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Population genetic structure of a rare unionid (Lampsilis cariosa) in a recently glaciated landscape

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Abstract

The yellow lampmussel (Lampsilis cariosa) is a rare unionid species in need of conservation, as it is declining throughout most of its Atlantic slope range in North America. Because freshwater mussels rely on a fish host for dispersal of their larvae, barriers to the movement of hosts, such as habitat fragmentation by dams, may indirectly affect population genetic structure. We used microsatellite loci to assess genetic variation for L. cariosa within and among three river drainages in the northern part of its range, which emerged from glaciation only ∼ ∼8–10 kya. Despite this relatively recent emergence, significant differences were observed among populations both within and among drainages, possibly because low effective population sizes meant that populations of these mussels achieved drift-migration equilibrium rapidly following glaciation. L. cariosa individuals could be assigned to their own drainages with 89.3% accuracy. Among-population differences were modest, however, in comparison to differences observed in another study of rare mussels south of the recently glaciated region. L. cariosa populations exhibited significant isolation by distance, but there was no additional variation explained by the number, size, or age of intervening dams. An understanding of mussel population genetic structure provides information, useful for conservation planning, on patterns of isolation and connectivity among populations.

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References

  • Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and population numbers of two populations using a coalescent approach. Genetics 152: 763–773

    PubMed  CAS  Google Scholar 

  • Beerli P (1997–2002) MIGRATE (v. 2.03): documentation and program, part of LAMARC. Version 1.6. Revised August 23, 2002. http://evolution.genetics.washington.edu/lamarc.html

  • Berg DJ, Cantonwine EG, Hoeh WR, Guttman SI (1998) Genetic structure of Quadrula quadrula (Bivalvia: Unionidae): Little variation across large distances. Journal of Shellfish Research 17: 1365–1373

    Google Scholar 

  • Berg DJ, Haag WR, Gutman SI, Sickel JB (1995) Mantle biopsy: A technique for nondestructive tissue sampling of freshwater mussels. Journal of the North American Benthological Society 14:577–581

    Article  Google Scholar 

  • Berg DJ, Hoeh WR, Guttman SI (1997) Alternative models of genetic structure in unionid populations: Conservation and management implications. Journal of Shellfish Research 16: 322–323

    Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5: 453–455

    Article  PubMed  CAS  Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol. Ecol. 7: 431–452

    Article  Google Scholar 

  • Bohonak AJ (2002) IBD (Isolation By Distance): a program for analyses of isolation by distance. Journal of Heredity, 93: 153–154

    Article  PubMed  CAS  Google Scholar 

  • Bowen BS (2004) The endangered Lampsilis higginsii: Using mitochondrial and microsatellite DNA data for developing propagation and recovery plans. Conservation Genetics Workshop on Imperiled Freshwater Mollusks and Fishes, National Conservation Training Center, Shepherdstown, WV. http://ellipse.inhs.uiuc.edu/FMCS/Meetings/GeneticsWorkshop.html

  • Carlander KD (1997) Freshwater Fishery Biology. Iowa State University Press, Ames, IA

    Google Scholar 

  • Cope WG, Waller DL (1995) Evaluation of freshwater mussel relocation as a conservation and management strategy. Regulated Rivers-Research & Management 11: 147–155

    Article  Google Scholar 

  • Cornuet J-M, 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

    PubMed  CAS  Google Scholar 

  • Davis GM, Heard WH, Fuller SLH, Hesterman C (1981) Molecular genetics and speciation in Elliptio and its relationships to other taxa of North American Unionidae: Bivalvia. Biological Journal of the Linnean Society 15: 131–150

    Article  Google Scholar 

  • Davis RB, Jacobson GL (1985) Late glacial and early Holocene landscapes in northern New England and adjacent areas in Canada. Quaternary Research 23: 341–368

    Article  Google Scholar 

  • Eackles MS, King TL (2002) Isolation and characterization of microsatellite loci in Lampsilis abrupta (Bivalvia: Unionidae) and cross-species amplification within the genus. Molecular Ecology Notes 2: 559–562

