We evaluate the performance of target enrichment for these heterogenous targets, and analyse the obtained data sets to illustrate their value for phylogenetics and population genetics. Finally, we built a custom, versatile pipeline to skim the raw sequencing data and to evaluate the possibility of recuperating off-target mitochondrial sequences, on which previous Sanger-sequencing studies of Unionidae (Lopes-Lima, Ortiz-Sepulveda et al., 2020;Whelan et al., 2011), and bivalves in general (Combosh et al., 2017), have relied heavily. ...
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Despite the increasing accessibility of high‐throughput sequencing, obtaining high‐quality genomic data on non‐model organisms without proximate well‐assembled and annotated genomes remains challenging. Here we describe a workflow that takes advantage of distant genomic resources and ingroup transcriptomes to select and jointly enrich long open reading frames (ORFs) and ultraconserved elements (UCEs) from genomic samples for integrative studies of microevolutionary and macroevolutionary dynamics. This workflow is applied to samples of the African unionid bivalve tribe Coelaturini (Parreysiinae) at basin and continent‐wide scales. Our results indicate that ORFs are efficiently captured without prior identification of intron‐exon boundaries. The enrichment of UCEs was less successful, but nevertheless produced substantial datasets. Exploratory continent‐wide phylogenetic analyses with ORF supercontigs (>515,000 parsimony informative sites) resulted in a fully resolved phylogeny, the backbone of which was also retrieved with UCEs (>11,000 informative sites). Variant calling on ORFs and UCEs of Coelaturini from the Malawi Basin produced ~2,000 SNPs per population pair. Estimates of nucleotide diversity and population differentiation were similar for ORFs and UCEs. They were low compared to previous estimates in mollusks, but comparable to those in recently diversifying Malawi cichlids and other taxa at an early stage of speciation. Skimming off‐target sequence data from the same enriched libraries of Coelaturini from the Malawi Basin, we reconstructed the maternally‐inherited mitogenome, which displays the gene order inferred for the most recent common ancestor of Unionidae. Overall, our workflow and results provide exciting perspectives for integrative genomic studies of microevolutionary and macroevolutionary dynamics in non‐model organisms.
... Statistically significant values are marked in bold (p < 0.05). Refs [67][68][69][70][71][72][73][74][75][76][77][78] ...
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The freshwater pearl mussel Margaritifera margaritifera is a unionid species distributed across Northwestern Russia, Fennoscandia, Western and Southwestern Europe, and the Atlantic Coast of North America. In this study, we reconstructed the post-glacial expansion routes of this species based on FST genetic distances and the fact that M. margaritifera distribution is directly connected with salmonid expansion. The freshwater-pearl-mussel populations from North America and Northeastern Europe were the closest groups, judging by FST distances, supporting the concept of the North Atlantic Salmo salar colonization of the Barents and White Sea basins. We also documented that unique haplotypes in the populations of the Baltic and White Sea basins may have originated in isolated glacial refugia in Eastern and Northeastern Europe. The Iberian clade was the most distant group of populations, which is consistent with the previously observed role of the Iberian Peninsula as a glacial refugium. The high genetic diversity in the populations of Northern and Eastern Karelia was facilitated by migrants utilizing complex periglacial hydrological networks and by admixture in the contact zone where the migration flows met. We confirm that this region should be considered as a major center of genetic diversity within the European part of the species’ range.
... We evaluate the relative performance of target enrichment for these heterogenous targets, and analyze the obtained data to demonstrate the value of such datasets for both phylogenetic and population genetic investigations. Finally, we skimmed the raw sequencing data to evaluate the possibility of recuperating non-target mitochondrial sequences, on which previous studies on Unionidae Ortiz-Sepulveda et al., 2020;Whelan et al., 2011) and bivalves in general (Combosh et al., 2017) with Sanger sequencing approaches have relied heavily. ...
Preprint
Despite the increasing accessibility of high-throughput sequencing, obtaining high-quality genomic data on non-model organisms without proximate well-assembled and annotated genomes remains challenging. Here we describe a workflow that takes advantage of distant genomic resources and ingroup transcriptomes to select and jointly enrich long open reading frames (ORFs) and ultraconserved elements (UCEs) from genomic samples for integrative studies of microevolutionary and macroevolutionary dynamics. This workflow is applied to samples of the African unionid bivalve tribe Coelaturini (Parreysiinae) at basin and continent-wide scales. Our results indicate that ORFs are efficiently captured without prior identification of intron-exon boundaries. The enrichment of UCEs was less successful, but nevertheless produced a substantial dataset. Exploratory continent-wide phylogenetic analyses with ORF supercontigs (>515,000 parsimony informative sites) resulted in a fully resolved phylogeny, the backbone of which was also retrieved with UCEs (>11,000 informative sites), although some branches lack support in the latter case. Variant calling on the exome of Coelaturini from the Malawi Basin produced ~2,000 SNPs per population pair. Nucleotide diversity and population differentiation was low compared to previous estimates in mollusks, but comparable to those in recently diversifying Malawi cichlids and other taxa at an early stage of speciation. Skimming non-specific sequence data obtained for Coelaturini of the Malawi Basin, we reconstructed the maternally-inherited mitogenome, which displays an identical gene order to that of the most recent common ancestor of Unionidae. Overall, our workflow and results provide exciting perspectives for the development of integrative genomic studies on micro- and macroevolutionary dynamics in non-model organisms.
... However, all of these taxonomic opinions were based mainly on shell morphology. Molecular phylogenetic studies do not accept Brandt's (1974) classification, but instead reassign Pseudodon and Pilsbryoconcha to Gonideinae (Whelan et al. 2011;Pfeiffer & Graf 2015). The nominal name was recently recognized as a valid tribe, Pseudodontini, within Gonideinae Ortmann, 1916by Lopes-Lima et al. (2017 with two genera, Pseudodon and Pilsbryoconcha. ...
Article
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A new genus of freshwater mussels (Bivalvia: Unionidae) is described from the Mekong River Basin as Namkongnaia gen. nov. The validity of the new genus is supported by its unique conchological characteristics, namely the lack of hinge dentition and elongated shells, together with its evolutionary distinctiveness as estimated by multi-locus phylogenetic analyses (mitochondrial COI and 16S, and nuclear 28S genes). The new genus includes two lineages with deep divergence, shown by 5.10% uncorrected COI p-distance. One lineage is a type species described herein as Namkongnaia inkhavilayi gen. et sp. nov. The other is a recognized species under the name 'Pilsbryoconcha lemeslei (Morelet, 1875)'. Molecular phylogenetic analysis further shows that the new genus belongs to the tribe Pseudodontini, and evolutionarily is closely related to the genus Monodontina Conrad, 1853. However, its conchology is similar to the genus Pilsbryoconcha Simpson, 1900. Time-calibrated phylogeny suggests that the main radiation events of the tribe Pseudodontini occurred during the Late Cretaceous to the Eocene, with the divergence between the new genus and Monodontina placed in the Miocene. The discovery of new freshwater mussel taxa in this study highlights the importance of the Mekong River Basin as one of the world's biodiversity hotspots for freshwater fauna.
