Abstract
Freshwater pearl mussels (Margaritifera margaritifera) are among the most critically threatened bivalve molluscs worldwide. An understanding of spatial patterns of genetic diversity is crucial for the development of integrative conservation strategies. We used microsatellites to study the genetic diversity and differentiation of 14 populations of M. margaritifera in central Sweden, an area which was described as a major secondary contact zone in postglacial colonisation for other species. Genetic diversity of Swedish pearl mussel populations was much greater than in central and southern Europe but similar to the genetic diversity observed in the northeastern portion of their European range. Genetic differentiation among populations was pronounced but to a large extent independent from present-day drainage systems. The complex patterns of genetic diversity and differentiation in pearl mussel seem to be strongly influenced by the species’ high degree of specialisation and extraordinary life history strategy which involves facultative hermaphrodism and an obligatory encystment stage on a host fish. Genetic drift effects and anthropogenic disturbances resulting in reduction of population size and loss of connectivity are less pronounced in northern pearl mussel populations compared to those in central and southern Europe.
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References
Bauer G (1987) Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J Anim Ecol 56:691–704. doi:10.2307/5077
Bauer G (1988) Threats to the freshwater pearl mussel Margaritifera margaritifera in central Europe. Biol Conserv 45:239–253. doi:10.1016/0006-3207(88)90056-0
Bauer G (1992) Variation in the life span and size of the freshwater pearl mussel. J Anim Ecol 61:425–436. doi:10.2307/5333
Berg DJ, Christian AD, Guttman SI (2007) Population genetic structure of three freshwater mussels (Unionidae) species within a small stream system: significant variation at local spatial scales. Freshw Biol 52:1427–1439. doi:10.1111/j.1365-2427.2007.01756.x
Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invetebrates. Annu Rev Ecol Syst 32:159–181. doi:10.1146/annurev.ecolsys.32.081501.114016
Bogan AE (1993) Freshwater bivalve extinctions (Mollusca: Unionoida): a search for causes. Am Zool 33:599–609
Bouza C, Castro J, Martínez P, Amaro R, Fernández C, Ondina P, Outeiro A, San Miguel E (2007) Threatened freshwater pearl mussel Margaritifera margaritifera L. in NW Spain: low and very structured genetic variation in southern peripheral populations assessed using microsatellite markers. Conserv Genet 8:937–948. doi:10.1007/s10592-006-9248-0
Ciofi C, Bruford MW (1999) Genetic structure and gene flow among komodo dragon populations inferred by microsatellite loci analysis. Mol Ecol 8:17–30. doi:10.1046/j.1365-294X.1999.00734.x
Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000
Elderkin CL, Christian AD, Metcalde-Smith JL, Berg DJ (2008) Population genetics and phylogeography of freshwater mussels in North America, Elliptio dilatata and Actinonaias ligamentina (Bivalvia: Unionidae). Mol Ecol 17:2149–2163. doi:10.1111/j.1365-294X.2008.03745.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Geist J (2005) Conservation genetics and ecology of european freshwater pearl mussels (Margaritifera margaritifera L.) Ph.D. thesis, Technische Universität München, Germany. Available at: http://tumb1.biblio.tu-muenchen.de/publ/diss/ww/2005/geist.pdf. Accessed 12 May 2009
Geist J, Auerswald K (2007) Physicochemical stream bed characteristics and recruitment of the freshwater pearl mussel (Margaritifera margaritifera). Freshw Biol 55:2299–2316. doi:10.1111/j.1365-2427.2007.01812.x
Geist J, Kuehn R (2005) Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Mol Ecol 14:425–439. doi:10.1111/j.1365-294X.2004.02420.x
Geist J, Kuehn R (2008) Host-parasite interactions in oligotrophic stream ecosystems: the roles of life history strategy and ecological niche. Mol Ecol 17:997–1008. doi:10.1111/j.1365-294X.2007.03636.x
Geist J, Rottmann O, Schröder W, Kühn R (2003) Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionoidea). Mol Ecol Notes 3:444–446. doi:10.1046/j.1471-8286.2003.00476.x
Geist J, Porkka M, Kuehn R (2006) The status of host fish populations and fish species richness in European freshwater pearl mussel (Margaritifera margaritifera) streams. Aquat Conserv 16:251–266. doi:10.1002/aqc.721
Geist J, Wunderlich H, Kuehn R (2008) Use of mollusc shells for DNA-based molecular analyses. J Molluscan Stud 74:337–343. doi:10.1093/mollus/eyn025
Geist J, Kolahsa M, Gum B, Kuehn R (2009) The importance of genetic cluster recognition for the conservation of migratory fish species: the example of the endangered European Huchen (Hucho hucho L.). J Fish Biol (in press)
Goudet J (1995) F-STAT version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486
Grobler PJ, Jones JW, Johnson NA, Beaty B, Struthers J, Neves RJ, Hallerman EM (2006) Patterns of genetic differentiation and conservation of the slabside pearlymussel, Lexingtonia dolabelloides (Lea, 1840) in the Tennessee river drainage. J Molluscan Stud 72:65–72. doi:10.1093/mollus/eyi055
Gross R, Kühn R, Baars M, Schröder W, Stein H, Rottmann O (2001) Genetic differentiation of European grayling populations across the Main, Danube and Elbe drainages in Bavaria. J Fish Biol 58:264–280. doi:10.1111/j.1095-8649.2001.tb00513.x
