Skip to main content

Advertisement

Log in

Population genetics of the freshwater mussel, Amblema plicata (Say 1817) (Bivalvia: Unionidae): Evidence of high dispersal and post-glacial colonization

  • Original Paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Over 70% of North American freshwater mussel species (families Unionidae and Margaritiferidae) are listed as threatened or endangered. Knowledge of the genetic structure of target species is essential for the development of effective conservation plans. Because Ambelma plicata is a common species, its population genetic structure is likely to be relatively intact, making it a logical model species for investigations of freshwater mussel population genetics. Using mtDNA and allozymes, we determined the genotypes of 170+ individuals in each of three distinct drainages: Lake Erie, Ohio River, and the Lower Mississippi River. Overall, within-population variation increased significantly from north to south, with unique haplotypes and allele frequencies in the Kiamichi River (Lower Mississippi River drainage). Genetic diversity was relatively low in the Strawberry River (Lower Mississippi River drainage), and in the Lake Erie drainage. We calculated significant among-population structure using both molecular markers (A.p. Φst = 0.15, θst = 0.12). Using a hierarchical approach, we found low genetic structure among rivers and drainages separated by large geographic distances, indicating high effective population size and/or highly vagile fish hosts for this species. Genetic structure in the Lake Erie drainage was similar to that in the Ohio River, and indicates that northern populations were founded from at least two glacial refugia following the Pleistocene. Conservation of genetic diversity in Amblema plicata and other mussel species with similar genetic structure should focus on protection of a number of individual populations, especially those in southern rivers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Avise JC (2000) Phylogeography: A history of formation of species. Harvard University Press, Cambridge, Massachusetts

    Google Scholar 

  • Berendzen PB, Simons AM, Wood RM (2003) Phylogeography of the northern hogsucker, Hypentelium nigricans (Teleostei: Cypriniformes): Genetic evidence for the existence of the ancient Teays River. J Biogeogr 30:1139–1152

    Article  Google Scholar 

  • Berg DJ, Berg PH (2000) Conservation genetics of freshwater mussels: Comments on Mulvey et al. Conserv Biol 14:1920–1923

    Article  Google Scholar 

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

    Google Scholar 

  • Berg DJ, Haag WR, Guttman SI, Sickel JB (1995) Mantle biopsy: A technique for nondestructive tissue sampling of freshwater mussels. J N Amer Benthol Soc 14:577–581

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bierne N, Launey S, Naciri-Graven Y, Bonhomme F (1998) Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae. Genetics 148:1893–1906

    PubMed  CAS  Google Scholar 

  • Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181

    Article  Google Scholar 

  • Bogan AE (1993) Fresh-water bivalve extinctions, Mollusca, Unionoida.; A search for causes. Amer Zool 33:599–609

    Google Scholar 

  • Bunn SE, Hughes JM (1997) Dispersal and recruitment in streams: Evidence from genetic studies. J N Amer Benth Soc 16:338–346

    Article  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Crandall KA (1996) Multiple interspecies transmissions of human and simian T-cell leukemia/lymphoma virus type I sequences. Mol Biol Evol 13:115–131

    PubMed  CAS  Google Scholar 

  • Crandall KA (1998) Conservation phylogenetics of Ozark crayfishes: Assigning priorities for aquatic habitat protection. Biol Conserv 84:107–117

    Article  Google Scholar 

  • Cummings KS, Mayer CA (1992) Field guide to freshwater mussels of the Midwest. Illinois Natural History Survey, Champaign, Illinois

  • Curole JP, Foltz DW, Brown KA (2004) Extensive allozyme monomorphism in a threatened species of freshwater mussel, Margaritifera hembeli Conrad, Bivalvia : Margaritiferidae. Conserv Genet 5:271–278

    Article  CAS  Google Scholar 

  • Elderkin CL, Klerks PL, Theriot E (2001) Shifts in allele and genotype frequencies in zebra mussels, Dreissena polymorpha, along the latitudinal gradient formed by the Mississippi River. J N Am Bethol Soc 20:595–605

    Article  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 

  • Fetzner JW, Crandall KA (2003) Linear habitats and the nested clade analysis: An empirical evaluation of geographic versus river distances using an Ozark crayfish (Decapoda: Cambaridae). Evolution 57:2101–2118

    Article  PubMed  CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Foltz DW (1986) Null alleles as a possible cause of heterozygote deficiencies in the oyster Crassostrea virginica and other bivalves. Evolution 40:869–870

    Article  Google Scholar 

  • Frankham R (2003) Genetics and conservation biology. Comptes Rendus Biologies 326:S22–S29

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gaffney PM, Scott TM, Koehn RK, Diehl WJ (1990) Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics 124:687–699

    PubMed  CAS  Google Scholar 

  • Graf DL (2002) Historical biogeography and late glacial origin of the freshwater pearly mussel (Bivalvia: Unionidae) faunas of Lake Erie, North America. Occasional Papers on Mollusks 6:175–211

