The genetic diversity and differentiation of mussels with complex life cycles and relations to host fish migratory traits and densities

Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–9013 (2000).

ADS  CAS  PubMed  Article  Google Scholar 

Dudaniec, R. Y. & Tesson, S. V. M. Applying landscape genetics to the microbial world. Mol. Ecol. 25, 3266–3275 (2016).

PubMed  Article  Google Scholar 

Froufe, E. et al. Phylogeny, phylogeography, and evolution in the Mediterranean region: News from a freshwater mussel (Potomida, Unionida). Mol. Phyl. Evol. 100, 322–332 (2016).

Article  Google Scholar 

Simmons, L., Mathieson, M. T., Lamont, R. W. & Shapcott, A. Genetic diversity of endangered orchid Phaius australis across a fragmented Australian landscape. Conserv. Genet. 19, 451–465 (2018).

CAS  Article  Google Scholar 

Chong, J. P. & Roe, K. J. A comparison of genetic diversity and population structure of the endangered scaleshell mussel (Leptodea leptodon), the fragile papershell (Leptodea fragilis) and their host-fish the freshwater drum (Aplodinotus grunniens). Conserv. Genet. 19(2), 425–437 (2018).

Article  Google Scholar 

Berg, D. J., Christian, A. D. & Guttman, S. I. Population genetic structure of three freshwater mussel (Unionidae) species within a small stream system: significant variation at local spatial scales. Freshw. Biol. 52, 1427–1439 (2007).

Article  Google Scholar 

Cornuet, J. M. & Luikart, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014 (1996).

CAS  PubMed  PubMed Central  Google Scholar 

Elderkin, C. L., Christian, A. D., Vaughn, C. C., Metcalfe-Smith, J. L. & Berg, D. J. Population genetics of the freshwater mussel, Amblema plicata (Say 1817) (Bivalvia: Unionidae): evidence of high dispersal and post-glacial colonization. Conserv. Genet. 8, 355–372 (2007).

CAS  Article  Google Scholar 

Mazé-Guilmo, E., Blanchet, S., McCoy, K. D. & Loot, G. Host dispersal as the driver of parasite genetic structure: a paradigm lost?. Ecol. Lett. 19, 336–347 (2016).

PubMed  Article  Google Scholar 

Karlsson, S., Larsen, B. M. & Hindar, K. Host-dependent genetic variation in freshwater pearl mussel (Margaritifera margaritifera L.). Hydrobiologia 735, 179–190 (2014).

Article  Google Scholar 

Östergren, J. & Nilsson, J. Importance of life-history and landscape characteristics for genetic structure and genetic diversity of brown trout (Salmo trutta L.). Ecol. Freshw. Fish 21, 119–133 (2012).

Article  Google Scholar 

Hendry, A. P. et al. Evolutionary principles and their practical application. Evol. Appl. 4, 159–183 (2011).

PubMed  PubMed Central  Article  Google Scholar 

Strayer, D. L. et al. Changing perspectives on pearly mussels, North America’s most imperiled animals. Bioscience 54, 429–439 (2004).

Article  Google Scholar 

Geist, J. et al. Genetic structure of Irish freshwater pearl mussels (Margaritifera margaritifera and Margaritifera durrovensis): Validity of subspecies, roles of host fish, and conservation implications. Aquat. Conserv. Mar. Freshw. Ecosyst. 28, 923–933 (2018).

Article  Google Scholar 

Arvidsson, B. L., Karlsson, J. & Österling, M. E. Recruitment of the threatened mussel Margaritifera margaritifera in relation to mussel population size, mussel density and host density. Aquat. Conserv. Mar. Freshw. Ecosyst. 22, 526–532 (2012).

Article  Google Scholar 

Young, M. & Williams, J. The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland 1 Field studies. Arch. Hydrobiol. 99, 405–422 (1984).

Google Scholar 

Hastie, L. C. & Young, M. R. Freshwater pearl mussel (Margaritifera margaritifera) glochidiosis in wild and farmed salmonid stocks in Scotland. Hydrobiologia 445, 109–119 (2001).

Article  Google Scholar 

Salonen, J. K. et al. Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) differ in their suitability as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera) in northern Fennoscandian rivers. Freshw. Biol. 62, 1346–1358 (2017).

Article  Google Scholar 

Österling, E. M. & Söderberg, H. Sea-trout habitat fragmentation affects threatened freshwater pearl mussel. Biol. Conserv. 186, 197–203 (2015).

Article  Google Scholar 

Taeubert, E. & Geist, J. The relationship between the freshwater pearl mussel (Margaritifera margaritifera) and its hosts. Biol. Bull. 44, 67–73 (2017).

Article  Google Scholar 

Stoeckle, B. C. et al. Strong genetic differentiation and low genetic diversity of the freshwater pearl mussel (Margaritifera margaritifera L.) in the southwestern European distribution range. Conserv. Genet. 18, 147–157 (2017).

Article  Google Scholar 

Mathias, P. T., Hoffman, J. R., Wilson, C. C. & Zanatta, D. T. Signature of postglacial colonization on contemporary genetic structure and diversity of Quadrula quadrula (Bivalvia: Unionidae). Hydrobiologia 810, 207–225 (2018).

CAS  Article  Google Scholar 

implications for conservation and management. Geist, J. & Kuehn, R. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations. Mol. Ecol. 14, 425–439 (2005).

Google Scholar 

Wacker, S., Larsen, B. M., Karlsson, S. & Hindar, K. Host specificity drives genetic structure in a freshwater mussel. Sci. Reports 9, 10409 (2019).

ADS  Google Scholar 

Geist, J. & Kuehn, R. Host-parasite interactions in oligotrophic stream ecosystems: The roles of life history strategy and ecological niche. Mol. Ecol. 17, 997–1008 (2008).

