The largest unassigned regions of the male- and female-transmitted mitochondrial DNAs in Musculista senhousia (Bivalvia Mytilidae)

Musculista senhousia is a marine mussel with doubly uniparental inheritance (DUI) of mitochondria. In this study we analyzed the largest unassigned region (LUR) of its female- and male-transmitted mitochondrial genomes, described their fine characteristics and searched for shared features. Our results suggest that both LURs contain the control region of their respective mitochondrial genomes. The female-transmitted control region is duplicated in tandem, with the two copies evolving in concert. This makes the F-mtDNA of M. senhousia the first Bivalve mitochondrial genome with this feature. We also compared M. senhousia control regions to that of other Mytilidae, and demonstrated that signals for basic mtDNA functions are retained over evolutionary times even among the fast-evolving mitochondrial genomes of DUI species. Finally, we discussed how similarities between female and male LURs may be explained in the context of DUI evolution and if the duplicated female control region might have influenced the DUI system in this species.     

Evolution of bilaterally asymmetrical larvae in freshwater mussels (Bivalvia: Unionoida: Unionidae)

Bilaterally asymmetrical glochidia (i.e. bivalved parasitic larvae bearing a large marginal appendage on a single valve) have been reported from five Asian freshwater mussel genera belonging to two separate subfamilies, the Gonideinae (i.e. Pseudodon, Solenaia, and Physunio) and Rectidentinae (i.e. Contradens and Trapezoideus). This classification requires that the bilaterally asymmetrical glochidium‐bearing mussels are not monophyletic, and suggests that this atypical larval morphology evolved twice in the same geographic region. Although homoplastic glochidium characters are known (e.g. marginal appendages and size), we hypothesized that bilaterally asymmetrical glochidia represent a novel morphological synapomorphy. We tested the monophyly of the mussels bearing bilaterally asymmetrical glochidia using a molecular matrix consisting of representatives from all six freshwater mussel families and three molecular markers (28S, 16S, and COI). Bayesian inference, maximum likelihood, and ancestral state reconstruction were employed to estimate the phylogeny and larval trait transformations. The reconstructed phylogeny rejects the monophyly of the asymmetrical glochidium‐bearing mussels and resolves two putative origins of asymmetrical glochidia; however, ancestral state reconstruction supports asymmetrical glochidia as a synapomorphy of only one supraspecific taxon of the Rectidentinae. In the Gonideinae, asymmetrical glochidia were autapomorphic of Pseudodon cambodjensis (Petit, 1865). That is, no other taxa resolved among the Gonideinae had bilaterally asymmetrical glochidia, including other Pseudodon species. We describe how the alleged intrageneric glochidial variation in Pseudodon, and in the other genera of the Gonideinae reported to have asymmetrical glochidia (i.e. Solenaia and Physunio), challenge the resolved convergence of asymmetrical glochidia. Our results are discussed in the context of freshwater mussel larval evolution, patterns in life‐history traits, and the classification of freshwater mussels generally. © 2015 The Linnean Society of London     

Mitochondrial genome of the cockscomb pearl mussel Cristaria plicata (Bivalvia, Unionoida, Unionidae)

The complete mitochondrial genome sequence of the cockscomb pearl mussel Cristaria plicata, which is an endangered species in South Korea, was sequenced. The circle genome (15,708 bp in size) consists of 13 protein-coding genes, 2 rRNA genes, and 22 tRNA genes. There were 26 noncoding regions (NCs) found throughout the mitogenome of C. plicata, ranging in size from 2 to 327 bp, and the two largest NC regions, NC286 and NC326, were found between ND5 and tRNA(Gln) (286 bp) and between tRNA(Glu) and ND2 (326 bp), respectively. The 13 mitochondrial protein-coding genes of a female individual of C. plicata collected from Korea (15,708 bp) were compared to those of the Chinese individual (15,712 bp) published before. The result showed that ND3 is the most conserved with 100% nucleotide similarity, and each of the other protein-coding genes has ca. 99%, respectively. The two largest NCs among 26 NCs have totally 98% nucleotide similarity between Korean and Chinese ones.     

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

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.     