... Hence, we screened genetic markers to characterize their molecular genetic and phylogenetic affinities. Genetic identification of tropical freshwater mussels has been approached through the amplification and sequencing of the cytochrome oxidase I (COI) gene of mitochondrial DNA and the 28S nuclear rDNA gene [71]. Because few genetic markers have been established for tropical freshwater mussels, we screened variation at three additional genes (mitochondrial 16S rRNA, nuclear 18S rRNA-ITS, and histone H3) that are sufficiently well conserved across a range of taxa that primers proving useful for PCR amplification are available. ...
Article
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The phylogeny and taxonomy of freshwater mussels of the genus Castalia in South America is complicated by issues of morphological plasticity and limited molecular genetic data. We present field data on the distributions of the nominal Castalia ambigua and C. inflata in the upper Paraguay River basin in Brazil based on original occurrence data at 23 sample sites and on historical records. The upper basin has distinct highland and lowland regions, the latter including the Pantanal wetland, where "C. ambigua" occurs in the highlands and "C. inflata" occurs in both regions. At Baixo Stream in the highlands, we observed individuals with shell morphologies of either C. ambigua or C. inflata, and also individuals with intermediate shell morphology. DNA sequence variation in the upland Baixo Stream and two representative lowland populations were screened. Two mitochondrial and three nuclear genes were sequenced to test hypotheses regarding the number of species-level phylogenetic lineages present. Reported individual DNA sequences from Amazon-basin C. ambigua and other Castalia and outgroup species were included in the analysis as outgroups. Individuals from the Paraguay River basin exhibited 17 haplotypes at the mitochondrial cytochrome oxidase I (COI) gene and nine at mitochondrial 16S rRNA. Analysis of haplotype networks and phylogenetic trees of combined COI + 16S rRNA sequences among individuals with the respective shell morphologies supported the hypothesis that C. ambigua and C. inflata from the Paraguay River basin belong to the same species and one phylogenetic lineage. No variation was observed at the nuclear 18S rRNA internal transcribed spacer, 28S rRNA, or H3NR histone genes among individuals used in this study. Across all markers, less variation was observed among Paraguay basin populations than between Paraguay and Amazon basin populations. Our results collectively suggest that: (1) "C. ambigua", "C. inflata", and morphologically intermediate individuals within the upper Paraguay drainage represent one phylogenetic lineage, (2) a phylogeographic divide exists between Castalia populations occurring in the Paraguay and Amazon River basins, and (3) the evolutionary and taxonomic uncertainties that we have identified among Castalia species should be thoroughly assessed across their distribution using both morphological and molecular characters.
... Geographically disjunct populations or species may exhibit relatively high levels of genetic differentiation, yet be confusingly similar in their morphology (Brandt, 1974;Do & Bogan, 2012a, b;Sutcharit et al., 2013), leading to the lumping of morphologically similar forms into species complexes of uncertain taxonomic status (Huff et al., 2004;Whelan, Geneva & Graf, 2011;Graf, 2013;Graf et al., 2015;Lopes-Lima et al., 2017). In view of their distribution across complex drainage systems, we hypothesized that the nominal taxa E. ingallsianus and E. sagittarius might include hitherto unrecognized species. ...
Article
The freshwater bivalve genus Ensidens Frierson, 1911 is widely distributed in Thailand and the surrounding parts of mainland Southeast Asia. While the identification of the two currently accepted species, Ensidens ingallsianus (Lea, 1852) and E. sagittarius (Lea, 1856) is based on external morphology, classification using only morphology can lead to underestimation of species diversity and misidentification, due to phenotypic plasticity. Here we present the results of a phylogeographic study of these two nominal species based on 82 individuals and using DNA sequence data from mitochondrial (COI and ND1) and nuclear (ITS1) gene fragments. Phylogenetic trees based on maximum likelihood and Bayesian inference revealed that both species contain deeply divergent clades that may represent previously unrecognized species. The six phylogenetic lineages within Thai Ensidens correspond to the geographic structure of Thailand’s river basins. These six consist of two lineages of E. ingallsianus from basins draining to the Gulf of Thailand (Chao Phraya, Mae Klong, Phetchaburi, Bang Prakong, Prasae and Ta Pi) and the Mekong River (Mun and Tonle Sap), and four lineages of E. sagittarius from the Khorat basin (Mekong). These geographically disjunct lineages are hypothesized to have formed during the complex drainage history of Indochina. The presence of multiple lineages of Ensidens endemic to the northern Khorat basin emphasizes the conservation importance of this region.
... Other nuclear loci, such as histone H3 and 28S, have been utilized in freshwater mussel phylogenetic studies; however, these markers are well known to show limited diversity at shallow taxonomic scales and have primarily been used to resolve deep level phylogeny [15][16][17][18][19][20]. ...
Article
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Molecular data have been an integral tool in the resolution of the evolutionary relationships and systematics of freshwater mussels, despite the limited number of nuclear markers available for Sanger sequencing. To facilitate future studies, we evaluated the phylogenetic informativeness of loci from the recently published anchored hybrid enrichment (AHE) probe set Unioverse and developed novel Sanger primer sets to amplify two protein-coding nuclear loci with high net phylogenetic informativeness scores: fem-1 homolog C (FEM1) and UbiA prenyltransferase domain-containing protein 1 (UbiA). We report the methods used for marker development, along with the primer sequences and optimized PCR and thermal cycling conditions. To demonstrate the utility of these markers, we provide haplotype networks, DNA alignments, and summary statistics regarding the sequence variation for the two protein-coding nuclear loci (FEM1 and UbiA). Additionally, we compare the DNA sequence variation of FEM1 and UbiA to three loci commonly used in freshwater mussel genetic studies: the mitochondrial genes cytochrome c oxidase subunit 1 (CO1) and NADH dehydrogenase subunit 1 (ND1), and the nuclear internal transcribed spacer 1 (ITS1). All five loci distinguish among the three focal species (Potamilus fragilis, Potamilus inflatus, and Potamilus purpuratus), and the sequence variation was highest for ND1, followed by CO1, ITS1, UbiA, and FEM1, respectively. The newly developed Sanger PCR primers and methodologies for extracting additional loci from AHE probe sets have great potential to facilitate molecular investigations targeting supraspecific relationships in freshwater mussels, but may be of limited utility at shallow taxonomic scales. Dataset: https://doi.org/10.5066/P9Q3CFL5.
... A partition-homogeneity test with heuristic search through PAUP* v4.0a165 59 shared the significant conflict of phylogenetic signals among the partitions in the dataset (P = 0.01). However, we considered that this conflict does not affect the phylogeny because it seems to reflect a copious homoplasy rather than independent histories of the genes 38,60 . The single gene alignments were joined to a two-locus alignment using FaBox v1.5 (http://users-birc.au.dk/palle/php/fabox) 61 . ...
Article
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Freshwater mussels (Unionida) are one of the most imperiled animal groups worldwide, revealing the fastest rates of extinction. Habitat degradation, river pollution and climate change are the primary causes of global decline. However, biological threats for freshwater mussels are still poorly known. Here, we describe a diverse ecological group of leeches (Hirudinea: Glossiphoniidae) inhabiting the mantle cavity of freshwater mussels. So far, examples of mussel-associated leech species are recorded from East Asia, Southeast Asia, India and Nepal, Africa, and North America. This group comprises a dozen glossiphoniid species with a hidden life style inside the mantle cavity of their hosts largely overlooked by researchers. We show that the association with freshwater mussels evolved independently in three leech clades, i.e. Batracobdelloides, Hemiclepsis, and Placobdella, at least since the Miocene. Seven mussel-associated leech species and two additional free-living taxa are described here as new to science.