    Article  CAS  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nature Reviews Genetics 5: 435–445

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Ewen KR, Bahlo M, Treloar SA, Levinson DF, Mowry B, Barlow JW, Foote SJ (2000) Identification and analysis of error types in high-throughput genotyping. American Journal of Human Genetics 67: 727–736

    Article  CAS  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: Towards a unified concept for defining conservation units. Molecular Ecology 10: 2741–2752

    PubMed  CAS  Google Scholar 

  • Geist J, Kuehn R (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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361–372

    Article  PubMed  CAS  Google Scholar 

  • Haberl M, Tautz D (1999) Comparative allele sizing can produce inaccurate allele size differences for microsatellites. Molecular Ecology 8: 1347–1349

    PubMed  CAS  Google Scholar 

  • Hartl DD, Clark AG (1997) Principles of Population Genetics, Third Edition. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53: 1898–1914

    Article  Google Scholar 

  • Johnson RL, Liang FQ, Farris JL (1998) Genetic relationships of several Amblemini species (Bivalvia: Unionidae) in Arkansas. Journal of Shellfish Research 17: 1237–1242

    Google Scholar 

  • Kat PW (1983a) Patterns of electrophoretic and morphologic variability in a widely distributed unionid an initial survey. Netherlands Journal of Zoology 33: 21–40

    Article  Google Scholar 

  • Kat PW (1983b) Morphologic divergence genetics and speciation among Lampsilis Bivalvia: Unionidae. Journal of Molluscan Studies 49: 133–145

    Google Scholar 

  • Kelly MW (2004) Conservation genetics of two rare freshwater mussel species: The tidewater mucket (Leptodea ochracea) and the yellow lampmussel (Lampsilis cariosa). Master’s Thesis. University of Maine, Orono, Maine, USA

  • King TL, Eackles MS, Gjetvaj B, Hoeh WR (1999) Intraspecific phylogeography of Lasmigona subviridis (Bivalvia: Unionidae): Conservation implications of range discontinuity. Molecular Ecology 8: S65–S78

    Article  PubMed  CAS  Google Scholar 

  • King TL, Morrison CL, Playfoot KM, Eackles MS, von Oettingen SL, Lellis WA (2004) Conservation genetics of the endangered dwarf wedgemussel (Alasmidonta heterodon): A hierarchical perspective. Conservation Genetics Workshop on Imperiled Freshwater Mollusks and Fishes, National Conservation Training Center, Shepherdstown, WV. http://ellipse.inhs.uiuc.edu/FMCS/Meetings/GeneticsWorkshop.html

  • Lai Y, Sun F (2003) The relationship between microsatellite slippage mutation rate and number of repeat units. Molecular Biology and Evolution 20(12): 2123–2131

    Article  CAS  Google Scholar 

  • Lydeard C, Mulvey M, Davis GM (1996) Molecular systematics and evolution of reproductive traits of North American freshwater unionacean mussels (Mollusca: Bivalvia) as inferred from 16S rRNA gene sequences. Philosophical Transactions of the Royal Society of London B Biological Sciences 351: 1593–1603

    Article  CAS  Google Scholar 

  • Lynch M (1996) A quantitative-genetic perspective on conservation issues. In: Avise J.C, Hamrick JL (eds) Conservation Genetics: Case Histories from Nature. Chapman and Hall, New York, NY

    Google Scholar 

  • McGoldrick DJ, Hedgecock D, English LJ, Baoprasertkul P, Ward RD (2000) The transmission of microsatellite alleles in Australian and North American stocks of the Pacific oyster (Crassostrea gigas): Selection and null alleles. Journal of Shellfish Research 19: 779–788

    Google Scholar 

  • Meldgaard T, Nielsen EE, Loeschcke V (2003) Fragmentation by weirs in a riverine system: A study of genetic variation in time and space among populations of European graylng (Thymallus thymallus). Conservation Genetics 4: 735–747

    Article  CAS  Google Scholar 

  • Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. Journal of Evolutionary Biology 14: 892–903