Molecular phylogenetics and morphological variation reveal recent speciation in freshwater mussels of the genera Arcidens and Arkansia (Bivalvia: Unionidae)

Intra‐ and interspecific morphological variation due to both phenotypic plasticity and evolutionary convergence hinder the work of taxonomists and lead to over‐ and underestimates of species richness. Nevertheless, most species on Earth are recognized solely based on morphological characters. We used molecular phylogenetic and morphometric techniques to examine two freshwater mussel species. One is common and widespread, while the other is imperiled and endemic to the Interior Highlands of the USA. Phylogenetic and molecular clock analyses revealed that divergence of Arcidens confragosus and Arkansia wheeleri is small and relatively recent. Divergence in these and other taxa is probably due to isolation of streams in the Interior Highlands. Morphometric analyses showed distinct shell shapes using traditional morphometrics, but not through geometric morphometrics. Outlined shell shapes are indistinguishable; geometric morphometrics could not capture a three‐dimensional component. Our analyses support the validity of these two species as congeners, with the nomen Arcidens (Simpson 1900) having priority. Because shell morphologies are both heritable and environmentally determined, our study emphasizes the importance of considering both molecular and morphometric analyses for identification of freshwater molluscs of conservation concern. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 535–545.     

Complete sequences of maternally inherited mitochondrial genomes in musselsUnio pictorum (Bivalvia, Unionidae)

Mitochondrial genomes are frequently used to infer phylogenetic relationships. Some taxa are, however, poorly represented. To facilitate better understanding of the potential of mitochondrial genome data in freshwater mussels, we present here, for the first time, the mitochondrial sequences of 4 complete F-type mitochondrial genomes from the European freshwater bivalveUnio pictorum (Unionidae). These genomes are very compact (15 761 bp) but have a typical gene complement for bilaterian mitochondrial genomes and a very similar organization to other unionid genomes available in databases. Very low nucleotide diversity within the species suggests a small effective population size of PolishU. pictorum, a phenomenon of potential importance for environmental management policies.     

Sexual selection and simultaneous hermaphroditism among the Unionidae (Bivalvia: Mollusca)

Simultaneous hermaphroditism is an infrequent mode of reproduction among bivalves of the family Unionidae: only five of the 220 North American species are simultaneous hermaphrodites. However, hermaphroditic individuals of otherwise predominantly dioecious species have been encountered in 30 of I01 species examined. These hermaphroditic individuals as well as simultaneous hermaphrodites can exhibit considerable variability in the ratio of spermatogenic: oogenic tissue within the gonad, and the purposes of this paper are to determine the underlying causes of both this variability and the occurrence of occasional hermaphroditic individuals among dioecious species. Results indicate that the ratio of male: female gonodal tissue of a simultaneous hermaphrodite is bimodally distributed, and several hypotheses to account for this observation are presented. It is proposed that populations occurring in different habitats and under conditions of different individual density are subject to fundamentally different sexual selection pressures acting on ratios of allocation to male and female gametes. Occasional hermaphroditism among otherwise predominantly dioecious species was in this study associated with infection of the gonads by digenean trematodes. A model of sexual determination among unionids presented in this paper proposes that sex is determined by genetically controlled hormone levels: occasional hermaphrodites result from alterations in these hormone levels caused by developmental errors and trematodal infections which mimic the results of such errors. Predictions of this model are consistent with observed levels of variability in male: females gonadal tissue among occasional hermaphrodites.     

Isolation and characterization of microsatellite loci in Alasmidonta heterodon (Bivalvia: Unionidae)

We developed 13 species‐specific microsatellite markers for the federally endangered Atlantic slope unionid Alasmidonta heterodon. Four to 18 alleles per locus were observed among 30 individuals. Observed heterozygosity throughout the loci ranged from 26.9 to 86.2% and averaged 63.6%. Estimates of individual pairwise genetic distances indicated that levels of genetic diversity among loci were sufficient to produce unique multilocus genotypes for all animals surveyed. Randomization tests showed that genotypes for this collection were consistent with Hardy–Weinberg expectations, and no significant linkage disequilibrium was observed between loci. These loci therefore appear suitable for population surveys, kinship assessment and other such applications.     