... The examined taxa in present study included all valid species of the genus Scabies: S. phaselus, S. anceps, S. scobinatus, S. crispata, S. mandarinus, S. nucleus and S. songkramensis, plus two closely related taxa currently ascribed to the genus Radiatula; R. pilata and R. humilis (Bolotov et al., 2018). Sequences from other taxa representing all the genera within the tribe Indochinellini, and some taxa from other tribes within the subfamily Parreysiinae were retrieved from the GenBank database (Bolotov et al., 2017a(Bolotov et al., , b, 2019Pfeiffer and Graf, 2015;Pfeiffer et al., 2018;Whelan et al., 2011), and used for phylogenetic reconstruction in this study. The list of the taxa analyzed, with the locality name, voucher specimen ID and GenBank accession number, are listed in Table 1. ...
Article
Molecular phylogeny of the Indochinese freshwater mussel genus Scabies Haas, 1911 was studied. The examined taxa included all seven recognized species of the genus Scabies (S. phaselus, S. anceps, S. scobinatus, S. crispata, S. mandarinus, S. nucleus and S. songkramensis) and two closely related Indochinese species currently assigned to the genus Radiatula Simpson, 1900 (R. humilis and R. pilata). Maximum likelihood (ML) and Bayesian Inference (BI) phylogenetic trees based on the concatenated sequences of two mitochondrial genes (cytochrome oxidase c subunit 1 and 16S ribosomal RNA) and one nuclear gene (28S ribosomal RNA) fragments (1,586 bp) revealed a polyphyletic relationship in both genera compared to the outgroups of other genera from the tribe Indochinellini. Scabies songkramensis was clustered separately from the congeners, whereas R. humilis and R. pilata were grouped within the Scabies clade with high support (88% bootstrap support for ML and a Bayesian posterior probability of 1 for BI), and separated from other members of Radiatula from western Indochina (Myanmar and India). Based on these phylogenetic results, in combination with morphological and biogeographic data, these two Indochinese Radiatula species were transferred to Scabies, as S. humilis (Lea, 1856) comb. nov. and S. pilata (Lea, 1866) comb. nov. The genus Radiatula s.s. should be implied only to taxa endemic to the western Indochinese region, while the genus Scabies are distributed in the Chao Phraya and Mekong River basins and other rivers that drain into the Gulf of Thailand.
... Molecular and morphological phylogenetic analyses sampling representatives of each unionoid family have consistently recovered the glochidia-bearing mussels as paraphyletic; either the Pfeiffer, et al. Molecular Phylogenetics and Evolution 136 (2019) xxx-xxx Hyriidae is recovered as sister to the remaining five families (the most common topology - Bogan and Hoeh, 2000;Hoeh et al., 2001Hoeh et al., , 2002Whelan et al., 2011;Pfeiffer and Graf, 2015;Graf et al., 2015;Lopes-Lima et al., 2017;Bolotov et al., 2017a;Huang et al., 2018Huang et al., , 2019 or the Hyriidae is recovered as sister to the lasidia-bearing mussels (Graf, 2000;Roe and Hoeh, 2003;Graf and Cummings, 2006) (Fig. 1). These two alternative topologies both suggest that glochidia are the plesiomorphic parasitic larval condition of freshwater mussels, and the ancestral state from which lasidia was derived. ...
Article
Freshwater mussels (order Unionoida) are a diverse radiation of parasitic bivalves that require temporary larval encystment on vertebrate hosts to complete metamorphosis to free-living juveniles. The freshwater mussel-fish symbiosis represents a useful relationship for understanding eco-evolutionary dynamics in freshwater ecosystems but the practicality of this promising model system is undermined by the absence of a stable freshwater mussel phylogeny. Inadequate character sampling is the primary analytical impediment obfuscating a coherent phylogeny of freshwater mussels, specifically the lack of nuclear molecular markers appropriate for reconstructing supraspecific relationships and testing macroevolutionary hypotheses. The objective of this study is to develop a phylogenomic resource, specifically an anchored hybrid enrichment probe set, capable of capturing hundreds of molecular markers from taxa distributed across the entirety of freshwater mussel biodiversity. Our freshwater mussel specific anchored hybrid enrichment probe set, called Unioverse, successfully captures hundreds of nuclear protein-coding loci from all major lineages of the Unionoida and will facilitate more data-rich and taxonomically inclusive reconstructions of freshwater mussel evolution. We demonstrate the utility of this resource at three disparate evolutionary scales by estimating a backbone phylogeny of the Bivalvia with a focus on the Unionoida, reconstructing the subfamily-level relationships of the Unionidae, and recovering the systematic position of the phylogenetically unstable genus Plectomerus.
... Globally, seven subfamilies (Unioninae, Pseudodontinae, Gonideinae, Ambleminae, Rectidentinae, Parreysiinae, and Modellnaiinae) are recognized in Unionidae (Bolotov et al., 2017b;Carter et al., 2011;Lopes-Lima et al., 2017b;Whelan et al., 2011). Modellnaiinae, which contains only one species Modellnaia siamensis from Thailand, has never been included in a phylogenetic analysis (Lopes-Lima et al., 2017b). ...
... Whelan et al. 10 recently transferred the tribe Oxynaiini from the subfamily Ambleminae to the Parreysiinae on the basis of recovering Oxynaia pugio (Benson, 1862) among the latter subfamily in a molecular phylogeny. Whereas, traditional morphological classifications consistently consider Oxynaia a member of the subfamily Unioninae (in its various usages [11][12][13][14]. ...
Article
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The freshwater mussel genus Oxynaia Haas, 1911 is thought to be comprised of two geographically disjunct and morphologically variable species groups but the monophyly of this taxon has yet to be tested in any modern cladistic sense. This generic hypothesis has important systematic and biogeographic implications as Oxynaia is the type genus of the currently recognized tribe Oxynaiini (Parreysiinae) and is one of the few genera thought to cross several biogeographically important barriers in Southeast Asia. Morphological and molecular data clearly demonstrate that Oxynaia is not monophyletic, and the type species and its allies (O. jourdyi group) belong to the Unioninae, and more specifically as members of the genus Nodularia Conrad, 1853. Therefore, neither Oxynaia syn. nov. nor Oxynaiini Starobogatov, 1970 are applicable to the Parreysiinae and in the absence of an available name, Indochinella gen. nov. and Indochinellini trib. nov. are described. Several combinations are proposed as follows: Indochinella pugio (Benson, 1862) gen. et comb. nov., Nodularia jourdyi (Morlet, 1886) comb. res., N. gladiator (Ancey, 1881) comb. res., N. diespiter (Mabille, 1887) comb. res. and N. micheloti (Morlet, 1886) comb. res. Finally, we provide an updated freshwater biogeographic division of Southeast Asia.