    Article  Google Scholar 

  • Miller LM (2003) Microsatellite DNA loci reveal genetic structure of yellow perch in Lake Michigan. Transactions of the American Fisheries Society 132: 503–513

    Article  CAS  Google Scholar 

  • Mock KE, Brim-Box JE, Miller MP, Downing ME, and Hoeh WR (2004) Genetic diversity and divergence among freshwater mussel (Anodonta) populations in the Bonneville Basin of Utah. Molecular Ecology 13: 1085–1098

    Article  PubMed  CAS  Google Scholar 

  • Mulvey M, Liu H-P, Kandl KL (1998) Application of molecular genetic markers conservation of freshwater bivalves. Journal of Shellfish Research 17: 1395–1405

    Google Scholar 

  • Mulvey M, Lydeard C, Pyer DL, Hicks KM, Brim-Box J, Williams JD, et al. (1997) Conservation genetics of North American freshwater mussels Amblema and Megalonaias. Conservation Biology, 11: 868–878

    Article  Google Scholar 

  • Nagel K-O, Badino G, Alessandria B (1996) Population genetics of European Anodontinae (Bivalvia: Unionidae). Journal of Molluscan Studies 62: 343–357

    Article  Google Scholar 

  • Nammack M (1998) National Marine Fisheries Service and the evolutionarily significant unit: Implications for management of freshwater mussels. Journal of Shellfish Research 17: 1415–1418

    Google Scholar 

  • Nedeau EJ, McCollough MA, Swartz BI (2000) The Freshwater Mussels of Maine. Maine Department of Inland Fisheries and Wildlife, Augusta, ME

    Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4: 347–354

    PubMed  CAS  Google Scholar 

  • Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: A caution for parentage and population studies. Molecular Ecology 4: 249–252

    PubMed  CAS  Google Scholar 

  • Petit RJ, El-Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12: 844–855

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2003) GeneClass2: A software for genetic assignment and first generation migrants detection

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America 94: 9197–9201

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2) population genetic software for exact tests and ecumenicism. Journal of Heredity 86: 248–249

    Google Scholar 

  • Raymond M, Vaanto RL, Thomas F, Rousset F, De Meuss T, Renaud F (1997) Heterozygote deficiency in the mussel Mytilus edulis species complex revisited. Marine Ecology. Progress Series 156: 225–237

    Article  Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55: 1095–1103

    PubMed  CAS  Google Scholar 

  • Rice W (1989) Analyzing tables of statistical tests. Evolution 43: 223–225

    Article  Google Scholar 

  • Rodhouse PG, McDonald JH, Newell RIE, Koehn RK. (1986) Gamete production somatic growth and multiple-locus enzyme heterozygosity in Mytilus edulis. Marine Biology 90: 209–214

    Article  Google Scholar 

  • Roe KJ, Hartfield PD, Lydeard C (2001) Phylogeographic analysis of the threatened and endangered superconglutinate-producing mussels of the genus Lampsilis (Bivalvia; Unionidae). Molecular Ecology 10: 2225–2234

    Article  PubMed  CAS  Google Scholar 

  • Roe KJ, Lydeard C (1998a) Molecular systematics of the freshwater mussel genus Potamilus (Bivalvia: Unionidae). Malacologia 39: 195–205

    Google Scholar 

  • Roe KJ, Lydeard C (1998b) Species delineation and the identification of evolutionarily significant units in the freshwater mussel genus Potamilus (Bivalvia: Unionidae). Journal of Shellfish Research 16: 326

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatas T (1989) Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000). Arlequin, v. 2.0: A software for population genetics analysis. Genetics and Biometry Laboratory, Geneva, Switzerland

    Google Scholar 

  • Serb JM, Buhay JE, Lydeard C (2003) Molecular systematics of the North American freshwater bivalve genus Quadrula (Unionidae: Arnbleininae) based on mitochondrial ND1 sequences. Molecular Phylogenetics & Evolution 28: 1–11