New Trigonioidoidea (Bivalvia; Unionoida) from the Early Cretaceous of Spain

Abstract: Two taxa belonging to the Trigonioidoidea (Order Unionoida) are described from the Early Cretaceous of Spain. Nippononaia (Paranippononaia) camerana subgen. et sp. nov. is described from the Aptian of the Cameros Basin of the north‐west Iberian Range. Subnippononaia fordi Barker et al., 1997 is described from new material from the Calizas de la Huérguina Formation (Late Barremian) from Las Hoyas and Buenache de la Sierra, Cuenca Province, and Subnippononaia is raised to generic status. The stratigraphy and palaeoenvironment of the Cornago G exposure of the Enciso Group where Nippononaia (Paranippononaia) camerana originates is interpreted as a fresh to brackish water system.     

Phosphorus cycling by mussels (Unionidae : Bivalvia) in Lake St. Clair

The role of mussels in cycling phosphorus in Lake St. Clair during the May–October period was examined by measuring concentrations in the water column and in mussel tissue, and by measuring rates of biodeposition and excretion. Mean rates of biodeposition and excretion for Lampsilis radiata siliquoidea, the most abundant species, were 6.3 µg P (g shell-free dry wt)^-1 h^-1 and 1.3 µg P (g shell-free dry wt)^-1 h^-1, respectively; body tissue phosphorus content was 2.7 percent of dry wt. Seasonal changes in excretion rates appeared to be related to the gametogenic cycle of the organism, but seasonal changes in biodeposition rates were not apparent. Phosphorus assimilation efficiency for this species was about 40 percent. Overall, the mussel population in Lake St. Clair filtered about 210 MT of phosphorus, or about 13.5 percent of the total phosphorus load for the May–October study period. Of this amount, about 134 MT was sedimented to the bottom via biodeposition. Mussel biodeposition may be an important source of nutrients to other biotic components in the lake such as macrophytes and invertebrate deposit-feeders.     

The Morphology, Growth and Reproduction of Unionidae (Bivalvia) in a Fenland Waterway

The shell morphology and population dynamics of the five BritishUnionidae are compared within a sympatric population. Pseudanodontacomplanata is distinguished from Anodonta anatina and A. cygneaby the hinge length–shell length relationship; this morphologicaldistinction may serve as a useful tool in the identificationof this threatened species. The shell length at a given annuluswas remarkably similar for all five species, although the asymptoticlength is reached most quickly in P. complanata and Unio pictorum.P. complanata is relatively short-lived and attains the lowest maximumlength, while A. cygnea lives more than twice as long and attainsalmost double the length of P. complanata. Unio spp. have ashort gravid season over the summer, while Anodonta spp. havea long gravid period, lasting from Autumn through to Spring.Unlike other members of the Anodontinae, P. complanata has ashort breeding season, overlapping with that of the Unio spp. (Received 4 March 1998; accepted 23 April 1998)     

Python phylogenetics: inference from morphology and mitochondrial DNA

We used nucleotide sequences from four mitochondrial genes and structural features of the mitochondrial control region, combined with a revised, previously published, morphological data set to infer phylogenetic relationships among the pythons. We aimed to determine which of two competing hypotheses of relationships of the genera Aspidites and Python best explains the evolutionary and bioegeographical history of the family. All analyses of the combined data recover a set of relationships in which (1) the genus Python is paraphyletic with the two east Asian species, P. reticulatus and P. timoriensis , as the sister lineage to the seven Australo-Papuan python genera. We support recognition of a distinct genus for the P. reticulatus  +  P. timoriensis clade; (2) the remaining species of the genus Python form a clade which is the sister lineage to the remainder of the family; (3) the genus Aspidites is embedded among the Australo-Papuan genera. The seemingly primitive characteristics of Aspidites may be better interpreted as reversals or specializations that have accompanied a switch to burrowing in this genus. Resolution of the relationships among the Australo-Papuan lineages is weak, possibly because of rapid diversification early in the history of the radiation. We assessed the tempo of the Indo-Australian python radiation using a maximum likelihood framework based on the birth–death process. We find strong support for elevated speciation rates during the period when Australia collided with the proto-Indonesian archipelago. The data support an origin for pythons outside Australia, followed by a radiation into Australia during the mid-Tertiary.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 603–619.     