... A preliminary list of freshwater bivalve taxa from Vietnam from literature and museum data was included in the summary of the East and Southeast Asia freshwater bivalve fauna by Zieritz et al. (2017). Analyzing molecular data, the Unionidae has been confirmed as a monophyletic clade (Hoeh et al. 1998, *Corresponding Author: arthur.bogan@naturalsciences.org 1 2001, 2002Roe and Hoeh 2003;Graf and Cummings 2006;Breton et al. 2007Breton et al. , 2010Doucet-Beaupré et al. 2010;Whelan et al. 2011;Pfeiffer and Graf 2015). The most recent phylogenetic classification within the modern Unionidae is that of Lopes-Lima et al. (2017) and Bolotov et al. (2017). ...
Article
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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.
... Graf & Cummins (2006) suggested that Paleoheterodonta is monophyletic and divided Unionoida in two clades: Unionoidea (Unionidae + Margaratiferidae) and Etherioidea (Hyriidae + Etheriidae + Mycetopodidae + Iridinidae). Unlike other authors (e.g., Hoeh et al. 2001), Graf & Cummings (2006) suggested the monophyly of Unionidae and Etheriidae, condition latter also supported by Whelan et al. (2011). In that scheme, Unionoidea is the basal group of Unionida, while Hyriidae is the basal group of Etherioidea. ...
Article
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Unionida is the most diverse clade of freshwater bivalves. Among the groups occurring in South America, one with the highest number of species is Rhipidodontini (Hyriidae, Unionida, Paleoheterodonta, Bivalvia). However several issues remains on taxonomy and systematic of this group, leading to problems on species identification, description, as also as a limiting factor to other type of studies (e.g., ecology, conservation,…). In this paper is presented a synthesis of available knowledge about Diplodon Spix in Wagner, 1827 and Rhipidodonta Mörch, 1853 in South America, as a first step in order to a better understating of Rhipidodontini. The evaluation of different authors exposes the little agreement between them that resulted in a sort of divergent taxonomical opinions. Some comments on ecology, conservation and habitat preferences were made. This work can also encourage future research on taxonomy, systematic, ecology and conservation of freshwater mussels in South America.
... The Unionidae is Earth's most diverse freshwater bivalve family and is well-known for its imperiled conservation status and remarkable parasitic life history (Barnhart et al., 2008;Graf, 2013;Haag & Williams, 2013). Although the higher-level classification of the Unionidae is unstable (Whelan et al., 2011;Pfeiffer & Graf, 2015;Lopes-Lima et al., 2016;Bolotov et al., 2017), it remains clear that the subfamily Ambleminae has experienced the most dramatic evolutionary radiation, representing over half of the species-level diversity of the family. The Ambleminae is distributed across much of North America, occupying most permanent freshwater habitats east of the Continental Divide of the Americas, from northern Canada south to the Isthmus of Panama. ...
Article
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Megalonaias is the most geographically widespread genus of the subfamily Ambleminae and is distributed across much of the eastern half of North America, from Minnesota to Nicaragua. Despite the large geographic distribution, the species-level diversity of Megalonaias is quite depauperate (2 spp.), suggesting the genus may not be constrained by the same physical, ecological, or physiological barriers that limit dispersal in many other amblemines. However, this hypothesis is contingent on the assumption that the current taxonomy of Megalonaias accurately reflects its evolutionary history, which remains incompletely understood due to the marginalization of Mesoamerican populations in systematic research. Using one mitochondrial (COI) and one nuclear marker (ITS1) sequenced from 41 individuals distributed across both the Neartic and Mesoamerican ecoregions, we set out to better understand the species boundaries and genetic diversity within Megalonaias. The reconstructed molecular phylogeny and the observed genetic diversity suggests that Megalonaias is a monotypic genus and that Megalonaias nickliniana, currently considered a federally endangered species, is not a valid species. These results are discussed in the context of their systematic and conservation implications, as well as how the unusual life history strategy of Megalonaias may be influencing its molecular diversity.
... Genetic studies, based on molecular data have been carried out on freshwater bivalves from Australia, North America, Europe and Africa, mainly to clarify systematic classifications (Graf et al., 2014Santos-Neto et al., 2016;Lopes-Lima et al., 2017), but also to evaluate their population structure, variability and demography (Hughes et al., 2004;Mock et al., 2010;Jones et al., 2015;Froufe et al., 2014Froufe et al., , 2016aInoue & Berg, 2017). Only a few genetic studies (Whelan et al., 2011;Graf et al., 2015;Santos-Neto et al., 2016;Combosch et al. 2017) have included Hyriidae from the Amazon region, all of which were used to establish phylogenetic relationships. ...
... Genetic studies, based on molecular data have been carried out on freshwater bivalves from Australia, North America, Europe and Africa, mainly to clarify systematic classifications (Graf et al., 2014Santos-Neto et al., 2016;Lopes-Lima et al., 2017), but also to evaluate their population structure, variability and demography (Hughes et al., 2004;Mock et al., 2010;Jones et al., 2015;Froufe et al., 2014Froufe et al., , 2016aInoue & Berg, 2017). Only a few genetic studies (Whelan et al., 2011;Graf et al., 2015;Santos-Neto et al., 2016;Combosch et al. 2017) have included Hyriidae from the Amazon region, all of which were used to establish phylogenetic relationships. ...
Article
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Triplodon corrugatus is a freshwater bivalve (Hyriidae) endemic to the Amazon, Orinoco and Tocantins basins, and the Piriá river. Our understanding of hyriid diversity at, and below, the species level, remains poor. The genetic diversity of T. corrugatus from the Tapajós, Amazon, Tocantins, Irituia and Piriá rivers in the north-eastern Brazilian Amazon was investigated. Except for the Irituia, where a single COII–COI haplotype had been fixed, all the other populations had medium to high haplotype diversities, and all populations had low nucleotide diversities. Pairwise fixation indices indicated that all populations were structured, except for comparisons between the Tapajós and Amazon, and the Amazon and Tocantins rivers, which may be explained by a stepping-stone model of migration. AMOVA detected that 81.28% of the variation was among populations. However, STRUCTURE analyses corroborated only the Piriá river specimens as comprising a distinct population, which is being maintained by allopatry due to the current isolation between the Piriá, and the Amazon and Tocantins basins.
... Graf & Cummings (2006 presented the first molecular phylogeny and subsequent classification for the Unionida, but resolution of (sub)tropical lineages was limited, particularly for Asia. Since then, further revisions, focused on including representatives from the (sub)tropical and Asian fauna, have substantially refined our understanding of freshwater mussel evolution and their higher-level classification (Zhou et al., 2007;Whelan et al., 2011;Pfeiffer & Graf, 2013. Very recently, Lopes-Lima et al. (2017b) published a long-overdue, revised molecular phylogeny of the most species-rich freshwater mussel family Unionidae with much improved taxon sampling, particularly with respect to Asian taxa. ...