    Google Scholar 

  • Grobler JP, Jones JW, Johnson NA, Beaty B, Struthers J, Neves RJ, Hallerman EM (2006) Patterns of genetic differentiation in the slabside pearlymussel, Lexingtonia dollabelloides Lea 1840, in the Tennessee drainage. J Molluscan Stud 72:65–75

    Google Scholar 

  • Haag WR, Berg DJ, Garton DW, Farris JL (1993) Reduced survival and fitness in native bivalves in response to fouling by the introduced zebra mussel, Dreissena polymorpha. in western Lake Erie. Can J Fish Aquat Sci 50:13–19

    Article  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Inc., Sunderland, Massachusetts

    Google Scholar 

  • Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont, Texas

    Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Hilbish TJ, Koehn RK (1985) Dominance in physiological phenotypes and fitness at an enzyme locus. Science 229:52–54

    Article  PubMed  CAS  Google Scholar 

  • Hoeh WR, Stewart DT, Guttman SI (2002) High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in freshwater mussels (Bivalvia: Unionoidea). Evolution 56:2252–2261

    Article  PubMed  CAS  Google Scholar 

  • Hoeh WR, Stewart DT, Sutherland BW, Zouros E (1996) Cytochrome oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia). Mol Biol Evol 13:418–421

    PubMed  CAS  Google Scholar 

  • Hoggarth MA (1995–1996) The Unionidae (Mollusca: Bivalvia) of the Walhonding River, Coshocton county, Ohio, including the federally endangered catspaw, Epioblasma obliquata obliquata, fanshell, Eyprogenia stegaria, and clubshell, Pleurobema clava mussels. Walkerana 8:149–176

    Google Scholar 

  • Hughes JM, Bunn SE, Cleary C, Hurwood DA (2000) A hierarchical analysis of the genetic structure of an aquatic insect Bungona (Baetidae: Ephemeroptera). Heredity 85:561–570

    Article  PubMed  CAS  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 diversity among four Amblemini species (Bivalvia: Unionidae) in the Cache and White rivers, Arkansas. Southwest Nat 43:321–332

    Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lessios HA (1992) Testing electrophoretic data for agreement with Hardy-Weinberg expectations. Mar Biol 112:517–523

    Article  Google Scholar 

  • Lewis PO, Zaykin D (1999) Genetic Data Analysis: Computer program for the analysis of allelic data. Version 1.0, d13. http://www.lewis.eeb.uconn.edu/lewishome/software.html

  • Lyons J, Kanehl P (2002) Seasonal movements of smallmouth bass in streams. In: Philipp DP, Ridgeway MS (eds) Black bass: Ecology, conservation, and management, symposium 31. American Fisheries Society, Bethesda, Maryland, pp␣149–160

    Google Scholar 

  • Machordom A, Araujo R, Erpenbeck D, Ramos MA (2003) Phylogeography and conservation genetics of endangered European Margaritiferidae, Bivalvia : Unionoidea. Biol J Linn Soc 78:235–252

    Article  Google Scholar 

  • Maddison DR, Maddison WP (2001) MacClade 4: Analysis of phylogeny and character evolution. Sunderland Associates, Sunderland, Massachusetts

    Google Scholar 

  • Mandrak NE, Crossman EJ (1992) Postglacial dispersal of freshwater fishes into Ontario. Can J Zool 70:2247–2259

    Article  Google Scholar 

  • Mayden RL (1985) Biogeography of Ouachita highland fishes. Southwest Nat 30:195–211

    Article  Google Scholar 

  • Mayden RL (1988) Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Syst Zool 37:329–355

    Article  Google Scholar 

  • McMahon RF (1991) Mollusca: Bivalvia. In: Thorpe JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, pp␣315–399

    Google Scholar 

  • Meffe GK, Vrijenhoek RC (1988) Conservation genetics in the management of desert fishes. Conserv Biol 2:157–169

    Article  Google Scholar 

  • Metcalfe-Smith JL, Staton SK, Mackie GL, Lane NM (1998) Changes in the biodiversity of freshwater mussels in the Canadian waters of the lower Great Lakes drainage basin over the past 140 years. J Great Lakes Res 24:845–858

    Article  Google Scholar 

  • Miller MP (1997) Tools for population genetic analyses, TFPGA. a Windows program for the analysis of allozyme and molecular population genetic data. Available from the author: M.P. Miller. http://www.bioweb.usu.edu/mpmbio/

  • 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, U.S.A. Freshw Biol 47:1660–1673

    Article  CAS  Google Scholar 

  • Moritz C (1994a) Applications of mitochondrial DNA analysis in conservation: A critical review. Mol Ecol 3:401–411

    Article  CAS  Google Scholar 

  • Moritz C (1994b) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the␣evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Nagel KO, Badino G, Alessandria B (1996) Population genetics of European Anodontinae (Bivalvia: Unionidae). J Mollus Stud 62:343–357

