Range-wide population genetic analysis of the endangered northern riffleshell mussel, <Emphasis Type="Italic">Epioblasma torulosa rangiana</Emphasis> (Bivalvia: Unionoida)

The northern riffleshell (Epioblasma torulosa rangiana) is a critically endangered unionoid species in need of conservation throughout its range. It is the only unionoid to be federally protected in both Canada and the U.S. We use sequences from two mtDNA genes and 15 microsatellite loci to assess genetic variation among 86 individuals from the four populations in the three remaining drainages in which E. t. rangiana is known to be reproducing. All of these populations are in formerly glaciated landscapes that emerged <10 kya. The mtDNA sequence data do not indicate significant geographic structure among the populations. However, allelic data from the microsatellite loci reveal highly significant population structuring. Individuals of E. t. rangiana can be assigned to their own river of origin with 98.8% accuracy. Significant isolation-by-distance occurs. This analysis will be useful to conservation managers in documenting the genetic structure, patterns of isolation, and genetic variability within and among populations of E. t. rangiana.     

Development and characterization of microsatellite markers for the endangered northern riffleshell mussel Epioblasma torulosa rangiana (Bivalvia: Unionidae)

Primers for six polymorphic microsatellite loci were developed for the endangered northern riffleshell Epioblasma torulosa rangiana from the Sydenham River, Ontario, Canada. These loci along with an additional nine microsatellite loci, developed from other unionoid species, available in the literature, were tested and characterized on individuals from two populations in the Allegheny River; one population in French Creek, PA, USA, and one population from the Sydenham River. Allelic diversity ranged from two to 28 alleles per locus and averaged 13.7 per locus. These primers are being used in a rangewide study on the conservation genetics of remaining extant populations of the northern riffleshell.     

Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionoidea)

Freshwater pearl mussels (Margaritifera margaritifera L.) are among the most critically endangered freshwater invertebrates. We describe the isolation and characterization of the first microsatellite markers for this species, which were obtained by screening 4900 recombinant clones from two genomic libraries. Thirteen loci revealed polymorphisms as demonstrated on 42 tested individuals from four river drainages. Allelic richness ranged from two to 12 alleles and averaged 6.8 alleles per locus with heterozygosity levels varying from 0 to 0.850 for observed heterozygosity (H_O) and from 0.174 to 0.850 for expected heterozygosity (H_E). Deficiency of heterozygous genotypes was observed in eight of 13 loci.     

Isolation and characterization of microsatellite loci in western North American Anodonta species

We have developed and characterized 13 microsatellite loci from a group of Anodonta species in western North America, and demonstrated their utility in populations representing two major clades in this genus. Allelic diversity and polymorphic information content were high for all loci, although these characteristics varied across populations. Deviations from Hardy-Weinberg genotypic ratios were not detected, although the estimated frequency of null alleles was high in one population for one locus. This is the first set of microsatellite loci to be developed for freshwater mussels in western North America, and will be useful for describing gene flow patterns among populations.     

Growth and longevity in freshwater mussels: evolutionary and conservation implications