Article
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Recent research efforts have significantly advanced our knowledge on Asian freshwater mussel (Bivalvia: Unionida) diversity and distribution. Here we provide a modern consensus of the diversity, biogeography and conservation of Unionida in the region comprising East and Southeast Asia (excluding Wallacea) and Asian Russia. A data review confirmed the presence of 228 native and 3 non-native Unionida (98% Unionidae, 2% Margaritiferidae), rendering the region a global hotspot of freshwater mussel diversity. Species richness was highest in China (particularly Yangtze basin) in absolute numbers and Cambodia when correcting for country area, and decreased gradually towards the south and steeply towards the north and east. Six of the seven unionid subfamilies are native to the region, with species richness peaking in Southeast Asia for Rectidentinae, Gonideinae, Parreysiinae and Modellnaiinae, China for Anodontinae and Unioninae, and Asian Russia for Margaritiferidae. Conservation status and data collected after 1980 were not available for 61 and 24% of species, respectively. Dams, deforestation and pollution are likely the major threats to mussels in the region, though data in this respect are scarce. The Philippines, Laos, Indonesia, Myanmar and Malaysia are among the countries with the poorest data availability and urgently require research.
... Therefore, most of the published Unionida phylogenies use a combination of two out of three mtDNA genes: Cytochrome c oxidase subunit 1 (COX1), 16S ribosomal RNA (16S-rRNA) and NADH ubiquinone oxidoreductase core subunit 1 (ND1) (e.g. Graf & Cummings 2006;Whelan et al. 2011;Campbell & Lydeard 2012;Pri e & Puillandre 2014). Curiously, no studies have been published so far, exploring which of these gene combinations best represent the concatenated mtDNA phylogeny. ...
Article
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We have sequenced the female and male mtDNA of Unio delphinus and inferred the Unionidae phylogeny using 41 complete mtDNA sequences. Additionally, we compared the concatenated mtDNA trees with those using single or combination of two mtDNA genes to identify the best genes to use in the absence of complete mitogenomes. The gender-specific mtDNAs of U. delphinus contain all Unionida mtDNA specific features. The mtDNA phylogeny supports the reciprocal monophyly of the gender-specific clades but it was inconclusive regarding Unionidae subfamilies relationships. The gene trees topologies using ND5 or 16S-rRNA with ND1 were the closest trees to the mtDNA trees.
... Heard [1977] also used the genus name Uniandra. According to Brandt [1974], the genus name Uniandra is used in this paper instead of Contradens; classification of subfamilies is given after Whelan et al. [2011] and Huang et al. [2013]. Previously, U. contradens together with many other Asian bivalves were included into the family Amblemidae [Panha, Eongprakornkeaw, 1995]. ...
Article
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Morphology of bilaterally asymmetrical (unequivalve, unequilateral) glochidia of the freshwater bivalve Uniandra contradens Lea, 1838 from the Binh Thien Lake, southern Vietnam, was studied by scanning electron microscopy. Unique characteristics of the outer valve microsculpture is described. Literature data on the south-east Asian freshwater mussels with asymmetrical glochidia are reviewed.
Article
The Xunhua Basin, a subbasin of the Longzhong Basin in an arid region of the northeastern Tibetan Plateau, hosts a thick succession of Upper Cenozoic fluvial-lacustrine sediments containing climate-sensitive freshwater mollusks, which can provide key insights into the uplift history of the Tibetan Plateau and its relationship to global climate change. In this study, we studied six genera and eleven species of freshwater mussels of the family Unionidae from the Upper Miocene Liushu Formation of the Xunhua Basin. These genera include Unio, Acuticosta, Anodonta, Cristaria, Lanceolaria and Ptychorhynchus. The fossils not only enhance our understanding of biological diversity on the Miocene Tibetan Plateau but also shed light on the biological response to Late Cenozoic orogenic uplift and environmental changes. The Unionidae family is present in modern China mainly in freshwater lakes on the middle and lower reaches of the Yangtze River Basin, i.e., in a humid subtropical monsoonal climate, and it has been extinct in northwestern China (including Qinghai Province) since the Late Miocene. This modern distribution implies that environmental conditions in the Xunhua Basin during the Late Miocene were substantially more humid than at present. Such a sharp contrast in habitat to that of the modern Xunhua Basin implies that a Late Miocene climate shift on the NE Tibetan Plateau occurred after 8.2 Ma, i.e., a climatic drying and cooling trend triggered both by regional tectonic uplift and global climate change, which significantly impacted freshwater ecosystems in the Xunhua Basin.
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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.
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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.
Preprint
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.
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Freshwater mussels cannot spread through oceanic barriers and represent a suitable model to test the continental drift patterns. Here, we reconstruct the diversification of Oriental freshwater mussels (Unionidae) and revise their taxonomy. We show that the Indian Subcontinent harbors a rather taxonomically poor fauna, containing 25 freshwater mussel species from one subfamily (Parreysiinae). This subfamily most likely originated in East Gondwana in the Jurassic and its representatives arrived to Asia on two Gondwanan fragments (Indian Plate and Burma Terrane). We propose that the Burma Terrane was connected with the Indian Plate through the Greater India up to the terminal Cretaceous. Later on, during the entire Paleogene epoch, these blocks have served as isolated evolutionary hotspots for freshwater mussels. The Burma Terrane collided with mainland Asia in the Late Eocene, leading to the origin of the Mekong’s Indochinellini radiation. Our findings indicate that the Burma Terrane had played a major role as a Gondwanan “biotic ferry” alongside with the Indian Plate.
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The tribes Contradentini and Rectidentini (Unionidae) comprise a diverse clade of freshwater mussels endemic to South-east Asia. Our understanding of the diversity and phylogeny of this radiation has improved dramatically in recent years, but this systematic transformation has not yet benefited from comprehensive museum sampling or phylogenomic methods. A synthetic taxonomic revision of the Contradentini+Rectidentini that leverages these useful and accessible methods is needed. We set out to (1) generate a phylogenomic reconstruction of the supraspecific relationships of the Contradentini+Rectidentini using anchored hybrid enrichment, (2) revise the taxonomy and geographic boundaries of the generic and species-level diversity of the radiation, and (3) identify patterns of freshwater mussel diversity and distribution in this clade and discuss the processes that may have precipitated them. Our phylogenomic reconstruction using over 1600 loci, with a total alignment length of over a half a million nucleotides, recovers a well supported phylogeny of the clade that resolves four independent multispecies radiations endemic to the Mekong drainage. We examined, digitised, and imaged 1837 records from 15 natural history museums that provided the necessary data to document the morphological variation and geographic distributions of the focal taxa. We also analysed 860 COI sequences, 519 of which were generated in this study, to better understand the species boundaries and geographic distributions of the recovered clades. We recognise 54 valid species in the tribes Contradentini and Rectidentini, including 9 described herein as new to science. Out of this revision emerged several interesting biogeographic patterns that appear to have resulted from recent stream capture, historical confluence, and intradrainage barriers to dispersal. We hypothesise that these phenomena shaped the diversity and distribution of the Contradentini+Rectidentini, contributing to the formation of several characteristic freshwater mussel provinces in South-east Asia.