Gum B, Gross R, Geist J (2009) Conservation genetics and management implications for European grayling, Thymallus thymallus: synthesis of phylogeography and population genetics. Fish Manag Ecol 16:37–51. doi:10.1111/j.1365-2400.2008.00641.x
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometric 48:361–372. doi:10.2307/2532296
Hamilton KE, Ferguson A, Taggart JB, Tomasson T, Walker A, Fahy E (1989) Post-glacial colonisation of brown trout, Salmo trutta L.: Ldh-5 as a phylogeographic marker locus. J Fish Biol 35:651–664. doi:10.1111/j.1095-8649.1989.tb03017.x
Hänfling B, Brandl R (1998) Genetic variability, population size and isolation in distinct populations in the freshwater fish Cottus gobio L. Mol Ecol 7:1625–1632. doi:10.1046/j.1365-294x.1998.00465.x
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc Lond 58:247–276
Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi:10.1093/bioinformatics/btm233
Journel A, Huijbregts C (1978) Mining geostatistics. Academic Press, London, UK
Jungbluth JR, Coomans HE, Groh H (1985) Bibliographie der Flussperlmuschel Margaritifera margaritifera (Linn. 1785). Verslagenen Technische Gegevens No. 41 Institut voor Taxonomische Zoologie, Universiteit Amsterdam
Lydeard C, Cowie RH, Ponder WF et al (2004) The global decline of nonmarine molluscs. Bioscience 54:321–330. doi:10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2
Marchordom A, Araujo R, Erpenbeck D, Ramos MA (2003) Phylogeography and conservation genetics of the endangered European Margaritiferidae (Bivalvia: Unionoidea). Biol J Linn Soc Lond 78:235–252. doi:10.1046/j.1095-8312.2003.00158.x
Miller MP, Blinn DW, Keim P (2002) Correlations between observed dispersal capabilities and patterns of genetic differentiation in populations of four aquatic insect species from the Arizona white mountains, USA. Freshw Biol 47:1660–1673. doi:10.1046/j.1365-2427.2002.00911.x
Nei M, Tajima F, Tateno Y (1983) Accuracy of genetic distances and phylogenetic trees from molecular data. J Mol Evol 19:153–170. doi:10.1007/BF02300753
Neves RJ, Bogan AE, Williams JD, Ahlstedt SA, Hartfield PW (1997) Status of aquatic molluscs in the southeastern United States: a downward spiral of diversity. In: Benz GW, Collins DE (eds) Aquatic fauna in peril: the southeastern perspective. Southeast Aquatic Research Institute, Lenz Design and Communications, Decatur Special Publication 1
Norrgrann O (2001) Spridningsavstånd mellan och fragmentering av bestånd av flodpärlmussla (Margaritifera margaritifera) i Västernorrlands län. Självständigt arbete Institutionen för Naturvetenskap och Miljö. Stencil. English abstract. Mitthögskolan, Härnösand. 21 pp
Ota T (1993) Dispan: genetic distance and phylogenetic analyses software. Pennsylvania State University, Pennsylvania
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–855. doi:10.1111/j.1471-8286.2005.01155.x
Piertney SB, MacColl ADC, Bacon PJ, Dallas JF (1998) Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers. Mol Ecol 7:1645–1654. doi:10.1046/j.1365-294x.1998.00493.x
Piry S, Cornuet JM (1999) GENECLASS: a program for assignation and exclusion using molecular markers. URLB/INRA, France
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:845–859
Ranke W, Rappe C, Soler T, Funegård P, Karlsson L, Thorell L (1999) Baltic salmon rivers—status in the late 1990 s as reported by the countries in the Baltic region. The Swedish Environmental Protection Agency, Gothenburg, Sweden, 69 pp
Raymond M, Rousset F (1995a) GENEPOP version 3.4: population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution 49:1280–1283. doi:10.2307/2410454
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. doi:10.2307/2409177
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Söderberg H, Karlberg A, Norrgrann O (2008) Status, trender och skydd för flodpärlmusslan I Sverige. ISBN: 1403-624X
Strayer DL, Downing JA, Haag WR et al (2004) Changing perspectives on pearly mussels, North America’s most imperilled animals. Bioscience 54:429–439. doi:10.1641/0006-3568(2004)054[0429:CPOPMN]2.0.CO;2
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. doi:10.1046/j.1365-294x.1998.00289.x
Vaughn CC, Hakenkamp CC (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol 46:1431–1446. doi:10.1046/j.1365-2427.2001.00771.x
Wächtler K, Dreher-Mansur MC, Richter T (2001) Larval types and early postlarval biology in naiads (Unionoida). In: Bauer G, Wächtler K (eds) Ecology and evolution of the freshwater mussels Unionoidea. Springer, Heidelberg. Ecol Stud 145:93–125
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi:10.2307/2408641
Young MR, Cosgrove PJ, Hastie LC (2001) The extent of, and causes for, the decline of a highly threatened naiad: Margaritifera margaritifera. In: Bauer G, Wächtler K (eds) Ecology and evolution of the freshwater mussels Unionoidea. Springer, Heidelberg. Ecol Stud 145:337–357
Ziuganov V, Zotin A, Nezlin L, Tretiakov V (1994) The freshwater pearl mussels and their relationships with salmonid fish. VNIRO, Russian Federal Institute of Fisheries and Oceanography, Moscow, 104 pp
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This work was initiated and financially supported by the Nature Conservation Office at the County Administrative Board of Västernorrland.
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Geist, J., Söderberg, H., Karlberg, A. et al. Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conserv Genet 11, 1339–1350 (2010). https://doi.org/10.1007/s10592-009-9963-4
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DOI: https://doi.org/10.1007/s10592-009-9963-4