The amount of energy allocated to growth versus other functions is a fundamental feature of an organism's life history. Constraints on energy availability result in characteristic trade‐offs among life‐history traits and reflect strategies by which organisms adapt to their environments. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems but little is known about their growth and longevity. Generalized depictions of freshwater mussels as ‘long‐lived and slow‐growing’ may give an unrealistically narrow view of life‐history diversity which is incongruent with the taxonomic diversity of the group and can result in development of inappropriate conservation strategies. We investigated relationships among growth, longevity, and size in 57 species and 146 populations of freshwater mussels using original data and literature sources. In contrast to generalized depictions, longevity spanned nearly two orders of magnitude, ranging from 4 to 190 years, and the von Bertalanffy growth constant, K, spanned a similar range (0.02–1.01). Median longevity and K differed among phylogenetic groups but groups overlapped widely in these traits. Longevity, K, and size also varied among populations; in some cases, longevity and K differed between populations by a factor of two or more. Growth differed between sexes in some species and males typically reached larger sizes than females. In addition, a population of Quadrula asperata exhibited two distinctly different growth trajectories. Most individuals in this population had a low‐to‐moderate value of K (0.15) and intermediate longevity (27 years) but other individuals showed extremely slow growth (K = 0.05) and reached advanced ages (72 years). Overall, longevity was related negatively to the growth rate, K, and K explained a high percentage of variation in longevity. By contrast, size and relative shell mass (g mm^?1 shell length) explained little variation in longevity. These patterns remained when data were corrected for phylogenetic relationships among species. Path analysis supported the conclusion that K was the most important factor influencing longevity both directly and indirectly through its effect on shell mass. The great variability in age and growth among and within species shows that allocation to growth is highly plastic in freshwater mussels. The strong negative relationship between growth and longevity suggests this is an important trade‐off describing widely divergent life‐history strategies. Although life‐history strategies may be constrained somewhat by phylogeny, plasticity in growth among populations indicates that growth characteristics cannot be generalized within a species and management and conservation efforts should be based on data specific to a population of interest.     

Parasitic mite and trematode abundance are associated with reduced reproductive output and physiological condition of freshwater mussels

Although historically understudied, parasites may play an important role in freshwater invertebrate population ecology and evolution. We quantified abundance of parasitic mites and trematodes in the freshwater mussel Pyganodon grandis, in a southeastern Alabama stream (USA), to assess parasite impact on adult mussel physiological condition and reproductive output. We used stepwise multiple regression analyses to assess the effects of mussel size and parasites on reproduction and condition. Multiple regression analysis found no multivariate models that predicted reproductive output or physiological condition. However, univariate models revealed that increased parasite densities predict reduced mussel reproductive output and physiological condition. These findings suggest that parasites may have important negative consequences for freshwater mussels. We hypothesize that elevated parasite loads may reduce mussel fitness in impounded or nutrient-enriched streams with high densities of intermediate hosts (chironomid midges).     

Genetic diversity and divergence among freshwater mussel (Anodonta) populations in the Bonneville Basin of Utah

Populations of the freshwater mussel genus Anodonta appear to be in a state of rapid decline in western North America, following a trend that unfortunately seems to be prevalent among these animals (Mollusca: Unionoida). Here we describe the patterns of molecular divergence and diversity among Anodonta populations in the Bonneville Basin, a large sub-basin of the Great Basin in western North America. Using amplified fragment length polymorphism (AFLP) analysis, we found a striking lack of nuclear diversity within some of these populations, along with a high degree of structuring among populations (FST = 0.61), suggesting post-Pleistocene isolation, due either to a long-term loss of hydrologic connectivity among populations or to more recent fish introductions. We also found evidence of recent hybridization in one of these populations, possibly mediated by fish-stocking practices. Using mitochondrial sequence data, we compared the Bonneville Basin populations to Anodonta in several other drainages in western North America. We found a general lack of resolution in these phylogenetic reconstructions, although there was a tendency for the Bonneville Basin Anodonta (tentatively A. californiensis) to cluster with A. oregonensis from the adjacent Lahontan Basin in Nevada. We recommend further investigation of anthropogenic factors that may be contributing to the decline of western Anodonta and a broad-scale analysis and synthesis of genetic and morphological variation among Anodonta in western North America.     