The origin and phylogeny of Margaritiferidae (Bivalvia,Unionoida): a synthesis of molecular and fossil data

The family Margaritiferidae is a small but widely distributed group within the Unionoida, or freshwater mussels, whose taxonomy and systematics has been the subject of numerous publications. Despite several efforts, there is no consensus on which characters reliably diagnose this family. Herein, we present the results of a phylogenetic analysis of the most comprehensive data set for Margaritiferidae in terms of taxa and phylogenetic markers assembled to date, including eleven out of the twelve margaritiferid species currently considered valid. In addition, we review the fossil record of the family and attempt to integrate fossil and DNA sequence data to provide a diagnosis of Margaritiferidae, identify its origin and biogeographic patterns, and determine the systematic relationships of its constituent species and their taxonomic affinities. We assembled a molecular data set comprised of five markers: COI, 16S, 28S, 18S and histone 3 for a total of 59 specimens representing eleven species of Margaritifera. Our results indicate that the family Margaritiferidae is a monophyletic group comprised of the single genus Margaritifera, which includes the following 12 species: M. dahurica, M. margaritifera, M. monodonta, M. middendorffi, M. laevis, M. marrianae, M. hembeli, M. falcata, M. laosensis, M. auricularia and M. marocana plus the unstudied M. homsensis. Estimates of divergence times using fossil calibrations or mean substitution rates produced dramatically different results. Divergence estimates based on the fossil calibrations were 10 times higher than those obtained applying the mean substitution rates. The current distribution of the family implies dispersal across marine or brackish waters by their host fish, leaving a fossil record on four continents that dates to the Mesozoic. Margaritiferidae appear to be derived from putative ancestor in the Silesunionidae, with a likely origin in Asia. We suggest that Margaritiferidae had spread along the Tethys margins and crossed the Atlantic already in the Late Triassic or Early Jurassic. Further dispersal events, in the Late Cretaceous or Eocene, may be linked to salinity‐depleted coastal waters or freshwater layering.     

Molecular genetics of peripheral populations of Nova Scotian Unionidae (Mollusca: Bivalvia)

Peripheral populations of eight species of freshwater bivalves (Unionidae.) extending their geographic ranges into Nova Scotia, Canada, were examined electrophoretically to determine both the extent of genetic variability within such populations, and whether the hypothesized pathway of colonization across the Isthmus of Chignecto is reflected in patterns of genetic resemblance among these populations. The Nova Scotian species examined could be separated into two groups based on levels of observed heterozygosity and levels of variability in allele frequencies. The first group is characterized by low levels of heterozygosity and polymorphism compared with north-eastern American populations, and in the case of one species, Elliptio complanala, considerable variability in allele frequencies among populations occurring in similar habitats in different drainages. Populations of E. complanata from Nova Scotia can be differentiated from conspecific populations on the southern Atlantic Slope by possession of fast alleles at two loci. Multivariate analyses define subgroups within populations of E. complanata consistent with hypothesis that the species invaded Nova Scotia by way of the Isthmus of Chignecto, and then split into two groups, one of which colonized Cape Breton to the north and the other of which colonized southern areas of the Province. The second group of Nova Scotian species is characterized by little reduction in heterozygosity and polymorphism compared with values observed among north-eastern American conspecifics or congeners, little variability in allele frequencies from population to population, and little evidence to suggest that these species were dependent on the land bridge to invade the Province. The type of dispersal is hypothesized to be responsible, in part, for these differences: larvae of species in the first group rely on a parasitic attachment to fish with territorial habits limited to fresh water, and are thus likely to invade new drainages separated by salt water by chance, in small numbers, and in stepping-stone fashion. Species in the second group parasitize anadromous or saltwater tolerant hosts, are likely to be introduced into new habitats in greater numbers and/or receive greater amounts of gene flow subsequent to colonization, and seem less dependent on land-bridges to colonize new habitats.     

