, Volume 735, Issue 1, pp 179–190 | Cite as

Host-dependent genetic variation in freshwater pearl mussel (Margaritifera margaritifera L.)

  • Sten Karlsson
  • Bjørn Mejdell Larsen
  • Kjetil Hindar


The endangered freshwater pearl mussel (Margaritifera margaritifera) requires brown trout or Atlantic salmon as a host to complete its life cycle. In Norway, populations have been identified using almost exclusively either salmon or trout as hosts, even when both hosts are present. In this study we tested the hypothesis that the genetic variation in freshwater pearl mussel is host-dependent. A total of 587 specimens from 25 different localities were assayed for genetic variation at eight microsatellite loci. Within populations, the trout-mussel populations had significantly lower allelic richness and expected heterozygosity than the salmon-mussel populations. The genetic differentiation among trout-mussel populations was very large (F ST = 0.332), and significantly larger than among salmon-mussel populations (F ST = 0.023). Host affiliation explained more of the genetic differentiation among freshwater pearl mussel populations (F CT = 0.150) than geographical location (F CT = 0.013). Collectively these results suggest that there is strong reproductive isolation between freshwater pearl mussel populations. More importantly, our results indicate that trout- and salmon-mussel populations are differently genetically structured. Because of the mandatory parasitic larval stage on trout and salmon, the host-dependent genetic variation has implications for restoration and management plans for this species.


Freshwater pearl mussel Margaritifera margaritifera Microsatellite Atlantic salmon Brown trout 



We gratefully acknowledge Torveig Balstad and Line Eriksen (NINA) for conducting the laboratory work. Our work was supported by the Norwegian Directorate for Nature Management.

Supplementary material

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Supplementary material 1 (DOCX 469 kb)