Chapter
Bivalves commonly associate with other organisms, however, examples of true parasitic associations are described only for members of the marine superfamily Galeommatoidea (two species of approximately 500 known species, facultative parasitism) and the larvae of members of the freshwater order Unionida (almost all of 958 known species, obligate parasitism). The evolution toward such a close relationship required establishing a close association with the host’s body, resulting in being enclosed within its tissues. Clear adaptations to the host species are observed in both groups. Most galeommatoideans live in soft sediments and are associated with other benthic organisms or their burrows—settlement in a burrow or on/within the host’s body protects these little bivalves, while life activity of the host possibly ensures oxygenated water currents with a food source for the bivalve. However, a few recent examples of bivalve settlement within the body cavity of crabs (believed as accidental, nevertheless bivalves feed in the crab's hemocoel), or in the oesophagus of holothurians (common, presumably nutrition from the host is possible) indicate possible pathways for an evolutionary transition from free- or commensal-living to a parasitic lifestyle. Unionoids, large freshwater bivalves, are characterized by their tiny larvae that parasitize fish. This close relationship primarily benefits bivalves through enhanced dispersal abilities, but fish tissues may also serve as a source of nutrients for the larvae. Parasitic association likely established when close and common contact of both associates could happen, thus one may hypothesize a fish that lived close to the bottom of lakes and rivers (including durophagous species) as a likely host at the beginning of their co-evolution. Accidental contact of the larvae with the body of fishes (during predation on bivalves or caused by anti-sinking mucous or the larval threads tangled with fish) could result in increased bivalve dispersal. Subsequently, firmer attachment on fish tissues was acquired, followed by encapsulation of the larva within the host epithelium. This might have allowed for the feeding on host tissues, but required developing resistance to the host’s immune system, which might have further strengthened their association.
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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/).
Article
The Indotropical freshwater mussel assemblage has more genera of uncertain subfamily-level position (i.e. genera incertae sedis) than all other regional faunas. Of the 16 genera incertae sedis in the Indotropics, only two, Harmandia and Unionetta, are distributed in the mainland southeast Asia subregion. Resolving the enigmatic systematic position of Harmandia and Unionetta would finally establish a complete subfamily-level classification for the freshwater mussel genera of southeast Asia and facilitate more comprehensive evaluation of regional freshwater mussel diversity and distribution. Molecular phylogenetic reconstructions using the nuclear–encoded large ribosomal subunit rRNA (28S) and the mitochondrial protein-coding cytochrome c oxidase subunit I (COI) recovered Harmandia and Unionetta in the Indo-Afrotropical subfamily Parreysiinae, and more specifically as members of the tribe Indochinellini (formerly Oxynaiini). Harmandia is shown to be polyphyletic with its former species belonging to three distantly related clades of the Unionoida (i.e. Parreysiinae, Rectidentinae and Hyriidae). Unionetta was likewise not recovered as monophyletic, despite the strong morphological similarities and close geographic proximity of the sequenced individuals. Based on a synthesis of molecular, morphological and biogeographic data, the taxonomy and geographic distributions of Harmandia and Unionetta are revised. These results are discussed in the context of the dispersal of the Parreyssiinae into Southeast Asia and the species-level diversity of the Indochinellini in the Mekong River.
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On the basis of previously published materials, which include data on the morphology of the shells of adult mollusks and larvae (glochidia), as well as the results of molecular phylogenetic studies, a critical analysis of the subspecies taxonomy of the Far Eastern Unionidae Rafinesque, 1820, namely, the subfamilies Unioninae Rafinesque, 1820 and Anodontinae Rafinesque, 1820, has been performed. It is noted that the previously described subfamily Nodulariinae Starobogatov et Zatrawkin, 1987 can be regarded as the tribe Nodulariini. The systematic position of all genera of Unionidae inhabiting the Russian Far East is discussed. An updated list of the genera, tribes, and subfamilies of Unionidae is given for this region.
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Accurate phylogenies are important for understanding the evolutionary histories of organisms, their reproductive traits and ecological habits. The freshwater mussel order Unionida is currently thought to include six families. However, assignment of particular species to these families has been unstable, particularly for species that have been described solely on conchological characters. Unio polystictus Heude, 1877 represents such a species. Based on DNA sequence data from five genes (COI, 16S rRNA, 18S rRNA, 28S rRNA and histone H3) and complete mitochondrial genomes, we investigated the phylogenetic position and generic affinities of U. polystictus using various analytical methods. Both the five-gene and mitogenome datasets strongly supported transferring U. polystictus from Margaritiferidae to Unionidae as Aculamprotula polysticta, comb. res. Our results also supported the following intrageneric relationships: (Aculamprotula tortuosa, ((Aculamprotula polysticta, Aculamprotula scripta), (Aculamprotula fibrosa, Aculamprotula tientsinersis))). In addition, by comparing the morphological features of Aculamprotula (Unionidae, Unioninae), Lamprotula (Unionidae, Gonideinae) and Gibbosula (Margaritiferidae, Gibbosulinae) species, potential issues of relying solely on shell morphology for high-level classification of freshwater mussels are highlighted. Confirmation of classification position and genetic relationship for Aculamprotula polysticta will helpful to understand the ecological characteristics, reproductive strategies and host-fish requirements, which can be inferred from closely related taxa.
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South-western Australia is isolated from other forested regions of Australia by desert and bounded on southern and western sides by the Southern and Indian Oceans, respectively, with Westralunio carteri (Iredale, 1934) as the sole endemic freshwater mussel. Its conservation status is vulnerable. This species has a history of nomenclatural change and its systematic placement and population genetic history are largely unknown. We sampled 46 individuals from 13 sites across W. carteri’s distribution and sequenced two mitochondrial genes (16S rDNA and cytochrome c oxidase subunit I) and one nuclear gene (28S rDNA). The mitochondrial haplotype networks and COI phylogenies revealed three evolutionarily significant units (ESUs): “W. carteri” I including the west coast populations, “W. carteri” II from the south and south-eastern range, and “W. carteri” III only occurring in the south-western tip of Australia. Four species delimitation methods identified two molecular operational taxonomic units supporting two distinct species (“W. carteri” I and “W. carteri” II + III). Phylogeographic patterns revealed herein confirm the historical separation of Western and Southern paleo-basins, also highlighting the isolation of the southwestern extremity of the region. This underlines the need for taxonomic revision and will require a reevaluation of W. carteri’s conservation status.
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Freshwater mussels (Bivalvia: Unionidae) is a diverse family with around 700 species being widespread in the Northern Hemisphere and Africa. These animals fulfill important ecological functions and provide important services to humans. Unfortunately, populations have declined dramatically over the last century, rendering Unionidae one of the world’s most imperiled taxonomic groups. In Far East Asia (comprising Japan, Korea, and Eastern Russia), conservation actions have been hindered by a lack of basic information on the number, identity, distribution and phylogenetic relationships of species. Available knowledge is restricted to studies on national and sub-national levels. The present study aims to resolve the diversity, biogeography and phylogenetic relationships of the Far East Asian Unionidae in a globally comprehensive phylogenetic and systematic context. We reassessed the systematics of all Unionidae species in the region, including newly collected specimens from across Japan, South Korea, and Russia, based on molecular (including molecular species delineation and a COI + 28S phylogeny) and comparative morphological analyses. Biogeographical patterns were then assessed based on available species distribution data from the authors and previous reference works. We revealed that Unionidae species richness in Far East Asia is 30% higher than previously assumed, counting 43 species (41 native + 2 alien) within two Unionidae subfamilies, the Unioninae (32 + 1) and Gonideinae (9 + 1). Four of these species are new to science, i.e. Beringiana gosannensis sp. nov., Beringiana fukuharai sp. nov., Buldowskia kamiyai sp. nov., and Koreosolenaia sitgyensis gen. & sp. nov.. We also propose a replacement name for Nodularia sinulata, i.e. Nodularia breviconcha nom. nov. and describe a new tribe (Middendorffinaiini tribe nov.) within the Unioninae subfamily. Biogeographical patterns indicate that this fauna is related to that from China south to Vietnam until the Mekong River basin. The Japanese islands of Honshu, Shikoku, Kyushu, Hokkaido, and the Korean Peninsula were identified as areas of particularly high conservation value, owing to high rates of endemism, diversity and habitat loss. The genetically unique species within the genera Amuranodonta, Obovalis, Koreosolenaia gen. nov. and Middendorffinaia are of high conservation concern.