PubMed  Article  Google Scholar 

Naimo, T. J., Damschen, E. D., Rada, R. G. & Monroe, E. M. Nonlethal evaluation of the physiological health of unionid mussels: methods for biopsy and glycogen analysis. J. North Am. Benth. Soc. 17, 121–128 (1998).

Article  Google Scholar 

Geist, J., Rottmann, O., Schroder, W. & Kuhn, R. Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia : Unionoidea). Mol. Ecol. Notes3, 444–446 (2003).

Raymond, M. & Rousset, F. An exact test for population differentiation. Evolution 49, 1280–1283 (1995).

PubMed  Article  Google Scholar 

Raymond, M. & Rousset, F. GENEPOP (version 1.2)—population genetics software for exact tests and ecumenicism. J Heredity 86, 248–249 (1995).

Article  Google Scholar 

Van Oosterhout, C., Hutchinson, W. F., Wilis, D. P. M. & Shipley, P. micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538 (2004).

Article  CAS  Google Scholar 

Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).

CAS  PubMed  Google Scholar 

Goudet, J. FSTAT (Version 1.2): a computer program to calculate F-statistics. J. Heredity 86, 485–486 (1995).

Article  Google Scholar 

Takezaki, N., Nei, M. & Tamura, K. POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with windows interface. Mol. Biol. Evol. 27, 747–752 (2009).

PubMed  PubMed Central  Article  CAS  Google Scholar 

Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

CAS  PubMed  PubMed Central  Google Scholar 

Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).

CAS  PubMed  Article  Google Scholar 

Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Res. 4, 359–361 (2012).

Article  Google Scholar 

Jombart, T. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).

CAS  PubMed  Article  Google Scholar 

Jombart, T. & Ahmed, I. Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).

CAS  PubMed  PubMed Central  Article  Google Scholar 

Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 10, 564–567 (2010).

Article  Google Scholar 

Di Rienzo, A. et al. Mutational processes of simple-sequence repeat loci in human populations. Proc. Nat. Acad. Sci. USA 91, 3166–3170 (1994).

ADS  PubMed  Article  Google Scholar 

Piry, S., Luikart, G. & Cornuet, J.-M. Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J. Heredity 90, 502–503 (1999).

Article  Google Scholar 

Wilson, G. A. & Rannala, B. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163, 1177–1191 (2003).

PubMed  PubMed Central  Google Scholar 

Moritz, C., Lavery, S. & Slade, R. Using allele frequency and phylogeny to define units for conservation and management. Am. Fish. Soc. Symp. 17, 249–262 (1995).

Google Scholar 

Zanatta, D. T. et al. High genetic diversity and low differentiation in North American Margaritifera margaritifera (Bivalvia: Unionida: Margaritiferidae). Biol. J. Linn. Soc. 123, 850–863 (2018).

Article  Google Scholar 

Geist, J., Söderberg, H., Karlberg, A. & Kuehn, R. Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conserv. Gen. 11, 1339–1350 (2010).

Article  Google Scholar 

Cortey, M., Vera, M., Pla, C. & Garcia-Marin, J.-L. Northern and Southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene. Biol. J. Linn. Soc. 97, 904–917 (2009).

Article  Google Scholar 

Schwalb, A. N., Garvie, M. & Ackerman, J. D. Dispersion of freshwater mussel larvae in a lowland river. Limnol. Oceanogr. 55, 628–638 (2010).

ADS  Article  Google Scholar 

Schwalb, A. N., Cottenie, K., Poos, M. S. & Ackerman, J. D. Dispersal limitation of unionid mussels and implications for their conservation. Freshw. Biol. 56, 1509–1518 (2011).

Article  Google Scholar 

Terui, A. et al. Dispersal of larvae of Margaritifera laevis by its host fish. Freshw. Sci. 33, 112–123 (2014).

Article  Google Scholar 

Frankham, R. Relationship of genetic variation to population size in wildlife. Conserv. Biol 10(6), 1500–1508 (1996).

Article  Google Scholar 

Leimu, R., Mutikainen, P., Koricheva, J. & Fischer, M. How general are positive relationships between plant population size, fitness and genetic variation?. J. Ecol. 94(5), 942–952 (2006).

Article  Google Scholar 

Lopes-Lima, M. et al. Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol. Rev. 92, 572–607 (2017).

PubMed  Article  Google Scholar 

Gum, B., Lange, M. & Geist, J. A critical reflection on the success of rearing and culturing juvenile freshwater mussels with a focus on the endangered freshwater pearl mussel (Margaritifera margaritifera L.). Aquat. Conserv. Mar. Freshw. Ecosyst. 21, 743–751 (2011).

Article  Google Scholar 

Geist, J. Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of conservation genetics and ecology. Hydrobiologia 644, 69–88 (2010).

Article  Google Scholar 

Schneider, L. D., Anders Nilsson, P., Höjesjö, J. & Österling, E. M. Local adaptation studies and conservation: parasite–host interactions between the endangered freshwater mussel Unio crassus and its host fish. Aquat. Conserv. Mar. Freshwater Ecosyst. 27, 1261–1269 (2017).

Article  Google Scholar 

Taeubert, J.-E., Denic, M., Gum, B., Lange, M. & Geist, J. Suitability of different salmonid strains as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera L.). Aquat. Conserv. Mar. Freshw. Ecosyst. 20, 728–734 (2010).

Article  Google Scholar 

Österling, M. E. & Larsen, B. M. Impact of origin and condition of host fish (Salmo trutta) on parasitic larvae of Margaritifera margaritifera. Aquat. Conserv. Mar. Freshw. Ecosyst. 23, 564–570 (2013).

Article  Google Scholar