  1. Bauer, G., 1987a. The parasitic stage of the freshwater pearl mussel (Margaritifera margaritifera L.). III. Host relationships. Archiv für Hydrobiologie Supplement 76: 413–423.Google Scholar
  2. Bauer, G., 1987b. The parasitic stage of the freshwater pearl mussel (Margaritifera margaritifera L.). II. Susceptibility of brown trout. Archiv für Hydrobiologie Supplement 76: 403–412.Google Scholar
  3. Bauer, G., 1988. Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe. Biological Conservation 45: 239–253.CrossRefGoogle Scholar
  4. Bolland, J. D., L. J. Bracken, R. Martin & M. C. Lucas, 2010. A protocol for stocking reared freshwater pearl mussel Margaritifera margaritifera. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 695–704.Google Scholar
  5. Cunjak, R. A. & S. E. McGladdery, 1991. The parasite–host relationship of glochidia (Mollusca: Margaritiferidae) on the gills of young-of-the-year Atlantic salmon (Salmo salar). Canadian Journal of Zoology 69: 353–358.CrossRefGoogle Scholar
  6. Dunca, E. & B. M. Larsen, 2012. Skillnader i skaltillväxt hos flodpärlmusslor från reglerade och icke-reglerade vattendrag i Norge. NINA Rapport 795: 63. [In Swedish with English summary].Google Scholar
  7. Earl, D. A. & B. M. vonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetic Resources 4: 359–361.CrossRefGoogle Scholar
  8. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.PubMedCrossRefGoogle Scholar
  9. Felsenstein, J., 2009. PHYLIP (Phylogeny Inference Package) Version 3.69. Distributed by the author. Department of Genetics, University of Washington, Seattle.Google Scholar
  10. Geist, J., 2010. Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of conservation genetics and ecology. Hydrobiologia 644: 69–88.CrossRefGoogle Scholar
  11. Geist, J. & R. Kuehn, 2005. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Molecular Ecology 14: 425–439.PubMedCrossRefGoogle Scholar
  12. Geist, J. & R. Kuehn, 2008. Host–parasite interaction in oligotrophic stream ecosystems: the roles of life-history strategy and ecological niche. Molecular Ecology 17: 997–1008.PubMedCrossRefGoogle Scholar
  13. Geist, J., O. Rottmann, W. Schröder & R. Kühn, 2003. Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionidea). Molecular Ecology Notes 3: 444–446.CrossRefGoogle Scholar
  14. Geist, J., M. Porkka & R. Kuehn, 2006. The status of host fish populations and fish species richness in European freshwater pearl mussel (Margaritifera margaritifera) streams. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 251–266.Google Scholar
  15. Geist, J., H. Söderberg, A. Karlberg & R. Kuehn, 2010. Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conservation Genetics 11: 1339–1350.CrossRefGoogle Scholar
  16. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from Accessed 9 Sept 2013.
  17. Hastie, L. C. & M. R. Young, 2001. Freshwater pearl mussel (Margaritifera margaritifera) glochidiosis in wild and farmed salmonid stocks in Scotland. Hydrobiologia 445: 109–119.CrossRefGoogle Scholar
  18. Hastie, L. C. & M. R. Young, 2003. Conservation of the Freshwater Pearl Mussel 2: Relationship with Salmonids. Conserving Natura 2000 Rivers Conservation Techniques Series No. 3 English Nature, Peterborough: 44 pp.Google Scholar
  19. Hastie, L. C., P. J. Boon & M. R. Young, 2000. Physical microhabitat requirements of freshwater pearl mussels, Margaritifera margaritifera (L.). Hydrobiologia 429: 59–71.CrossRefGoogle Scholar
  20. IUCN, 2011. IUCN Red List of Threatened Species. Version 2011.2. Accessed 9 Sept 2013.
  21. Johnsen, B. O., P. I. Møkkelgjerd & A. J. Jensen, 1999. Parasitten Gyrodactylus salaris på laks i norske vassdrag, statusrapport ved inngangen til år 2000. NINA Oppdragsmelding 617: 1–129. [In Norwegian].Google Scholar
  22. Karlsson, S., B. M. Larsen, L. Eriksen & M. Hagen. 2013. Four methods of non-destructive DNA sampling from fresh-water pearl mussels Margaritifera margaritifera L. (Bivalvia: Unionoida). Freshwater Science 32: 525–530.Google Scholar
  23. Larsen, B. M., 2002. Overvåking av elvemusling Margaritifera margaritifera i Norge. Årsrapport 2001. NINA Oppdragsmelding 762: 46. [In Norwegian].Google Scholar
  24. Larsen, B. M., 2005. Handlingsplan for elvemusling Margaritifera margaritifera i Norge. Innspill til den faglige delen av handlingsplanen. NINA Rapport 122: 33. [In Norwegian].Google Scholar
  25. Larsen, B. M., 2010. Distribution and status of the freshwater pearl mussel (Margaritifera margaritifera) in Norway. In Ieshko, E. P. & T. Lindholm (eds), Conservation of Freshwater Pearl Mussel, Margaritifera margaritifera Populations in Northern Europe. Proceedings of the International Workshop. Karelien Research Centre of RAS. Karelian Research Centre of RAS, Petrozavodsk: 35–43.Google Scholar
  26. Larsen, B. M., K. Hårsaker, J. Bakken & D. V. Barstad, 2000. The freshwater pearl mussel Margaritifera margaritifera in Steinkjervassdraget and Figga, Nord-Trøndelag. Preliminary survey in connection with planned rotenone treatment. NINA Fagrapport 39: 1–39. [In Norwegian with English summary].Google Scholar
  27. Larsen, B. M., M. Eken & K. Hårsaker, 2002. Freshwater pearl mussel Margaritifera margaritifera and stocking of fish in the river Hoenselva and Bingselva, Buskerud county in Norway. NINA Fagrapport 56: 1–33. [In Norwegian with English summary].Google Scholar
  28. Larsen, B. M., T. Forseth & R. Saksgård, 2012. Host specificity in freshwater pearl mussel Margaritifera margaritifera populations in Norway – experimental studies. In International Meeting on Biology and Conservation of Freshwater Bivalves: Book of Abstracts. Instituto Politécnico de Bragança: 58 pp.Google Scholar
  29. Mantel, N. A., 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220.PubMedGoogle Scholar
  30. Meyers, T. R. & R. E. Millemann, 1977. Glochidiosis of salmonid fishes. I. Comparative susceptibility to experimental infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritanidae). Journal of Parasitology 63: 728–733.PubMedCrossRefGoogle Scholar
  31. Nei, M., 1972. Genetic distance between populations. American Naturalist 106: 283–392.CrossRefGoogle Scholar
  32. Nei, M., 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.PubMedCentralPubMedGoogle Scholar
  33. Peakall, R. & P. E. Smouse, 2006. GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.Google Scholar
  34. Piry, S., A. Alapetite, J. M. Cornuet, D. Paetkau, L. Baudouin & A. Estoup, 2004. GeneClass2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 95: 536–539.PubMedCrossRefGoogle Scholar
  35. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedCentralPubMedGoogle Scholar
  36. Rannala, B. & J. L. Mountain, 1997. Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences 94: 9197–9201.Google Scholar
  37. Raymond, M. & F. Rousset, 1995. Genepop (version 2.1): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.Google Scholar
  38. Rousset, F., 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228.Google Scholar
  39. Schneider S., D. Roessli & L. Excoffier, 2000. Arlequin Ver. 2.0: A Software for Population Genetic Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva.Google Scholar
  40. Smith, D. G., 1976. Notes on the biology of Margaritifera margaritifera margaritifera (Lin.) in Central Massachusetts. American Midland Naturalist 96: 252–256.CrossRefGoogle Scholar
  41. Thomas, G. R., J. Taylor & C. Garcia de Leaniz, 2010. Captive breeding of the endangered freshwater pearl mussel Margaritifera margaritifera. Endangered Species Research 12: 1–9.CrossRefGoogle Scholar
  42. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  43. Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.Google Scholar
  44. Young, M. & J. Williams, 1984. The reproductive biology of the freshwater mussel Margaritifera margaritifera (Linn.) in Scotland. I. Field studies. Archiv für Hydrobiologie 99: 405–422.Google Scholar
  45. Young, M. R., P. J. Cosgrove & L. C. Hastie, 2001. The extent of, and causes for, the decline of a highly threatened naiad: Margaritifera margaritifera. In Bauer, G. & K. Wächtler (eds), Ecology and Evolution of the Freshwater Mussels Unionoida. Ecological Studies, Vol. 145. Springer Verlag, Heidelberg: 337–357.Google Scholar
  46. Ziuganov, V., A. Zotin, L. Nezlin & V. Tretiakov, 1994. The Freshwater Pearl Mussels and Their Relationships with Salmonid Fish. VNIRO Publishing House, Moscow: 104 pp.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sten Karlsson
    • 1
  • Bjørn Mejdell Larsen
    • 1
  • Kjetil Hindar
    • 1
  1. 1.Norwegian Institute for Nature Research (NINA)TrondheimNorway

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