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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.
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Doubt regarding the history of phylogenesis within the Unionoida have hampered attempts to understand evolution within the group and to establish a stable classification system. To test alternative hypotheses of unionoid phylogeny, 630 base pairs of DNA sequence for the cytochrome c oxidase subunit I (COl) gene were obtained from 30 species representing the higher taxa within the Unionoida (= ingroup) and one species (Neotrigonia margaritacea) representing the Trigonioida (= outgroup). Both parsimony and neighbor-joining algorithms were employed to generate phylogenetic trees from rhe COl nucleotide sequences. All phy-logenetic analyses produced trees with the following topology: ((Unionidae rexcluding CoelatllraJ, Margaritiferidae), Coelatura). (Mutelidae. Myceropodidae». Hyriidae). The Hyriidae, Margaritiferidae, Mutelidae. Mycetopodidae. and Etherioidea were supported as monophyletic groups while the Unionidae and Unionoidea were judged paraphyletic. These phylogenetic relationships suggest that (1) hyriids. rather than margaritiferids, are a product of the most basal cladogenic event in the ancestral unionoid lineage, (2) the lineage ancestral to unionoids arose on one of the Gondwanalandian landmasses. (3) the glochidium is the ancestral unionoid larval type, and (4) endobranchial brooding is ancestral in unionoids followed by a transition to tetrageny which subsequently gave rise to eClobranchy.
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Some anatomical, adult shell and larval features of Unto coffer Krauss are described and compared to those reported in previous accounts of this and other species. The findings necessitate the removal of U. caffer from the nominal genus Cafferia Simpson, for which it is the type species, and its return to the genus Unio Pbilipsson, in the Unionidae: Unioninae. Cafferia consequently becomes a junior subjective synonym of Unto.Unio caffer is characterized in part by zigzag beak sculpture, dimorphic septal spacing between the marsupial, outer (comparatively dense) and the non-marsupial, inner (more distant) demibranchs and also within the marsupial demibranchs, the presence of perforated marsupial septa and imperforate non-marsupial septa, the occurrence of hermaphrodites in some but apparently not all populations, production of subtriangular glochidia with a hook at the ventral margin of each valve, short-term incubation of larvae in the marsupial demibranchs, and by its disjunct occurrence in the southern Ethiopian region (other Unio occurring only in the Palearctic).These adult shell and anatomical features relate this species to those of several nominal genera in the Oriental region, although the latter are distinguished from it by the production of subovate, hookless glochidia.
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The Hyriidae (Mollusca: Bivalvia: Unionoida) have a disjunct distribution, occurring on South America, Australia, and New Zealand. Most previous macroevolutionary studies of the Hyriidae pre-dated widespread acceptance of both continental drift and phylogenetic systematics. For this study, we applied molecular phylogenetic techniques to test the hypothesis that the observed disjunction of Australasian hyriids across the Tasman Sea is due to the disintegration of Gondwanaland (>80 million years ago). We sequenced a fragment of 28S rDNA for representative hyriid Velesunionini (Australia), Hyridellini (Australia and New Zealand), and Hyriinae (South America) and for outgroups belonging to the unionoid families Margaritiferidae and Unionidae. The topology of the single 28S tree [i.e., (Margaritiferidae, Unionidae, (Velesunionini, (Hyridellini, Hyriinae)))] recovered by both maximum parsimony and maximum likelihood did not support a monophyletic Australasian clade, and the branch lengths were consistent with Mesozoic vicariance. We also acquired COI sequences for the Australian subset of mussels to corroborate the 28S branch lengths. Our results suggest that (1) the Hyriidae pre-date the break up of Gondwanaland and (2) the New Zealand Hyridellini are relics rather than colonizers. Alternative long-distance dispersal hypotheses are discussed in the context of our results, historical geology, and mussel life history.
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In freshwater bivalves development takes place in three ways (Fig. 6.1). 1. By producing veliger larvae as in Dreissena polymorpha, which is particularly successful wherever it first appears. 2. By releasing fully developed young mussels from brood pouches (viviparity) as in Sphaeriidae. 3. By passing early development as a parasitic stage on a host as in naiads (Unionoida).
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Some 1,048 names at the rank of subtribe, tribe, subfamily, family and superfamily have been proposed for Recent and fossil bivalves. All names are listed in a nomenclator giving full bibliographical reference, date of publication, type genus, and their nomenclatural availability and validity under the International Code of Zoological Nomenclature. Another 274 names, established for categories above the family-group are listed separately. A working classification attempts to group all bivalve family-group names into a single system based on current hypotheses of relations and synonymies. At several rank levels, the groups are given in alphabetical rather than some assumed phylogenetic arrangement, reflecting current uncertainties and conflicting results from anatomical, molecular, and fossil data. Altogether, the classification recognizes as valid a total of 324 families, of which 214 are known exclusively as fossils and 110 occur in the Recent with or without a fossil record. Key words: Bivalvia, nomenclature, taxonomy, taxon listing.
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Using an approach based on molecular, reproductive and morphological characters, four independent evolutionary lineages represented by the following species were identified in Tunisia: Unio ravoisieri Deshayes, U. gibbus Spengler, U. durieui Deshayes and Potomida littoralis (Cuvier). The species U. ravoisieri and U. durieui are redescribed, including details of their distribution, biology and glochidium morphology. The puzzling distribution of the former (Algeria, Tunisia and two localities in Northeast Spain) could reflect introduction or natural dispersal. In Tunisia, the release of the glochidia of U. ravoisieri starts in March, but in Spain this is delayed until August or September. The entire interlamellar space of the outer demibranchs acts as a marsupium (ectobranchy). Glochidia are rounded-triangular, globose, and either hooked or hookless. Unio durieui is distributed across Algeria and Tunisia, where it releases glochidia in December and in March. Glochidia are always hooked, but the elaboration of the hook is variable. The molecular phylogenetic analysis supports two clusters within Unio, each including both European and North African species. Strong bootstrap support was obtained for the two clades within U. ravoisieri, of which one includes specimens from the Iberian Peninsula as well as Tunisia. Unio durieui appeared as the sister species of U. gibbus. The Tunisian populations of P. littoralis were not segregated from those in Europe, and U. fellmanni should be considered a synonym.