    Article  Google Scholar 

  • Nei M (1978) Estimating average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Neves RJ (1999) Conservation and commerce: Management of freshwater mussel, Bivalvia : Unionoidea, resources in the United States. Malacologia 41:461–474

    Google Scholar 

  • Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: Experimental populations of Clarkia pulchella. Evolution 51:354–362

    Article  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis: A handbook for animal and population studies. Academic Press, New York

    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). Mol Ecol 10:2225–2234

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419

    PubMed  CAS  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494

    Article  CAS  Google Scholar 

  • Schmidt PS, Rand DM (1999) Intertidal microhabitat and selection at Mpi: Interlocus contrasts in the northern acorn barnacle, Semibalanus balanoides. Evolution 53:135–146

    Article  Google Scholar 

  • Schneider SH, Kueffer J, Roessli D, Excoffier L (2000) Arlequin: A software for population genetic data analysis, Version 2.0. Geneva, Switzerland

  • Schultheis AS, Weigt LA, Hendricks AC (2002) Gene flow, dispersal, and nested clade analysis among populations of the stonefly Peltoperla tarteri in the southern Appalachians. Mol Ecol 11:317–327

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Slatkin M (1981) Estimating levels of gene flow in natural populations. Genetics 99:323–335

    PubMed  Google Scholar 

  • Sokal RR, Sneath PHA (1963) Principles of Numerical Taxonomy. W. H. Freeman, San Francisco, CA

    Google Scholar 

  • Stiven AE, Alderman J (1992) Genetic similarities among certain freshwater mussel populations of the Lampsilis genus in North Carolina. Malacologia 34:355–369

    Google Scholar 

  • Swofford DL (2000) PAUP*; phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Swofford DL, Selander RB (1981) BIOSYS-1: a FORTRAN program for the comparative analysis of electrophoretic data in population genetics and systematics. J Hered 72:281–283

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Templeton AR (1998) Nested clade analyses of phylogeographic data: Testing hypotheses about gene flow and population history. Mol Ecol 7:381–397

    Article  PubMed  CAS  Google Scholar 

  • Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping 4. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669

    PubMed  CAS  Google Scholar 

  • Turner TF, Trexler JC, Harris JL, Haynes JL (2000) Nested cladistic analysis indicates population fragmentation shapes genetic diversity in a freshwater mussel. Genetics 154:777–785

    PubMed  CAS  Google Scholar 

  • Vaughn CC, Mather CM, Pyron M, Mehlhop P, Miller EK (1996) The current and historical mussel fauna of the Kiamichi River, Oklahoma. Southwest Nat 41:325–328

    Google Scholar 

  • Vaughn CC, Spooner DE (2004) Status of the mussel fauna of the Poteau River and implications for commercial harvest. Amer Mid Nat 152:336–346

    Article  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Wares JP, Turner TF (2003) Phylogeography and diversification in aquatic mollusks. In: Lydeard C, Lindberg DR (eds) Molecular systematics and phylogeography of mollusks. Smithsonian Books, Washington, D.C, pp 229–269

    Google Scholar 

  • Watt WB (1977) Adaptation at specific loci. 1. Natural selection on phosphoglucose isomerase of Colias butterflies: Biochemical and population aspects. Genetics 87:177–194

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: Fst≠1/(4 Nm  +  1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Williams JD, Warren ML, Cummings KS, Harris JL, Neves RJ (1993) Conservation status of freshwater mussels of the United States and Canada. Fisheries 18:6–21

    Article  Google Scholar 

  • Wright S (1942) Isolation by distance. Genetics 28:114–138

    Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

  • Zouros E, Foltz D (1984) Possible explanations of heterozygote deficiency in bivalve mollusks. Malacologia 25:583–591

    Google Scholar 

Download references

Acknowledgements

We thank S. Guttman and W. Hoeh for assistance and advice with methodologies. We thank the following field assistants: J. Di Maio, S. Staton, S. Roark, K. Elderkin , J. Harris, S. Chordas , C. Meier, and D. Spooner. B. Jack, J. Trybula, S. Roark, V. Gervasio, and numerous undergraduate students assisted with the laboratory work. E. Cunningham calculated geographic distances among populations. This manuscript was greatly improved by the comments of R. Waples and two anonymous reviewers. Mussels were collected under multiple permits from Division of Wildlife, Ohio Department of Natural Resources, and Oklahoma Department of Wildlife Conservation. Tissue collection by C. Vaughn was supported by NSF grants DEB-9306687 and DEB-9870092. This project was supported by Ohio’s Lake Erie Protection Fund (grant 00–01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. L. Elderkin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elderkin, C.L., Christian, A.D., Vaughn, C.C. et al. 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). https://doi.org/10.1007/s10592-006-9175-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9175-0

Keywords

Navigation