Thermal sensitivity of metabolic enzymes in subarctic and temperate freshwater mussels (Bivalvia: Unionoida)

Temperature has a major impact on the physiological processes of freshwater invertebrates. Despite the endangered status of many freshwater mussel species and the potential effect of global warming on North America’s northern aquatic habitats, thermal sensitivity of the metabolic apparatus of freshwater bivalves has received little attention. By examining the thermal sensitivity of 10 key metabolic enzymes and in situ growth rates of latitudinally separated populations (temperate and subarctic) of two closely-related Pyganodon species from northeastern North America, we provide the first insights into thermal sensitivity of key enzymes of energy and reactive oxygen species metabolism in relation to habitat localization and growth performance. The subarctic population of Pyganodon grandis displayed higher in situ growth rates than the temperate population of Pyganodon fragilis. The subarctic population of P. grandis had a lower mitochondrial capacity as expressed by citrate synthase and cytochrome c oxidase but displayed similar electron transport system (ETS) and higher isocitrate dehydrogenase capacities. Our results suggest that higher growth performance of the subarctic population of P. grandis is not associated with higher aerobic capacity. The high thermal sensitivity of mitochondrial enzymes in subarctic population of P. grandis might rather reflect enhanced stenothermy. The higher electron transport system/cytochrome c oxidase ratio for the subarctic P. grandis species than P. fragilis might affect mitochondrial regulation or reactive oxygen species production. Antioxidant enzymes displayed lower Q₁₀s suggesting thermal independence of antioxidant capacity.     

Estimating the biomass of freshwater mussels (Bivalvia: Unionidae) from shell dimensions

Packs of autumn-shed maple leaves were placed at coal ash effluent-exposed and reference sites in streams on December 5, 1977 and removed after 27 and 96 days. Leaf surface area (cm²/leaf) and disc weight (ash-free dry wt/15 mm disc) were greater at the effluent-exposed site than at the reference site after 96 days (p < .001). ATP content of leaves from the reference stream quadrupled between 27 and 96 days while ATP content of effluent-exposed leaves remained low. Macroinvertebrates colonized the leaf packs in the reference site but were not found on or in effluent-exposed packs. We concluded that leaf processing beyond the leaching of soluble organics did not occur in the effluent-exposed packs owing to reduced colonization and decomposition by fungi. Since stream invertebrates prefer decomposed leaf material and animals grow faster on leaves colonized by microbes, the ash effuent appears to indirectly affect macroinvertebrates by interfering with leaf decomposition and thus reducing the quality of their food.     

Bivalves in a bottleneck: taxonomy,phylogeography and conservation of freshwater mussels (Bivalvia: Unionoida) in Australasia

The conservation biology of Australasian freshwater mussels is hindered by lack of a taxonomic framework that employs molecular data as a complement to shell characters, larval forms and internal anatomy. The fauna includes more than 32 known species (30+ Hyriidae, 2 Unionidae), but has not been revised for 55 years, despite minor amendments. The hyriids are relics of Gondwana, represented in Australia and New Guinea by the ancestral Velesunioninae and in Australia and New Zealand by the Hyriinae (Tribe Hyridellini). Many taxonomic and phylogeographic issues await resolution, including the relationships between Australasian and South American species, and between Australian and New Zealand species, and the status of species in New Guinea (including uncertain reports of Unionidae) and the Solomon Islands. Once these are clarified, it will be easier to identify threatened species and evaluate the conservation status of the fauna. At present, only seven taxa are named in the IUCN Red List or under national/state legislation, and these are not representative. Threatening processes include altered flow regimes, catchment disturbances, salinisation, pollution and invasive species. While the need for a taxonomic revision is paramount, progress in conservation may depend also upon involving the wider community.     

Anatomical Features of Modellnaia siamensis (Mollusca, Bivalvia, Unionidae)

Although conchologically an etheriid mussel, M. siamensis from northeastern Thailand is, according to anatomical and larval features, an unionid. Its unique character states among the Unionidae are: relatively distant spacing of septa in all four demibranchs in both, males and females, absence of a foot in adults, and generation of subelliptical glochidial larvae. This species is seemingly a phylogenetic relic.     

Freshwater mussels (genus Anodonta) from Anatolia and adjacent areas (Bivalvia,Unionidae)

Abstract

A review is given of the species of Anodontinae in Anatolia and the adjacent areas, based mainly on the author’s collections. Five species (A. anatina, A. cygnae, A. palustris, A. pseudodopsis, A. vescoiana) and several subspecies are recognized. Their distribution and the patterns of subspeciation are discussed.