Asymmetric dispersal structures a riverine metapopulation of the freshwater pearl mussel Margaritifera laevis

Unidirectional water flow results in the downstream‐biased, asymmetric dispersal of many riverine organisms. However, little is known of how asymmetric dispersal influences riverine population structure and dynamics, limiting our ability to properly manage riverine organisms. A metapopulation of the freshwater pearl mussel Margaritifera laevis may be sensitive to river currents because mussels are repeatedly exposed to downstream drift during floods—a parasitic life stage is the only, limited period (~40 days) during which larvae (glochidia) can move upstream with the aid of host fish. We hypothesized that water‐mediated dispersal would overwhelm upstream dispersal via host fish, and therefore, that upstream subpopulations play a critical role as immigrant sources. To test this hypothesis, we examined the effects of both up‐ and downstream immigrant sources on the size of target subpopulations in the Shubuto River system, Hokkaido, Japan. We found that target subpopulation size was dependent on the upstream distribution range of reproductive subpopulations and the number of upstream tributaries, which are proxies for the number of potential immigrants moving downstream. In contrast, little influence was observed of downstream immigrant sources (proximity to downstream reproductive subpopulations). These results were consistent even after accounting for local environments and stream size. Our finding suggests that upstream subpopulations can be disproportionately important as immigrant sources when dispersal is strongly asymmetric.     

Sexual,habitat‐constrained and parasite‐induced dimorphism in the shell of a freshwater mussel (Anodonta anatina,Unionidae)

Intraspecific trends in freshwater mussel (unionoid) shells that are consistently associated with differences in the mussels' sex and/or parasitic infestation can potentially be used to reconstruct sex ratios or parasitic levels of modern and ancient unionoid populations. In contrast to morphological patterns within mammal species, such dimorphic trends within unionoid species are, however, poorly understood. This study investigates, for the first time, to what extent sex, trematode infection and indirect habitat effects determine shell morphology in the freshwater mussel Anodonta anatina. Three of the five study populations displayed significant sexual shell width dimorphism. Here, shells of females were significantly wider than males, probably as a result of altered shell growth to accommodate marsupial gills. In two of these populations, female shells were additionally significantly thinner than those of males, which could be a result of resource depletion by offspring production. Two other A. anatina populations showed no significant dimorphic patterns, and our results indicate that this interpopulational difference in the degree of sexual dimorphism may reflect the overarching effect of habitat on morphology. Thus, populations in the most favourable habitats exhibit faster growth rates, attain larger maximum sizes and produce more offspring, which results in more swollen gills and consequently more inflated shells of gravid females compared to less fecund populations. None of the populations showed any evidence for sexual dimorphism in overall size, growth rate, sagittal shape and density of shells. In addition to sexual dimorphisms, infestation by bucephalid trematode parasites (Rhipidocotyle sp.) significantly altered sagittal and lateral shell shape of A. anatina in one of the populations, with infected specimens growing wider and more elongated. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Effects of dams and their environmental impacts on the genetic diversity and connectivity of freshwater mussel populations in Poyang Lake Basin,China

1. Habitat fragmentation is one of the main threats to biodiversity. Barriers to dispersal caused by anthropogenic habitat alteration may affect phylogeographic patterns in freshwater mussels. Knowledge of the phylogenetic and phylogeographic patterns of unionoids is vital to inform protection of their biodiversity.
2. Here, we assessed influences of dams and their environmental effects on the genetic diversity and population connectivity of a broadly distributed freshwater mussel, Nodularia douglasiae, in Poyang Lake Basin.
3. The results showed high genetic diversity in areas without dams and low genetic diversity in areas with dams. High genetic differentiation and low gene flow were found among the 11 populations. Genetic variation was significantly correlated with dissolved oxygen levels.
4. The observation of low genetic diversity in populations separated by dams indicated that those populations were subjected to genetic erosion and demographic decline because they are disconnected from other populations with higher diversity. High genetic differentiation and low gene flow among the 11 populations could be correlated with anthropogenic habitat alteration.
5. These results indicated that anthropogenic habitat alterations have led to the decline in freshwater mussel diversity. Therefore, we recommend maintaining favourable habitat conditions and connectivity of rivers or lakes, and strengthening study of life histories with host-test experiments to identify potential host fish species to strengthen the knowledge base underpinning freshwater mussel conservation.