    Article  CAS  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47: 264–279

    Article  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457–462

    PubMed  CAS  Google Scholar 

  • Small MP, Beacham TD, Withler RE, Nelson RJ (1998) Discriminating coho salmon (Oncorhynchus kisutch) populations within the Fraser River, British Columbia, using microsatellite DNA markers. Molecular Ecology 7: 141–155

    Article  CAS  Google Scholar 

  • Strayer DL, Smith LC (1996) Relationships between zebra mussels (Dreissena polymorpha) and unionid clams during the early stage of the zebra mussel invasion of the Hudson River. Freshwater Biology 36: 771–779

    Google Scholar 

  • Turgeon DD, Quinn JF Jr., Bogan AE, Coan EV, Hochberg FG, Lyons WG, et al. (1998) Common and scientific names of aquatic invertebrates from the United States and Canada: mollusks, 2nd edition. American Fisheries Society, Bethesda MD

    Google Scholar 

  • Van Treuren R (1998) Estimating null allele frequencies at a microsatellite locus in the oystercatcher (Haematopus ostralegus). Molecular Ecology 7: 1413–1417

    Article  Google Scholar 

  • van Oosterhout C, Hutchison WF, Wills DPM, Shipley PF (2003). Microchecker. University of Hull, Hull, UK. http://www.microchecker.hull.ac.uk

  • Villella RF, King TL, Starliper CE (1998) Ecological and evolutionary concerns in freshwater bivalve relocation programs. Journal of Shellfish Research 17: 1407–1413

    Google Scholar 

  • Villella RF, Smith DR, Lemarie DP (2004) Estimating survival and recruitment in a freshwater mussel population using mark-recapture techniques. American Midland Naturalist 151: 114–133

    Article  Google Scholar 

  • Waiters GT (1996) Small dams as barriers to freshwater mussels, (Bivalvia, Unionoida) and their hosts. Biological Conservation 75: 79–85

    Article  Google Scholar 

  • Wattier R, Engel CR, Saumitou-Laprade P, Valero M (1998) Short allele dominance as a source of heterozygote deficiency at microsatellite loci: Experimental evidence at the dinucleotide locus Gv1 CT in Gracilaria gracilis. Molecular Ecology 7: 1569–1573

    Article  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370

    Article  Google Scholar 

  • Wick PC (2005) Fish hosts and population status of two threatened freshwater mussels (Unionidae) in Maine. Master’s thesis, University of Maine, Orono, Maine, USA

    Google Scholar 

  • Williams JD, Warren ML, Jr., Cummings KS, Harris JL, Neves RJ (1993) Conservation status of freshwater mussels of the United States and Canada. Fisheries 18: 6–22

    Article  Google Scholar 

  • Zigler SJ, Dewey MR, Knights BC, Runstrom AL, Steingraeber MT (2004) Hydrologic and hydraulic factors affecting passage of paddlefish through dams in the upper Mississippi River. Transactions of the American Fisheries Society 133: 160–172

    Article  Google Scholar 

  • Zouros E, Foltz DW (1984) Possible examinations of heterozygote deficiency in bivalve mollusks. Malacologia 25: 583–592

    Google Scholar 

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Acknowledgements

We would like to thank Kristin Savicki and Stephen Kneeland for field and lab assistance. We would also like to thank Tim King of USGS for sharing primers before publication and Patty Singer of the University of Maine DNA Sequencing Center for processing samples. Beth Swartz, Maine Department of Inland Fisheries & Wildlife Endangered Species Group provided expertise on freshwater mussel distributions and Cyndy Loftin provided assistance with the GIS analysis. Funding sources include Maine Outdoor Heritage Fund (JR), USGS State Partnerships Program (JR), Maine Department Inland Fisheries and Wildlife (JR), and University of Maine (MK, JR). Article 2815 Maine Agricultural and Forest Research Station.

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Kelly, M.W., Rhymer, J.M. Population genetic structure of a rare unionid (Lampsilis cariosa) in a recently glaciated landscape. Conserv Genet 6, 789–802 (2005). https://doi.org/10.1007/s10592-005-9037-1

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