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Summary •For biological community data (species-by-sample abundance matrices), Warwick & Clarke (1995) defined two biodiversity indices, capturing the structure not only of the distribution of abundances amongst species but also the taxonomic relatedness of the species in each sample. The first index, taxonomic diversity (), can be thought of as the average taxonomic ‘distance’ between any two organisms, chosen at random from the sample: this distance can be visualized simply as the length of the path connecting these two organisms, traced through (say) a Linnean or phylogenetic classification of the full set of species involved. The second index, taxonomic distinctness (*), is the average path length between any two randomly chosen individuals, conditional on them being from different species. This is equivalent to dividing taxonomic diversity, , by the value it would take were there to be no taxonomic hierarchy (all species belonging to the same genus). * can therefore be seen as a measure of pure taxonomic relatedness, whereas  mixes taxonomic relatedness with the evenness properties of the abundance distribution. •This paper explores the statistical sampling properties of  and *. Taxonomic diversity is seen to be a natural extension of a form of Simpson's index, incorporating taxonomic (or phylogenetic) information. Importantly for practical comparisons, both  and * are shown not to be dependent, on average, on the degree of sampling effort involved in the data collection; this is in sharp contrast with those diversity measures that are strongly influenced by the number of observed species. •The special case where the data consist only of presence/absence information is dealt with in detail:  and * converge to the same statistic (+), which is now defined as the average taxonomic path length between any two randomly chosen species. Its lack of dependence, in mean value, on sampling effort implies that + can be compared across studies with differing and uncontrolled degrees of sampling effort (subject to assumptions concerning comparable taxonomic accuracy). This may be of particular significance for historic (diffusely collected) species lists from different localities or regions, which at first sight may seem unamenable to valid diversity comparison of any sort. •Furthermore, a randomization test is possible, to detect a difference in the taxonomic distinctness, for any observed set of species, from the ‘expected’+ value derived from a master species list for the relevant group of organisms. The exact randomization procedure requires heavy computation, and an approximation is developed, by deriving an appropriate variance formula. This leads to a ‘confidence funnel’ against which distinctness values for any specific area, pollution condition, habitat type, etc., can be checked, and formally addresses the question of whether a putatively impacted locality has a ‘lower than expected’ taxonomic spread. The procedure is illustrated for the UK species list of free-living marine nematodes and sets of samples from intertidal sites in two localities, the Exe estuary and the Firth of Clyde.
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INTRODUCTIONHoeh, Bogan, Heard & Chapman (2009; hereafter HBHC) raise a number of important criticisms of our recent analysis of family-level relationships among the lineages of the Palaeoheterodonta, Graf & Cummings (2006; hereafter G&C). We are pleased to have our conclusions scrutinized from other perspec-tives. HBHC also raise a number of questions about issues that we apparently did not explain LQ�VXI?FLHQW�GHWDLO��DQG�WKH\�UHSRUW�WKDW�WKH�results of their reanalyses challenge our conclu-sions. We welcome their reanalysis and discus-sion.The objective of this article is to keep that debate alive by replying to HBHC.+%+&�GLVFXVV�DW�OHDVW�?YH�SRLQWV�RI�GLV-agreement with our methods of analysis or conclusions:(1) We did not include (or adequately jus-tify exclusion of) COI sequences from the non-palaeoheterodont outgroup taxa (i.e.,
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A robust phylogeny for the Unionoida is emerging and presumed relationships of home major clades are being questioned. The Etheriidae or freshwater oysters has been a distinct family for over 160 years and currently contains three cemented genera: Acostaea (Columbia. South America), Pseudomulleria (India) and Etheria (Africa and Madagascar). Starobogatov (1970 Nauka. 1-372). Mansur and da Silva (1990, Amazoniana. 11(2), 147-166) and Bonetto (1997, Biociencias, 5, 113-142) present conflicting testable hypotheses regarding the evolution of these taxa. Using cytochrome c oxidase subunit I DNA sequences the evolutionary relationships of these three genera has been examined, by comparing them to representatives of 30 other unionoid taxa from around the world. These analyses place Acostaea and Etheria within the Mycetopodidae while Pseudomulleria falls within the Unionidae. A monophyletic Etheriidae. composed of cemented freshwater bivalves, is not supported by the present analyses. Furthermore. the analyses indicate that cementation in the Unionoida has evolved at least twice.
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The freshwater mussel genera Unio (Palearctic) and Gonidea (Pacific Nearctic drainages) have been difficult to place in the classification of the Unionidae. This has been principally due to (1) a lack of appreciation for derived vs. ancestral characters and (2) a decoupling of taxonomy from evolutionary theory. To test cladistically the positions of Unio and Gonidea relative to the well-studied Nearctic genera of the Atlantic/Gulf of Mexico drainages, partial nuclear large-ribosomal subunit (28S rDNA) sequences were obtained from representative freshwater mussel lineages, including three genera from Southeast Asia. The phylogenetic reconstruction differs from the traditional placement of Unio among the Ambleminae; instead, Unio falls sister to anodontine mussels. Gonidea is sister to the remaining Nearctic Ambleminae, and these are distinct from the Asian 'amblemine' genera. Based on these results, the classification of the New World Unionidae is updated [i.e., Unioninae (= Unionini + Anodontini) + Ambleminae], and synapomorphies of the family are discussed.
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Bootstrapping is a common method for assessing confidence in phylogenetic analyses. Although bootstrapping was first applied in phylogenetics to assess the repeatability of a given result, bootstrap results are commonly interpreted as a measure of the probability that a phylogenetic estimate represents the true phylogeny. Here we use computer simulations and a laboratory-generated phylogeny to test bootstrapping results of parsimony analyses, both as measures of repeatability (i.e., the probability of repeating a result given a new sample of characters) and accuracy (i.e., the probability that a result represents the true phylogeny). Our results indicate that any given bootstrap proportion provides an unbiased but highly imprecise measure of repeatability, unless the actual probability of replicating the relevant result is nearly one. The imprecision of the estimate is great enough to render the estimate virtually useless as a measure of repeatability. Under conditions thought to be typical of most phylogenetic analyses, however, bootstrap proportions in majority-rule consensus trees provide biased but highly conservative estimates of the probability of correctly inferring the corresponding clades. Specifically, under conditions of equal rates of change, symmetric phylogenies, and internodal change of less-than-or-equal-to 20% of the characters, bootstrap proportions of greater-than-or-equal-to 70% usually correspond to a probability of greater-than-or-equal-to 95% that the corresponding clade is real. However, under conditions of very high rates of internodal change (approaching randomization of the characters among taxa) or highly unequal rates of change among taxa, bootstrap proportions >50% are overestimates of accuracy.
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Brooding characters have figured prominently in the classification of North American freshwater pearly mussels (Bivalvia: Unionoidea). The purpose of our study was to evaluate phylogenetic hypotheses of brooding character evolution in order to test homology statements suggested by earlier taxonomic systems of the Unionoidea. Parsimony analysis of partial COI sequences from 29 species of freshwater mussels and 13 outgroups were used to derive a phylogeny. Thirteen brooding characters (e.g., brooding period, marsupium arrangement, structure of interlamellar septa, etc.) were traced onto this phylogeny. Results indicate that long-term brooding (bradytictia) is the derived state among North American freshwater mussels; short-term brooding (tachytictia) is plesiomorphic. Bradytictia evolved independently in the Anodontinae and Lampsilini, with unique morphological modifications derived in those clades to facilitate long-term brooding.
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